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Genomic profiling of childhood tumor patient-derived xenograft models to enable rational clinical trial design

View ORCID ProfileJo Lynne Rokita, Komal S. Rathi, Maria F. Cardenas, Kristen A. Upton, Joy Jayaseelan, Katherine L. Cross, Jacob Pfeil, Laura E. Ritenour, Apexa Modi, Alvin Farrel, View ORCID ProfileGregory P. Way, View ORCID ProfileNathan M. Kendsersky, Khushbu Patel, View ORCID ProfileGonzalo Lopez, View ORCID ProfileZalman Vaksman, View ORCID ProfileChelsea Mayoh, Jonas Nance, Kristyn McCoy, View ORCID ProfileMichelle Haber, Kathryn Evans, Hannah McCalmont, Katerina Bendak, Julia W. Böhm, Glenn M. Marshall, Vanessa Tyrrell, View ORCID ProfileKarthik Kalletla, Frank K. Braun, Lin Qi, Yunchen Du, Huiyuan Zhang, Holly B. Lindsay, Sibo Zhao, Jack Shu, Patricia Baxter, Christopher Morton, Dias Kurmashev, Siyuan Zheng, Yidong Chen, Jay Bowen, Anthony C. Bryan, Kristen M. Leraas, Sara E. Coppens, HarshaVardhan Doddapaneni, Zeineen Momin, Wendong Zhang, Gregory I. Sacks, Lori S. Hart, Kateryna Krytska, Yael P. Mosse, Gregory J. Gatto, Yolanda Sanchez, View ORCID ProfileCasey S. Greene, Sharon J. Diskin, Olena Morozova Vaske, View ORCID ProfileDavid Haussler, Julie M. Gastier-Foster, E. Anders Kolb, Richard Gorlick, Xiao-Nan Li, C. Patrick Reynolds, Raushan T. Kurmasheva, Peter J. Houghton, Malcolm A. Smith, Richard B. Lock, Pichai Raman, David A. Wheeler, John M. Maris
doi: https://doi.org/10.1101/566455
Jo Lynne Rokita
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
3Center for Data-Driven Discovery in Biomedicine, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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  • ORCID record for Jo Lynne Rokita
Komal S. Rathi
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
3Center for Data-Driven Discovery in Biomedicine, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Maria F. Cardenas
4Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA
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Kristen A. Upton
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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Joy Jayaseelan
4Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA
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Katherine L. Cross
5Guardian Forensic Sciences, Abington, PA, 19001, USA
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Jacob Pfeil
6UC Santa Cruz Genomics Institute, Santa Cruz, CA, 95064, USA
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Laura E. Ritenour
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
7Cell and Molecular Biology Graduate Group, University of Pennsylvania, Philadelphia, PA, 19104, USA
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Apexa Modi
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
8Genomics and Computational Biology Graduate Group, University of Pennsylvania, Philadelphia, PA, 19104, USA
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Alvin Farrel
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Gregory P. Way
8Genomics and Computational Biology Graduate Group, University of Pennsylvania, Philadelphia, PA, 19104, USA
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Nathan M. Kendsersky
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
9Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania, Philadelphia, PA, 19104, USA
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Khushbu Patel
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Gonzalo Lopez
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Zalman Vaksman
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Chelsea Mayoh
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Jonas Nance
11Cancer Center, Texas Tech University Health Sciences Center School of Medicine, Lubbock, TX, 79430, USA
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Kristyn McCoy
11Cancer Center, Texas Tech University Health Sciences Center School of Medicine, Lubbock, TX, 79430, USA
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Michelle Haber
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Kathryn Evans
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Hannah McCalmont
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Katerina Bendak
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Julia W. Böhm
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
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Glenn M. Marshall
10Children’s Cancer Institute, School of Women’s and Children’s Health, UNSW Sydney, Australia
12Sydney Children’s Hospital, Sydney, Australia
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Vanessa Tyrrell
13Children’s Cancer Institute, Australia
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Karthik Kalletla
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
3Center for Data-Driven Discovery in Biomedicine, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Frank K. Braun
14Texas Children’s Cancer and Hematology Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Lin Qi
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Yunchen Du
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Huiyuan Zhang
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Holly B. Lindsay
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Sibo Zhao
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Jack Shu
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Patricia Baxter
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
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Christopher Morton
17Department of Surgery, St. Jude Children’s Research Hospital, Memphis, TN, 38105, USA
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Dias Kurmashev
