Pan-cancer analysis of whole genomes identifies driver rearrangements promoted by LINE-1 retrotransposition
Authors: Bernardo Rodriguez-Martin, Eva G. Alvarez, Adrian Baez-Ortega, Jorge Zamora, Fran Supek, Jonas Demeulemeester, Martin Santamarina, Young Seok Ju, Javier Temes, Daniel Garcia-Souto, Harald Detering, Yilong Li, Jorge Rodriguez-Castro, Ana Dueso-Barroso, Alicia L. Bruzos, Stefan C. Dentro, Miguel G. Blanco, Gianmarco Contino, Daniel Ardeljan, Marta Tojo, Nicola D. Roberts, Sonia Zumalave, Paul A. Edwards, Joachim Weischenfeldt, Montserrat Puiggròs, Zechen Chong, Ken Chen, Eunjung Alice Lee, Jeremiah A. Wala, Keiran M. Raine, Adam Butler, Sebastian M. Waszak, Fabio C. P. Navarro, Steven E. Schumacher, Jean Monlong, Francesco Maura, Niccolo Bolli, Guillaume Bourque, Mark Gerstein, Peter J. Park, David C. Wedge, Rameen Beroukhim, David Torrents, Jan O. Korbel, Iñigo Martincorena, Rebecca C. Fitzgerald, Peter Van Loo, Haig H. Kazazian, Kathleen H. Burns, Kadir C. Akdemir, Eva G. Alvarez, Adrian Baez-Ortega, Rameen Beroukhim, Paul C. Boutros, David D. L. Bowtell, Benedikt Brors, Kathleen H. Burns, Peter J. Campbell, Kin Chan, Ken Chen, Isidro Cortés-Ciriano, Ana Dueso-Barroso, Andrew J. Dunford, Paul A. Edwards, Xavier Estivill, Dariush Etemadmoghadam, Lars Feuerbach, J. Lynn Fink, Milana Frenkel-Morgenstern, Dale W. Garsed, Mark Gerstein, Dmitry A. Gordenin, David Haan, James E. Haber, Julian M. Hess, Barbara Hutter, Marcin Imielinski, David T. W. Jones, Young Seok Ju, Marat D. Kazanov, Leszek J. Klimczak, Youngil Koh, Jan O. Korbel, Kiran Kumar, Eunjung Alice Lee, Jake June-Koo Lee, Yilong Li, Andy G. Lynch, Geoff Macintyre, Florian Markowetz, Iñigo Martincorena, Alexander Martinez-Fundichely, Matthew Meyerson, Satoru Miyano, Hidewaki Nakagawa, Fabio C. P. Navarro, Stephan Ossowski, Peter J. Park, John V. Pearson, Montserrat Puiggròs, Karsten Rippe, Nicola D. Roberts, Steven A. Roberts, Bernardo Rodriguez-Martin, Steven E. Schumacher, Ralph Scully, Mark Shackleton, Nikos Sidiropoulos, Lina Sieverling, Chip Stewart, David Torrents, Jose M. C. Tubio, Izar Villasante, Nicola Waddell, Jeremiah A. Wala, Joachim Weischenfeldt, Lixing Yang, Xiaotong Yao, Sung-Soo Yoon, Jorge Zamora, Cheng-Zhong Zhang, Peter J. Campbell, Jose M. C. Tubio, Lauri A. Aaltonen, Federico Abascal, Adam Abeshouse, Hiroyuki Aburatani, David J. Adams, Nishant Agrawal, Keun Soo Ahn, Sung-Min Ahn, Hiroshi Aikata, Rehan Akbani, Kadir C. Akdemir, Hikmat Al-Ahmadie, Sultan T. Al-Sedairy, Fatima Al-Shahrour, Malik Alawi, Monique Albert, Kenneth Aldape, Ludmil B. Alexandrov, Adrian Ally, Kathryn Alsop, Eva G. Alvarez, Fernanda Amary, Samirkumar B. Amin, Brice Aminou, Ole Ammerpohl, Matthew J. Anderson, Yeng Ang, Davide Antonello, Pavana Anur, Samuel Aparicio, Elizabeth L. Appelbaum, Yasuhito Arai, Axel Aretz, Koji Arihiro, Shun-ichi Ariizumi, Joshua Armenia, Laurent Arnould, Sylvia Asa, Yassen Assenov, Gurnit Atwal, Sietse Aukema, J. Todd Auman, Miriam R. R. Aure, Philip Awadalla, Marta