Comprehensive Characterization of Cancer Driver Genes and Mutations
Matthew H. Bailey(James S. McDonnell Foundation), Collin Tokheim(Johns Hopkins University), Eduard Porta‐Pardo(Sanford Burnham Prebys Medical Discovery Institute), Sohini Sengupta(James S. McDonnell Foundation), Denis Bertrand(Genome Institute of Singapore), Amila Weerasinghe(James S. McDonnell Foundation), Antonio Colaprico(Université Libre de Bruxelles), Michael C. Wendl(James S. McDonnell Foundation), Jaegil Kim(Broad Institute), Brendan Reardon(Broad Institute), Patrick Kwok‐Shing Ng(The University of Texas MD Anderson Cancer Center), Kang Jin Jeong(The University of Texas MD Anderson Cancer Center), Song Cao(James S. McDonnell Foundation), Zixing Wang(The University of Texas MD Anderson Cancer Center), Galen F. Gao(Memorial Sloan Kettering Cancer Center), Qingsong Gao(James S. McDonnell Foundation), Fang Wang(The University of Texas MD Anderson Cancer Center), Eric Minwei Liu(Cornell University), Loris Mularoni(Institute for Research in Biomedicine), Carlota Rubio-Pérez(Institute for Research in Biomedicine), Niranjan Nagarajan(Genome Institute of Singapore), Isidro Cortés‐Ciriano(Harvard University), Daniel Cui Zhou(James S. McDonnell Foundation), Wen-Wei Liang(James S. McDonnell Foundation), Julian M. Hess(Broad Institute), Venkata Yellapantula(James S. McDonnell Foundation), David Tamborero(Institute for Research in Biomedicine), Abel González-Pérez(Institute for Research in Biomedicine), Chayaporn Suphavilai(Genome Institute of Singapore), Jia Yu Ko(Genome Institute of Singapore), Ekta Khurana(Cornell University), Peter J. Park(Harvard University), Eliezer M. Van Allen(Broad Institute), Han Liang(The University of Texas MD Anderson Cancer Center), Rory Johnson(Broad Institute), John A. Demchok(Sanford Burnham Prebys Medical Discovery Institute), Ina Felau(Institució Catalana de Recerca i Estudis Avançats), Melpomeni Kasapi(University of California, Santa Cruz), Martin L. Ferguson(Baylor College of Medicine), Carolyn M. Hutter(Broad Institute), Heidi J. Sofia(The University of Texas MD Anderson Cancer Center), Roy Tarnuzzer(The University of Texas MD Anderson Cancer Center), Zhining Wang(The University of Texas MD Anderson Cancer Center), Liming Yang(Johns Hopkins University), Jean C. Zenklusen(James S. McDonnell Foundation), Jiashan Zhang, Sudha Chudamani, Jia Liu, Laxmi Lolla, Rashi Naresh, Todd Pihl, Qiang Sun, Yunhu Wan, Ye Wu(The University of Texas MD Anderson Cancer Center), Juok Cho, Timothy Defreitas, Scott Frazer, Nils Gehlenborg, Gad Getz(Broad Institute), David I. Heiman, Jaegil Kim(Broad Institute), Michael S. Lawrence(Broad Institute), Pei Lin, Sam Meier(The University of Texas MD Anderson Cancer Center), Michael S. Noble(James S. McDonnell Foundation), Gordon Saksena, Doug Voet, Hailei Zhang, Brady Bernard, Nyasha Chambwe(Broad Institute), Varsha Dhankani, Theo Knijnenburg(Broad Institute), Roger Kramer(Broad Institute), Kalle Leinonen(Johns Hopkins University), Yuexin Liu, Michael Miller(Broad Institute), Sheila M. Reynolds(The University of Texas MD Anderson Cancer Center), Ilya Shmulevich, Vésteinn Thórsson, Wei Zhang, Rehan Akbani, Bradley M. Broom, Apurva M. Hegde, Zhenlin Ju, Rupa S. Kanchi, Anil Korkut(Cornell University), Jun Li(Broad