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Implications of TP53 Allelic State for Genome Stability, Clinical Presentation and Outcomes in Myelodysplastic Syndromes

View ORCID ProfileElsa Bernard, Yasuhito Nannya, Robert P. Hasserjian, Sean M. Devlin, Heinz Tuechler, Juan S. Medina-Martinez, View ORCID ProfileTetsuichi Yoshizato, Yusuke Shiozawa, Ryunosuke Saiki, Luca Malcovati, Max F. Levine, Juan E. Arango, Yangyu Zhou, Francesc Sole, Catherine A. Cargo, Detlef Haase, Maria Creignou, Ulrich Germing, Yanming Zhang, Gunes Gundem, Araxe Sarian, Arjan A. van de Loosdrecht, Martin Jädersten, Magnus Tobiasson, Olivier Kosmider, Matilde Y. Follo, Felicitas Thol, Ronald F. Pinheiro, Valeria Santini, Ioannis Kotsianidis, Jacqueline Boultwood, Fabio P.S. Santos, Julie Schanz, Senji Kasahara, Takayuki Ishikawa, Hisashi Tsurumi, Akifumi Takaori-Kondo, Toru Kiguchi, Chantana Polprasert, John M. Bennett, Virginia M. Klimek, Michael R. Savona, Monika Belickova, Christina Ganster, Laura Palomo, Guillermo Sanz, Lionel Ades, Matteo Giovanni Della Porta, Alexandra G Smith, Yesenia Werner, Minal Patel, Agnès Viale, Katelynd Vanness, Donna S. Neuberg, Kristen E. Stevenson, Kamal Menghrajani, Kelly L. Bolton, Pierre Fenaux, Andrea Pellagatti, Uwe Platzbecker, Michael Heuser, Peter Valent, Shigeru Chiba, Yasushi Miyazaki, Carlo Finelli, Maria Teresa Voso, Lee-Yung Shih, Michaela Fontenay, Joop H. Jansen, José Cervera, Yoshiko Atsuta, Norbert Gattermann, Benjamin L. Ebert, Rafael Bejar, Peter L. Greenberg, Mario Cazzola, Eva Hellström-Lindberg, Seishi Ogawa, Elli Papaemmanuil
doi: https://doi.org/10.1101/2019.12.19.868844
Elsa Bernard
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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  • ORCID record for Elsa Bernard
Yasuhito Nannya
3Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan
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Robert P. Hasserjian
4Department of Pathology, Massachusetts General Hospital, Boston, MA, USA
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Sean M. Devlin
5Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Heinz Tuechler
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Juan S. Medina-Martinez
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Tetsuichi Yoshizato
3Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan
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Yusuke Shiozawa
3Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan
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Ryunosuke Saiki
3Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan
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Luca Malcovati
6Department of Molecular Medicine, University of Pavia, Pavia. Italy
7Department of Hematology, IRCCS Fondazione Policlinico S. Matteo, Pavia. Italy
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Max F. Levine
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Juan E. Arango
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Yangyu Zhou
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Francesc Sole
8MDS Group, Institut de Recerca Contra la Leucèmia Josep Carreras, Barcelona, Spain
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Catherine A. Cargo
9Haematological Malignancy Diagnostic Service, St James’s University Hospital, Leeds, United Kingdom
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Detlef Haase
10Clinics of Hematology and Medical Oncology, University Medical Center. Göttingen, Germany
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Maria Creignou
11Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden
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Ulrich Germing
12Department of Hematology, Oncology and Clinical Immunology, Heinrich Heine University, Düsseldorf, Germany
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Yanming Zhang
13Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Gunes Gundem
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Araxe Sarian
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Arjan A. van de Loosdrecht
14Department of Hematology, VU University Medical Center Amsterdam, The Netherlands
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Martin Jädersten
11Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden
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Magnus Tobiasson
11Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden
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Olivier Kosmider
15Department of Hematology, Assistance Publique-Hôpitaux de Paris, Hôpital Cochin and Université de Paris, Université Paris Descartes, Paris, France
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Matilde Y. Follo
16Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy
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Felicitas Thol
17Department of Hematology, Hemostasis, Oncology and Stem Cell Transplantation, Hannover Medical School, Hannover, Germany
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Ronald F. Pinheiro
18Drug Research and Development Center, Federal University of Ceara, Ceara, Brazil
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Valeria Santini
19MDS Unit, Hematology, AOU Careggi, University of Florence, Italy
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Ioannis Kotsianidis
20Department of Hematology, Democritus University of Thrace Medical School, Alexandroupolis, Greece
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Jacqueline Boultwood
21Radcliffe Department of Medicine, University of Oxford and Oxford BRC Haematology Theme, Oxford, United Kingdom
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Fabio P.S. Santos
22Oncology-Hematology Center, Hospital Israelita Albert Einstein, São Paulo, Brazil
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Julie Schanz
10Clinics of Hematology and Medical Oncology, University Medical Center. Göttingen, Germany
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Senji Kasahara
23Department of Hematology, Gifu Municipal Hospital, Gifu, Japan
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Takayuki Ishikawa
24Department of Hematology, Kobe City Medical Center General Hospital, Kobe, Japan
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Hisashi Tsurumi
25Department of Hematology, Gifu University Graduate School of Medicine, Gifu, Japan
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Akifumi Takaori-Kondo
26Department of Hematology and Oncology, Graduate School of Medicine, Kyoto University, Japan
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Toru Kiguchi
27Department of Hematology, Chugoku Central Hospital, Fukuyama, Japan
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Chantana Polprasert
28Department of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Bangkok, Thailand
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John M. Bennett
29Lab. Medicine and Pathology, Hematology/Oncology, University of Rochester Medical Center, Rochester, NY, USA
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Virginia M. Klimek
30Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Michael R. Savona
31Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA
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Monika Belickova
32Department of Genomics, Institute of Hematology and Blood Transfusion, Prague, Czech Republic
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Christina Ganster
10Clinics of Hematology and Medical Oncology, University Medical Center. Göttingen, Germany
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Laura Palomo
8MDS Group, Institut de Recerca Contra la Leucèmia Josep Carreras, Barcelona, Spain
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Guillermo Sanz
33Department of Hematology, Hospital Universitario y Politécnico La Fe, Valencia, Spain
34CIBERONC, Instituto de Salud Carlos III, Madrid, Spain
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Lionel Ades
35Department of Hematology, hôpital St Louis, and Paris University, Paris, France
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Matteo Giovanni Della Porta
36Cancer Center, Humanitas Research Hospital & Humanitas University, Milan Italy
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Alexandra G Smith
37Department of Health Sciences, University of York, United Kingdom
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Yesenia Werner
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Minal Patel
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Agnès Viale
38Integrated Genomics Operation, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Katelynd Vanness
38Integrated Genomics Operation, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Donna S. Neuberg
39Department of Data Sciences, Dana-Farber Cancer Institute, Boston, MA, USA
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Kristen E. Stevenson
39Department of Data Sciences, Dana-Farber Cancer Institute, Boston, MA, USA
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Kamal Menghrajani
30Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Kelly L. Bolton
30Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Pierre Fenaux
35Department of Hematology, hôpital St Louis, and Paris University, Paris, France
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Andrea Pellagatti
21Radcliffe Department of Medicine, University of Oxford and Oxford BRC Haematology Theme, Oxford, United Kingdom