Aymerich, Gary D. Bader, Adrian Baez-Ortega, Matthew H. Bailey, Peter J. Bailey, Miruna Balasundaram, Saianand Balu, Pratiti Bandopadhayay, Rosamonde E. Banks, Stefano Barbi, Andrew P. Barbour, Jonathan Barenboim, Jill Barnholtz-Sloan, Hugh Barr, Elisabet Barrera, John Bartlett, Javier Bartolome, Claudio Bassi, Oliver F. Bathe, Daniel Baumhoer, Prashant Bavi, Stephen B. Baylin, Wojciech Bazant, Duncan Beardsmore, Timothy A. Beck, Sam Behjati, Andreas Behren, Beifang Niu, Cindy Bell, Sergi Beltran, Christopher Benz, Andrew Berchuck, Anke K. Bergmann, Erik N. Bergstrom, Benjamin P. Berman, Daniel M. Berney, Stephan H. Bernhart, Rameen Beroukhim, Mario Berrios, Samantha Bersani, Johanna Bertl, Miguel Betancourt, Vinayak Bhandari, Shriram G. Bhosle, Andrew V. Biankin, Matthias Bieg, Darell Bigner, Hans Binder, Ewan Birney, Michael Birrer, Nidhan K. Biswas, Bodil Bjerkehagen, Tom Bodenheimer, Lori Boice, Giada Bonizzato, Johann S. De Bono, Arnoud Boot, Moiz S. Bootwalla, Ake Borg, Arndt Borkhardt, Keith A. Boroevich, Ivan Borozan, Christoph Borst, Marcus Bosenberg, Mattia Bosio, Jacqueline Boultwood, Guillaume Bourque, Paul C. Boutros, G. Steven Bova, David T. Bowen, Reanne Bowlby, David D. L. Bowtell, Sandrine Boyault, Rich Boyce, Jeffrey Boyd, Alvis Brazma, Paul Brennan, Daniel S. Brewer, Arie B. Brinkman, Robert G. Bristow, Russell R. Broaddus, Jane E. Brock, Malcolm Brock, Annegien Broeks, Angela N. Brooks, Denise Brooks, Benedikt Brors, Søren Brunak, Timothy J. C. Bruxner, Alicia L. Bruzos, Alex Buchanan, Ivo Buchhalter, Christiane Buchholz, Susan Bullman, Hazel Burke, Birgit Burkhardt, Kathleen H. Burns, John Busanovich, Carlos D. Bustamante, Adam P. Butler, Atul J. Butte, Niall J. Byrne, Anne-Lise Børresen-Dale, Samantha J. Caesar-Johnson, Andy Cafferkey, Declan Cahill, Claudia Calabrese, Carlos Caldas, Fabien Calvo, Niedzica Camacho, Peter J. Campbell, Elias Campo, Cinzia Cantù, Shaolong Cao, Thomas E. Carey, Joana Carlevaro-Fita, Rebecca Carlsen, Ivana Cataldo, Mario Cazzola, Jonathan Cebon, Robert Cerfolio, Dianne E. Chadwick, Dimple Chakravarty, Don Chalmers, Calvin Wing Yiu Chan, Kin Chan, Michelle Chan-Seng-Yue, Vishal S. Chandan, David K. Chang, Stephen J. Chanock, Lorraine A. Chantrill, Aurélien Chateigner, Nilanjan Chatterjee, Kazuaki Chayama, Hsiao-Wei Chen, Jieming Chen, Ken Chen, Yiwen Chen, Zhaohong Chen, Andrew D. Cherniack, Jeremy Chien, Yoke-Eng Chiew, Suet-Feung Chin, Juok Cho, Sunghoon Cho, Jung Kyoon Choi, Wan Choi, Christine Chomienne, Zechen Chong, Su Pin Choo, Angela Chou, Angelika N. Christ, Elizabeth L. Christie, Eric Chuah, Carrie Cibulskis, Kristian Cibulskis, Sara Cingarlini, Peter Clapham, Alexander Claviez, Sean Cleary, Nicole Cloonan, Marek Cmero, Colin C. Collins, Ashton A. Connor, Susanna L. Cooke, Colin S. Cooper, Leslie Cope, Vincenzo Corbo, Matthew G. Cordes, Stephen M. Cordner, Isidro Cortés-Ciriano, Kyle Covington, Prue A. Cowin, Brian Craft, David Craft, Chad J. Creighton, Yupeng Cun, Erin Curley, Ioana Cutcutache, Karolina