18Greehey Children’s Cancer Research Institute, University of Texas Health Science Center, San Antonio, TX, 78229, USA
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Siyuan Zheng
18Greehey Children’s Cancer Research Institute, University of Texas Health Science Center, San Antonio, TX, 78229, USA
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Yidong Chen
18Greehey Children’s Cancer Research Institute, University of Texas Health Science Center, San Antonio, TX, 78229, USA
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Jay Bowen
19The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA
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Anthony C. Bryan
19The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA
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Kristen M. Leraas
19The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA
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Sara E. Coppens
19The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA
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HarshaVardhan Doddapaneni
4Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA
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Zeineen Momin
4Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA
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Wendong Zhang
20Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX, 77030, USA
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Gregory I. Sacks
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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Lori S. Hart
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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Kateryna Krytska
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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Yael P. Mosse
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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Gregory J. Gatto
21Department of Global Health Technologies, RTI International, Research Triangle Park, NC 27709, USA
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Yolanda Sanchez
22Department of Molecular and Systems Biology, Geisel School of Medicine at Dartmouth, Hanover, NH, 03755, USA
23Norris Cotton Cancer Center, Lebanon, NH, 03766, USA
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Casey S. Greene
24Childhood Cancer Data Lab, Alex’s Lemonade Stand Foundation, Philadelphia, PA, 19102, USA
9Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania, Philadelphia, PA, 19104, USA
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Sharon J. Diskin
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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Olena Morozova Vaske
25Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, CA, 95064, USA
6UC Santa Cruz Genomics Institute, Santa Cruz, CA, 95064, USA
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David Haussler
6UC Santa Cruz Genomics Institute, Santa Cruz, CA, 95064, USA
26Howard Hughes Medical Institute, University of California, Santa Cruz, CA, 95064, USA
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Julie M. Gastier-Foster
19The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA
27The Ohio State University College of Medicine, Departments of Pathology and Pediatrics, Columbus, OH, 43210, USA
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E. Anders Kolb
28Department of Pediatrics, Sidney Kimmel Medical College at Thomas Jefferson University, Philadelphia, PA, 19107, USA
29Nemours Center for Cancer and Blood Disorders, Nemours/Alfred I. duPont Hospital for Children, Wilmington, DE, 19803, USA
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Richard Gorlick
20Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX, 77030, USA
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Xiao-Nan Li
15Preclinical Neurooncology Research Program, Texas Children’s Cancer Research Center, Texas Children’s Hospital, Houston, TX, 77030, USA
16Department of Pediatrics, Baylor College of Medicine, Houston, TX, 77030, USA
30Division of Hematology, Oncology, Neuro-oncology and Stem Cell Transplant, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, 60611, USA
31Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA
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C. Patrick Reynolds
11Cancer Center, Texas Tech University Health Sciences Center School of Medicine, Lubbock, TX, 79430, USA
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Raushan T. Kurmasheva
18Greehey Children’s Cancer Research Institute, University of Texas Health Science Center, San Antonio, TX, 78229, USA
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Peter J. Houghton
18Greehey Children’s Cancer Research Institute, University of Texas Health Science Center, San Antonio, TX, 78229, USA
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Malcolm A. Smith
32National Cancer Institute, National Institutes of Health, Bethesda, MD, 20814, USA
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Richard B. Lock
13Children’s Cancer Institute, Australia
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Pichai Raman
2Department of Bioinformatics and Health Informatics, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
3Center for Data-Driven Discovery in Biomedicine, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA
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David A. Wheeler
4Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA
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John M. Maris
1Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-4318, USA
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  • For correspondence: maris@email.chop.edu
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Summary

