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Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes

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  • Andrew V. Biankin

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    Bankstown Hospital, Eldridge Road, Bankstown, Sydney, New South Wales 2200, Australia.
    South Western Sydney Clinical School, Faculty of Medicine, University of NewSouth Wales)

  • Nicola Waddell

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Karin S. Kassahn

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Marie-Claude Gingras

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.
    Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030-3411, USA.)

  • Lakshmi B. Muthuswamy

    (Ontario Institute for Cancer Research)

  • Amber L. Johns

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • David K. Miller

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Peter J. Wilson

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Ann-Marie Patch

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Jianmin Wu

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • David K. Chang

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    Bankstown Hospital, Eldridge Road, Bankstown, Sydney, New South Wales 2200, Australia.
    South Western Sydney Clinical School, Faculty of Medicine, University of NewSouth Wales)

  • Mark J. Cowley

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Brooke B. Gardiner

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Sarah Song

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Ivon Harliwong

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Senel Idrisoglu

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Craig Nourse

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Ehsan Nourbakhsh

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Suzanne Manning

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Shivangi Wani

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Milena Gongora

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Marina Pajic

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Christopher J. Scarlett

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    School of Environmental & Life Sciences, University of Newcastle)

  • Anthony J. Gill

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    Royal North Shore Hospital, St Leonards
    University of Sydney)

  • Andreia V. Pinho

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Ilse Rooman

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Matthew Anderson

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Oliver Holmes

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Conrad Leonard

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Darrin Taylor

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Scott Wood

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Qinying Xu

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Katia Nones

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • J. Lynn Fink

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Angelika Christ

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Tim Bruxner

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Nicole Cloonan

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Gabriel Kolle

    (Life Technologies)

  • Felicity Newell

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • Mark Pinese

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • R. Scott Mead

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    Sydpath, St Vincent’s Hospital)

  • Jeremy L. Humphris

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Warren Kaplan

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Marc D. Jones

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Emily K. Colvin

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Adnan M. Nagrial

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Emily S. Humphrey

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Angela Chou

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    Sydpath, St Vincent’s Hospital)

  • Venessa T. Chin

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Lorraine A. Chantrill

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Amanda Mawson

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Jaswinder S. Samra

    (Royal North Shore Hospital, St Leonards
    Royal North Shore Hospital, St Leonards)

  • James G. Kench

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    University of Sydney
    Tissue Pathology and Diagnostic Oncology, Royal Prince Alfred Hospital)

  • Jessica A. Lovell

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Roger J. Daly

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Neil D. Merrett

    (Bankstown Hospital, Eldridge Road, Bankstown, Sydney, New South Wales 2200, Australia.
    School of Medicine, University of Western Sydney)

  • Christopher Toon

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.)

  • Krishna Epari

    (Fremantle Hospital, Alma Street, Fremantle, Western Australia 6160, Australia.)

  • Nam Q. Nguyen

    (Royal Adelaide Hospital, North Terrace, Adelaide, South Australia 5000, Australia.)

  • Andrew Barbour

    (The University of Queensland, Princess Alexandra Hospital, Ipswich Road, Woollongabba, Queensland 4102, Australia.)

  • Nikolajs Zeps

    (School of Surgery M507, University of Western Australia, 35 Stirling Hwy, Nedlands 6009, Australia and St John of God Pathology, 12 Salvado Road, Subiaco, Western Australia 6008, USA.)

  • Nipun Kakkar

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Fengmei Zhao

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Yuan Qing Wu

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Min Wang

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Donna M. Muzny

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • William E. Fisher

    (Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030-3411, USA.
    The Elkins Pancreas Center atBaylor College ofMedicine, 6620 Main Street, Suite 1450, Houston, Texas 77030, USA.)

  • F. Charles Brunicardi

    (David Geffen School of Medicine at UCLA)

  • Sally E. Hodges

    (Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030-3411, USA.
    The Elkins Pancreas Center atBaylor College ofMedicine, 6620 Main Street, Suite 1450, Houston, Texas 77030, USA.)