Institute), Han Liang(The University of Texas MD Anderson Cancer Center), Shiyun Ling, Wenbin Liu, Yiling Lu(James S. McDonnell Foundation), Gordon B. Mills(The University of Texas MD Anderson Cancer Center), Kwok-Shing Ng, Arvind Rao, Michael P. Ryan(Broad Institute), Jing Wang, John N. Weinstein, Jiexin Zhang(James S. McDonnell Foundation), Adam Abeshouse(The University of Texas MD Anderson Cancer Center), Joshua Armenia, Debyani Chakravarty(Cornell University), Walid K. Chatila, Ino de Bruijn(The University of Texas MD Anderson Cancer Center), Galen F. Gao(Memorial Sloan Kettering Cancer Center), Benjamin E. Gross, Zachary Heins(Broad Institute), Ritika Kundra(The University of Texas MD Anderson Cancer Center), Konnor La, Marc Ladanyi, Augustin Luna(Sanford Burnham Prebys Medical Discovery Institute), Moriah G. Nissan, Angelica Ochoa, Sarah Phillips, Ed Reznik, Francisco Sánchez-Vega(Memorial Sloan Kettering Cancer Center), Chris Sander, Nikolaus Schultz, Robert E. Sheridan, S. Onur Sumer(The University of Texas MD Anderson Cancer Center), Yichao Sun, Barry S. Taylor, Jioajiao Wang, Hongxin Zhang, Pavana Anur, Myron Peto(Sanford Burnham Prebys Medical Discovery Institute), Paul T. Spellman, Christopher C. Benz, Joshua M. Stuart(University of California, Santa Cruz), Christopher K. Wong, Christina Yau, D. Neil Hayes, Joel S. Parker, Matthew D. Wilkerson(The University of Texas MD Anderson Cancer Center), Adrian Ally, Miruna Balasundaram, Reanne Bowlby, Denise Brooks, Rebecca Carlsen, Eric Chuah(University of California, Santa Cruz), Noreen Dhalla, Robert A. Holt, Steven J.M. Jones, Katayoon Kasaian, Darlene Lee, Yussanne Ma, Marco A. Marra, Michael Mayo, Richard A. Moore, Andrew J. Mungall, Karen Mungall(Cornell University), A. Gordon Robertson, Sara Sadeghi, Jacqueline E. Schein, Payal Sipahimalani, Angela Tam, Nina Thiessen(James S. McDonnell Foundation), Kane Tse, Tina Wong(Broad Institute), Ashton C. Berger, Rameen Beroukhim, Andrew D. Cherniack, Carrie Cibulskis(The University of Texas MD Anderson Cancer Center), Stacey Gabriel, Galen F. Gao, Gavin Ha, Matthew Meyerson(Institute for Research in Biomedicine), Steven E. Schumacher, Juliann Shih, Melanie H. Kucherlapati, Raju Kucherlapati, Stephen B. Baylin, Leslie Cope, Ludmila Danilova, Moiz S. Bootwalla, Phillip H. Lai(James S. McDonnell Foundation), Dennis T. Maglinte(Broad Institute), David Van Den Berg(James S. McDonnell Foundation), Daniel J. Weisenberger, J. Todd Auman, Saianand Balu, Tom Bodenheimer, Cheng Fan, Katherine A. Hoadley, Alan P. Hoyle, Stuart R. Jefferys, Corbin D. Jones(Genome Institute of Singapore), Shaowu Meng, Piotr A. Mieczkowski, Lisle E. Mose, Amy H. Perou, Charles M. Perou, Jeffrey Roach, Yan Shi(The University of Texas MD Anderson Cancer Center), Janae V. Simons, Tara Skelly, Matthew G. Soloway, Donghui Tan, Umadevi Veluvolu, Huihui Fan, Toshinori Hinoue, Peter W. Laird, Hui Shen, Wanding Zhou, Michelle Bellair(The University of Texas MD Anderson Cancer Center), Kyle Chang, Kyle R. Covington, Chad J. Creighton, Huyen Dinh, HarshaVardhan Doddapaneni, Lawrence A. Donehower(The University of Texas MD Anderson Cancer Center), Jennifer Drummond, Richard A. Gibbs, Robert Glenn, Walker Hale(James S. McDonnell Foundation), Yi Han, Hai Hu, Viktoriya Korchina, Sandra