Czajka, Bogdan Czerniak, Rebecca A. Dagg, Ludmila Danilova, Maria Vittoria Davi, Natalie R. Davidson, Helen Davies, Ian J. Davis, Brandi N. Davis-Dusenbery, Kevin J. Dawson, Francisco M. De La Vega, Ricardo De Paoli-Iseppi, Timothy Defreitas, Angelo P. Dei Tos, Olivier Delaneau, John A. Demchok, Jonas Demeulemeester, German M. Demidov, Deniz Demircioğlu, Nening M. Dennis, Robert E. Denroche, Stefan C. Dentro, Nikita Desai, Vikram Deshpande, Amit G. Deshwar, Christine Desmedt, Jordi Deu-Pons, Noreen Dhalla, Neesha C. Dhani, Priyanka Dhingra, Rajiv Dhir, Anthony DiBiase, Klev Diamanti, Li Ding, Shuai Ding, Huy Q. Dinh, Luc Dirix, HarshaVardhan Doddapaneni, Nilgun Donmez, Michelle T. Dow, Ronny Drapkin, Oliver Drechsel, Ruben M. Drews, Serge Serge, Tim Dudderidge, Ana Dueso-Barroso, Andrew J. Dunford, Michael Dunn, Lewis Jonathan Dursi, Fraser R. Duthie, Ken Dutton-Regester, Jenna Eagles, Douglas F. Easton, Stuart Edmonds, Paul A. Edwards, Sandra E. Edwards, Rosalind A. Eeles, Anna Ehinger, Juergen Eils, Roland Eils, Adel El-Naggar, Matthew Eldridge, Kyle Ellrott, Serap Erkek, Georgia Escaramis, Shadrielle M. G. Espiritu, Xavier Estivill, Dariush Etemadmoghadam, Jorunn E. Eyfjord, Bishoy M. Faltas, Daiming Fan, Yu Fan, William C. Faquin, Claudiu Farcas, Matteo Fassan, Aquila Fatima, Francesco Favero, Nodirjon Fayzullaev, Ina Felau, Sian Fereday, Martin L. Ferguson, Vincent Ferretti, Lars Feuerbach, Matthew A. Field, J. Lynn Fink, Gaetano Finocchiaro, Cyril Fisher, Matthew W. Fittall, Anna Fitzgerald, Rebecca C. Fitzgerald, Adrienne M. Flanagan, Neil E. Fleshner, Paul Flicek, John A. Foekens, Kwun M. Fong, Nuno A. Fonseca, Christopher S. Foster, Natalie S. Fox, Michael Fraser, Scott Frazer, Milana Frenkel-Morgenstern, William Friedman, Joan Frigola, Catrina C. Fronick, Akihiro Fujimoto, Masashi Fujita, Masashi Fukayama, Lucinda A. Fulton, Robert S. Fulton, Mayuko Furuta, P. Andrew Futreal, Anja Füllgrabe, Stacey B. Gabriel, Steven Gallinger, Carlo Gambacorti-Passerini, Jianjiong Gao, Shengjie Gao, Levi Garraway, Øystein Garred, Erik Garrison, Dale W. Garsed, Nils Gehlenborg, Josep L. L. Gelpi, Joshy George, Daniela S. Gerhard, Clarissa Gerhauser, Jeffrey E. Gershenwald, Mark Gerstein, Moritz Gerstung, Gad Getz, Mohammed Ghori, Ronald Ghossein, Nasra H. Giama, Richard A. Gibbs, Bob Gibson, Anthony J. Gill, Pelvender Gill, Dilip D. Giri, Dominik Glodzik, Vincent J. Gnanapragasam, Maria Elisabeth Goebler, Mary J. Goldman, Carmen Gomez, Santiago Gonzalez, Abel Gonzalez-Perez, Dmitry A. Gordenin, James Gossage, Kunihito Gotoh, Ramaswamy Govindan, Dorthe Grabau, Janet S. Graham, Robert C. Grant, Anthony R. Green, Eric Green, Liliana Greger, Nicola Grehan, Sonia Grimaldi, Sean M. Grimmond, Robert L. 