Research

Pan-cancer analysis of the prognosis and immune infiltration of NSUN7 and its potential function in renal clear cell carcinoma

Jinwei Cui1,2 . Shiye Ruan2 . Zhongyan Zhang2 . Hailiang Wang3 . Qian Yan2 . Yubin Chen2 . Jiayu Yang2 . Jike Fang2 . Qianlong Wu4,5 . Sheng Chen1,2 . Shanzhou Huang1,2 . Chuanzhao Zhang1,2 . Baohua Hou1,2

Received: 18 October 2024 / Accepted: 5 March 2025

Published online: 18 March 2025

@ The Author(s) 2025 OPEN

Abstract

Background NSUN7, an enzyme responsible for the RNA m5c modification, has been recognized as a valuable indicator for predicting and diagnosing an array of cancer. Nevertheless, there is still a scarcity of thorough analyses exploring its diagnostic, predictive, and immune system-related importance in various types of cancer.

Methods We integrated multiple publicly available databases, including TCGA, TISIDB, TISCH2, and UALCAN, to compre- hensively investigate the role of NSUN7 in pan-cancer across various omics data types. The research included examining survival rates, genetic mutations, immune cell presence in tumors, analyzing differences in gene expression, and studying individual cells, among other things.

Results NSUN7 expression showed an increase across 12 cancer types and a decrease in another 12 types. NSUN7 was discovered to be linked with enhanced survival rates in bladder urothelial carcinoma (BLCA), kidney renal clear cell carcinoma (KIRC), kidney renal papillary cell carcinoma (KIRP), lung adenocarcinoma (LUAD), pheochromocytoma and paraganglioma (PCPG), skin cutaneous melanoma (SKCM), and uveal melanoma (UVM).On the other hand, NSUN7 seemed to have a detrimental impact on the prognosis of glioblastoma multiforme/brain lower grade glioma (GBMLGG), adrenocortical carcinoma (ACC),acute myeloid leukemia (LAML), stomach adenocarcinoma (STAD), and brain lower grade glioma (LGG). Furthermore, our experimental validation confirmed the inhibitory effect of NSUN7 on proliferation of renal clear cell carcinoma while elucidating its specific part in blocking cell cycle progression.

Conclusions The findings underscore the potential utility of NSUN7 as a valuable prognostic indicator for patients and offer insights into the mechanisms underlying cancer initiation and progression.

Keywords NSUN7 . TCGA . Diagnosis . Bioinformatics

Jinwei Cui, Shiye Ruan and Zhongyan Zhang have contributed equally to this work.

Shanzhou Huang, Chuanzhao Zhang and Baohua Hou have contributed equally as co-corresponding authors.

Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/s12672-025-02061- W.

☒ Shanzhou Huang, hshanzh@163.com; ☒ Chuanzhao Zhang, zhangchuanzhao@gpdh.org.cn; ☒ Baohua Hou, hbh1000@126.com 1South China University of Technology School of Medicine, Guangzhou 51000, China. 2Department of General Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Guangzhou 510080, China. 3Department of Hepatobiliary Surgery, Weihai Central Hospital, Qingdao University, Weihai 264400, China. 4Department of General Surgery, Heyuan People’s Hospital, Heyuan 517000, China. 5Heyuan Key Laboratory of Molecular Diagnosis and Disease Prevention and Treatment, Heyuan People’s Hospital, Heyuan 517000, China.

Check for updates

Discover Oncology (2025) 16:345

| https://doi.org/10.1007/s12672-025-02061-w

Discover

Abbreviations

NSUN2NOP2/Sun RNA methyltransferase 2
DNMT2DNA methyltransferase 2
m5c5-Methylcytosine
cGASCyclic GMP-AMP synthase
STINGStimulator of Interferon Response CGAMP Interactor 1
TREX2Three Prime Repair Exonuclease 2
SLC7A11Solute Carrier Family 7 Member 11
QSOX1Quiescin sulfhydryl oxidase 1
CDK13Cyclin dependent kinase 13
NSUN5NOP2/Sun RNA methyltransferase 5
ACC1Acetyl-CoA carboxylase 1
ALYREFAly/REF Export Factor
NSUN7NOP2/Sun RNA methyltransferase 7
PGC-1aPPAR-y coactivator1a
eRNAsEnhancer RNAs
TIMER2.0Tumor Immune Estimation Resource 2.0
TCGAThe Cancer Genome Atlas
UALCANThe University of ALabama at Birmingham CANcer data analysis Portal
TMETumor microenvironment
TMBTumor mutational burden
MSIMicrosatellite instability
TPMTranscripts per million
GTExGenotype-tissue expression
HPAThe Human Protein Atlas
ROCReceiver operating characteristic
cBioPortalThe cBio cancer genomics portal
TISCH2Tumor immune single-cell hub 2
HRHazard ratio
CIConfidence interval
GSEAGene set enrichment analysis
SİRNASmall interfering RNA
GAPDHGlyceraldehyde-3-phosphate dehydrogenase
CCK-8Cell counting kit-8
ANOVAAnalysis of variance
OSOverall survival
PFIProgress free interval
DSSDisease specific survival
CDK2Cyclin dependent kinase 2
CCNE1CyclinE1
MiRNAMicroRNA
TERTTelomerase reverse transcriptase
SMARCAL1SWI/SNF-related matrix-associated actin-dependent regulator of chromatin subfamily A-like protein 1
PD-L1Programmed cell death 1 ligand 1
ACE2Angiotensin converting enzyme 2
ACCAdrenocortical carcinoma
BLCABladder urothelial carcinoma
BRCABreast invasive carcinoma
CESCCervical squamous cell carcinoma and endocervical adenocarcinoma
CHOLCholangiocarcinoma
COADColon adenocarcinoma
COADREADAdenocarcinoma of the colon and rectum
DLBCDiffuse large B-cell lymphoma, a type of lymphoid neoplasm

☒ Discover

ESCAEsophageal carcinoma
GBMGlioblastoma multiforme
GBMLGGGlioma
HNSCSquamous cell carcinoma of the head and neck
KICHKidney chromophobe
KIRCRenal clear cell carcinoma of the kidney
KIRPRenal papillary cell carcinoma of the kidney
LAMLAcute myeloid leukemia
LGGBrain lower grade glioma
LIHCLiver hepatocellular carcinoma
LUADLung adenocarcinoma
LUSCLung squamous cell carcinoma
MESOMesothelioma
NSCLCNon-small cell lung carcinoma
OVOvarian serous cystadenocarcinoma
PAADPancreatic adenocarcinoma
PCPGPheochromocytoma and paraganglioma
PRADProstate adenocarcinoma
READRectum adenocarcinoma
SARCSarcoma
STADStomach adenocarcinoma
SKCMSkin cutaneous melanoma
TGCTTesticular germ cell tumors
THCAThyroid carcinoma
THYMThymoma
UCECUterine corpus endometrial carcinoma
UCSUterine carcinosarcoma
UVMUveal melanoma

1 Introduction

Recently, the global incidence and mortality rates of cancer have markedly escalated, posing a critical public health and remaining a primary cause of death [1]. Despite the progress made in cancer treatment over the last few decades [2], such as the development of superior prevention strategies and medical innovations, many patients continue to face treatment failures and ultimately lose the battle against illness. Renal clear cell carcinoma is characterized by its complex nature, and notable immunological and metabolic heterogeneity [3]. Deciphering the common molecular mechanisms underlying cancer development patterns is crucial, along with identifying reliable biomarkers for early detection, diag- nosis, and therapeutic interventions [4, 5]. Multi-omics analysis is commonly used in pan-cancer research has become common, allowing for the discovery of more molecular markers for tumors [6].

RNA modifications serve as a key factors in determining the ultimate outcome of RNAs, exerting a substantial influence on various biological processes and cellular phenotypes, thereby holding immense potential for metabolic therapy and immunotherapy [7]. The 5-methylcytosine (m5c) is widely distributed among different types of RNAs, with the highest abundance observed in transfer RNAs and ribosomal RNAs. However, they have also been detected in messenger RNAs and other non-coding RNAs [8]. Members of the NOL1/NOP2/sun (NSUN) family and DNA methyltransferase 2 (DNMT2) enzymes are the main catalysts for the methylation of m5c in human RNA [9]. There is growing evidence indicating that m5c alteration promotes cell growth, development, cell death, and other crucial biological processes by controlling RNA stability, translation effectiveness, and transcription [9]. NOP2/Sun RNA methyltransferase2 (NSUN2), increases the durability of solute carrier family 7 member 11 (SLC7A11) mRNA through m5c modification, leading to resistance to iron- induced cell death in endometrial cancer cells and slowing down cancer advancement [10]. m5c modification has been implicated in cellular metabolism, and NSUN2 acts as a direct glucose sensor that leads to cyclic GMP-AMP synthase/ stimulator of interferon response CGAMP interactor 1 (cGAS/STING) inactivation through the maintenance of three prime repair exonuclease 2 (TREX2) expression, subsequently driving tumorigenesis and immunotherapy insensitivity [11]. In

Discover

Fig. 1 Differential expression and subcellular localization of NSUN7. a Analysis of NSUN7 expression in TIMER2.0. b Differentiation analysis of NSUN7 expression in TCGA-GTEx database. c, d In the HPA database of NSUN7 protein in OS-U2OS, A-431 cell lines. e-m. Exploiting the HPA database to analyze the protein of NSUN7 in various cancers. (* p<0.05, ** p<0.01, *** p <0.001, ns no significance.)

non-small cell lung carcinoma, NSUN2 facilitates quiescin sulfhydryl oxidase 1 (QSOX1) m5c methylation modification by targeting the thioredoxin 1 encoding region [12]. Consequently, increased NSUN2 expression contributes to gefitinib resistance and tumor recurrence [12]. Cyclin dependent kinase 13 (CDK13) promotes the phosphorylation of NOP2/Sun RNA methyltransferase 5 (NSUN5). The phosphorylated version helps with the m5c alteration of acetyl-CoA carboxylase 1 (ACC1) mRNA. Afterwards, the m5c-altered ACC1 messenger RNA binds with Aly/REF export factor (ALYREF) to enhance its durability and aid in nuclear export, ultimately advancing prostate development [13]. NOP2/Sun RNA methyltransferase7 (NSUN7) is epigenetically silenced in hepatocellular carcinoma, leading to decreased mRNA methylation. Additionally, silencing of NSUN7 through DNA methylation has been linked to clinical results and possible susceptibility to treat- ment [14]. Moreover, NSUN7 interacts with PPAR-y coactivator 1 a (PGC-1a), aiding in the transcription of genes related to fasting and causing m5c modification of Enhancer RNAs [15]. Moreover, NSUN7 has been classified as a prognostic diagnostic symbol of sepsis, early lung adenocarcinoma, and Alzheimer’s disease [16-18]. However, an extensive pan- cancer bioinformatic analysis investigating the significance of NSUN7 remains unavailable. Therefore, an extensive and thorough analysis of the association between NSUN7 and cancer will reveal innovative biomarkers and new approaches to cancer therapy.

