IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29767-7.html
   My bibliography  Save this article

Somatic whole genome dynamics of precancer in Barrett’s esophagus reveals features associated with disease progression

Author

Listed:
  • Thomas G. Paulson

    (Fred Hutchinson Cancer Research Center)

  • Patricia C. Galipeau

    (Fred Hutchinson Cancer Research Center)

  • Kenji M. Oman

    (Fred Hutchinson Cancer Research Center)

  • Carissa A. Sanchez

    (Fred Hutchinson Cancer Research Center)

  • Mary K. Kuhner

    (University of Washington
    Brotman Baty Institute for Precision Medicine)

  • Lucian P. Smith

    (University of Washington)

  • Kevin Hadi

    (New York Genome Center (NYGC))

  • Minita Shah

    (New York Genome Center (NYGC))

  • Kanika Arora

    (New York Genome Center (NYGC))

  • Jennifer Shelton

    (New York Genome Center (NYGC))

  • Molly Johnson

    (New York Genome Center (NYGC))

  • Andre Corvelo

    (New York Genome Center (NYGC))

  • Carlo C. Maley

    (Arizona State University)

  • Xiaotong Yao

    (New York Genome Center (NYGC))

  • Rashesh Sanghvi

    (New York Genome Center (NYGC))

  • Elisa Venturini

    (New York Genome Center (NYGC))

  • Anne-Katrin Emde

    (Variant Bio)

  • Benjamin Hubert

    (New York Genome Center (NYGC))

  • Marcin Imielinski

    (New York Genome Center (NYGC)
    Weill Cornell Medical College)

  • Nicolas Robine

    (New York Genome Center (NYGC))

  • Brian J. Reid

    (Fred Hutchinson Cancer Research Center
    University of Washington
    Brotman Baty Institute for Precision Medicine
    University of Washington)

  • Xiaohong Li

    (Fred Hutchinson Cancer Research Center)

Abstract

While the genomes of normal tissues undergo dynamic changes over time, little is understood about the temporal-spatial dynamics of genomes in premalignant tissues that progress to cancer compared to those that remain cancer-free. Here we use whole genome sequencing to contrast genomic alterations in 427 longitudinal samples from 40 patients with stable Barrett’s esophagus compared to 40 Barrett’s patients who progressed to esophageal adenocarcinoma (ESAD). We show the same somatic mutational processes are active in Barrett’s tissue regardless of outcome, with high levels of mutation, ESAD gene and focal chromosomal alterations, and similar mutational signatures. The critical distinction between stable Barrett’s versus those who progress to cancer is acquisition and expansion of TP53−/− cell populations having complex structural variants and high-level amplifications, which are detectable up to six years prior to a cancer diagnosis. These findings reveal the timing of common somatic genome dynamics in stable Barrett’s esophagus and define key genomic features specific to progression to esophageal adenocarcinoma, both of which are critical for cancer prevention and early detection strategies.

