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Genomic and TCR profiling data reveal the distinct molecular traits in epithelial ovarian cancer histotypes

Oncogene volume 41, pages 3093–3103 (2022)Cite this article

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Abstract

Epithelial ovarian cancer (EOC) is classified into five major histotypes: high-grade serous (HGSOC), low-grade serous (LGSOC), clear cell (CCOC), endometrioid (ENOC), and mucinous (MOC). However, the landscape of molecular and immunological alterations in these histotypes, especially LGSOC, CCOC, ENOC, and MOC, is largely uncharacterized. We collected 101 treatment-naive EOC patients. The resected tumor tissues and paired preoperative peripheral blood samples were collected and subjected to target sequencing of 1021 cancer-associated genes and T cell repertoire sequencing. Distinct characteristics of mutations were identified among the five histotypes. Furthermore, tumor mutation burden (TMB) was found to be higher in CCOC and ENOC, but lower in LGSOC and HGSOC. Alterations associated with DNA damage repair (DDR) pathways and homologous recombination deficiencies (HRD) were prevalent in five histotypes. CCOC demonstrated increased level of T cell clonality compared with HSGOC. Interestingly, the proportion of the 100 most common T cell clones was associated with TMB and tumor neoantigen burden in CCOC, highlighting more sensitive anti-tumor responses in this histotype, which was also evidenced by the enhanced convergent recombination of T cell clones. These findings shed light on the molecular traits of genomic alteration and T cell repertoire in the five major EOC histotypes and may help optimize clinical management of EOC with different histotypes.

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Fig. 1: The mutation landscape in EOC histotypes.
Fig. 2: Mutational signatures in EOC histotypes.
Fig. 3: The prevalence of alterations in DDR pathways in EOC histotypes.
Fig. 4: The comparisons of TCR metrics between HGSOC and CCOC in tumors.
Fig. 5: The interplay between T cell expanding and somatic mutations.
Fig. 6: The associations between ctDNA detection and clinicopathological features.

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Funding

This work was supported by grants from the National Natural Science Foundation of China (Nos. 81772783 and 81971475) and the Chinese Academy of Medical Sciences Initiative for Innovative Medicine (Nos. CAMS-2017-I2M-1–002).

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Author notes

  1. These authors contributed equally: Shan Zhu, Chunliu Zhang.

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, National Clinical Research Centre for Obstetric and Gynecologic Diseases, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

    Shan Zhu, Dongyan Cao, Tong Ren, Jiaxin Yang, Mei Yu & Yang Xiang

  2. Geneplus institute, Beijing, China

    Chunliu Zhang, Jing Bai, Yuhua Gong, Yanfang Guan, Xuefeng Xia & Ling Yang

  3. Department of Pathology, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing, China

    Shuangni Yu & Jie Chen

  4. Department of Gynecology Oncology, Hunan Cancer Hospital and the Affiliated Cancer Hospital of Xiangya School of Medicine, Central South University, Changsha, China

    Jing Wang

  5. Geneplus-Shenzhen, Shenzhen, China

    Xiao Xiao

  6. Department of Obstetrics and Gynecolgoy, The Second Affiliated Hospital of Harbin Medical University, Harbin, China

    Peiling Li

  7. Department of Gynecological Oncology, First Hospital of Jilin University, Changchun, China

    Ying Yue

  8. Department of Obstetrics and Gynecology, West China Second Hospital of Sichuan University, Chengdu, China

    Rutie Yin

  9. Department of Obstetrics and Gynecology, Peking University International Hospital, Beijing, China

    Yongjun Wang

  10. Department of Obstetrics and Gynecology, The First Affiliated Hospital of Xi’an Jiaotong University, Shaanxi, China

    Ruifang An

  11. Department of Gynecology Oncology, Harbin Medical University Cancer Hospital, Harbin, China

    Ge Lou

  12. Department of Gynecology, Affiliated Tumor Hospital of Xinjiang Medical University, Urumqi, China

    Jianlin Yuan

  13. Department of Gynecologic Oncology, Sichuan Cancer Hospital, Chengdu, China

    Guonan Zhang

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  1. Shan Zhu
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Contributions

YX, LY, XX conceived and designed the study. DC, JW, TR, JY, MY, YY, PL, RY, YW, RA, GL, JY collected samples as well as clinical information. SZ, CZ performed the experiments. SZ, CZ, JB, XX, YG, Yanf-G analyzed the data. SZ, CZ, XX, YX, LY wrote the paper. SZ, CZ, XX, Yanf-G, Xuef-X, YX provided intellectual discussions and ideas regarding the content of paper. YX, LY supervised the study. All authors read and approved the final paper.

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Correspondence to Ling Yang or Yang Xiang.

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The authors declare no competing interests.

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This study was reviewed and approved by the institutional ethics committee of Peking Union Medical College Hospital (No. HS-1437). The participants provided their written informed consent in this study.

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Zhu, S., Zhang, C., Cao, D. et al. Genomic and TCR profiling data reveal the distinct molecular traits in epithelial ovarian cancer histotypes. Oncogene 41, 3093–3103 (2022). https://doi.org/10.1038/s41388-022-02277-y

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