  • Jeffrey G. Reid

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Jennifer Drummond

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Kyle Chang

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Yi Han

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Lora R. Lewis

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Huyen Dinh

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Christian J. Buhay

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Timothy Beck

    (Ontario Institute for Cancer Research)

  • Lee Timms

    (Ontario Institute for Cancer Research)

  • Michelle Sam

    (Ontario Institute for Cancer Research)

  • Kimberly Begley

    (Ontario Institute for Cancer Research)

  • Andrew Brown

    (Ontario Institute for Cancer Research)

  • Deepa Pai

    (Ontario Institute for Cancer Research)

  • Ami Panchal

    (Ontario Institute for Cancer Research)

  • Nicholas Buchner

    (Ontario Institute for Cancer Research)

  • Richard De Borja

    (Ontario Institute for Cancer Research)

  • Robert E. Denroche

    (Ontario Institute for Cancer Research)

  • Christina K. Yung

    (Ontario Institute for Cancer Research)

  • Stefano Serra

    (University Health Network)

  • Nicole Onetto

    (Ontario Institute for Cancer Research)

  • Debabrata Mukhopadhyay

    (Mayo Clinic)

  • Ming-Sound Tsao

    (University Health Network)

  • Patricia A. Shaw

    (University Health Network)

  • Gloria M. Petersen

    (Mayo Clinic)

  • Steven Gallinger

    (University Health Network
    Mount Sinai Hospital)

  • Ralph H. Hruban

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Anirban Maitra

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Christine A. Iacobuzio-Donahue

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Richard D. Schulick

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Christopher L. Wolfgang

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Richard A. Morgan

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Rita T. Lawlor

    (ARC-NET center for applied research on cancer, University and Hospital Trust of Verona)

  • Paola Capelli

    (University of Veron)

  • Vincenzo Corbo

    (ARC-NET center for applied research on cancer, University and Hospital Trust of Verona)

  • Maria Scardoni

    (University of Veron)

  • Giampaolo Tortora

    (University and Hospital Trust of Verona)

  • Margaret A. Tempero

    (University of California)

  • Karen M. Mann

    (Cancer Research Program, The Methodist Hospital Research Institute, 6670 Bertner Avenue, Houston, Texas 77030, USA.)

  • Nancy A. Jenkins

    (Cancer Research Program, The Methodist Hospital Research Institute, 6670 Bertner Avenue, Houston, Texas 77030, USA.)

  • Pedro A. Perez-Mancera

    (Li Ka Shing Centre, Cambridge Research Institute, Cancer Research UK)

  • David J. Adams

    (Experimental Cancer Genetics, Wellcome Trust Sanger Institute)

  • David A. Largaespada

    (Masonic Cancer Center, University of Minnesota)

  • Lodewyk F. A. Wessels

    (Bioinformatics and Statistics, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands.)

  • Alistair G. Rust

    (Experimental Cancer Genetics, Wellcome Trust Sanger Institute)

  • Lincoln D. Stein

    (Ontario Institute for Cancer Research)

  • David A. Tuveson

    (Li Ka Shing Centre, Cambridge Research Institute, Cancer Research UK)

  • Neal G. Copeland

    (Cancer Research Program, The Methodist Hospital Research Institute, 6670 Bertner Avenue, Houston, Texas 77030, USA.)

  • Elizabeth A. Musgrove

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales)

  • Aldo Scarpa

    (ARC-NET center for applied research on cancer, University and Hospital Trust of Verona
    University of Veron)

  • James R. Eshleman

    (The Sol Goldman Pancreatic Cancer Research Center, the Johns Hopkins University School of Medicine)

  • Thomas J. Hudson

    (Ontario Institute for Cancer Research)

  • Robert L. Sutherland

    (The Kinghorn Cancer Centre, 370 Victoria Street, Darlinghurst, and the Cancer Research Program, Garvan Institute of Medical Research, 384 Victoria Street, Darlinghurst, Sydney, New South Wales 2010, Australia.
    St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales)

  • David A. Wheeler

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • John V. Pearson

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

  • John D. McPherson

    (Ontario Institute for Cancer Research)

  • Richard A. Gibbs

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, MS226, Houston, Texas 77030-3411, USA.)

