AbstractRecent studies have linked elevated tumor aneuploidy to anti-tumor immune suppression and adverse survival following immunotherapy. Herein, we provide supportive evidence for tumor aneuploidy as a biomarker of response to immunotherapy in patients with non-small cell lung cancer (NSCLC). We identify a dose–response relationship between aneuploidy score and patient outcomes.

摘要最近的研究将肿瘤非整倍体升高与免疫治疗后的抗肿瘤免疫抑制和不良生存联系起来。在此，我们为肿瘤非整倍体作为非小细胞肺癌（NSCLC）患者免疫治疗反应的生物标志物提供了支持性证据。我们确定了非整倍体评分与患者结局之间的剂量-反应关系。

In two independent NSCLC cohorts (n = 659 patients), we demonstrate a novel association between elevated aneuploidy and non-smoking-associated oncogenic driver mutations. Lastly, we report enrichment of TERT amplification and immune-suppressive phenotypes of highly aneuploid NSCLC. Taken together, our findings emphasize a potentially critical role for tumor aneuploidy in guiding immunotherapy treatment strategies..

在两个独立的NSCLC队列（n=659名患者）中，我们证明了非整倍体升高与非吸烟相关的致癌驱动突变之间的新关联。最后，我们报道了高度非整倍体NSCLC的TERT扩增和免疫抑制表型的富集。综上所述，我们的研究结果强调了肿瘤非整倍性在指导免疫治疗策略中的潜在关键作用。。

IntroductionAneuploidy, an unbalanced chromosome or chromosome arm number, is the most common somatic alteration in human cancer1. While our understanding of the role of aneuploidy in the initiation and propagation of cancer cells is evolving, recent studies have indicated that elevated levels of aneuploidy may provide a fitness advantage for malignant cells2, resulting in a more aggressive tumor phenotype and deleterious prognosis3,4.

引言非整倍体是一种不平衡的染色体或染色体臂数，是人类癌症中最常见的体细胞改变1。虽然我们对非整倍体在癌细胞起始和增殖中的作用的理解正在发展，但最近的研究表明，非整倍体水平升高可能为恶性细胞提供适应性优势2，导致更具侵袭性的肿瘤表型和有害的预后3,4。

In addition, the available evidence suggests that aneuploidy may promote cancer growth in part through impairing innate and adaptive anti-tumor immunity5,6,7. For instance, aneuploidy has been shown to reduce CD8+ T cell and natural killer cell function and infiltration. This has raised questions about whether aneuploidy may impact the efficacy of immunotherapy, with recent studies showing an adverse prognosis following treatment with immune checkpoint inhibitors (ICIs)8,9.

此外，现有证据表明，非整倍体可能部分通过损害先天性和适应性抗肿瘤免疫来促进癌症生长5,6,7。例如，非整倍体已被证明可以减少CD8+T细胞和自然杀伤细胞的功能和浸润。这引发了关于非整倍体是否可能影响免疫疗法疗效的问题，最近的研究显示，用免疫检查点抑制剂（ICIs）治疗后预后不良8,9。

This work has indicated that aneuploidy provides synergistic prognostic value with established predictors of ICI response, such as tumor mutational burden (TMB)8,10. Validation of these findings in large, multi-institutional datasets will be critical in assessing the reliability and generalizability of aneuploidy as a biomarker of ICI response.ICIs have been particularly central to modern therapeutic strategies for metastatic non-small cell lung cancer (NSCLC).

这项工作表明，非整倍体与ICI反应的既定预测因子（如肿瘤突变负荷（TMB））8,10具有协同的预后价值。在大型多机构数据集中验证这些发现对于评估非整倍体作为ICI反应生物标志物的可靠性和普遍性至关重要。ICI对于转移性非小细胞肺癌（NSCLC）的现代治疗策略尤其重要。

However, patients exhibit strikingly heterogeneous responses to ICIs, and NSCLC remains the leading cause of cancer related death in the United States. In particular, patients whose tumors exhibit a lower TMB or tumor programmed-cell death ligand 1 (PD-L1) expression and patients without a history of smoking (whose tumors tend to be driven by oncogenic alterations such as EGFR mutations), frequently have a poor .

然而，患者对ICI表现出明显的异质性反应，NSCLC仍然是美国癌症相关死亡的主要原因。特别是，肿瘤表现出较低TMB或肿瘤程序性细胞死亡配体1（PD-L1）表达的患者和没有吸烟史的患者（其肿瘤倾向于由致癌改变如EGFR突变驱动）通常表现不佳。

Data availability

数据可用性

All original data for the SU2C-MARK Foundation cohort15 are available from the original manuscript’s Zenodo repository: https://zenodo.org/records/7849582. All data for the MSK-IMPACT cohort10 is deposited at the following cBioPortal repository: https://www.cbioportal.org/study/summary?id=tmb_mskcc_2018 and AACR Project GENIE: https://www.synapse.org/#!Synapse:syn7222066/wiki/405659.

