Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation: construction of a 274-gene proliferation candidate set and <italic style="font-style: italic">in vitro</italic> validation with Silvestrol

Xu Lei; Huang Maoling; Zhong Cheng

doi:10.16016/j.2097-0927.202607110

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Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation: construction of a 274-gene proliferation candidate set and in vitro validation with Silvestrol

Basic Medicine | 更新时间：2026-10-19

- Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation: construction of a 274-gene proliferation candidate set and in vitro validation with Silvestrol
- Journal of Army Medical University Vol. 48, Issue 19, Pages: 2755-2769(2026)
- 作者机构：
  
  陆军军医大学（第三军医大学）第一附属医院耳鼻咽喉科，重庆
- 作者简介：
  
  Zhong Cheng，E-mail： agm95zc@tmmu.edu.cn
- 基金信息：
  
  the General Project of Natural Science Foundation of Chongqing(CSTB2023NSCQ-MSX0676);the Key Project of 2024 Science and Technology Research Program of Chongqing Education Commission(KJZD-K202412806);the 100 Young Academic Talent Support Program of the First Affiliated Hospital of Army Medical University(2025BQCX-4)
- DOI：10.16016/j.2097-0927.202607110
  CLC： R318.04;R394.3;R739.63
- Received：28 July 2026，
  
  Revised：2026-08-18，
  
  Accepted：01 September 2026，
  
  Published：15 October 2026
- 稿件说明：
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徐磊，黄茂凌，钟诚.鼻咽癌增殖转录程序的跨队列鉴定及eIF4A相关翻译调控的定位：274个基因增殖候选集构建与Silvestrol体外验证［J］.陆军军医大学学报，2026，48（19）：2755-2769.DOI：10.16016/j.2097-0927.202607110.

Xu L，Huang M L，Zhong C.Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation： construction of a 274-gene proliferation candidate set and in vitro validation with Silvestrol［J］.J Army Med Univ，2026，48（19）：2755-2769.DOI：10.16016/j.2097-0927.202607110.
徐磊，黄茂凌，钟诚.鼻咽癌增殖转录程序的跨队列鉴定及eIF4A相关翻译调控的定位：274个基因增殖候选集构建与Silvestrol体外验证［J］.陆军军医大学学报，2026，48（19）：2755-2769.DOI：10.16016/j.2097-0927.202607110. DOI：

Xu L，Huang M L，Zhong C.Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation： construction of a 274-gene proliferation candidate set and in vitro validation with Silvestrol［J］.J Army Med Univ，2026，48（19）：2755-2769.DOI：10.16016/j.2097-0927.202607110. DOI：

摘要

目的

鼻咽癌（nasopharyngeal carcinoma， NPC）具有显著地域聚集性、EB病毒（Epstein-Barr virus， EBV）相关性和生物学异质性，局部复发、远处转移及获得性耐药仍是制约长期获益的关键瓶颈，且单基因差异表达易受队列和检测平台影响。为此，本研究识别NPC中具有跨队列可重复性并与疾病进展相关的转录程序，构建具有独立表达支持的增殖候选集，并评估其与真核翻译起始因子4A（eukaryotic translation initiation factor 4A， eIF4A）相关翻译调控及Silvestrol体外药理反应的关系。

方法

①公共数据库生信分析：整合GSE12452、GSE53819、GSE102349、GSE68799和GSE150430公共转录组数据。在GSE12452和GSE53819中开展不预设候选通路的基因集富集分析，筛选跨队列方向一致且均满足错误发现率（false discovery rate，FDR）<0.05的通路；在GSE102349中采用加权基因共表达网络分析构建模块，并通过分期分层Cox模型探索模块与疾病进展的关系。基于跨队列差异表达和模块成员关系，构建274基因增殖候选集，并以Top50、Top100和Top150三个嵌套基因子集，在开展整合网络细胞特征库（library of integrated network-based cellular signatures，LINCS）开展连接性及作用机制分析。进一步评价翻译相关程序及eIF4A相关转录本的样本内相关性，并在GSE68799中进行外部评价。采用scTenifoldKnk模拟恶性细胞中EIF4A1功能缺失，分析其网络扰动特征。②体外细胞实验：采用CCK-8、细胞杀伤、克隆形成和划痕实验评价Silvestrol对5-8F和CNE-2Z培养细胞的体外作用。