Our study thoroughly examined the expression patterns, prognostic significance, and molecular mechanisms of NSUN7 in various types of cancer using multiple databases for comprehensive understanding. For instance, we used TCGA [19], TIMER2.0 [20], TISDIB [21], and UALCAN [22-24] for a universal evaluation of NSUN7 in pan-cancer prognosis and immune responses. NSUN7 showed increased expression in 12 types of tumors and decreased expression in 12 types of tumors and has been associated with survival rates across various cancer types. Our results indicate that NSUN7 exhibits differ- ent levels of expression across various molecular and immune subtypes in multiple forms of cancer. This demonstrated a connection between NSUN7 expression and microsatellite instability (MSI), tumor mutational burden (TMB), and the tumor microenvironment (TME). Furthermore, we provide experimental proof of the connection between NSUN7 and renal clear cell carcinoma. The findings of our study demonstrate that NSUN7 exerts inhibitory effects on the growth of renal clear cell carcinoma by slowing cell cycle progression and consequently limiting cell growth.

2 Methods and materials

2.1 RNA expression

TIMER2.0 and mRNA sequence data in TPM format for TCGA and GTEx were uniformly processed using the Toil process by UCSC XENA [25]. The pan-cancer information was acquired from the TCGA database, while the normal tissue data were obtained from GTEx.

2.2 Subcellular localization and immunohistochemical

Immunohistochemical andimmunofluorescent staining images of NSUN7 were collected from Human Protein Atlas (HPA) Data storage.

2.3 Diagnostic and prognostic importance of NSUN7

Relationship between NSUN7 levels and survival rates, and ROC curves for NSUN7 diagnosis in different types of cancer. NUSN7 interacting proteins in TCGA-KIRC are plotted as heatmaps.

Discover

Discover

k

h

e

The expression of NSUN7 Log2 (TPM+1)

0

1

2

00

A

ch

0

Normal

Normal

Normal

ACC

1:

BLCA

BRCA

CESC

CHOL

1:

COAD

1:

DLBC

J:

ESCA

J:

GBM

J

TGCT

BLCA

HNSC

J

OV

KICH

J:

KIRC

Ji

KIRP

LAML

J:

f

LGG

I

i

J:

LUAD

Normal

Normal

Normal

LUSC

J:

MESO

B

ov

J:

PAAD

1:

HPA Database

PCPG

1

PRAD

J:

READ

]:

SARC

SKCM

J:

STAD

THCA

PRAD

COADREAD

TGCT

JA

THCA

1:

THYM

J:

UCEC

UCS

]+

UVM

m

j

g

=

Normal

Normal

Normal

Tumor Normal

UCEC

STAD

LUAD

A-431

a

TCGA-GTEx Database

0

A

0%

ACC.Tumor

BLCA. Tumor

BLCA.Normal-

BRCA. Tumor

BRCA.Normal-

BRCA-Basal. Tumor

BRCA-Her2.Tumor

BRCA-Luminal. Tumor

CESC.Tumor

CHOL.Tumor-

=

CHOL Normal 1

COAD.Tumor

¥

COAD.Normal-

DLBC. Tumor

ESCA.Tumor

ESCA.Normal-

GBM.Tumor

HNSC.Tumor

HINSC.Normal -

HNSC-HPVpos. Tumor

HNSC-HPVneg.Tumor-

KICH.Tumor


KICH.Normal

KIRC.Tumor


KIRC.Normal

KIRP.Tumor

M


KIRP.Normal -

LAML. Tumor

LGG.Tumor

LIHC.Tumor-


LIHC.Normal

LUAD. Tumor


LUAD.Normal-

LUSC.Tumor


LUSC.Normal -

MESO.Tumor

OV.Tumor

PAAD.Tumor

PCPG.Tumor-


PRAD.Normal

READ.Tumor

READ.Normal -

SARC.Tumor

SKCM. Tumor

SKCM.Metastasis

STAD.Tumor

STAD.Normal-

TGCT.Tumor

THCA.Tumor


THCA.Normal

THYM.Tumor

UCEC.Tumor

UCEC.Normal-

UCS.Tumor

UVM.Tumor

TCGA Database

b

d

C

U2OS


PRAD.Tumor



NSUN7 Expression Level (log2 TPM)

Fig. 2 K-M curve and Receiver operating characteristic curve. a Relationship between NSUN7 level of expression and overall survival in can- cer. b Receiver operating characteristic curve for NSUN7 expression in pan-cancer

a

ACC

BLCA

GBMLGG

KIRC

1.0

NSUN7

1.00

NSUN7

1.00

NSUN7

1.00

NSUN7

Survival probability

Low

Survival probability

Low

Survival probability

Low

0.75

High

Survival probability

Low

0.8

High

0.75

High

0.75

High

0.6

0.50

0.50

0.50

0.4

Overall Survival HR = 2.72 (1.20 - 6.17)

Overall Survival

0.25

0.25

HR = 0.73 (0.55 - 0.99)

Overall Survival HR = 8:00 (6.16 - 10.39)

0.25

Overall Survival HR = 0.62 (0.46 - 0.85)

0.2

P = 0.017

P = 0.040

0.00

P < 0.001

P= 0.003

0

50

100

150

0

40

80

120

160

0

50

100

150

200

0

50

100

150

Time (months)

Time (months)

Time (months)

Time (months)

Low

39

16

4

1

Low

217

39

11

5

3

Low

443

83

20

6

0

Low

140

55

6

High

40

12

3

1

High

194

38

11

1

0

High

255

9

4

1

1

High

401

146

33

KIRP

LAML

LGG

LUAD

1.0

NSUN7

1.00

NSUN7

1.00

NSUN7

1.00

NSUN7

Survival probability

Low

Low

Low

0.8

High

Survival probability

0.75

High

Survival probability

0.75

High

Survival probability

Low

0.75

High

0.6

0.50

0.50

0.50

0.4

Overall Survival

0.25

Overall Survival

0.25

HR = 0.30 (0.17 - 0.55)

HR = 1.91 (1.11 - 3.29)

Overall Survival- HR = 4.16 (2.96 - 5.84)

0.25

Overall Survival

0.2

HR = 0.70 (0.52,, 0,94)

P < 0.001

P = 0.020

0.00

P < 0.001

P = 0.017

0

50

100

150

0

25

50

75

0

50

100

150

200

0

50

100

150

200

Time (months)

Time (months)

Time (months)

Time (months)

Low

88

18

3

0

Low

34

14

3

0

Low

389

76

20

6

0

Low

168

20

5

1

0

High

202

53

6

1

High

105

24

13

2

High

141

13

4

1

1

High

362

51

11

5

3

PCPG

SKCM

STAD

UVM

1.0

NSUN7

1.00

NSUN7

1.0

NSUN7

1.0

14

NSUN7

Survival probability

0.9

Low

Survival probability

Low

High

0.75

High

Survival probability

Low

Low

0.8

High

Survival probability

0.8

High

0.8

0.50

0.6

0.6

0.7

0.6

Overall Survival HR = 0.20 (0.05 - 0.92)

0.25

Overall Survival HR = 0.69 (0.52 - 0.92)

0.4

Overall Survival HR = 1.52 (1.00 -

0.4

2.29)

Overall Survival HR = 0.37 (0.14 - 0.94)

0.5

P = 0.038

0.00

P = 0.011

0.2

P = 0.049

0.2

P = 0.036

0

100

200

300

0

100

200

300

0

30

60

90

120

0

20

40

60

80

Time (months)

Time (months)

Time (months)

Time (months)

Low

45

0

0

0

Low

299

46

7

1

Low

91

23

3

0

0

Low

48

25

8

2

1

High

139

14

1

1

High

158

43

15

4

High

279

47

11

4

1

High

32

26

10

1

1

b

CHOL

1.0

DLBC

GBM

1.0

1.0

1.0

KICH

1.0

TGCT

0.8

0.8

0.8

Sensitivity (TPR)

0.8

0.8

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

0.6

0.6

0.6

0.6

0.6

0.4

0.4

0.4

0.4

0.4

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

0.2

AUC: 0.784

AUC: 0.903

AUC: 0.885

0.2

NSUN7

NSUN7

AUC: 0.802

AUC: 0.958

0.0

CI: 0.653-0.915

0.0

CI: 0.860-0.946

0.0

CI: 0.853-0.918

CI: 0.721-0.882

0.0

CI: 0.932-0.985

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1-Specificity (FPR)

1-Specificity (FPR)

1.0

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

1.0

KIRC

1.0

LAML

1.0

LIHC

LUSC

1.0

THCA

1.0

0.8

0.8

0.8

0.8

0.8

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

0.6

0.6

0.6

0.6

0.6

0.4

0.4

0.4

0.4

0.4

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

AUC: 0.833

AUC: 0.852

AUC: 0.710

AUC: 0.765

AUC: 0.769

0.0

CI: 0.788-0.878

0.0

CI: 0.807-0.898

0.0

CI: 0.668-0.753

0.0

CI: 0.733-0.797

0.0

CI: 0.737-0.801

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

OSCc

PCPG

1.0

1.0

1.0

SARC

UCEC

1.0

SKCM

1.0

0.8

0.8

0.8

0.8

0.8

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

0.6

0.6

0.6

0.6

0.6

0.4

0.4

0.4

0.4

0.4

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

0.2

NSUN7

AUC: 0.744

AUC: 0.795

AUC: 0.795

AUC: 0.734

AUC: 0.736

0.0

Cl: 0.661-0.826

0.0

CI: 0.706-0.885

0.0

CI: 0.568-1.000

0.0

CI: 0.707-0.762

0.0

CI: 0.676-0.795

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

1-Specificity (FPR)

Discover

2.4 Immune cell infiltration evaluation

TCGA tumors were analyzed using the XCELL and TIMER algorithms to examine the correlation between NSUN7 expres- sion and immune infiltration levels [26, 27]. The strength of the correlation is indicated by the intensity of the color. Data were visualized as heat maps.

2.5 Connections between NSUN7 levels and TMB, MSI, tumor purity, immunomodulatory genes, and RNA editing genes

All data were analyzed using the Sangerbox tool and their Pearson correlations were calculated for each tumor.

2.6 Analysis of NSUN7 expression in relation to immunological and molecular subtypes

The TISIDB portal identified associations between NSUN7 expression and the immune and molecular subtypes of cancer.

2.7 Investigate the genomic alterations of NSUN7 in multiple tumor categories

Comprehensive analysis of NSUN7 gene variants was performed using the cBioPortal website following the online instruc- tions [28]. This study examined the characteristics of NSUN7 variants across various tumors in TCGA database.