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Uwe Platzbecker
40Medical Clinic and Policlinic 1, Hematology and Cellular Therapy, University of Leipzig, Leipzig, Germany
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Michael Heuser
17Department of Hematology, Hemostasis, Oncology and Stem Cell Transplantation, Hannover Medical School, Hannover, Germany
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Peter Valent
41Department of Internal Medicine I, Division of Hematology and Hemostaseology and Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Austria
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Shigeru Chiba
42Department of Hematology, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan
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Yasushi Miyazaki
43Department of Hematology, Atomic Bomb Disease Institute, Nagasaki University, Japan
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Carlo Finelli
44Institute of Hematology, S.Orsola-Malpighi University Hospital, Bologna, Italy
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Maria Teresa Voso
45MDS Cooperative Group GROM-L, Department of Biomedicine and Prevention, Tor Vergata University, Rome, Italy
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Lee-Yung Shih
46Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taiwan
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Michaela Fontenay
15Department of Hematology, Assistance Publique-Hôpitaux de Paris, Hôpital Cochin and Université de Paris, Université Paris Descartes, Paris, France
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Joop H. Jansen
47Laboratory Hematology, Deptartment LABGK, Radboud University Medical Centre, Nijmegen, The Netherlands
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José Cervera
48Department of Hematology and Genetics Unit, University Hospital La Fe, Valencia, Spain
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Yoshiko Atsuta
49Japanese Data Center for Hematopoietic Cell Transplantation, Nagoya, Japan
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Norbert Gattermann
12Department of Hematology, Oncology and Clinical Immunology, Heinrich Heine University, Düsseldorf, Germany
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Benjamin L. Ebert
50Department of Medical Oncology and Howard Hughes Medical Institute, Dana-Farber Cancer Center, Boston, MA, USA
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Rafael Bejar
51UC San Diego Moores Cancer Center, La Jolla, California, USA
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Peter L. Greenberg
52Stanford University Cancer Institute, Stanford, CA, USA
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Mario Cazzola
6Department of Molecular Medicine, University of Pavia, Pavia. Italy
7Department of Hematology, IRCCS Fondazione Policlinico S. Matteo, Pavia. Italy
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Eva Hellström-Lindberg
11Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden
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Seishi Ogawa
3Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan
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Elli Papaemmanuil
1Computational Oncology Service, Department of Epidemiology & Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
2Center for Hematologic Malignancies, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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  • For correspondence: papaemme@mskcc.org
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ABSTRACT

TP53 mutations are associated with poor clinical outcomes and treatment resistance in myelodysplastic syndromes. However, the biological and clinical relevance of the underlying mono- or bi-allelic state of the mutations is unclear. We analyzed 3,324 MDS patients for TP53 mutations and allelic imbalances of the TP53 locus and found that 1 in 3 TP53-mutated patients had mono-allelic targeting of the gene whereas 2 in 3 had multiple hits consistent with bi-allelic targeting. The established associations for TP53 with complex karyotype, high-risk presentation, poor survival and rapid leukemic transformation were specific to patients with multi-hit state only. TP53 multi-hit state predicted risk of death and leukemic transformation independently of the Revised International Prognostic Scoring System, while mono-allelic patients did not differ from TP53 wild-type patients. The separation by allelic state was retained in therapy-related MDS. Findings were validated in a cohort of 1,120 patients. Ascertainment of TP53 allelic state is critical for diagnosis, risk estimation and prognostication precision in MDS, and future correlative studies of treatment response should consider TP53 allelic state.