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Nahal-Bose, Hitoshi Nakagama, Hidewaki Nakagawa, Hiromi Nakamura, Toru Nakamura, Kaoru Nakano, Tannistha Nandi, Jyoti Nangalia, Mia Nastic, Arcadi Navarro, Fabio C. P. Navarro, David E. Neal, Gerd Nettekoven, Felicity Newell, Steven J. Newhouse, Yulia Newton, Alvin Wei Tian Ng, Anthony Ng, Jonathan Nicholson, David Nicol, Yongzhan Nie, G. Petur Nielsen, Morten Muhlig Nielsen, Serena Nik-Zainal, Michael S. Noble, Katia Nones, Paul A. Northcott, Faiyaz Notta, Brian D. O’Connor, Peter O’Donnell, Maria O’Donovan, Sarah O’Meara, Brian Patrick O’Neill, J. Robert O’Neill, David Ocana, Angelica Ochoa, Layla Oesper, Christopher Ogden, Hideki Ohdan, Kazuhiro Ohi, Lucila Ohno-Machado, Karin A. Oien, Akinyemi I. Ojesina, Hidenori Ojima, Takuji Okusaka, Larsson Omberg, Choon Kiat Ong, Stephan Ossowski, German Ott, B. F. 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Soulette, Paul N. Span, Paul T. Spellman, Nicola Sperandio, Andrew J. Spillane, Oliver Spiro, Jonathan Spring, Johan Staaf, Peter F. Stadler, Peter Staib, Stefan G. Stark, Lucy Stebbings, Ólafur Andri Stefánsson, Oliver Stegle, Lincoln D. Stein, Alasdair Stenhouse, Chip Stewart, Stephan Stilgenbauer, Miranda D. Stobbe, Michael R. Stratton, Jonathan R. Stretch, Adam J. Struck, Joshua M. Stuart, Henk G. Stunnenberg, Hong Su, Xiaoping Su, Ren X. Sun, Stephanie Sungalee, Hana Susak, Akihiro Suzuki, Fred Sweep, Monika Szczepanowski, Holger Sültmann, Takashi Yugawa, Angela Tam, David Tamborero, Benita Kiat Tee Tan, Donghui Tan, Patrick Tan, Hiroko Tanaka, Hirokazu Taniguchi, Tomas J. Tanskanen, Maxime Tarabichi, Roy Tarnuzzer, Patrick Tarpey, Morgan L. Taschuk, Kenji Tatsuno, Simon Tavaré, Darrin F. Taylor, Amaro Taylor-Weiner, Jon W. Teague, Bin Tean Teh, Varsha Tembe, Javier Temes, Kevin Thai, Sarah P. Thayer, Nina Thiessen, Gilles Thomas, Sarah Thomas, Alan Thompson, Alastair M. Thompson, John F. F. Thompson, R. Houston Thompson, Heather Thorne, Leigh B. Thorne, Adrian Thorogood, Grace Tiao, Nebojsa Tijanic, Lee E. Timms, Roberto Tirabosco, Marta Tojo, Stefania Tommasi, Christopher W. Toon, Umut H. Toprak, David Torrents, Giampaolo Tortora, Jörg Tost, Yasushi Totoki, David Townend, Nadia Traficante, Isabelle Treilleux, Jean-Rémi Trotta, Lorenz H. P. Trümper, Ming Tsao, Tatsuhiko Tsunoda, Jose M. C. Tubio, Olga Tucker, Richard Turkington, Daniel J. Turner, Andrew Tutt, Masaki Ueno, Naoto T. Ueno, Christopher Umbricht, Husen M. Umer, Timothy J. Underwood, Lara Urban, Tomoko Urushidate, Tetsuo Ushiku, Liis Uusküla-Reimand, Alfonso Valencia, David J. Van Den Berg, Steven Van Laere, Peter Van Loo, Erwin G. Van Meir, Gert G. Van den Eynden, Theodorus Van der Kwast, Naveen Vasudev, Miguel Vazquez, Ravikiran Vedururu, Umadevi Veluvolu, Shankar Vembu, Lieven P. C. Verbeke, Peter Vermeulen, Clare Verrill, Alain Viari, David Vicente, Caterina Vicentini, K. VijayRaghavan, Juris Viksna, Ricardo E. Vilain, Izar Villasante, Anne Vincent-Salomon, Tapio Visakorpi, Douglas Voet, Paresh Vyas, Ignacio Vázquez-García, Nick M. Waddell, Nicola Waddell, Claes Wadelius, Lina Wadi, Rabea Wagener, Jeremiah A. Wala, Jian Wang, Jiayin Wang, Linghua Wang, Qi Wang, Wenyi Wang, Yumeng Wang, Zhining Wang, Paul M. Waring, Hans-Jörg Warnatz, Jonathan Warrell, Anne