结果

GSE12452和GSE53819队列中共同可评价的5 124条通路归一化富集分数（normalized enrichment score， NES）呈正相关（Spearman

=0.55，

2.2×10⁻¹⁶），共识别314条一致激活通路和21条一致抑制通路，分别以细胞周期、DNA复制和染色体调控增强，以及纤毛和轴丝相关过程降低为主要特征。GSE102349中共识别15个非grey模块；在68例临床资料完整的患者中，共记录14个疾病进展事件，Turquoise、Tan、Blue和Pink模块达到名义

0.05。结合Turquoise模块归属及2个外部队列中的一致上调，获得274个跨队列表达支持的增殖候选基因，主要富集于E2F、G2/M、MYC、DNA代谢和染色体分离程序。LINCS分析中，8 140个化合物在3种查询规模下的连接性排序高度相关（

=0.909~0.955）；蛋白质合成抑制剂在Top50和Top100查询中呈显著负向连接（FDR分别为0.016和0.040）。翻译程序分析显示，NPC中的改变具有环节选择性，而非整个翻译系统同步激活。GSE68799外部评价中，EIF4B与一般翻译起始、PDCD4与mRNA监控/NMD的增殖校正相关分别为

=0.510和0.505，FDR均为0.012，经典

EIF4A1

与部分程序的关联具有模型敏感性。GSE150430单细胞分析显示，

EIF4A1

在95.81%的恶性细胞中可检测；其虚拟扰动信号主要集中于RPL/RPS核糖体蛋白及线粒体编码转录本，且完整增殖候选集未富集于高扰动端（FDR=1.000）。Silvestrol

对5-8F和CNE-2Z细胞的半数抑制浓度分别为26和12 nmol/L，并降低细胞存留、克隆形成及划痕闭合。

结论

NPC存在以增殖激活为特征的跨队列可重复转录状态，eIF4A相关翻译调控被多层级分析优先定位为候选干预机制；Silvestrol在NPC细胞中表现出纳摩尔级体外抑制活性。

Abstract

Objective

Nasopharyngeal carcinoma (NPC) is characterized by marked geographic aggregation

Epstein-Barr virus (EBV) association

and biological heterogeneity; local recurrence

distant metastasis

and acquired resistance remain major obstacles to long-term benefit

while single-gene differential expression is vulnerable to cohort and platform effects. This study aims to identify transcriptional programs in NPC with cross-cohort reproducibility and relevance to disease progression

construct a proliferation candidate gene set supported by independent expression data

and evaluate its relationship with eukaryotic translation initiation factor 4A (eIF4A)-associated translational regulation and the

in vitro

pharmacological effects of Silvestrol.

Methods

① Bioinformatic analyses of public datasets: Public transcriptomic datasets (GSE12452

GSE53819

GSE102349

GSE68799

and GSE150430) were integrated. Unbiased gene set enrichment analysis was performed in GSE12452 and GSE53819 to identify pathways showing concordant enrichment directions and a false discovery rate (FDR)

0.05 in both cohorts. Weighted gene co-expression network analysis was conducted in GSE102349

and stage-stratified Cox models were applied to explore the associations between module eigengenes and disease progression. A 274-gene proliferation candidate set was constructed by integrating cross-cohort differential expression with module membership

and Top50

Top100

and Top150 nested gene sets were then used for Library of Integrated Network-based Cellular Signatures (LINCS) connectivity and mechanism-of-action analyses. Within-sample associations between translation-related programs and eIF4A-related transcripts were further eval

uated and externally assessed in GSE68799. EIF4A1 functional loss was simulated in malignant cells using scTenifoldKnk to characterize network perturbation patterns. ②

In vitro

experiments: CCK-8

cell-killing

colony formation

and wound-healing assays were used to determine the effects of Silvestrol on cultured 5-8F and CNE-2Z cells.