2.8 Correlation analysis between tumor stemness and NSUN7 expression

Pan-cancer data were analyzed using UCSC data. We obtained the expression profiles of NSUN7 for each sample. DNAss tumor stemness scores were calculated based on the methylation profile of each tumor [29].

2.9 Single cell analysis and drug sensitivity

Correlation analyses were conducted between NSUN7 and 14 cancer states based on the cancerSEA database [30]. The corresponding single-cell data were downloaded from. h5 format and annotation results from TISCH2 using the R software MAESTRO and Seurat to process and analyze single-cell data [31]. The cells were re-clustered using the t-SNE method. The correlation between NSUN7 expression and numerous drugs in the Cancer Therapeutics Response Portal database was investigated. Supplementary Material 2 contains the documentation of single-cell datasets ..

2.10 The differential expression of NSUN7 promote methylation

Differential NSUN7 promoter methylation was assessed using UALCAN and differences in NSUN7 promoter methylation were further analyzed in the KIRC cohort based on individual cancer stage, tumor grade, ethnicity, body weight, and other clinicopathological characteristics.

2.11 Differential analysis of NSUN7 in different clinical subgroups of KIRC and correlation with overall survival (OS) within dissimilar clinical segments of KIRC

RNA-seq data from the TCGA-KIRC project were extracted in TPM format from TCGA database. Clinical information was obtained from TCGA-KIRC database. The Survminer and ggplot2 packages were used to display the results.

2.12 Protein interaction analysis

GeneMANIA [32], a prediction site for intergenic interactions, was used to identify proteins that may interact with NSUN7.

Discover

Fig. 3 Correlation of NSUN7 mRNA expression and immune cell infiltration levels and its role in TME. a Exploring the relationship between ▸ NSUN7 and immune cells using the TIMER algorithm. b Relationship between immune cell infiltration and NSUN7 using XCELL algorithm. c Correlation analysis between high and low expression of NSUN7 and genes related to immune regulation. d Correlation between TMB and NSUN7 expression. e MSI and NSUN7 expression correlation. f NSUN7 expression correlates with tumor purity. g, h The expression of NSUN7 in different cancer Molecular Subtype and Immune Subtype

2.13 Prognosis model assessment

Data from RNA sequencing of KIRC samples and clinical information about the patients corresponding to these samples were acquired from TCGA database. A survival curve was constructed using Kaplan-Meier analysis. Based on the provided formula, the risk score was calculated as follows

n 1 i=1 Di

Using the regression coefficients and standard errors obtained from the Cox regression analysis, the hazard ratios and their 95% confidence intervals were calculated.

2.14 GSEA enrichment analysis

To investigate how NSUN7 expression affects KIRC prognosis, gene enrichment was predefined between groups with high and low expression levels. Significantly enriched gene sets were screened with a typical value of p <0.05.

2.15 Cell lines and culture

Renal cell carcinoma lines (786-o, item no. TCH-C107; and A498 item mo.TCH-C147) and human embryonic kidney cells (293T, item no.TCH-C101) were acquired from Suzhou Starfish Biotechnology Co. Ltd. (. We cultured A498 and 786-o cells in RPMI- 1640 medium (Gibco, Carlsbad, California, USA) and 293T cells in Dulbecco’s modified Eagle’s medium. The cells were cultured at 37 ℃ in a 5% CO2 incubator supplemented with 10% fetal bovine serum (Gibco). Short tandem repeat (STR) analysis and mycoplasma contamination were performed by a cell supplier to verify the authenticity of these cell lines.

2.16 Plasmid and small interfering RNA transfection

The procedure for transfecting siRNA and transforming plasmids into six-well plates is described below. Lipofectamine 2000 (Invitrogen, USA) was used for transient transfection following the manufacturer’s instructions, using siRNA and a plasmid sourced from Ruibo (Guangzhou, China). When the cells reached approximately 80% confluence, a mixture of the diluted siRNA or plasmid and Lipofectamine 2000 was added and incubated for 15 min. After rinsing the cells with PBS, 1750 ul of medium without serum was added to each well, then the siRNA or plasmid mixture was added. The medium was changed to complete medium for additional incubation after being incubated at 37 ℃ with 5% CO2 for 6-8 h. RNA and proteins were extracted from the cells 48 h after transfection to assess transfection success. The sequence of NSUN7 siRNA was as follows: si-NSUN7-1 (forward: 5’-CACAGAAAGUCUUAAUCAATT-3’, reverse: 5’-UUGAUUAAGACUUUCUGU GTT-3’); si-NSUN7-2 (forward: 5’-GAGUACAAUCACAAGCUAATT-3’, reverse: 5’-UUAGCUUGUGAUUGUACUCTT-3’); and si- NSUN7-3 (forward: 5’-GAGUUGGGUAAAUCAUCAATT-3’, reverse: 5’-UUGAUGAUUUACCCAACUCTT-3’).

2.17 Real-time fluorescence quantitative PCR

The FastPure Cell Total RNA Isolation Kit V2 (RC112-01; Vazyme, Nanjing, China) was used to isolate total RNA from specific cells. RNA and complementary DNA were extracted using the HiScript II First Strand cDNA Synthesis Kit (R333-00-AC, Vazyme). The SYBR Green Master Mix (Q411-02; Vazyme) was used for quantitative real-time PCR (qRT-PCR). The qTOW- ER3G System from Analytics Jena (Germany) was used to run the PCR program and to gather data. GAPDH base-pair

Discover

a

C

1




**


.**

** p<001

.




..


.

**


Correlation

Myeloid dendritic Del




·


..





8.25

Masonophage

-

*

**

.

.**


..

..


**

.

F

4

b

++ …

..






.

-

.


*


Torti CDS Faire

**

*


**


.



**




**

**

.

*


.

**

..

.

.

**

**



** P=0.01

Pistesacy seid dendritic-cell



..

.**

.

.**

.**

A

Correlation

NCELL


.

*

**

.

*

**


650

Macrophago ME

..


*


.



**

.


**


**

*



**

.

.

+

B-och roive

B cell memon



**



a

gde

3

4

8

NÃO

e

TMB

ACC

UCEC

0.6

BRCA

0,4

THYM

0.2

COAD

0

THCA

-0.4

GBM

STAD

HNSC

SARC

KIRC

LUSC

LGG

f

DERCIN-46

SampleSize

200

GEM

·

400

600

1,000

pValue

0.00

0.01

0.02

0.03

0.04

0.05

0.6

-0.4

0.2

0.2

Correlation coefficient(pearson)

0.4

0.6

d

MSI

BLCA

0.4

UCS

0.2

LUAD

0

-0,2

0.4

UCEC

SARC

TGCT

STAD

.

*

Gmodocyte monocyte progenitor

..


.

.


**

**

.**

A


8

P

$ 2

-

4

6

..


**

·

*




.

*

*

**

**

+++ p-00.001


..

. .

Myeloid dendritic-cell




*

.**

*

Mask quelli


*

+

*

..

**

.

**

·

..

Til NK

.

*** p-08.001

ES

Nowtrophdl



**

**

.

**


.

.

-

*p<0.05

TRUTHLA

g

BRCA

COAD

ESCA

HNSC

KIRP

Expression (log2CPM)

Expression (log2CPM)

6

Expression (log2CPM)

Expression (log2CPM)

5

Expression (log2CPM)

4

4

i

5

!

H

H

!

:

:

4

8

J

2

i

i

8

0

H

i

1

0

1

0

0

C

5

S

2

2

4

5

P<0.001

P<0.001

P<0.001

P<0.001

8

4

P<0.001

Basal

Her2

LumA

LumB

Normal

CIN

HM-SNV

HM-indel

CIN

ESCC

HM-SNV

HM-indel

Atypical

Basal

Classical

Mesenchymal

10

GS

8

GS

0

C2a

C2b

C2c-CIMP

Subtype

Subtype

Subtype READ

Subtype STAD

Subtype

LIHC

LUSC

UCEC

Expression (log2CPM)

5

Expression (log2CPM)

Expression (log2CPM)

Expression (log2CPM)

10

Expression (log2CPM)

5.0

-

U

5

8

8

0

:

H

2.5

i

:

3

C

i

A

1

0

H

N

0

-5

i

0.0

-5

a

P<0.001

P<0.001

0

2.5

10

P=0.0326

10

P.

<0.001

P<0.001

-5.0

iCluster:1

iCluster:2

iCluster:3

basal

classical

primitive

secretory

CIN

GS

HM-SNV

HM-indel

CIN

EBV

GS

HM-SNV

HM-indel

CN_HIGH

CN_LOW

MSI

POLE

Subtype

Subtype

Subtype

Subtype

Subtype

0

BLCA

BRCA

KIRP

LGG

LIHC

Expression (log2CPM)

8

Expression (log2CPM)

Expression (log2CPM)

8

Expression (log2CPM)

Expression (log2CPM)

8

4

5

V

¥

H

:

*

Y

I

I

:

I

å

8

8

-

:

!

0

0

H

A

C

0

H

-5

H

4

5

A

4

P<0.001

P<00001

P=0.00801

P -< 0.001

10

P<01001

C1

C2

C3

C4

C6

C1

C2

C3

C4

C6

C1

C2

C3

C4

C5

C6

C3

C4

C5

C6

C1

C2

C3

C4

C6

PCPG

PRAD

TGCT

THCA

UVM

Expression (log2CPM)

5

Expression (log2CPM)

Expression (log2CPM)

Expression (log2CPM)

6

Expression (log2CPM)

5.0

4

i

E

Y

4

0

N

9

A

!

2.5

H

A

L

8

i

i

0

0

N

En

0

W

!

0.0

N

4

i

10

P=0.00158

P=0.0113

P<0.001

P=0.001

2

2.5

P=0.0366

C2

C3

C4

C5

C6

C1

C2

C3

C4

C1

C2

C3

C4

C1

C2

C3

C4

C6

C3

C4

C5

Discover

CERE

+

.


.

.

**

*

.

*

**

*

**

Fig. 4 Cancer cell expression of NSUN7 analyzed at the single-cell level. The t-SNE plot of single-cell clustering, where different colors rep- resent different types of cells. The t-SNE plot of the expression distribution of selected genes in different cells, where different colors repre- sent expression abundance. The darker the color, the lower the expression of the gene in the cell, and the brighter the color, the higher the expression of the gene in the cell. The bar chart of the expression abundance of selected genes in different cells. (a BLCA; b GBM; c KIRC; d LAML; e LIHC; f LUAD; g PAAD; h PRAD; i SKCM; j STAD; k OV; l THCA)

normalization was applied to the RT-qPCR results by subtracting the GAPDH value from the GAPDH value. The experi- ments were performed in triplicates. The forward primer sequence for NSUN7 is 5’-GGACTCCGTTTATGTCATGGC-3’ and reverse primer, 5’-CTCAGACTCGGACAAGGACC-3’.