Accelerating cures for children with cancer remains an immediate challenge due to extensive oncogenic heterogeneity between and within histologies, distinct molecular mechanisms evolving between diagnosis and relapsed disease, and limited therapeutic options. To systematically prioritize and rationally test novel agents in preclinical murine models, researchers within the Pediatric Preclinical Testing Consortium are continuously developing patient-derived xenografts (PDXs) from high-risk childhood cancers, many refractory to current standard-of-care treatments. Here, we genomically characterize 261 PDX models from 29 unique pediatric cancer malignancies and demonstrate faithful recapitulation of histologies, subtypes, and refine our understanding of relapsed disease. Expression and mutational signatures are used to classify tumors for TP53 and NF1 inactivation, as well as impaired DNA repair. We anticipate that these data will serve as a resource for pediatric oncology drug development and guide rational clinical trial design for children with cancer.

Highlights

  • Multiplatform genomic analysis defines landscape of 261 pediatric cancer patient derived xenograft (PDX) models

  • Pediatric patient derived xenografts faithfully recapitulate relapsed disease

  • Inferred TP53 pathway inactivation correlates with pediatric cancer copy number burden

  • Somatic mutational signatures predict impaired DNA repair across multiple histologies

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Genomic profiling of childhood tumor patient-derived xenograft models to enable rational clinical trial design
Jo Lynne Rokita, Komal S. Rathi, Maria F. Cardenas, Kristen A. Upton, Joy Jayaseelan, Katherine L. Cross, Jacob Pfeil, Laura E. Ritenour, Apexa Modi, Alvin Farrel, Gregory P. Way, Nathan M. Kendsersky, Khushbu Patel, Gonzalo Lopez, Zalman Vaksman, Chelsea Mayoh, Jonas Nance, Kristyn McCoy, Michelle Haber, Kathryn Evans, Hannah McCalmont, Katerina Bendak, Julia W. Böhm, Glenn M. Marshall, Vanessa Tyrrell, Karthik Kalletla, Frank K. Braun, Lin Qi, Yunchen Du, Huiyuan Zhang, Holly B. Lindsay, Sibo Zhao, Jack Shu, Patricia Baxter, Christopher Morton, Dias Kurmashev, Siyuan Zheng, Yidong Chen, Jay Bowen, Anthony C. Bryan, Kristen M. Leraas, Sara E. Coppens, HarshaVardhan Doddapaneni, Zeineen Momin, Wendong Zhang, Gregory I. Sacks, Lori S. Hart, Kateryna Krytska, Yael P. Mosse, Gregory J. Gatto, Yolanda Sanchez, Casey S. Greene, Sharon J. Diskin, Olena Morozova Vaske, David Haussler, Julie M. Gastier-Foster, E. Anders Kolb, Richard Gorlick, Xiao-Nan Li, C. Patrick Reynolds, Raushan T. Kurmasheva, Peter J. Houghton, Malcolm A. Smith, Richard B. Lock, Pichai Raman, David A. Wheeler, John M. Maris
bioRxiv 566455; doi: https://doi.org/10.1101/566455
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Genomic profiling of childhood tumor patient-derived xenograft models to enable rational clinical trial design
Jo Lynne Rokita, Komal S. Rathi, Maria F. Cardenas, Kristen A. Upton, Joy Jayaseelan, Katherine L. Cross, Jacob Pfeil, Laura E. Ritenour, Apexa Modi, Alvin Farrel, Gregory P. Way, Nathan M. Kendsersky, Khushbu Patel, Gonzalo Lopez, Zalman Vaksman, Chelsea Mayoh, Jonas Nance, Kristyn McCoy, Michelle Haber, Kathryn Evans, Hannah McCalmont, Katerina Bendak, Julia W. Böhm, Glenn M. Marshall, Vanessa Tyrrell, Karthik Kalletla, Frank K. Braun, Lin Qi, Yunchen Du, Huiyuan Zhang, Holly B. Lindsay, Sibo Zhao, Jack Shu, Patricia Baxter, Christopher Morton, Dias Kurmashev, Siyuan Zheng, Yidong Chen, Jay Bowen, Anthony C. Bryan, Kristen M. Leraas, Sara E. Coppens, HarshaVardhan Doddapaneni, Zeineen Momin, Wendong Zhang, Gregory I. Sacks, Lori S. Hart, Kateryna Krytska, Yael P. Mosse, Gregory J. Gatto, Yolanda Sanchez, Casey S. Greene, Sharon J. Diskin, Olena Morozova Vaske, David Haussler, Julie M. Gastier-Foster, E. Anders Kolb, Richard Gorlick, Xiao-Nan Li, C. Patrick Reynolds, Raushan T. Kurmasheva, Peter J. Houghton, Malcolm A. Smith, Richard B. Lock, Pichai Raman, David A. Wheeler, John M. Maris
bioRxiv 566455; doi: https://doi.org/10.1101/566455

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