Results

The normalized enrichment score (NES) of 5 124 commonly evaluable pathways exhibited a positive Spearman-rank correlation between the GSE12452 and GSE53819 cohorts (Spearman ρ

2.2×10

-16

). A total of 314 concordantly activated and 21 concordantly suppressed pathways were identified

characterized mainly by enhanced cell cycle

DNA replication

and chromosome regulation programs and reduced cilium- and axoneme-related processes

respectively. Fifteen non-grey modules were identified in GSE102349. Among 68 patients with complete clinical data

14 disease progression events were recorded

and the Turquoise

Tan

Blue

and Pink modules reached nominal

0.05. Integration of Turquoise-module membership with concordant upregulation in the 2 external cohorts yielded 274 proliferation candidate genes with cross-cohort expression support

which were enriched mainly in E2F

G2/M

MYC

DNA metabolism

and chromosome segregation programs. In the LINCS analysis

connectivity rankings for 8 140 compounds were highly correlated (

=0.909 to 0.955). Protein-synthesis inhibitors showed significant negative connectivity in the Top50 and Top100 analyses

with FDR values of 0.016 and 0.040

respectively. Translation program analysis indicated process-selective alterations in NPC rather than coordinated activation of the entire translation system. In the external GSE68799 cohort

the proliferation-adjusted correlations of EIF4B with general translation initiation and of PDCD4 with mRNA surveillance/NMD were

=0.510 and 0.505

respectively

with FDR=0.012 for both

; associations between canonical

EIF4A1

and selected programs were model-sensitive. Single-cell analysis of GSE150430 showed that

EIF4A1

was detectable in 95.81% of malignant cells. Virtual perturbation signals were concentrated mainly in RPL/RPS ribosomal-protein genes and mitochondrially encoded transcripts

whereas the complete proliferation candidate set was not enriched at the high-perturbation end of the ranking (FDR=1.000). The half-maximal inhibitory concentrations of Silvestrol were 26 and 12 nmol/L in 5-8F and CNE-2Z cells

respectively

and Silvestrol reduced cell retention

colony formation

and wound closure.

Conclusion

NPC exhibits a cross-cohort reproducible transcriptional state characterized by enhanced proliferative programs

with eIF4A-associated translational regulation prioritized by multi-level analyses as a candidate intervention mechanism; Silvestrol exhibits nanomolar in vitro inhibitory activity in NPC cells.

关键词

Keywords

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Related Author

LI Jiarui

QIAN Li

SHEN Junjie

GUO Honglin

QIN Maoyang

WU Yazhou

Mingjing JIN

Yanping LI

Related Institution

Department of Military Health Statistics， Faculty of Military Preventive Medicine， Army Medical University （Third Military Medical University）

Department of Scientific Research Affairs, Nanning First People's Hospital, Nanning, Guangxi Zhuang Autonomous Region

Medical Experimental Center, Nanning First People's Hospital, Nanning, Guangxi Zhuang Autonomous Region

Laboratory of Zhuang & Yao Medicine, Guangxi International Zhuang Medicine Hospital Affiliated to Guangxi University of Chinese Medicine, Nanning, Guangxi Zhuang Autonomous Region

Department of Pediatric Surgical Oncology, Children's Hospital, Chongqing Medical University

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Cross-cohort identification of proliferative transcriptional programs in nasopharyngeal carcinoma and mapping of eIF4A-related translational regulation: construction of a 274-gene proliferation candidate set and in vitro validation with Silvestrol

DOI：10.16016/j.2097-0927.202607110

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