  • Sean M. Grimmond

    (Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, The University of Queensland, St Lucia)

Abstract

Pancreatic cancer is a highly lethal malignancy with few effective therapies. We performed exome sequencing and copy number analysis to define genomic aberrations in a prospectively accrued clinical cohort (n = 142) of early (stage I and II) sporadic pancreatic ductal adenocarcinoma. Detailed analysis of 99 informative tumours identified substantial heterogeneity with 2,016 non-silent mutations and 1,628 copy-number variations. We define 16 significantly mutated genes, reaffirming known mutations (KRAS, TP53, CDKN2A, SMAD4, MLL3, TGFBR2, ARID1A and SF3B1), and uncover novel mutated genes including additional genes involved in chromatin modification (EPC1 and ARID2), DNA damage repair (ATM) and other mechanisms (ZIM2, MAP2K4, NALCN, SLC16A4 and MAGEA6). Integrative analysis with in vitro functional data and animal models provided supportive evidence for potential roles for these genetic aberrations in carcinogenesis. Pathway-based analysis of recurrently mutated genes recapitulated clustering in core signalling pathways in pancreatic ductal adenocarcinoma, and identified new mutated genes in each pathway. We also identified frequent and diverse somatic aberrations in genes described traditionally as embryonic regulators of axon guidance, particularly SLIT/ROBO signalling, which was also evident in murine Sleeping Beauty transposon-mediated somatic mutagenesis models of pancreatic cancer, providing further supportive evidence for the potential involvement of axon guidance genes in pancreatic carcinogenesis.

Suggested Citation

  • Andrew V. Biankin & Nicola Waddell & Karin S. Kassahn & Marie-Claude Gingras & Lakshmi B. Muthuswamy & Amber L. Johns & David K. Miller & Peter J. Wilson & Ann-Marie Patch & Jianmin Wu & David K. Chan, 2012. "Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes," Nature, Nature, vol. 491(7424), pages 399-405, November.
    • Handle: RePEc:nat:nature:v:491:y:2012:i:7424:d:10.1038_nature11547
    DOI: 10.1038/nature11547
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    Cited by:

    1. Hongjuan Yao & Wenping Song & Rui Cao & Cheng Ye & Li Zhang & Hebing Chen & Junting Wang & Yuchen Shi & Rui Li & Yi Li & Xiujun Liu & Xiaofei Zhou & Rongguang Shao & Liang Li, 2022. "An EGFR/HER2-targeted conjugate sensitizes gemcitabine-sensitive and resistant pancreatic cancer through different SMAD4-mediated mechanisms," Nature Communications, Nature, vol. 13(1), pages 1-24, December.
    2. Qing Li & Xiao-Xin Zhang & Li-Peng Hu & Bo Ni & Dong-Xue Li & Xu Wang & Shu-Heng Jiang & Hui Li & Min-Wei Yang & Yong-Sheng Jiang & Chun-Jie Xu & Xue-Li Zhang & Yan-Li Zhang & Pei-Qi Huang & Qin Yang , 2023. "Coadaptation fostered by the SLIT2-ROBO1 axis facilitates liver metastasis of pancreatic ductal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Jérémy Guillot & Chloé Dominici & Adrien Lucchesi & Huyen Thi Trang Nguyen & Angélique Puget & Mélanie Hocine & Martha M. Rangel-Sosa & Milesa Simic & Jérémy Nigri & Fabienne Guillaumond & Martin Bigo, 2022. "Sympathetic axonal sprouting induces changes in macrophage populations and protects against pancreatic cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Haochen Zhang & Elias-Ramzey Karnoub & Shigeaki Umeda & Ronan Chaligné & Ignas Masilionis & Caitlin A. McIntyre & Palash Sashittal & Akimasa Hayashi & Amanda Zucker & Katelyn Mullen & Jungeui Hong & A, 2023. "Application of high-throughput single-nucleus DNA sequencing in pancreatic cancer," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Gaurav Mendiratta & Eugene Ke & Meraj Aziz & David Liarakos & Melinda Tong & Edward C. Stites, 2021. "Cancer gene mutation frequencies for the U.S. population," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    6. James T. Topham & Erica S. Tsang & Joanna M. Karasinska & Andrew Metcalfe & Hassan Ali & Steve E. Kalloger & Veronika Csizmok & Laura M. Williamson & Emma Titmuss & Karina Nielsen & Gian Luca Negri & , 2022. "Integrative analysis of KRAS wildtype metastatic pancreatic ductal adenocarcinoma reveals mutation and expression-based similarities to cholangiocarcinoma," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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