Evolutionary history of human colitis-associated colorectal cancer

Ann-Marie Baker, William Cross, Kit Curtius, Ibrahim Al Bakir, Chang-Ho Ryan Choi, Hayley Louise Davis, Daniel Temko, Sujata Biswas, Pierre Martinez, Marc J. Williams, James O. Lindsay, Roger Feakins, Roser Vega, Stephen J. Hayes, Tomlinson, I., Stuart A.C. McDonald, Morgan Moorghen, Andrew Silver, James E. East, Nicholas A. Wright, Lai Mun Wang, Manuel Rodriguez-Justo, Marnix Jansen, Ailsa L. Hart, Simon J. Leedham and Trevor Graham 2019. Evolutionary history of human colitis-associated colorectal cancer. Gut. 68, pp. 985-995. https://doi.org/10.1136/gutjnl-2018-316191

TitleEvolutionary history of human colitis-associated colorectal cancer
TypeJournal article
AuthorsAnn-Marie Baker, William Cross, Kit Curtius, Ibrahim Al Bakir, Chang-Ho Ryan Choi, Hayley Louise Davis, Daniel Temko, Sujata Biswas, Pierre Martinez, Marc J. Williams, James O. Lindsay, Roger Feakins, Roser Vega, Stephen J. Hayes, Tomlinson, I., Stuart A.C. McDonald, Morgan Moorghen, Andrew Silver, James E. East, Nicholas A. Wright, Lai Mun Wang, Manuel Rodriguez-Justo, Marnix Jansen, Ailsa L. Hart, Simon J. Leedham and Trevor Graham
Abstract

Objective: IBD confers an increased lifetime risk of developing colorectal cancer (CRC), and colitis-associated CRC (CA-CRC) is molecularly distinct from sporadic CRC (S-CRC). Here we have dissected the evolutionary history of CA-CRC using multiregion sequencing.

Design: Exome sequencing was performed on fresh-frozen multiple regions of carcinoma, adjacent non-cancerous mucosa and blood from 12 patients with CA-CRC (n=55 exomes), and key variants were validated with orthogonal methods. Genome-wide copy number profiling was performed using single nucleotide polymorphism arrays and low-pass whole genome sequencing on archival non-dysplastic mucosa (n=9), low-grade dysplasia (LGD; n=30), high-grade dysplasia (HGD; n=13), mixed LGD/HGD (n=7) and CA-CRC (n=19). Phylogenetic trees were reconstructed, and evolutionary analysis used to reveal the temporal sequence of events leading to CA-CRC.

Results: 10/12 tumours were microsatellite stable with a median mutation burden of 3.0 single nucleotide alterations (SNA) per Mb, ~20% higher than S-CRC (2.5 SNAs/Mb), and consistent with elevated ageing-associated mutational processes. Non-dysplastic mucosa had considerable mutation burden (median 47 SNAs), including mutations shared with the neighbouring CA-CRC, indicating a precancer mutational field. CA-CRCs were often near triploid (40%) or near tetraploid (20%) and phylogenetic analysis revealed that copy number alterations (CNAs) began to accrue in non-dysplastic bowel, but the LGD/HGD transition often involved a punctuated ‘catastrophic’ CNA increase.

Conclusions: Evolutionary genomic analysis revealed precancer clones bearing extensive SNAs and CNAs, with progression to cancer involving a dramatic accrual of CNAs at HGD. Detection of the cancerised field is an encouraging prospect for surveillance, but punctuated evolution may limit the window for early detection.

JournalGut
Journal citation68, pp. 985-995
ISSN0017-5749
1468-3288
Year2019
PublisherBMJ
Publisher's version
License
CC BY 4.0
File Access Level
Open (open metadata and files)
Digital Object Identifier (DOI)https://doi.org/10.1136/gutjnl-2018-316191
Web address (URL)http://dx.doi.org/10.1136/gutjnl-2018-316191
Publication dates
Published in printJun 2019
Published online08 May 2019

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