Y. Warren, Sebastian M. Waszak, David C. Wedge, Dieter Weichenhan, Paul Weinberger, John N. Weinstein, Joachim Weischenfeldt, Daniel J. Weisenberger, Ian Welch, Michael C. Wendl, Johannes Werner, Justin P. Whalley, David A. Wheeler, Hayley C. Whitaker, Dennis Wigle, Matthew D. Wilkerson, Ashley Williams, James S. Wilmott, Gavin W. Wilson, Julie M. Wilson, Richard K. Wilson, Boris Winterhoff, Jeffrey A. Wintersinger, Maciej Wiznerowicz, Stephan Wolf, Bernice H. Wong, Tina Wong, Winghing Wong, Youngchoon Woo, Scott Wood, Bradly G. Wouters, Adam J. Wright, Derek W. Wright, Mark H. Wright, Chin-Lee Wu, Dai-Ying Wu, Guanming Wu, Jianmin Wu, Kui Wu, Yang Wu, Zhenggang Wu, Liu Xi, Tian Xia, Qian Xiang, Xiao Xiao, Rui Xing, Heng Xiong, Qinying Xu, Yanxun Xu, Hong Xue, Shinichi Yachida, Sergei Yakneen, Rui Yamaguchi, Takafumi N. Yamaguchi, Masakazu Yamamoto, Shogo Yamamoto, Hiroki Yamaue, Fan Yang, Huanming Yang, Jean Y. Yang, Liming Yang, Lixing Yang, Shanlin Yang, Tsun-Po Yang, Yang Yang, Xiaotong Yao, Marie-Laure Yaspo, Lucy Yates, Christina Yau, Chen Ye, Kai Ye, Venkata D. Yellapantula, Christopher J. Yoon, Sung-Soo Yoon, Fouad Yousif, Jun Yu, Kaixian Yu, Willie Yu, Yingyan Yu, Ke Yuan, Yuan Yuan, Denis Yuen, Christina K. Yung, Olga Zaikova, Jorge Zamora, Marc Zapatka, Jean C. Zenklusen, Thorsten Zenz, Nikolajs Zeps, Cheng-Zhong Zhang, Fan Zhang, Hailei Zhang, Hongwei Zhang, Hongxin Zhang, Jiashan Zhang, Jing Zhang, Junjun Zhang, Xiuqing Zhang, Xuanping Zhang, Yan Zhang, Zemin Zhang, Zhongming Zhao, Liangtao Zheng, Xiuqing Zheng, Wanding Zhou, Yong Zhou, Bin Zhu, Hongtu Zhu, Jingchun Zhu, Shida Zhu, Lihua Zou, Xueqing Zou, Anna deFazio, Nicholas van As, Carolien H. M. van Deurzen, Marc J. van de Vijver, L. van’t Veer, Christian von Mering
Journal: Nature Genetics (2020)

Abstract About half of all cancers have somatic integrations of retrotransposons. Here, to characterize their role in oncogenesis, we analyzed the patterns and mechanisms of somatic retrotransposition in 2,954 cancer genomes from 38 histological cancer subtypes within the framework of the Pan-Cancer Analysis of Whole Genomes (PCAWG) project. We identified 19,166 somatically acquired retrotransposition events, which affected 35% of samples and spanned a range of event types. Long interspersed nuclear element (LINE-1; L1 hereafter) insertions emerged as the first most frequent type of somatic structural variation in esophageal adenocarcinoma, and the second most frequent in head-and-neck and colorectal cancers. Aberrant L1 integrations can delete megabase-scale regions of a chromosome, which sometimes leads to the removal of tumor-suppressor genes, and can induce complex translocations and large-scale duplications. Somatic retrotranspositions can also initiate breakage–fusion–bridge cycles, leading to high-level amplification of oncogenes. These observations illuminate a relevant role of 22 L1 retrotransposition in remodeling the cancer genome, with potential implications for the development of human tumors.