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Multi-region exome sequencing reveals genomic evolution from preneoplasia to lung adenocarcinoma

Author

Listed:
  • Xin Hu

    (The University of Texas MD Anderson Cancer Center)

  • Junya Fujimoto

    (The University of Texas MD Anderson Cancer Center)

  • Lisha Ying

    (Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital & Key Laboratory Diagnosis and Treatment Technology on Thoracic Oncology of Zhejiang Province)

  • Junya Fukuoka

    (Nagasaki University Graduate School of Biomedical Sciences)

  • Kazuto Ashizawa

    (Nagasaki University Graduate School of Biomedical Sciences)

  • Wenyong Sun

    (Institute of Cancer Research and Basic Medical Sciences of Chinese Academy of Sciences, Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital)

  • Alexandre Reuben

    (The University of Texas MD Anderson Cancer Center)

  • Chi-Wan Chow

    (The University of Texas MD Anderson Cancer Center)

  • Nicholas McGranahan

    (Cancer Research United Kingdom-University College London Lung Cancer Centre of Excellence)

  • Runzhe Chen

    (The University of Texas MD Anderson Cancer Center)

  • Jinlin Hu

    (Institute of Cancer Research and Basic Medical Sciences of Chinese Academy of Sciences, Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital)

  • Myrna C. Godoy

    (The University of Texas MD Anderson Cancer Center)

  • Kazuhiro Tabata

    (Nagasaki University Graduate School of Biomedical Sciences)

  • Kishio Kuroda

    (Nagasaki University Graduate School of Biomedical Sciences)

  • Lei Shi

    (Institute of Cancer Research and Basic Medical Sciences of Chinese Academy of Sciences, Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital)

  • Jun Li

    (The University of Texas MD Anderson Cancer Center)

  • Carmen Behrens

    (The University of Texas MD Anderson Cancer Center)

  • Edwin Roger Parra

    (The University of Texas MD Anderson Cancer Center)

  • Latasha D. Little

    (The University of Texas MD Anderson Cancer Center)

  • Curtis Gumbs

    (The University of Texas MD Anderson Cancer Center)

  • Xizeng Mao

    (The University of Texas MD Anderson Cancer Center)

  • Xingzhi Song

    (The University of Texas MD Anderson Cancer Center)

  • Samantha Tippen

    (The University of Texas MD Anderson Cancer Center)

  • Rebecca L. Thornton

    (The University of Texas MD Anderson Cancer Center)

  • Humam Kadara

    (The University of Texas MD Anderson Cancer Center)

  • Paul Scheet

    (The University of Texas MD Anderson Cancer Center
    The University of Texas MD Anderson Cancer Center
    The University of Texas MD Anderson Cancer Center)

  • Emily Roarty

    (The University of Texas MD Anderson Cancer Center)

  • Edwin Justin Ostrin

    (The University of Texas MD Anderson Cancer Center)

  • Xu Wang

    (Institute of Cancer Research and Basic Medical Sciences of Chinese Academy of Sciences, Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital)

  • Brett W. Carter

    (The University of Texas MD Anderson Cancer Center)

  • Mara B. Antonoff

    (The University of Texas MD Anderson Cancer Center)

  • Jianhua Zhang

    (The University of Texas MD Anderson Cancer Center)

  • Ara A. Vaporciyan

    (The University of Texas MD Anderson Cancer Center)

  • Harvey Pass

    (New York University Langone Medical Center)

  • Stephen G. Swisher

    (The University of Texas MD Anderson Cancer Center)

  • John V. Heymach

    (The University of Texas MD Anderson Cancer Center)

  • J. Jack Lee

    (The University of Texas MD Anderson Cancer Center)

  • Ignacio I. Wistuba

    (The University of Texas MD Anderson Cancer Center
    The University of Texas MD Anderson Cancer Center)

  • Waun Ki Hong

    (The University of Texas MD Anderson Cancer Center)

  • P. Andrew Futreal

    (The University of Texas MD Anderson Cancer Center)

  • Dan Su

    (Institute of Cancer Research and Basic Medical Sciences of Chinese Academy of Sciences, Cancer Hospital of University of Chinese Academy of Sciences, Zhejiang Cancer Hospital)