2.18 Western blotting procedure

A498 and 786-o cell lines were lysed on ice for 20 min with RIPA lysis buffer (P0013B; Beyotime, Shanghai, China) to obtain proteins. A solution containing proteins was obtained after spinning at 13,000 x g for 20 min at 4 ℃. To denature the proteins, 5 x loading buffers (CW0027, CWBIO, China) were boiled for 15 min. The denatured proteins were subjected to electrophoresis, membrane transfer, blocking, and incubation with primary and secondary antibodies. Following these steps, proteins were visualized using a luminescent solution. The specific antibody stock numbers and dilution ratios are provided in Supplementary Material 1.

2.19 CCK-8 assay for cell proliferation assay

For cell proliferation experiments, 1500 cells were seeded into each well of a 96-well plate and fixed for transfection. The absorbance at 450 nm nanometers was determined following a 2 h incubation in the cell incubator with a full-wavelength enzyme marker, followed by the addition of CCK-8 reagent to the plates at 0, 24, 48, 72, and 96 h our post-inoculation.

2.20 Flow cytometry

Approximately 500,000 cells were transfected with NSUN7 siRNA and control for 48 h, then underwent the Cell Cycle Assay Kit (E-CK-A351, Elabscience, Wuhan, China) followed by analysis using flow cytometry on a CytoFLEX machine (Beck- man, USA). Cells transfected with NSUN7-oe plasmid and control plasmid were also experimented as described above.

2.21 Statistical analysis

Each experiment was repeated thrice. GraphPad Prism 9.0 or R software, version 4.1.2, was used for statistical analyses. Two groups were compared using Student’s t-test, and multiple groups were compared using one-way and repeated measures ANOVA. The following symbols were used to establish statistical significance: p <0.05 is significant.

3 Results

3.1 Diverse expression of NSUN7 and subcellular localization

NSUN7 mRNA expression was markedly higher in Cholangiocarcinoma (CHOL), Colon adenocarcinoma (COAD), Kidney Chromophobe (KICH)), Lung adenocarcinoma (LUAD), Pancreatic adenocarcinoma (PAAD), and Uterine Corpus Endome- trial Carcinoma (UCEC) than in adjacent non-tumor tissue samples using the TIMER2.0 database. Conversely, NSUN7 levels were significantly reduced in Squamous cell carcinoma of the head and neck (HNSC), Renal clear cell carcinoma of the kidney (KIRC), Renal papillary cell carcinoma of the kidney (KIRP), Liver hepatocellular carcinoma (LIHC), Lung squamous cell carcinoma (LUSC), Skin Cutaneous Melanoma (SKCM), and Thyroid carcinoma (THCA) (Fig. 1a). NSUN7 expression was markedly increased in 12 types of cancer, such as CHOL, COAD, Esophageal carcinoma (ESCA), Glioblastoma multiforme (GBM), KICH, Acute Myeloid Leukemia (LAML), LUAD, Ovarian serous cystadenocarcinoma (OV), Prostate adenocarci- noma (PRAD), Rectum adenocarcinoma (READ), UCEC, and Uterine Carcinosarcoma (UCS) in TCGA tumor-GTEx normal tissues (Fig. 1b). We further analyzed the immunohistochemical data using the HPA database. In PRAD, UCEC, OV, Bladder

Discover

a

BLCA

b

GBM

Celltype major lineage

NSUN7

Mean Expression

Celltype major lineage

NSUNT

Mean Expression

404

20

20

30

ISNE_1

A

0

CDATortw

2.00

CD4TONN

2.00

ISNE 2

ISNE_1

P-

CHẤT

ISNE 2

0

Mono/Macse

0

Mono( Macro-

NK

2

1.00

Treg

1.00

-20

-20

-20

-40

-20

ISNE_1

20

-20

ISNE_1

20

-20

30

40

-

-20

0

40

NSUNT

ESNE_I

ISNE_1

NHƯỢNG

-

C

KIRC

d

LAML

Celltype major lineage

NSUNT

Mean Expression

..

Celltype major lineage

NSUNT

Mean Expression

50-1

Mulignam

25

25

25

#

2:00

1.75

ISNE_2

CORT

2.00

ISNE_1

0

ISNE 2

Mono/Macro

0

0-

ISNE 2

0

I

N

$

1.25

1.00

Meso/Macta

1.00

Ting

-28

-25

-25

-25

5

-90

-10

ISNE_1

25

50

-25

ISNE_1

25

-15

ISNE_1

-50

-35

25

NSUN?

ISNE_1

-

NSUNT

-

e

LIHC

f

LUAD

Celltype major lineage

NSUN7

Mean Expression

Celltype major lineage

NSUN7

Mean Expression

DC

40

at-

4.

20

CENTcom

20

1

20

2.00

CD4TONN

ISNE_2

0

ILC

ISNE 2

ISNE_2

2.00

ISNE 2

M Mono/Macte

0

Nije

0

0

9

NK

1.00

Taeg.

CEniTam

-20

Tivg

-20

1

-20

CENTmn

2

-40

.

20

ISNE_1

20

-40

20

ISNE_1

20

-40

-20

40

0

NSUNT

ISNE_1

ISNE_1

20

40

NILINT

-

g

PAAD

h

PRAD

Celltype major lineage

NSUNT

Mean Expression

Celltype major lineage

NSUN7

Mean Expression

504

50-

-

2

25

25

M

25

25

B CD&T

COST

Ľadothelial

2.00

Epithelial

ISNE_1

ISNE 2

0

0

1.75

ISNE_1

Fibroblasts

0

ISNE 2

2.00

0

1KS

Morav Macro

Mono Mammo

Myfibroblasts

1.00

Pengeniter

1.00

Tivg

-25

-25

-25

-25

NA

&

-50

-30

ISNE_1

25

25

ISNE_1

25

25

V

25

NHƯỢNG

ã

ISNE_1

ISNE_1

a

NSUNT

SKCM

STAD

Celltype major lineage

NSUNT

Mean Expression

Celltype major lineage

NSUNT

Mean Expression

40

40-

.

20

20

DC

ISNE 2

2.00

2.00

COST

ISNE 2

1.75

SNE_2

1.75

0

1.50

0-

Gland moon Malotant

ISNE

0

1.50

Mono Macre

0

1.25

Trog

1.00

1.00

-30

Plasma

-20

-20

-25

ISNE_1

30

-40

16

10

ISNE_1

30

NSUNT

7

8

-30

ISNE_

50

-40

ISNE_1

30

NSUNT

k

OV

THCA

Celltype major lineage

NSUNT

Mean Expression

Celltype major lineage

NSUNT

Mean Expression

20

20

Malignant

25

.

r

· I

25

CDITeo

ER:

200

CONT

ISNE_2

2.00

-

0

CLINT

ISNE 2

Malignant

0

1.75

ISNE_2

1.35

0

Endothehal

ISNE 2

0

IT’S

1.00

Malignant

1.00

coTam

-10

-10

-as

Tpoobe

-25

-

-20

-20

%

-

-30

-10

-20

-10

6

-30

I

ISNE_1

ISNE_1

10

50

ISNE_1

25

-25

0

25

NSUNT

ISNE_1

NSUNT

0

Discover

Fig. 5 Analysis of NSUN7 mutations and function. a Frequency of NSUN7 alternation in pan-cancer. b Types of mutant NSUN7 in pan-can- cers. c A number, type, and location of mutations in the NSUN7 gene. d An analysis of the relationship between NSUN7 expression and tumor stemness in pan-cancer. e Analysis of NSUN7 expression in relation to apoptosis, cell cycle, DNA damage, DNA replication, invasion, metastasis, angiogenesis, differentiation, and inflammation. f Analysis of NSUN7 expression and genes related to RNA modification. g Analy- sis of the relationship between NSUN7 expression and IC50 of different drugs using CTRP

Urothelial Carcinoma (BLCA), LUAD, and Adenocarcinoma of the colon and rectum (COADREAD), tumor tissues contained higher levels of NSUN7 than that in normal tissues. Conversely, NSUN7 expression was higher in abnormal tissues than in normal tissues in the Stomach adenocarcinoma (STAD), Testicular Germ Cell Tumors (TGCT), and THCA (Fig. 1e-m). To elucidate the intracellular distribution of NSUN7, we used indirect immunofluorescence to detect NSUN7 distribution in OS-U2OS and A-431 cells using data acquired from the HPA database. These findings indicate the predominant localiza- tion of NSUN7 within vesicular structures in both cell types (Fig. 1c, d).

3.2 NSUN7 plays dual prognostic roles in human cancers

Elevated NSUN7 expression was associated with better OS. NSUN7 was identified as a negative prognostic indicator for ACC, GBMLGG, LAML, LGG, and STAD (Fig. 2a). We examined the diagnostic utility of NSUN7 for distinguishing malignant tissues from normal tissues using ROC curves (Fig. 2b) and confirmed its potential diagnostic value.

3.3 NSUN7 exhibits a robust correlation with immune cell infiltration

TIMER plus XCELL algorithms were used to estimate the relationship between NSUN7 expression and immune cell infiltration to study the influence of NSUN7 on immune cell infiltration. The TIMER algorithm revealed a strong correla- tion between NSUN7 expression and the presence of immune cells infiltrating. Fourteen markers were associated with CD8 +T cells, 17 with CD4+T cells and 18 with B cells (Fig. 3a). Subsequently, the XCELL algorithm was used to analyze the relationship between NSUN7 expression and a broader spectrum of immune cell subtypes. In some cancers, immune cell subtypes are inversely correlated with NSUN7 expression. Low-grade glioma, NSUN7, and most other subtypes positively correlated with diffuse large B-cell lymphoma (Fig. 3b). Cancer progression is significantly influenced by the TME [33]. Within the pan-cancer dataset, it was crucial to assess the relationship between NSUN7 expression and TME in detail. Furthermore, we performed a comparative analysis of NSUN7 in relation to the genes involved in immune regulation (Fig. 3c). NSUN7 expression was exhibited a positive relationship with most immune checkpoint inhibitory molecules. NSUN7 expression showed an almost inverse correlation with five gene families in various cancerous tumors. We studied the immune relevance of NSUN7 in the TME by analyzing the relationship between NSUN7 levels, TMB, and MSI, which significantly affected immunotherapy results. In ACC, GBM, HNSC, LGG, LUSC, and THYM, NSUN7 expression was positively associated with TMB, whereas it was negatively correlated with BRCA, COAD, KIRC, SARC, STAD, THCA, and UCEC (Fig. 3d). BLCA, LUAD, and TGCT showed a positive correlation with MSI and NSUN7 expression, while SARC, STAD, UCEC, and UCS were negatively correlated (Fig. 3e). Moreover, we examined the correlation between NSUN7 expression and tumor purity by calculating the Pearson correlation within each tumor. We identified a considerable correlation among the 36 tumors, with a negative correlation in eight cancers. In contrast, a strong association was observed in 28 different cancer types. NSUN7 levels and tumor purity were negatively correlated in these cases (Fig. 3f). These results implied that NSUN7 may have a substantial impact on antitumor immunity by influencing the composition of the TME.