Lee, Lora Lewis, Wei Li, Xiuping Liu(Broad Institute), Margaret Morgan, Donna Morton, Donna M. Muzny, Jireh Santibanez, Margi Sheth(The University of Texas MD Anderson Cancer Center), Eve Shinbrot(Cornell University), Linghua Wang, Min Wang, David A. Wheeler(Baylor College of Medicine), Liu Xi(James S. McDonnell Foundation), Fengmei Zhao(Cornell University), Julian M. Hess(Broad Institute), Elizabeth L. Appelbaum, Matthew H. Bailey(Washington University in St. Louis), Matthew G. Cordes, Li Ding(Washington University in St. Louis), Catrina C. Fronick, Lucinda A. Fulton(The University of Texas MD Anderson Cancer Center), Robert S. Fulton(The University of Texas MD Anderson Cancer Center), Cyriac Kandoth(Baylor College of Medicine), Elaine R. Mardis(The University of Texas MD Anderson Cancer Center), Michael D. McLellan, Christopher A. Miller(Broad Institute), Heather K. Schmidt, Richard K. Wilson(James S. McDonnell Foundation), Daniel Crain, Erin Curley(James S. McDonnell Foundation), Johanna Gardner, Kevin Lau, David Mallery, Scott Morris, Joseph Paulauskis, Robert Penny, Candace Shelton, Troy Shelton, Mark E. Sherman, Eric Thompson(James S. McDonnell Foundation), Peggy Yena, Jay Bowen, Julie M. Gastier‐Foster, Mark Gerken(Baylor College of Medicine), Kristen M. Leraas, Tara M. Lichtenberg, Nilsa C. Ramirez, Lisa Wise, Erik Zmuda, Niall M. Corcoran, Tony Costello(Cornell University), Christopher M. Hovens, André Lopes Carvalho, Ana Carolina de Carvalho, José Humberto Tavares Guerreiro Fregnani, Adhemar Longatto‐Filho, Rui Manuel Reis, Cristovam Scapulatempo‐Neto, Henrique C.S. Silveira, Daniel Onofre Vidal, Andrew Burnette, Jennifer Eschbacher, Beth Hermes, Ardene Noss, Rosy Singh, Matthew L. Anderson, Patricia D. Castro, Michael Ittmann, David G. Huntsman, Bernard Kohl, Xuan Le, Richard Thorp, Chris Andry, Elizabeth R. Duffy, Vladimir Lyadov, Oxana Paklina(James S. McDonnell Foundation), Galiya Setdikova, Shabunin Av, Mikhail Tavobilov(Broad Institute), Christopher McPherson(Baylor College of Medicine), Ronald E. Warnick, Ross S. Berkowitz(The University of Texas MD Anderson Cancer Center), Daniel Cramer, Colleen M. Feltmate, Neil S. Horowitz, Adam S. Kibel, Michael G. Muto, Chandrajit P. Raut, Andrei Malykh, Jill S. Barnholtz‐Sloan, Wendi Barrett, Karen Devine, Jordonna Fulop, Quinn T. Ostrom(James S. McDonnell Foundation), Kristen Shimmel, Yingli Wolinsky, Andrew E. Sloan(Sanford Burnham Prebys Medical Discovery Institute), Agostino Maria De Rose(Broad Institute), Felice Giuliante, Marc T. Goodman, Beth Y. Karlan, Curt H. Hagedorn, John Eckman, Jodi Harr, Jerome Myers, Kelinda Tucker, Leigh Anne Zach, Brenda Deyarmin, Hai Hu, Leonid Kvecher, Caroline Larson, Richard Mural, Stella Somiari, Aleš Vícha, Tomáš Zelinka, Joseph Bennett, Mary Iacocca, Brenda Rabeno, Patricia Swanson(Broad Institute), Mathieu Latour(Cornell University), Louis Lacombe, Bernard Têtu, Alain Bergeron, Mary McGraw, Susan M. Staugaitis, John A. Chabot, Hanina Hibshoosh, Antonia R. Sepulveda, Tao Su(Broad Institute), Timothy C. Wang, Olga Potapova, Olga Voronina, Laurence Desjardins, Odette Mariani, Sergio Roman‐Roman, Xavier Sastre, Marc‐Henri Stern, Feixiong Cheng, Sabina Signoretti, Andrew Berchuck(Genome Institute of Singapore), Darell D. Bigner(The University of Texas