SU2C-MARK基金会队列15的所有原始数据均可从原始手稿的Zenodo存储库中获得：https://zenodo.org/records/7849582.MSK-IMPACT队列10的所有数据都保存在以下cBioPortal存储库中：https://www.cbioportal.org/study/summary?id=tmb_mskcc_2018和AACR项目精灵：https://www.synapse.org/#哦！突触：syn7222066/wiki/405659。

All modified and/or newly generated data are available at this manuscript’s associated Zenodo repository: https://zenodo.org/records/1167161036..

所有修改和/或新生成的数据都可以在本手稿的相关Zenodo存储库中找到：https://zenodo.org/records/1167161036..

Code availability

代码可用性

All proprietary code necessary to replicate the results and figures in this manuscript are available at this manuscript’s associated Zenodo repository: https://zenodo.org/records/1167161036.

复制本手稿中的结果和数字所需的所有专有代码都可以在本手稿的相关Zenodo存储库中找到：https://zenodo.org/records/1167161036.

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Spurr，L。＆Pitroda，S。转移性非小细胞肺癌中肿瘤非整倍体的临床和分子相关性。泽诺多https://doi.org/10.5281/zenodo.11671610（2024年）。下载参考文献致谢这项工作得到了路德维希癌症研究基金会（S.P.P.）的支持，肺活量基金会（S.P.P.）的职业发展奖，芝加哥大学综合癌症中心（UCCCC）的Ullman转化癌症免疫学奖学金（S.P.P.），UCCCC的癌症聚光灯赠款（S.P.P.），美国肺协会（S.P.P.）的肺癌发现奖，福尔克医学研究信托基金（S.P.P.）的催化剂奖和约翰D。

Arnold, MD Scientific Research Prize from the University of Chicago Pritzker School of Medicine (L.F.S.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.Author informationAuthors and AffiliationsPritzker School of Medicine, The University of Chicago, Chicago, IL, USALiam F.

芝加哥大学普利茨克医学院（L.F.S.）医学博士阿诺德（Arnold）获得科学研究奖。资助者在研究设计，数据收集和分析，决定发表或准备稿件方面没有任何作用。作者信息作者和附属机构芝加哥大学斯普里茨克医学院，伊利诺伊州芝加哥，USALiam F。

SpurrDepartment of Radiation and Cellular Oncology, The University of Chicago, Chicago, IL, USALiam F. Spurr & Sean P. PitrodaLudwig Center for Metastasis Research, The University of Chicago, 5758 S. Maryland Ave. MC 9006, Chicago, IL, 60637, USASean P. PitrodaAuthorsLiam F. SpurrView author publicationsYou can also search for this author in.

芝加哥大学放射与细胞肿瘤学系，芝加哥，伊利诺伊州，USALiam F.Spurr＆Sean P.PitrodaLudwig转移研究中心，芝加哥大学，5758 S.Maryland Ave.MC 9006，芝加哥，伊利诺伊州，60637，USASean P.PitrodaAuthorsLiam F.Spurview作者出版物您也可以在中搜索这位作者。

PubMed Google ScholarSean P. PitrodaView author publicationsYou can also search for this author in

PubMed Google ScholarSean P.PitrodaView作者出版物您也可以在

PubMed Google ScholarContributionsBoth authors contributed to the conceptualization, investigation, visualization, writing and editing of this work.Corresponding authorCorrespondence to

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Competing interests

相互竞争的利益

L.F.S. and S.P.P. have filed patents related to the use of tumor aneuploidy as a predictor of response to radiotherapy and immunotherapy. S.P.P. holds other patents outside the submitted work.

五十、 F.S.和S.P.P.已经申请了与使用肿瘤非整倍体作为放射治疗和免疫治疗反应预测因子有关的专利。S、 P.P.拥有提交作品之外的其他专利。

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Reprints and permissionsAbout this articleCite this articleSpurr, L.F., Pitroda, S.P. Clinical and molecular correlates of tumor aneuploidy in metastatic non-small cell lung cancer.

转载和许可本文引用本文Spurr，L.F.，Pitroda，S.P。转移性非小细胞肺癌中肿瘤非整倍体的临床和分子相关性。

Sci Rep 14, 19375 (2024). https://doi.org/10.1038/s41598-024-66062-5Download citationReceived: 07 April 2024Accepted: 26 June 2024Published: 21 August 2024DOI: https://doi.org/10.1038/s41598-024-66062-5Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

科学报告1419375（2024）。https://doi.org/10.1038/s41598-024-66062-5Download引文接收日期：2024年4月7日接受日期：2024年6月26日发布日期：2024年8月21日OI：https://doi.org/10.1038/s41598-024-66062-5Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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KeywordsAneuploidyImmunotherapyAnti-tumor immunityLung cancer

关键词抗肿瘤免疫肺癌的超倍体免疫治疗

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