  • Jianjun Zhang

    (The University of Texas MD Anderson Cancer Center
    The University of Texas MD Anderson Cancer Center)

Abstract

There has been a dramatic increase in the detection of lung nodules, many of which are preneoplasia atypical adenomatous hyperplasia (AAH), adenocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA) or invasive adenocarcinoma (ADC). The molecular landscape and the evolutionary trajectory of lung preneoplasia have not been well defined. Here, we perform multi-region exome sequencing of 116 resected lung nodules including AAH (n = 22), AIS (n = 27), MIA (n = 54) and synchronous ADC (n = 13). Comparing AAH to AIS, MIA and ADC, we observe progressive genomic evolution at the single nucleotide level and demarcated evolution at the chromosomal level supporting the early lung carcinogenesis model from AAH to AIS, MIA and ADC. Subclonal analyses reveal a higher proportion of clonal mutations in AIS/MIA/ADC than AAH suggesting neoplastic transformation of lung preneoplasia is predominantly associated with a selective sweep of unfit subclones. Analysis of multifocal pulmonary nodules from the same patients reveal evidence of convergent evolution.

Suggested Citation

  • Xin Hu & Junya Fujimoto & Lisha Ying & Junya Fukuoka & Kazuto Ashizawa & Wenyong Sun & Alexandre Reuben & Chi-Wan Chow & Nicholas McGranahan & Runzhe Chen & Jinlin Hu & Myrna C. Godoy & Kazuhiro Tabat, 2019. "Multi-region exome sequencing reveals genomic evolution from preneoplasia to lung adenocarcinoma," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10877-8
    DOI: 10.1038/s41467-019-10877-8
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    Citations

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    Cited by:

    1. Wenying Peng & Bin Li & Jin Li & Lianpeng Chang & Jing Bai & Yuting Yi & Rongrong Chen & Yanyan Zhang & Chen Chen & Xingxiang Pu & Meilin Jiang & Jia Li & Rui Zhong & Fang Xu & Bolin Chen & Li Xu & Ni, 2022. "Clinical and genomic features of Chinese lung cancer patients with germline mutations," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Yasuhiko Haga & Yoshitaka Sakamoto & Keiko Kajiya & Hitomi Kawai & Miho Oka & Noriko Motoi & Masayuki Shirasawa & Masaya Yotsukura & Shun-Ichi Watanabe & Miyuki Arai & Junko Zenkoh & Kouya Shiraishi &, 2023. "Whole-genome sequencing reveals the molecular implications of the stepwise progression of lung adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Ming Tang & Hussein A. Abbas & Marcelo V. Negrao & Maheshwari Ramineni & Xin Hu & Shawna Marie Hubert & Junya Fujimoto & Alexandre Reuben & Susan Varghese & Jianhua Zhang & Jun Li & Chi-Wan Chow & Xiz, 2021. "The histologic phenotype of lung cancers is associated with transcriptomic features rather than genomic characteristics," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    4. Ming Chen & Runzhe Chen & Ying Jin & Jun Li & Xin Hu & Jiexin Zhang & Junya Fujimoto & Shawna M. Hubert & Carl M. Gay & Bo Zhu & Yanhua Tian & Nicholas McGranahan & Won-Chul Lee & Julie George & Xiao , 2021. "Cold and heterogeneous T cell repertoire is associated with copy number aberrations and loss of immune genes in small-cell lung cancer," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    5. Zhoufeng Wang & Zhe Li & Kun Zhou & Chengdi Wang & Lili Jiang & Li Zhang & Ying Yang & Wenxin Luo & Wenliang Qiao & Gang Wang & Yinyun Ni & Shuiping Dai & Tingting Guo & Guiyi Ji & Minjie Xu & Yiying , 2021. "Deciphering cell lineage specification of human lung adenocarcinoma with single-cell RNA sequencing," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Meng Nie & Ke Yao & Xinsheng Zhu & Na Chen & Nan Xiao & Yi Wang & Bo Peng & LiAng Yao & Peng Li & Peng Zhang & Zeping Hu, 2021. "Evolutionary metabolic landscape from preneoplasia to invasive lung adenocarcinoma," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

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