3.4 Correlation of NSUN7 with molecular and immune subtypes

We examined the effects of NSUN7 on immunological and molecular subtypes of human tumors using the TISDIB data- base portal. Different molecular subtypes showed different NSUN7 expression levels in BRCA, COAD, ESCA, HNSC, KIRP, LIHC, LUSC, READ, STAD, and UCEC (Fig. 3g). Furthermore, NSUN7 expression in BLCA, BRCA, KIRP, LGG, LIHC, PCPG, PRAD, TGCT, THCA, and UVM was found to be associated with immune subtypes (Fig. 3h).

Discover

a

b

6%-

Mutation

NSUN7: mRNA Expression, RSEM (Batch normalized from Illumina HiSeq_RNASeqV2)

5k-

5%

Structural Variant

.

Amplification

4k

Alteration Frequency

4%

Deep Deletion

3k

o

3%

o

2k

2%

o

1k

1%

088

O

8

o

8

0

Structural variant data

Mutation data

+

Deep Deletion

Shallow Deletion

Diploid

Gain

Amplification

CNA data

+

SKCM

UCEC

BLCA

ACC

CESC

LUSC

STAD

OV

ESCA

PAAD

LUAD

KIRP

HNSC

BRCA

GBM

COADREAD

PRAD

LIHC

SARC

THCA

KIRC

LGG

LAML

KICH

THYM

MESO

UCS

PCPG

CHOL

TGCT

UVM

DLBC

NSUN7: Putative copy-number alterations from GISTIC

NSUN7

Splice (VUS)

· Truncating (VUS)

Inframe (VUS)

Missense (VUS)

Not mutated

Not profiled for mutations

Amplification

o Gain

Diploid

Shallow Deletion

Deep Deletion

Structural Variant [8]

C

R176Q/

NSUNT_Human

Somatic Mutation Frequency O 0.8%

5

.

Driver

Vus

VUS

# NSUN7 Mutation

Missense

L

C

truncating

F

Ő

3

Fusion

O

O

.. .

..

0

0

100

200

300

400

500

600

718aa

d

f

PCPG(N-176)

SampleSize

Modification

TGCTIN-147)

·

100

LIHCIN-3663

.

200

Z

SARCIN-253)

UVMIN-T

309

TRMTGIA

correlation coefficient

-500 -600

A

TRMT61B

-10-05 00 0.5

BRCA(N-774

-700

pValue

KIRCIN-309 PALADIN-156

TRMTIOC

pValue

0.00 0.02

0.04

ESCAN IT

0.00

TRMT6

Modification:

KIRPIN-168

KIPANIN 642)

0.01

YTHDCI

STAD(N-369)

0.02

YTHOF2

16A

STESIN-548)

LOADIN-271

0.03

YTHDFI

writer

O reader eraser

COADREADIN 15

0.04

PRADIN 491

MESOON-87

0.05

YTHDFS

UCECIN-173

ALKBHI

ALKBIS

LAML(N=170

NSUNT

GBMIN-SI

THYMIN-119)

DNMT3A

GBMLOGIN-558)

NSUNG

-0.6

-0.4

-0.2

0.0

0.2

0.4

Comrelation coefficient(pearson)

0.6

NSUN3

TROMTI

e

NSUN2

NSUN4

Angiogenesis

NSUNS

Apoptosis CellCycle

DNMT3B

NOP2

Differentiation

DNMTI

DNAdamage

TE12

ALYREF

DNArepair

Cor

1.0

KIAA1429

EMT

0.5

METTL14

Hypoxia

0.0

DC3H13

Inflammation

-0.5

-1.0

METTL3

Invasion

RBMIS8

Metastasis

WTAP

Proliferation

RBMIS

CBLLI

Quiescence

ALKBHS

Stemness

TO

CRC

BRCA

GBM

Glioma

HNSCC

LUAD

RB

UM

YTHDCI

FMRI

g

HNRNPC

Correlation between CTRP drug sensitivity and mRNA expression

YTHDF2

ELAVLI

FOR

YTHDE1

· == 0.05

HNRNPAZBI

FOR

0 0.001

YTHDC2

SUNT

o

O

0

YTHIDES

Comelation -83

GF2BP1

RPPRC

2

660-NASTY

KIRANIN-884)

STINKIN

ESCAP

COADREADY(NBRE

STESINOSOS

THCA(N=560)

CHOLIN-

PRAIXNATO

KIRGIN.CZ

SKCM(N=10

CESCIN-360

GLI-NXTVY

86-NOS

B

-

LAM

P

ME

yturbine

Drugs

-

Discover

Fig. 6 NSUN7 promoter methylation analysis. a, b Differential methylation of the NSUN7 promoter is observed in both normal and neoplas- tic individuals. Beta values represent levels of DNA methylation ranging from 0 (unmethylated) to 1 (fully methylated). Various cut-off values of ß values are used to indicate hypermethylation. c In KIRC patients, the difference in NSUN7 promoter methylation in different groups: age, sex, race, cancer stage, lymph node metastasis, tumor grade. (* p<0.05, ** p<0.01, *** p <0.001, ns, no significance.)

3.5 Analysis of NSUN7 expression in single cell level

Numerous cells within the TME play a decisive role in facilitating cancer progression [34]. The relationship between NSUN7 relationship between NSUN7 expression and a variety of cell types was determined using publicly available single-cell datasets, to understand the various functions of NSUN7 in diverse types of cancer and to improve our understanding of its role. Single-cell studies have shown that NSUN7 is predominantly expressed in B cells, DC, and monomacro-cells in BLCA, KIRC, LUAD, and SKCM cancers (Fig. 4a, c, f, i). These cell types have been implicated in enhancing immune responses and inhibiting tumor growth, consistent with the observed positive correlation between elevated NSUN7 expression levels in BLCA, KIRC, SKCM, and LUAD cancers and overall survival. Conversely, in LAML, OV, PRAD, and THCA cancers, NSUN7 is primarily expressed in malignant cells and epithelial cells (Fig. 4d, k, h, l), which are associated with tumor progression. In these cancers, high NSUN7 expression levels are inversely correlated with overall survival. Specifically, NSUN7 was predominantly expressed in oligodendrocytes, dendritic cells, malignant cells, and gland mucous cells of GBM, LIHC, PAAD, and STAD (Fig. 4b, e, g, j). These results demonstrate the importance of NSUN7 in the TME.

3.6 Gene alterations, functions, and drug sensitivity of NSUN7

Gene variants regarding NSUN7 in different tumors were analyzed using cBioPortal. We found that SKCM, UCEC, and BLCA tumor samples exhibited the highest frequency of NSUN7 genetic changes, which were the most predominant types of gene alterations in all TCGA tumor samples (Fig. 5a). Diploidy, gain functions, and shallow deletions are typical alterations in NSUN7 (Fig. 5b, c). Recent studies have identified more than 100 RNA modifications that are closely associated with tumor progression. This assertion is supported by the significant correlation between NSUN7 expression and the genes involved in RNA modification. A strong positive relationship was observed between NSUN7 and most genes related to RNA modifica- tions, such as METTL3, METTL14, and YTHDF1, as depicted in (Fig. 5f). Additionally, we compared the relationship between tumor stemness and NSUN7 expression in different tumors. Thus, 15 tumors showed significant associations, including seven tumors with a marked positive correlation (Fig. 5d). Furthermore, our findings revealed that NSUN7 expression was negatively associated with pathways linked to apoptosis, DNA damage, cell cycle, DNA replication, invasion, metastasis, and invasion, while displaying a positive correlation with differentiation, angiogenesis, and inflammation, based on data from the cancer SEA single-cell database (Fig. 5e). To analyze effect of NSUN7 undergoing chemotherapy or targeted therapy, we obtained information from the Cancer Therapy Response Portal database. Pearson’s correlation analysis revealed a significant nega- tive association between NSUN7 expression and the IC50 of drugs, such as afatinib and austocystin D. Conversely, NSUN7 expression was positively correlated with the IC50 of drugs such as AT7867, BMS-345541, and teniposide (Fig. 5g).

3.7 NSUN7 promoter methylation analysis

We used the UALCAN database to examine methylation of the NSUN7 promoter. We found that NSUN7 showed methylation in the promoters of various cancer types, such as COAD, HNSC, and KIRC, but showed different patterns in GBM, LUAD, TGCT, and UCEC (Fig. 6a). However, the methylation status of the NSUN7 promoter was two-sided, although the p-value was not statistically significant (Fig. 6b). We also examined whether NSUN7 promoter methylation was related to the clinical charac- teristics of KIRC. A strong association was found between increased NSUN7 promoter methylation and different demographic and clinical characteristics of individuals diagnosed with KIRC, such as age, sex, ethnicity, N stage, cancer stage, and tumor grade (Fig. 6c). Interventions targeting NSUN7 promoter hypermethylation may offer promising therapeutic strategies for the treatment of KIRC.