MD Anderson Cancer Center), Eric Lipp, Jeffrey R. Marks, Shannon J. McCall, Roger E. McLendon, Angeles Alvarez Secord, Alexis Sharp, Madhusmita Behera, Daniel J. Brat, Amy Chen, Keith A. Delman, Seth Force, Fadlo R. Khuri(Cornell University), Kelly R. Magliocca, Shishir K. Maithel, Jeffrey J. Olson, Taofeek K. Owonikoko, Alan Pickens, Suresh S. Ramalingam, Dong Min Shin, Gabriel Sica(The University of Texas MD Anderson Cancer Center), Erwin G. Van Meir, Hongzheng Zhang, Wil Eijckenboom, Ad Gillis, Esther Korpershoek, Leendert H. J. Looijenga, Wolter Oosterhuis, Hans Stoop, Kim E. van Kessel, Ellen C. Zwarthoff(The University of Texas MD Anderson Cancer Center), Chiara Calatozzolo, Lucia Cuppini, Stefania Cuzzubbo, Francesco DiMeco, Gaetano Finocchiaro(Broad Institute), Luca Mattei, Alessandro Perin, Bianca Pollo, Chu Chen, J. C. Houck, Pawadee Lohavanichbutr, Arndt Hartmann, Robert Stoehr, Robert Stoehr, Helge Täubert, Sven Wach, Bernd Wullich, Witold Kycler, Dawid Murawa, Maciej Wiznerowicz(The University of Texas MD Anderson Cancer Center), Ki Wung Chung, W. Jeffrey Edenfield, Julie Martin, Éric Baudin, Glenn J. Bubley, Raphael Bueno, Assunta De Rienzo, William G. Richards, Steven N. Kalkanis, Tom Mikkelsen, Houtan Noushmehr, Lisa Scarpace(Broad Institute), Nicolas Girard, Marta Aymerich, Elı́as Campo(Cornell University), Eva Giné, Armando López Guillermo, Nguyen Van Bang, Phan Thi Hanh, Bùi Đức Phú, Yufang Tang, Howard Colman, Kimberley Evason, Peter Dottino, John A. Martignetti, Hani Gabra, Hartmut Juhl, Teniola Akeredolu, Serghei Stepa, Dave S.�B. Hoon, Keunsoo Ahn, Koo Jeong Kang, Felix Beuschlein, Anne Breggia, Michael Birrer, Debra Bell, Mitesh J. Borad, Alan H. Bryce, Erik P. Castle, Vishal S. Chandan, John C. Cheville, John A. Copland, Michael B. Farnell(The University of Texas MD Anderson Cancer Center), Thomas J. Flotte, Nasra H. Giama, Thai H. Ho(Broad Institute), Michael L. Kendrick, Jean‐Pierre Kocher, Karla Kopp, Catherine D. Moser, David M. Nagorney, Daniel J. O’Brien, Brian Patrick O’Neill, Tushar Patel(Broad Institute), Gloria M. Petersen, Florencia G. Que, Michael Rivera(James S. McDonnell Foundation), Lewis R. Roberts(Broad Institute), Robert C. Smallridge, Thomas C. Smyrk, Melissa Stanton, R. Houston Thompson(Baylor College of Medicine), Michael Torbenson(James S. McDonnell Foundation), Ju Yang, Lizhi Zhang, Fadi Brimo, Jaffer A. Ajani, Ana Maria Angulo Gonzalez(Broad Institute), Carmen Behrens, Jolanta Bondaruk, Russell Broaddus, Bogdan Czerniak, Bita Esmaeli, Junya Fujimoto(Broad Institute), Jeffrey Gershenwald, Charles C. Guo, Alexander J. Lazar(The University of Texas MD Anderson Cancer Center), Christopher J. Logothetis, Funda Meric‐Bernstam(Institute for Research in Biomedicine), César A. Moran, Lois M. Ramondetta, David C. Rice, Anil K. Sood, Pheroze Tamboli, Timothy Thompson, Patricia Troncoso, Anne S. Tsao, Ignacio Wistuba(The University of Texas MD Anderson Cancer Center), Candace Carter, Lauren E. Haydu, Peter Hersey, Valerie Jakrot, Hojabr Kakavand(Baylor College of Medicine), Richard Kefford, Kenneth Lee, Georgina V. Long, Graham J. Mann, Michael C. Quinn, Robyn P.M. Saw, Richard A. Scolyer, Kerwin F. Shannon, Andrew J. Spillane(Harvard University), Jonathan R. Stretch, Maria Synott, John F. Thompson, James