Suggested Citation

  • Thomas G. Paulson & Patricia C. Galipeau & Kenji M. Oman & Carissa A. Sanchez & Mary K. Kuhner & Lucian P. Smith & Kevin Hadi & Minita Shah & Kanika Arora & Jennifer Shelton & Molly Johnson & Andre Co, 2022. "Somatic whole genome dynamics of precancer in Barrett’s esophagus reveals features associated with disease progression," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29767-7
    DOI: 10.1038/s41467-022-29767-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29767-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29767-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. P. Diggle & M. G. Kenward, 1994. "Informative Drop‐Out in Longitudinal Data Analysis," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 43(1), pages 49-73, March.
    2. Serena Nik-Zainal & Helen Davies & Johan Staaf & Manasa Ramakrishna & Dominik Glodzik & Xueqing Zou & Inigo Martincorena & Ludmil B. Alexandrov & Sancha Martin & David C. Wedge & Peter Van Loo & Young, 2016. "Landscape of somatic mutations in 560 breast cancer whole-genome sequences," Nature, Nature, vol. 534(7605), pages 47-54, June.
    3. Ludmil B. Alexandrov & Serena Nik-Zainal & David C. Wedge & Samuel A. J. R. Aparicio & Sam Behjati & Andrew V. Biankin & Graham R. Bignell & Niccolò Bolli & Ake Borg & Anne-Lise Børresen-Dale & Sandri, 2013. "Correction: Corrigendum: Signatures of mutational processes in human cancer," Nature, Nature, vol. 502(7470), pages 258-258, October.
    4. Akira Yokoyama & Nobuyuki Kakiuchi & Tetsuichi Yoshizato & Yasuhito Nannya & Hiromichi Suzuki & Yasuhide Takeuchi & Yusuke Shiozawa & Yusuke Sato & Kosuke Aoki & Soo Ki Kim & Yoichi Fujii & Kenichi Yo, 2019. "Age-related remodelling of oesophageal epithelia by mutated cancer drivers," Nature, Nature, vol. 565(7739), pages 312-317, January.
    5. Pierre Martinez & Diego Mallo & Thomas G. Paulson & Xiaohong Li & Carissa A. Sanchez & Brian J. Reid & Trevor A. Graham & Mary K. Kuhner & Carlo C. Maley, 2018. "Evolution of Barrett’s esophagus through space and time at single-crypt and whole-biopsy levels," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    6. Ludmil B. Alexandrov & Jaegil Kim & Nicholas J. Haradhvala & Mi Ni Huang & Alvin Wei Tian Ng & Yang Wu & Arnoud Boot & Kyle R. Covington & Dmitry A. Gordenin & Erik N. Bergstrom & S. M. Ashiqul Islam , 2020. "The repertoire of mutational signatures in human cancer," Nature, Nature, vol. 578(7793), pages 94-101, February.
    7. Katia Nones & Nicola Waddell & Nicci Wayte & Ann-Marie Patch & Peter Bailey & Felicity Newell & Oliver Holmes & J. Lynn Fink & Michael C. J. Quinn & Yue Hang Tang & Guy Lampe & Kelly Quek & Kelly A. L, 2014. "Genomic catastrophes frequently arise in esophageal adenocarcinoma and drive tumorigenesis," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    8. Henry Lee-Six & Sigurgeir Olafsson & Peter Ellis & Robert J. Osborne & Mathijs A. Sanders & Luiza Moore & Nikitas Georgakopoulos & Franco Torrente & Ayesha Noorani & Martin Goddard & Philip Robinson &, 2019. "The landscape of somatic mutation in normal colorectal epithelial cells," Nature, Nature, vol. 574(7779), pages 532-537, October.
    9. Yilong Li & Nicola D. Roberts & Jeremiah A. Wala & Ofer Shapira & Steven E. Schumacher & Kiran Kumar & Ekta Khurana & Sebastian Waszak & Jan O. Korbel & James E. Haber & Marcin Imielinski & Joachim We, 2020. "Patterns of somatic structural variation in human cancer genomes," Nature, Nature, vol. 578(7793), pages 112-121, February.
    10. Ludmil B. Alexandrov & Serena Nik-Zainal & David C. Wedge & Samuel A. J. R. Aparicio & Sam Behjati & Andrew V. Biankin & Graham R. Bignell & Niccolò Bolli & Ake Borg & Anne-Lise Børresen-Dale & Sandri, 2013. "Signatures of mutational processes in human cancer," Nature, Nature, vol. 500(7463), pages 415-421, August.
    11. Malgorzata Krajewska & Ruben Dries & Andrew V. Grassetti & Sofia Dust & Yang Gao & Hao Huang & Bandana Sharma & Daniel S. Day & Nicholas Kwiatkowski & Monica Pomaville & Oliver Dodd & Edmond Chipumuro, 2019. "CDK12 loss in cancer cells affects DNA damage response genes through premature cleavage and polyadenylation," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    12. Thanos P. Mourikis & Lorena Benedetti & Elizabeth Foxall & Damjan Temelkovski & Joel Nulsen & Juliane Perner & Matteo Cereda & Jesper Lagergren & Michael Howell & Christopher Yau & Rebecca C. Fitzgera, 2019. "Patient-specific cancer genes contribute to recurrently perturbed pathways and establish therapeutic vulnerabilities in esophageal adenocarcinoma," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Michelle Dietzen & Haoran Zhai & Olivia Lucas & Oriol Pich & Christopher Barrington & Wei-Ting Lu & Sophia Ward & Yanping Guo & Robert E. Hynds & Simone Zaccaria & Charles Swanton & Nicholas McGranaha, 2024. "Replication timing alterations are associated with mutation acquisition during breast and lung cancer evolution," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Mischan Vali-Pour & Solip Park & Jose Espinosa-Carrasco & Daniel Ortiz-Martínez & Ben Lehner & Fran Supek, 2022. "The impact of rare germline variants on human somatic mutation processes," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    3. Marjan M. Naeini & Felicity Newell & Lauren G. Aoude & Vanessa F. Bonazzi & Kalpana Patel & Guy Lampe & Lambros T. Koufariotis & Vanessa Lakis & Venkateswar Addala & Olga Kondrashova & Rebecca L. John, 2023. "Multi-omic features of oesophageal adenocarcinoma in patients treated with preoperative neoadjuvant