3.8 Expression of NSUN7 in clinical subgroups of KIRC and its interaction network

A variety of clinical subgroups were examined for the differential expression of NSUN7. NSUN7 expression demonstrated an inverse relationship with age, TNM stage, tumor stage, tissue grading, and primary therapy outcomes. In addition, low NSUN7

Discover

a

Promoter methylation level of NSUN7 in COAD

Promoter methylation level of NSUN7 in GBM

Promoter methylation level of NSUN7 in HNSC

Promoter methylation level of NSUN7 in KIRC

0.325

0.6-

0:45-

0.35-

0.3-

0.4

0.325


0.5

0.35

Beta value

0.275

Beta value

Beta value

Beta value

03-

0.3

0275

0.25

025

0.3

0.2

0.25-

0.225

0.15

0.225

0.2

0.2

0.1

0.2

Normal (n=37)

Primary tumor

Normal

Primary tumor (rm5-40)

Nommal (n=50)

Primary tumor

Normal

Primary tumor

TCGA samples

TCGA samples

TCGA samples

TCGA samples

Promoter methylation level of NSUN7 in LIHC

Promoter methylation level of NSUN7 in LUAD

Promoter methylation level of NSUN7 in LUSC

Promoter methylation level of NSUN7 in PRAD

1 -

0.375-

0.35

0.3-


0.35

0.325

0.20

0.325

0.3

Beta value

0.6

Beta value

Beta value

Beta value

0.275

0.26

0.3

0.25

0.275

0.225

0.2

0.25

02

0.22

0

0.225

02

Primary tuner (-377)

Nonnal

0.175

Primary tumor

TCGA samples

TCGA samples

(rm473)

Normal

Primary tumor

Normal (m=50)

Primary tuamor

TCGA samples

TCGA samples

Promoter methylation level of NSUN7 in SARC

Promoter methylation level of NSUN7 in TGCT

Promoter methylation level of NSUN7 in UCEC

0.4

0.325


0.35

0.3

0.6

Beta value

0.5

Beta value

0.3

Beta value

0.275

9.4

025

025

03

02

0.225

0.1

0.15-

0.2

0

0.1

0.175

Primary tumor

Seminoma

Non-seminoma

Nommal

Primary tumor

TCGA samples

TCGA samples

TCGA samples

b

Promoter methylation level of NSUN7 in BLCA

Promoter methylation level of NSUN7 in BRCA

Promoter methylation level of NSUN7 in CESC

Promoter methylation level of NSUN7 in CHOL

0.35-

0.35-

0.35-

0.45-

0.325

ns

0.325

0.325

0.4-

Beta value

0.3

Beta value

03-

Beta value

0.3

Beta value

0.35

0.275

0275

275

0.3

025

0.25

0.25-

0.225

0.225

0.225

0.25

0.2

02

0.2

02

Nommal

Primary lamor

Primary Tumor

Normal

Primary luamor

Normal

Primary Buamor

TCGA samples

TCGA samples

TCGA samples

TCGA samples

Promoter methylation level of NSUN7 in ESCA

Promoter methylation level of NSUN7 in KIRP

Promoter methylation level of NSUN7 in PAAD

Promoter methylation level of NSUN7 in PCPG

0.35

0.29-

0.32-

0.325

0.5

Beta value

0.3

0.27

Beta value

Beta value

0.28

Beta value

4

0.275

0 25

0.20

025-

0.24

0.225

0.23

0.24

02

0.2

Noenal

0 22

0.22

0.1

Primary tuamor (mt05)

Primary tumser

Primary tumor

Normal

Primary tumor

TCGA samples

TCGA samples

0-275%

TCGA samples

TCGA samples

Promoter methylation level of NSUN7 in STAD

Promoter methylation level of NSUN7 in THCA

Promoter methylation level of NSUN7 in THYM

06-

0.32

03-

0.5

0.25

Beta value

Beta value

Beta value

0.20

4

0.26

0.24

0.3

0.24

0.22

02

0.22

02

Normal

Primary tumor (n=305)

Normal

Primary tumor

(- 500)

Normal (n=2)

Primary tumor (=124)

TCGA samples

TCGA samples

TCGA samples

C

Promoter methylation level of NSUN7 in KIRC

Promoter methylation level of NSUN7 in KIRC

Promoter methylation level of NSUN7 in KIRC

Promoter methylation level of NSUN7 in KIRC

0.35

0.35

0.35

0.375

0.325

*

0.325

0.325

0.35

0.3

0.3

0.325

Beta value

Beta value

Beta value

0.3

=

Beta value

0.3

0.275

0275-

2.275

0.275-

0.25

-

0.25-

0.25-

0.25

0.225

0.225

0.225-

0.225

0.2

0.2

0.2

0.2

Normal

21 - 40 Yrs

41 - 60 Yes

09#141)

61 - 80 Yrs

(=154)

81 - 100 Yrs

(n=17)

()= 160)

Mais

Female ()=154)

Nommal (n=160)

Caucasian

African-american

Asian

Normal

N1

TCGA samples

TCGA samples

(n=135)

TCGA samples

TCGA samples

Promoter methylation level of NSUN7 in KIRC

Promoter methylation level of NSUN7 in KIRC

0.375

0.35

-

0.35

1

0.325

-

0.325

-

Beta value

Beta value

0.3

0.3

0 275

0.275

-

0.25

0.25-

0.225

1

0.225

0.2

0.2

Stage1

Stage3

Snage4

Nomal

Grade1

Grade2

Grade3 (n=123)

Grade4 (n=50)

(n= 150)

(m=73)

TCGA samples

TCGA samples

Discover

Fig. 7 A comprehensive analysis of NSUN7 in KIRC clinical subgroups and a molecular study of its interaction network. a NSUN7 expression differs among KIRC clinical subgroups. b Different clinical subgroups of KIRC were analyzed for K-M survival of NSUN7. c NSUN7 differential analysis in TCGA-KIRC using paired samples. d The molecular network of NSUN7 interactions using Genemania database. e, f A heatmap of co-expression and correlation analysis between NSUN7 and its interacting molecules in the KIRC cohort

expression was positively correlated with OS, Disease Specific Survival (DSS), and Progression Free Interval (PFI) (Fig. 7a). Furthermore, high NSUN7 expression was associated with better OS in most clinical subgroups, including age, sex, gender, T-stage (T3), and pathologic staging subgroups (III and IV). Histological grade subgroups: G1, G2, G3, and G4. However, the low NSUN7 group demonstrated improved overall survival in stages I and II (Fig. 7b). In the TCGA-KIRC paired cohort, NSUN7 expression was reduced in most tumor samples (Fig. 7c). Using the GeneMania database to analyze molecules interacting with NSUN7, we found that PTPN6, NUSN3, NSUN4, NSUN5, and 20 other molecules interacted with NSUN7 (Fig. 7d). We then investigated the co-expression of NSUN7 and its interacting proteins in the TCGA-KIRC cohort (Fig. 7f). We found that NSUN7, MYRIP, ZNF165, ASAP2, HOOK1, CCDC186, and RSPH3 were significantly and positively correlated (Fig. 7e). These findings indicate that NSUN7 is a significant factor in KIRC.

3.9 The GSEA enrichment and in vitro analysis

After a detailed and extensive assessment, we explored the involvement of NSUN7 in KIRC. We obtained RNA sequencing data and survival information for patients with KIRC from the TCGA. In this study, high expression of NSUN7 identified as a protective factor (Fig. 8a, b). The ROC curve areas were 0.626, 0.582, and 0.550 for the 1-, 3-, and 5-year OS rates, respectively (Fig. 8c). In the TCGA-KIRC dataset, we performed differential analysis of a single gene, comparing NSUN7 High with NSUN7 Low. GSEA showed that NSUN7 mainly negatively regulated cycle-related processes or pathways, including cell cycle progres- sion, DNA synthesis, and DNA Replication (Fig. 8d-f). Therefore, we speculate that NSUN7 may inhibit proliferation of KIRC via hindering cell cycle processes. To elucidate the impact of NSUN7 in KIRC tumorigenesis, we transfected siRNA targeting NSUN7 and overexpressed NSUN7 plasmid. We confirmed its efficacy in the 786-O and A498 cell lines to elucidate the biologi- cal functions of NSUN7 in KIRC. The expression of NSUN7 was decreased in renal clear-cell carcinoma (Fig. 8g). RT-qPCR and western blotting were used to confirm the knockdown and overexpression effectiveness (Fig. 8h, i). After transfection, the proliferation of 786-O cells was assessed using a CCK-8 assay. In A498 cells, increased expression of NSUN7 led to a notable suppression of cell growth, whereas reduced expression of NSUN7 led to enhanced cell proliferation in 786-o cells. (Fig. 8j, k). Western blotting showed that increased NSUN7 levels resulted in reduced CDK2 and CCNE1 expression, whereas decreased NSUN7 levels led to the increased expression of both (Fig. 8l, m). Flow cytometry results indicated that NSUN7 knockdown boosted cell proliferation. A decrease in S-phase cells was accompanied by an increase in the number of cells in the G2/M phase. The opposite effect was observed when NSUN7 was overexpressed (Fig. 8n). Overall, reducing NSUN7 expression in renal clear cell carcinoma enhances cell growth, whereas increasing NSUN7 levels hinders cell proliferation.

4 Discussion

The rising rates of different types of cancer have made it crucial to identify predictive biomarkers linked to tumors for diagnosis, prognosis, and treatment [35]. Owing to advancements in bioinformatic tools and databases, numerous studies have been conducted to discover molecular biomarkers that can be applied to a wide range of cancer types, revealing their potential medical and functional significance [36]. Researchers have recently utilized a signature of cell- free immune-related miRNAs for early characterization of various cancers detecting cancer early with a noninvasive diagnostic biomarker [37]. Research has indicated that pan-cancer genome-wide analyses show promise for detecting advanced tumor characteristics and may offer important targets for investigating the biological foundation of cancer [38]. Thus, there is a need to continuous research for more sensitive cancer diagnostic biomarkers and therapeutic targets for the inhibition of cell cycle progression NSUN7 is involved in the biological process of m5c, and is associated with multiple forms of cancer. However, the role of NSUN7 in pan-cancer has not been thoroughly investigated. Based on these reports, our study aimed to thoroughly examine the expression, prognostic significance, and role of NSUN7. In addition, we performed experimental validation using KIRC cells to demonstrate that NSUN7 acts as an anti-oncogene by hindering cell cycle progression. Initially, our research involved a comprehensive analysis of the predictive significance of NSUN7 across various cancer categories, including its expression levels, staging implications, immune cell penetration, biological roles, and promoter methylation patterns in a wide range of cancers. TCGA and GTEx databases were used to

Discover

a

GT

..

-

m

-

3

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

0

6

6

4

6

3

4 .

A

A

&

2

2

2

2

1

0

0

0

:

0

0

Stage I

Stage II Stage III Stage IV Pathologic stage

T1

T2

T3

T4

N1

M1

G2

G3

Pathologic T stage

Pathologic N stage

NO

Pathologic M stage

MO

G1

G4

Histologic grade

AS

6

6-

6.

6-

The expression of NSUN7 Log2 (TPM+1)

6

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

A

4

4 .

4

4.

2

I.

2

2

2.

2

.

0

0

0

0

0

PD

SD

PR

CR

60

>60

Alive

No

No

Primary therapy outcome

Age

OS event

Dead

DSS event

Yes

PFI event

Yes

b

Age: 60

Gender: Male

Gender: Female

Pathologic stage: Stage I&Stage II

1.0

NSUN7

1.0

NSUN7

1.0

NSUN7

1.0

NSUN7

Low

Low

High

0.9

Low

High

Low

0.9

High

High

Survival probability

Survival probability

Survival probability

0.9

0.8

0.8

Survival probability

0.8

0.7

0.8

0.7

0.6

0.6

0.7

0.6

Overall Survival HR = 0.54 (0.33

0.5

Overall Survival HR = 0.65 (0.45 … 0.95)

Overall Survival HR = 0.41 (0.25

0.6

Overall Survival HR = 1.52 (0.83

0.5

P = 0.016

.89)

0.4

0.4

P= 0.026

P < 0.001

0.69)

P= 0.174

2.78)

0

1000

2000

3000

4000

0

1000

2000

3000

4000

Time (days)

0

1000

2000

3000

4000

0

1000

2000

3000

4000

Time (days)

Time (days)

Time (days)

Pathologic stage: Stage III&Stage IV

Pathologic T stage: T3

Histologic grade: G1&G2

Histologic grade: G3&G4

1.0

NSUN7

1.0

NSUN7

1.0

NSUN7

1.00

NSUN7

Low

High

Low

High

Low

High

Low

High

Survival probability

0.8

Survival probability

0.8

Survival probability

0.9

Survival probability

0.75

0.6

0.6

0.8

0.50

0.7

0.4

0.4

0.25

Overall Survival HR = 0.66 (0.45-

10.96)

Overall Survival HR = 0.62 (0.40)

0.96)

0.6

Overall Survival HR = 0.64 (0.31

Overall Survival

P = 0.030

0.2

P = 0.031

P = 0.209

1.29).