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  • ↵* Shared senior authorship

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Implications of TP53 Allelic State for Genome Stability, Clinical Presentation and Outcomes in Myelodysplastic Syndromes
Elsa Bernard, Yasuhito Nannya, Robert P. Hasserjian, Sean M. Devlin, Heinz Tuechler, Juan S. Medina-Martinez, Tetsuichi Yoshizato, Yusuke Shiozawa, Ryunosuke Saiki, Luca Malcovati, Max F. Levine, Juan E. Arango, Yangyu Zhou, Francesc Sole, Catherine A. Cargo, Detlef Haase, Maria Creignou, Ulrich Germing, Yanming Zhang, Gunes Gundem, Araxe Sarian, Arjan A. van de Loosdrecht, Martin Jädersten, Magnus Tobiasson, Olivier Kosmider, Matilde Y. Follo, Felicitas Thol, Ronald F. Pinheiro, Valeria Santini, Ioannis Kotsianidis, Jacqueline Boultwood, Fabio P.S. Santos, Julie Schanz, Senji Kasahara, Takayuki Ishikawa, Hisashi Tsurumi, Akifumi Takaori-Kondo, Toru Kiguchi, Chantana Polprasert, John M. Bennett, Virginia M. Klimek, Michael R. Savona, Monika Belickova, Christina Ganster, Laura Palomo, Guillermo Sanz, Lionel Ades, Matteo Giovanni Della Porta, Alexandra G Smith, Yesenia Werner, Minal Patel, Agnès Viale, Katelynd Vanness, Donna S. Neuberg, Kristen E. Stevenson, Kamal Menghrajani, Kelly L. Bolton, Pierre Fenaux, Andrea Pellagatti, Uwe Platzbecker, Michael Heuser, Peter Valent, Shigeru Chiba, Yasushi Miyazaki, Carlo Finelli, Maria Teresa Voso, Lee-Yung Shih, Michaela Fontenay, Joop H. Jansen, José Cervera, Yoshiko Atsuta, Norbert Gattermann, Benjamin L. Ebert, Rafael Bejar, Peter L. Greenberg, Mario Cazzola, Eva Hellström-Lindberg, Seishi Ogawa, Elli Papaemmanuil
bioRxiv 2019.12.19.868844; doi: https://doi.org/10.1101/2019.12.19.868844
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Implications of TP53 Allelic State for Genome Stability, Clinical Presentation and Outcomes in Myelodysplastic Syndromes
Elsa Bernard, Yasuhito Nannya, Robert P. Hasserjian, Sean M. Devlin, Heinz Tuechler, Juan S. Medina-Martinez, Tetsuichi Yoshizato, Yusuke Shiozawa, Ryunosuke Saiki, Luca Malcovati, Max F. Levine, Juan E. Arango, Yangyu Zhou, Francesc Sole, Catherine A. Cargo, Detlef Haase, Maria Creignou, Ulrich Germing, Yanming Zhang, Gunes Gundem, Araxe Sarian, Arjan A. van de Loosdrecht, Martin Jädersten, Magnus Tobiasson, Olivier Kosmider, Matilde Y. Follo, Felicitas Thol, Ronald F. Pinheiro, Valeria Santini, Ioannis Kotsianidis, Jacqueline Boultwood, Fabio P.S. Santos, Julie Schanz, Senji Kasahara, Takayuki Ishikawa, Hisashi Tsurumi, Akifumi Takaori-Kondo, Toru Kiguchi, Chantana Polprasert, John M. Bennett, Virginia M. Klimek, Michael R. Savona, Monika Belickova, Christina Ganster, Laura Palomo, Guillermo Sanz, Lionel Ades, Matteo Giovanni Della Porta, Alexandra G Smith, Yesenia Werner, Minal Patel, Agnès Viale, Katelynd Vanness, Donna S. Neuberg, Kristen E. Stevenson, Kamal Menghrajani, Kelly L. Bolton, Pierre Fenaux, Andrea Pellagatti, Uwe Platzbecker, Michael Heuser, Peter Valent, Shigeru Chiba, Yasushi Miyazaki, Carlo Finelli, Maria Teresa Voso, Lee-Yung Shih, Michaela Fontenay, Joop H. Jansen, José Cervera, Yoshiko Atsuta, Norbert Gattermann, Benjamin L. Ebert, Rafael Bejar, Peter L. Greenberg, Mario Cazzola, Eva Hellström-Lindberg, Seishi Ogawa, Elli Papaemmanuil
bioRxiv 2019.12.19.868844; doi: https://doi.org/10.1101/2019.12.19.868844

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