therapy," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Ambrocio Sanchez & Pedro Ortega & Ramin Sakhtemani & Lavanya Manjunath & Sunwoo Oh & Elodie Bournique & Alexandrea Becker & Kyumin Kim & Cameron Durfee & Nuri Alpay Temiz & Xiaojiang S. Chen & Reuben , 2024. "Mesoscale DNA features impact APOBEC3A and APOBEC3B deaminase activity and shape tumor mutational landscapes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Sujath Abbas & Oriol Pich & Ginny Devonshire & Shahriar A. Zamani & Annalise Katz-Summercorn & Sarah Killcoyne & Calvin Cheah & Barbara Nutzinger & Nicola Grehan & Nuria Lopez-Bigas & Rebecca C. Fitzg, 2023. "Mutational signature dynamics shaping the evolution of oesophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Bernard C. H. Lee & Philip S. Robinson & Tim H. H. Coorens & Helen H. N. Yan & Sigurgeir Olafsson & Henry Lee-Six & Mathijs A. Sanders & Hoi Cheong Siu & James Hewinson & Sarah S. K. Yue & Wai Yin Tsu, 2022. "Mutational landscape of normal epithelial cells in Lynch Syndrome patients," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    7. Amanda Fitzpatrick & Marjan Iravani & Adam Mills & David Vicente & Thanussuyah Alaguthurai & Ioannis Roxanis & Nicholas C. Turner & Syed Haider & Andrew N. J. Tutt & Clare M. Isacke, 2023. "Genomic profiling and pre-clinical modelling of breast cancer leptomeningeal metastasis reveals acquisition of a lobular-like phenotype," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Sebastian Carrasco Pro & Heather Hook & David Bray & Daniel Berenzy & Devlin Moyer & Meimei Yin & Adam Thomas Labadorf & Ryan Tewhey & Trevor Siggers & Juan Ignacio Fuxman Bass, 2023. "Widespread perturbation of ETS factor binding sites in cancer," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Heather E. Machado & Nina F. Øbro & Nicholas Williams & Shengjiang Tan & Ahmed Z. Boukerrou & Megan Davies & Miriam Belmonte & Emily Mitchell & E. Joanna Baxter & Nicole Mende & Anna Clay & Philip Anc, 2023. "Convergent somatic evolution commences in utero in a germline ribosomopathy," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. A. C. Katz-Summercorn & S. Jammula & A. Frangou & I. Peneva & M. O’Donovan & M. Tripathi & S. Malhotra & M. Pietro & S. Abbas & G. Devonshire & W. Januszewicz & A. Blasko & K. Nowicki-Osuch & S. MacRa, 2022. "Multi-omic cross-sectional cohort study of pre-malignant Barrett’s esophagus reveals early structural variation and retrotransposon activity," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Luan Nguyen & Arne Hoeck & Edwin Cuppen, 2022. "Machine learning-based tissue of origin classification for cancer of unknown primary diagnostics using genome-wide mutation features," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Caralyn Reisle & Laura M. Williamson & Erin Pleasance & Anna Davies & Brayden Pellegrini & Dustin W. Bleile & Karen L. Mungall & Eric Chuah & Martin R. Jones & Yussanne Ma & Eleanor Lewis & Isaac Beck, 2022. "A platform for oncogenomic reporting and interpretation," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Antonio Rodriguez-Calero & John Gallon & Dilara Akhoundova & Sina Maletti & Alison Ferguson & Joanna Cyrta & Ursula Amstutz & Andrea Garofoli & Viola Paradiso & Scott A. Tomlins & Ekkehard Hewer & Ver, 2022. "Alterations in homologous recombination repair genes in prostate cancer brain metastases," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    15. Se Jin Park & Gwan Woo Ku & Su Yel Lee & Daeun Kang & Wan Jin Hwang & In Beom Jeong & Sun Jung Kwon & Jaeku Kang & Ji Woong Son, 2021. "Analysis of Single Nucleotide Variants (SNVs) Induced by Exposure to PM 10 in Lung Epithelial Cells Using Whole Genome Sequencing," IJERPH, MDPI, vol. 18(3), pages 1-11, January.
    16. Mei Lin & Xiao-Long Zhang & Rui You & You-Ping Liu & Hong-Min Cai & Li-Zhi Liu & Xue-Fei Liu & Xiong Zou & Yu-Long Xie & Ru-Hai Zou & Yi-Nuan Zhang & Rui Sun & Wei-Yi Feng & Hai-Yan Wang & Gui-Hua Tao, 2023. "Evolutionary route of nasopharyngeal carcinoma metastasis and its clinical significance," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    17. Josefine Radke & Naveed Ishaque & Randi Koll & Zuguang Gu & Elisa Schumann & Lina Sieverling & Sebastian Uhrig & Daniel Hübschmann & Umut H. Toprak & Cristina López & Xavier Pastor Hostench & Simone B, 2022. "The genomic and transcriptional landscape of primary central nervous system lymphoma," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    18. Yasha Butt & Ramin Sakhtemani & Rukshana Mohamad-Ramshan & Michael S. Lawrence & Ashok S. Bhagwat, 2024. "Distinguishing preferences of human APOBEC3A and APOBEC3B for cytosines in hairpin loops, and reflection of these preferences in APOBEC-signature cancer genome mutations," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Peter Georgeson & Tabitha A. Harrison & Bernard J. Pope & Syed H. Zaidi & Conghui Qu & Robert S. Steinfelder & Yi Lin & Jihoon E. Joo & Khalid Mahmood & Mark Clendenning & Romy Walker & Efrat L. Amita, 2022. "Identifying colorectal cancer caused by biallelic MUTYH pathogenic variants using tumor mutational signatures," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    20. Chunyang Bao & Richard W. Tourdot & Gregory J. Brunette & Chip Stewart & Lili Sun & Hideo Baba & Masayuki Watanabe & Agoston T. Agoston & Kunal Jajoo & Jon M. Davison & Katie S. Nason & Gad Getz & Ken, 2023. "Genomic signatures of past and present chromosomal instability in Barrett’s esophagus and early esophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29767-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.