HR = 0.59 (0.40 … 0.85)

0.2

0.00

P = 0.005

0

1000

2000

3000

4000

0

1000

2000

3000

4000

0

1000

2000

3000

4000

0

1000

2000

3000

Time (days)

4000

Time (days)

Time (days)

Time (days)

C

e

f

TCGA-KIRC

.

TCGA-KIRC

-

·

6

5

6

The expression of NSUN7 Log2 (TPM+1)

The expression of CCDC186 Log2 (TPM+1)

The expression of ASAP2 Log2 (TPM+1)

4

4

.

NSUN7

Log2 (TPM+1)

3

·

4

Low

2

Normal

3

Tumor

2

High

2

2

1.

Pearson

R = 0,414

Pearson ·R = 0.277 P < 0.001

0

-

1

.

P < 0.001

0

PTPN6

0

Normal

Tumor

0

2

4

6

0

2

4

6

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

NSUN4

d

NSUN5

MYRP

MING

NSUN2

8

.

The expression of HOOK1 Log2 (TPM+1)

The expression of MYRIP

6

NOP2

RSPHS

NSLIN2

6

NSUN6

.

Log2 (TPM+1)

4

CÔỐC TẠI

NSUN?

.

4

SEMG1

NSUING

SPAG1

Z-score

2

2

2.5

TLX1

Pearson

R = 0.336

Pearson

ZNF165

CARMIL

0

0

P < 0.001

R= 0.494

0

P < 0.001

HOOK!

0.0

AŠLAPS

2

ASAP2

0

2

4

6

0

4

6

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

HOOK1

-2.5

CARMIL1

6

.

5.5

TLX1

The expression of ZNF165 Log2 (TPM+1)

The expression of RSPH3 Log2 (TPM+1)

4.5

DHX32

·

4

CCDC186

3.5

RSPH3

2

Pearson R= 0.478

2.5

Pearson

OR2H1

P < 0.001

R = 0.360

1.5

P < 0.001

MYRIP

0

2

4

6

0

2

4

6

The expression of NSUN7 Log2 (TPM+1)

The expression of NSUN7 Log2 (TPM+1)

Discover

Fig. 8 Prognostic model construction and GSEA enrichment analysis and vitro experiment. a Relationship between NSUN7 expression and survival time and survival status in TCGA data. b KM survival curves of NSUN7 in TCGA-KIRC data, in which different groups were tested by log rank. c ROC curves and AUC VALUE values of NSUN7 at different times. d-f Results of GSEA enrichment analysis. g The expression of NSUN7 exhibits differential patterns in clear cell renal cell carcinoma. h, i The knockdown and overexpression efficiency of NSUN7 were assessed using RT-qPCR and Western blot techniques. j, k The cell proliferation was assessed using the CCK-8 assay. l, m The Western blot was employed to detect proteins associated with the cell cycle. n Cell cycle was detected by flow cytometry. (The experiments were con- ducted in triplicate and quantified. The values are presented as the mean+SD of three independent experiments. P value was shown as * P<0.05, ** P<0.01, *** P <0.001, **** P < 0.0001, independent Student’s t test)

analyze NSUN7 expression across 33 different types of tumors. NSUN7 was differentially expressed in 24 tumor types. High NSUN7 expression was associated with better OS in patients with BLCA, KIRC, KIRP, LUAD, PCPG, SKCM, and UVM. Conversely, elevated levels of NSUN7 been linked to poor survival rates in patients with ACC, GBMLGG, LAML, LGG, and STAD. This suggests that the role of NSUN7 in cancer is twofold. This phenomenon is prevalent in tumors. Cancer cells precisely regulate telomerase reverse transcriptase (TERT) expression via allele-specific DNA methylation of the TERT pro- moter [39]. Recent studies have revealed that SWI/SNF-related matrix-associated actin-dependent regulator of chromatin subfamily a-like protein 1 (SMARCAL1) inhibits the cGAS-STING pathway by maintaining genomic stability. In contrast, SMARCAL1 serves as a dual regulator that influences both the expression of programmed cell death 1 ligand 1 (PD-L1) and congenital immune signaling, thus promoting immune evasion in tumors [40]. Studies have shown that tumor pro- gression is significantly correlated with the TME, a complex ecosystem within the body that surrounds the tumor [41]. Understanding the TME is crucial for recognizing the immune-related factors that play a role in cancer advancement and developing cancer immunotherapy [42]. The TMB indicates the likelihood of mutations arising due to a malfunction in the DNA mismatch repair system, which in turn indicates the capacity and level of neoantigen generation in tumors [43]. The therapeutic outcomes of immunotherapy are expected to be more effective in patients with high MSI or TMB. The analysis revealed an inverse correlation between MSI, TMB, and NSUN7 expression in specific cancer types, such as BRCA and COAD. This indicates that NSUN7 may be involved in regulating the tumor immune microenvironment. Thus, we investigated the role of NSUN7 in the immune response to tumors and in the TME. Variations in NSUN7 expression levels have been noted within the TME in various cancers, showing a close correspondence with overall prognosis in comprehensive cancer research. As a systemic ailment, tumors exhibit repetitive occurrence and development accom- panied by intricate microscopic molecular mechanisms [44]. Examining the impact of genes on different types of cancer from various perspectives is crucial for gaining a thorough understanding of the underlying factors that lead to cancer- related deaths. Two factors must be considered when analyzing NSUN7 promoter methylation. Our research revealed that NSUN7 showed increased methylation in the promoters of COAD, HNSC, KIRC, LIHC, LUSC, PRAD, and SARC, but displayed the opposite pattern in GBM, LUAD, TGCT, and UCEC. Scientists have discovered reduced DNA methylation of angiotensin-converting enzyme 2 (ACE2) in most tumors exhibiting high ACE2 levels, prompting further exploration into the genetic and epigenetic changes of ACE2 [45]. This partly explains the differential expression of NSUN7 in pan-cancers.

Our findings indicate that NSUN7 may serve as a potential molecular indicator. To verify the function of NSUN7 in vitro, we confirmed its precise role of NSUN7 in the renal clear-cell carcinoma cell lines (786-o and A498). The CCK-8 proliferation assay demonstrated that knockdown of NSUN7 promoted the proliferation of renal clear-cell carcinoma cells, and conversely, overexpression of NSUN7 in A498 cells inhibited cancer cell proliferation. Analysis of the TCGA- KIRC GSEA results revealed a negative correlation between NSUN7 expression and the cell cycle. Tumor progression is significantly influenced by the cell cycle [46]. Therefore, we hypothesized that NSUN7 inhibits cell proliferation by inhibiting cell cycle progression. Western blotting experiments showed that knockdown of NSUN7 resulted in elevated expression of CDK2 and CCNE1. In summary, NSUN7 may inhibit tumor progression by blocking the cell cycle.

In addition, we must recognize the limitations of our study. First, most pan-cancer study data were obtained from publicly accessible online databases. The lack of comprehensive clinical cohort data could introduce systematic biases requiring validation [47]. Second, our experimental studies were primarily conducted in vitro without valida- tion through in vivo experiments, and therefore offer limited clinical applicability. Third, we identified a significant association between NSUN7 and the immune microenvironment; however, direct evidence elucidating the impact of NSUN7 on immunotherapy is lacking. Further research is required to substantiate this correlation and elucidate the mechanisms underlying the interaction between NSUN7 and immunotherapeutic processes. Nonetheless, it serves as a novel avenue for future research on clinical conversion therapies.c

Discover

a

b

d

Risk Type

1.00

Log-rank P = 0.0201

Groups

Cell Cycle

HR(High groups)-0.698

groups-High groups

0.0

NES == 1.703

High groups

Pady < 0.001

95%CI(0.515, 0.945)

groups=Low groups

FDR < 0.001

Low groups

Log2(TPM+1)

Overall suvival probability

Enrichment Score

-0.1

0.75

4

-0.2

-0.3

0.50

Ranked list metric

6

2

4

0,25

2

-2

-4

Median time:7.6 and 6.3

0

5000

10000

1500

0.00

Rank in Ordered Dataset

0

Groups

groups”High groups 266

167

67

23

3

0

e

Status

Synthesis of DNA

12

groups=Low groups

266

157

85

32

10

0

0.0

NES_1.998

Alive

Padi < 0.001

Dead

0

25

S

7.5

10

12.5

Enrichment Score

-0.1

FOR < 0.001

Time (years)

-0.2

-0.3

8

C

-0.4

Time

1.00

Ranked list metric

6

4

4

2

0

2

0.75

-4

0

5000

10000

1500

f

Rank in Ordered Dataset

0

True positive fraction

DNA Replication

0,50

0.0

NES == 2.131

Enrichment Score

Padi < 0.001

-0.1

FOR - 10/001

-0.2

-0.3

NSUN7

0.25

-0.4

Type

1-Years,AUC=0.626,95%C1(0.558-0.694)

3-Years,AUC=0.582,95%C1(0.529-0.635)

Ranked list metric

6

0,00

5-Years,AUC=0.55,95%CI(0.494-0.606)

4

2

0.00

0.25

0.50

False positive fraction

0.75

1.00

O

1

-4

0

5000

10000

1500

2-score of expression

-2 -101 2

Rank in Ordered Dataset

g

293-T

786-0

A498

h

786-0

i

A498

kDa

A498

Vector OE

kDa

Relative NSUN7 mRNA levels

Scramble si1 si2 si3 kDa

786-0

1,5-

.

-

15-

**

NSUN7

-81

Relative NSUNT miRNA levels

Relative NSUN7 mRNA levels

1.5

-81

NSUN7

1.0-

NSUN7

10-

-81

0.5-

0. 5

5-

0,0-

2937

786-0

A498

GAPDH

-36

a

H

Scramble

GAPDH

-36

GAPDH

-36

¢

, 9

0.