S. Wilmott, Hikmat Al‐Ahmadie, Timothy A. Chan, Ronald Ghossein(Broad Institute), Anuradha Gopalan, Douglas A. Levine, Victor E. Reuter, Samuel Singer, Bhuvanesh Singh, Nguyen Viet Tien, Thomas Broudy, Cyrus Mirsaidi, Praveen Nair, Paul Drwiega, Judy Miller, J. M. Smith, Howard A. Zaren, Joong‐Won Park, Nguyễn Phi Hùng, Electron Kebebew(James S. McDonnell Foundation), W. Marston Linehan, Adam R. Metwalli, Karel Pacák, Peter A. Pinto, Mark Schiffman, Laura S. Schmidt, Cathy D. Vocke, Nicolas Wentzensen, Robert Worrell(Harvard University), Hannah Yang, Marc Moncrieff, Chandra Goparaju, Jonathan Melamed, Harvey I. Pass, Natalia Botnariuc(Harvard University), Irina Caraman, Mircea Cernat, Inga Chemencedji, Adrian Clipca, Serghei Doruc, Ghenadie Gorincioi, Sergiu Mura, Maria Pirtac, Irina Stancul, Diana Tcaciuc, Monique Albert, Iakovina Alexopoulou, Angel Arnaout, John Bartlett, Jay Engel, Sébastien Gilbert, Jeremy Parfitt, Harman Sekhon, George Thomas, Doris M. Rassl, Robert C. Rintoul, Carlo Bifulco, Raina Tamakawa, Walter J. Urba, Nicholas K. Hayward, Henri Timmers, Anna Antenucci, Francesco Facciolo, Gian Luca Grazi, Mirella Marino, Roberta Merola, Ronald R. de Krijger, Anne‐Paule Gimenez‐Roqueplo(Institute for Research in Biomedicine), Alain Piché, Simone Chevalier, Ginette McKercher, Kıvanç Birsoy, Gene H. Barnett(Genome Institute of Singapore), Cathy Brewer, Carol Farver, Theresa Naska, Nathan A. Pennell, Daniel P. Raymond, Cathy Schilero, Kathy Smolenski, Felicia Williams, Quaid Morris, Jeffrey A. Borgia, Michael J. Liptay, Mark Pool, Christopher W. Seder, Kerstin Junker, Larsson Omberg, Mikhail Dinkin(James S. McDonnell Foundation), George Manikhas, Domenico Alvaro, Maria Consiglia Bragazzi, Vincenzo Cardinale(Institute for Research in Biomedicine), Guido Carpino, Eugenio Gaudio, David Chesla, Sandra Cottingham, Michael Dubina, Fedor Moiseenko, Renumathy Dhanasekaran, Karl‐Friedrich Becker, Klaus‐Peter Janssen, Julia Slotta‐Huspenina, Mohamed H. Abdel‐Rahman, Dina Aziz, Sue Bell, Colleen M. Cebulla(Baylor College of Medicine), Amy Davis, Rebecca Duell(Broad Institute), J. Bradley Elder, Joe Hilty, Bahavna Kumar, James C. Lang, Norman L. Lehman(Broad Institute), Randy Mandt, Phuong Nguyen, Robert Pilarski, Karan Rai, Lynn Schoenfield, Kelly Senecal, Paul E. Wakely, Paul Hansen, Ronald M. Lechan, James F. Powers, Arthur S. Tischler, William E. Grizzle, Katherine C. Sexton, Alison Kastl, Joel Henderson, Sima P. Porten, Jens Waldmann, Martin Faßnacht, L. Sylvia, Dirk Schadendorf, Marta Couce, Markus Graefen, Hartwig Huland, Guido Sauter, Thorsten Schlomm, Ronald Simon, Pierre Tennstedt, Oluwole Olabode, Mark A. Nelson, Oliver F. Bathe, Peter R. Carroll, June M. Chan, Philip J. DiSaia, Pat Glenn, Robin Kate Kelley, Charles N. Landen, Joanna Phillips, Michael Prados, Jeffry Simko, Karen Smith‐McCune, Scott R. VandenBerg, Kevin K. Roggin, Ashley Fehrenbach, Ady Kendler, Suzanne Sifri(The University of Texas MD Anderson Cancer Center), Ruth Steele, Antonio Jimeno, Francis A. Carey, Ian Forgie(Broad Institute), Massimo Mannelli, Michael E. Carney, Brenda Hernandez, Benito Campos, Christel Herold‐Mende, Christin Jungk(James S. McDonnell Foundation), Andreas Unterberg, Andreas von Deimling, Aaron Bossler(Université Libre de Bruxelles), Joseph