Vector

DE

786-0

A498

1

k

I

Scramble

si1

si2

kDa

m

Vector

OE

kDa

786-0

A498

2.5-

Scramble

OD Value 450(nm)

CDK2

-33

CDK2

2.5

-33

2.0-

si1

Vector

OD Value 450(nm)

2.0

OE

1.5-

.

52

1.5

1.0-

1.0

9.5-

0.5-

CCNE1

-47

CCNE1

i

-

-47

0.0-

0

1

2

3

4

0.0

6

1

2

3

4

days

days

-36

GAPDH

n

GAPDH

-36

Scramble

si1

si2

786-0

80-

nc

si1

300

60-

si2

*

200

200

40-

Count

786-0

Percentage of cells (%)

-

**

-

20-

T

**

1 1

200K

0

7

1

200K

a

400K

0

G1

s

G2

Vector

OE

A498

Percentage of cells (%)

80-

**

Vector

-

A498

60

OE

400

-

40-

**

200

20-

300K

400Kč

..

200K

-

0

G1

s

G2

PE

Discover

5 Conclusion

The discovery of the significance of NSUN7 in cancer diagnosis and prognosis has established a solid foundation for understanding its pivotal role in tumor progression.

Acknowledgements None.

Author contributions Jinwei cui: Writing original draft, Investigation, Data curation, review and editing, Visualization, Validation. Shiye Ruan contributed to writing, reviewing, editing, formal analysis, visualization, validation, and software development. Zhongyan Zhang: Writ- ing-review and editing, Visualization, Experiment validation. Hailiang Wang: Writing-original draft. Qian Yan: Investigation, Visualization. Yubin Chen: Validation, Methodology. Jiayu Yang: Writing-original draft. Jike Fang: Writing-original draft. Qianlong Wu: Visualization. Sheng Chen: Visualization. Shanzhou Huang: Validation, methodology, investigation, and funding acquisition. Chuanzhao Zhang: Writing-review editing, validation, supervision, and funding acquisition; conceptualization. Baohua Hou: Writing-review and editing, writing-first draft-review, validation, supervision of data management and funding acquisition.

Funding This work was supported by grants from the Science and Technology Program of Maoming (2024kjcxLX046), High-level Hospital Construction Research Project of Heyuan People’s Hospital (YNKT202202), Guangdong Province’s Special Fund for Science and Technol- ogy Innovation Strategy (“Major Project + Task List”) Project of Heyuan (23051017147335/2022001), the Science and Technology Program of Guangzhou (2024A04J10016 and 202201011642).

Data availability The original data of this study are available from the corresponding authors.

Declarations

Ethics approval and consent to participate Not applicable.

Competing interests The authors declare no competing interests.

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativeco mmons.org/licenses/by-nc-nd/4.0/.

References

1. Siegel RL, Giaquinto AN, Jemal A. Cancer statistics, 2024. CA Cancer J Clin. 2024;74(1):12-49.

2. Wahida A, et al. The coming decade in precision oncology: six riddles. Nat Rev Cancer. 2023;23(1):43-54.

3. Hu J, et al. Multi-omic profiling of clear cell renal cell carcinoma identifies metabolic reprogramming associated with disease progres- sion. Nat Genet. 2024;56(3):442-57.

4. He K, et al. Decoding the glycoproteome: a new frontier for biomarker discovery in cancer. J Hematol Oncol. 2024;17(1):12.

5. Hedou J, et al. Discovery of sparse, reliable omic biomarkers with Stabl. Nat Biotechnol. 2024. https://doi.org/10.1038/ s41587-023-02033-x.

6. Qin Y, et al. Cuproptosis correlates with immunosuppressive tumor microenvironment based on pan-cancer multiomics and single-cell sequencing analysis. Mol Cancer. 2023;22(1):59.

7. Liu WW, et al. RNA modifications in cellular metabolism: implications for metabolism-targeted therapy and immunotherapy. Signal Transduct Target Ther. 2024;9(1):70.

8. Song H, et al. Biological roles of RNA m (5)C modification and its implications in cancer immunotherapy. Biomark Res. 2022;10(1):15.

9. Li M, et al. 5-methylcytosine RNA methyltransferases and their potential roles in cancer. J Transl Med. 2022;20(1):214.

10. Chen SJ, et al. Epigenetically upregulated NSUN2 confers ferroptosis resistance in endometrial cancer via m (5)C modification of SLC7A11 mRNA. Redox Biol. 2024;69: 102975.

11. Chen T, et al. NSUN2 is a glucose sensor suppressing cGAS/STING to maintain tumorigenesis and immunotherapy resistance. Cell Metab. 2023;35(10):1782-1798 e8.

12. Wang Y, et al. Aberrant m5C hypermethylation mediates intrinsic resistance to gefitinib through NSUN2/YBX1/QSOX1 axis in EGFR-mutant non-small-cell lung cancer. Mol Cancer. 2023;22(1):81.

13. Zhang Y, et al. CDK13 promotes lipid deposition and prostate cancer progression by stimulating NSUN5-mediated m5C modification of ACC1 mRNA. Cell Death Differ. 2023;30(12):2462-76.

14. Ortiz-Barahona V, et al. Epigenetic inactivation of the 5-methylcytosine RNA methyltransferase NSUN7 is associated with clinical outcome and therapeutic vulnerability in liver cancer. Mol Cancer. 2023;22(1):83.

Discover

15. Aguilo F, et al. Deposition of 5-methylcytosine on enhancer RNAs enables the coactivator function of PGC-1alpha. Cell Rep. 2016;14(3):479-92.

16. Zhang Q, et al. Identification and validation of key biomarkers based on RNA methylation genes in sepsis. Front Immunol. 2023;14:1231898.

17. Tian L, et al. Prognostic value and genome signature of m6A/m5C regulated genes in early-stage lung adenocarcinoma. Int J Mol Sci. 2023. https://doi.org/10.3390/ijms24076520.

18. PerezGrovas-Saltijeral A, Rajkumar AP, Knight HM. Differential expression of m (5)C RNA methyltransferase genes NSUN6 and NSUN7 in Alzheimer’s disease and traumatic brain injury. Mol Neurobiol. 2023;60(4):2223-35.

19. Cancer Genome Atlas Research, N., et al., The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet. 2013;45(10): 1113-20.

20. Li T, et al. TIMER20 for analysis of tumor-infiltrating immune cells. Nucleic Acids Res. 2020;48(W1):W509-14.

21. Ru B, et al. TISIDB: an integrated repository portal for tumor-immune system interactions. Bioinformatics. 2019;35(20):4200-2.

22. Zhang Y, et al. Proteogenomic characterization of 2002 human cancers reveals pan-cancer molecular subtypes and associated pathways. Nat Commun. 2022;13(1):2669.

23. Chen F, et al. Pan-cancer molecular subtypes revealed by mass-spectrometry-based proteomic characterization of more than 500 human cancers. Nat Commun. 2019;10(1):5679.

24. Chandrashekar DS, et al. UALCAN: An update to the integrated cancer data analysis platform. Neoplasia. 2022;25:18-27.

25. Zhu J, et al. The UCSC cancer genomics browser. Nat Methods. 2009;6(4):239-40.

26. Aran D, Hu Z, Butte AJ. xCell: digitally portraying the tissue cellular heterogeneity landscape. Genome Biol. 2017;18(1):220.

27. Li B, et al. Comprehensive analyses of tumor immunity: implications for cancer immunotherapy. Genome Biol. 2016;17(1):174.

28. Cerami E, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401-4.

29. Malta TM, et al. Machine learning identifies stemness features associated with oncogenic dedifferentiation. Cell. 2018;173(2):338-354 e15.

30. Yuan H, et al. CancerSEA: a cancer single-cell state atlas. Nucleic Acids Res. 2019;47(D1):D900-8.

31. Han Y, et al. TISCH2: expanded datasets and new tools for single-cell transcriptome analyses of the tumor microenvironment. Nucleic Acids Res. 2023;51(D1):D1425-31.

32. Franz M, et al. GeneMANIA update 2018. Nucleic Acids Res. 2018;46(W1):W60-4.

33. Hoffmann E, et al. Multiparametric MRI for characterization of the tumour microenvironment. Nat Rev Clin Oncol. 2024;21(6):428-48.

34. Du Y, et al. Integration of pan-cancer single-cell and spatial transcriptomics reveals stromal cell features and therapeutic targets in tumor microenvironment. Cancer Res. 2024;84(2):192-210.

35. El-Serag H, et al. Serum biomarker signature is predictive of the risk of hepatocellular cancer in patients with cirrhosis. Gut. 2024. https:// doi.org/10.1136/gutjnl-2024-332034.

36. Huang X, et al. Identification of HSP90B1 in pan-cancer hallmarks to aid development of a potential therapeutic target. Mol Cancer. 2024;23(1):19.

37. Wu P, et al. Pan-cancer characterization of cell-free immune-related miRNA identified as a robust biomarker for cancer diagnosis. Mol Cancer. 2024;23(1):31.

38. Martinez-Jimenez F, et al. Pan-cancer whole-genome comparison of primary and metastatic solid tumours. Nature. 2023;618(7964):333-41.

39. Lee DD, et al. Dual role of allele-specific DNA hypermethylation within the TERT promoter in cancer. J Clin Invest. 2021. https://doi.org/ 10.1172/JCI146915.

40. Leuzzi G, et al. SMARCAL1 is a dual regulator of innate immune signaling and PD-L1 expression that promotes tumor immune evasion. Cell. 2024;187(4):861-881 e32.

41. Niu N, et al. Tumor cell-intrinsic epigenetic dysregulation shapes cancer-associated fibroblasts heterogeneity to metabolically support pancreatic cancer. Cancer Cell. 2024;42(5):869-884 e9.

42. Liu D, et al. Tumor microenvironment-responsive nanoparticles amplifying STING signaling pathway for cancer immunotherapy. Adv Mater. 2024;36(6): e2304845.

43. Westcott PMK, et al. Mismatch repair deficiency is not sufficient to elicit tumor immunogenicity. Nat Genet. 2023;55(10):1686-95.

44. Swanton C, et al. Embracing cancer complexity: hallmarks of systemic disease. Cell. 2024;187(7):1589-616.

45. Chai P, et al. Genetic alteration, RNA expression, and DNA methylation profiling of coronavirus disease 2019 (COVID-19) receptor ACE2 in malignancies: a pan-cancer analysis. J Hematol Oncol. 2020;13(1):43.

46. Matthews HK, Bertoli C, de Bruin RAM. Cell cycle control in cancer. Nat Rev Mol Cell Biol. 2022;23(1):74-88.

47. Sosinsky A, et al. Insights for precision oncology from the integration of genomic and clinical data of 13,880 tumors from the 100,000 Genomes Cancer Programme. Nat Med. 2024;30(1):279-89.

Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Discover