Galbraith, Laura Jacobus(The University of Texas MD Anderson Cancer Center), Michael Knudson, Tina Knutson(Broad Institute), Deqin Ma(Broad Institute), Mohammed Milhem, Rita Sigmund, Andrew K. Godwin, Rashna Madan, Howard G. Rosenthal, Clement Adebamowo, Sally N. Adebamowo, Alex Boussioutas, David G. Beer(Broad Institute), Thomas J. Giordano, Anne‐Marie Mes‐Masson(James S. McDonnell Foundation), Fred Saad, Thèrése Bocklage, Lisa M. Landrum, Robert S. Mannel, Kathleen Moore, Katherine Moxley, Russel Postier, Joan L. Walker(The University of Texas MD Anderson Cancer Center), Rosemary E. Zuna(Baylor College of Medicine), Michaël Feldman, Federico Valdivieso, Rajiv Dhir, James D. Luketich, Edna M. Mora Pinero, Mario Quintero-Aguilo, Carlos Gilberto Carlotti, José Sebastião dos Santos, Rafael Kemp, Ajith Sankarankuty, Daniela Pretti da Cunha Tirapelli, James W.F. Catto(Broad Institute), Kathy Agnew, Elizabeth M. Swisher, Jenette Creaney, Bruce Robinson, Carl Simon Shelley, Eryn M. Godwin, Sara Kendall, Cassaundra Shipman, Carol R. Bradford, Thomas E. Carey, Andrea Haddad, Jeffey Moyer, Lisa A. Peterson, Mark E. Prince, Laura S. Rozek, Gregory T. Wolf, Rayleen Bowman, Kwun M. Fong, Ian A. Yang, Robert J. Korst, W. Kimryn Rathmell, J. Leigh Fantacone-Campbell, Jeffrey A. Hooke, Albert J. Kovatich, Craig D. Shriver, John F. DiPersio, Bettina F. Drake, Ramaswamy Govindan, Sharon E. Heath, Timothy J. Ley(The University of Texas MD Anderson Cancer Center), Brian A. Van Tine, Peter Westervelt, Mark A. Rubin, Jung Il Lee, Natália D. Aredes, Armaz Mariamidze, Michael S. Lawrence(Broad Institute), Adam Godzik(Sanford Burnham Prebys Medical Discovery Institute), Núria López-Bigas(Institució Catalana de Recerca i Estudis Avançats), Joshua M. Stuart(University of California, Santa Cruz), David A. Wheeler(James S. McDonnell Foundation), Gad Getz(Broad Institute), Ken Chen(The University of Texas MD Anderson Cancer Center), Alexander J. Lazar(The University of Texas MD Anderson Cancer Center), Gordon B. Mills(The University of Texas MD Anderson Cancer Center), Rachel Karchin(Johns Hopkins University), Li Ding(Washington University in St. Louis)
Cited by 2,497Open Access
Abstract
Identifying molecular cancer drivers is critical for precision oncology. Multiple advanced algorithms to identify drivers now exist, but systematic attempts to combine and optimize them on large datasets are few. We report a PanCancer and PanSoftware analysis spanning 9,423 tumor exomes (comprising all 33 of The Cancer Genome Atlas projects) and using 26 computational tools to catalog driver genes and mutations. We identify 299 driver genes with implications regarding their anatomical sites and cancer/cell types. Sequence- and structure-based analyses identified >3,400 putative missense driver mutations supported by multiple lines of evidence. Experimental validation confirmed 60%-85% of predicted mutations as likely drivers. We found that >300 MSI tumors are associated with high PD-1/PD-L1, and 57% of tumors analyzed harbor putative clinically actionable events. Our study represents the most comprehensive discovery of cancer genes and mutations to date and will serve as a blueprint for future biological and clinical endeavors.
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