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Spectrum and prevalence of genetic predisposition in medulloblastoma: a retrospective genetic study and prospective validation in a clinical trial cohort
SM. Waszak, PA. Northcott, I. Buchhalter, GW. Robinson, C. Sutter, S. Groebner, KB. Grund, L. Brugières, DTW. Jones, KW. Pajtler, AS. Morrissy, M. Kool, D. Sturm, L. Chavez, A. Ernst, S. Brabetz, M. Hain, T. Zichner, M. Segura-Wang, J....
Jazyk angličtina Země Anglie, Velká Británie
Typ dokumentu časopisecké články, multicentrická studie, Research Support, N.I.H., Extramural, práce podpořená grantem, validační studie
Grantová podpora
T32 HL007901
NHLBI NIH HHS - United States
R01 CA159859
NCI NIH HHS - United States
U01 CA184898
NCI NIH HHS - United States
P30 CA021765
NCI NIH HHS - United States
R01 CA109467
NCI NIH HHS - United States
R01 CA148699
NCI NIH HHS - United States
U54 HD090255
NICHD NIH HHS - United States
P01 CA096832
NCI NIH HHS - United States
336045
European Research Council - International
143234
CIHR - Canada
A17197
Cancer Research UK - United Kingdom
FDN 143288
CIHR - Canada
NV15-30657A
MZ0
CEP - Centrální evidence projektů
Digitální knihovna NLK
Plný text - Článek
Zdroj
NLK
ProQuest Central
od 2000-09-01 do Před 2 měsíci
Nursing & Allied Health Database (ProQuest)
od 2000-09-01 do Před 2 měsíci
Health & Medicine (ProQuest)
od 2000-09-01 do Před 2 měsíci
Public Health Database (ProQuest)
od 2000-09-01 do Před 2 měsíci
- MeSH
- dědičnost MeSH
- dítě MeSH
- doba přežití bez progrese choroby MeSH
- dospělí MeSH
- fenotyp MeSH
- genetická predispozice k nemoci MeSH
- genetické testování metody MeSH
- kojenec MeSH
- lidé MeSH
- meduloblastom genetika mortalita patologie terapie MeSH
- metylace DNA * MeSH
- mladiství MeSH
- mladý dospělý MeSH
- modely genetické * MeSH
- mutační analýza DNA MeSH
- nádorové biomarkery genetika MeSH
- nádory mozečku genetika mortalita patologie terapie MeSH
- prediktivní hodnota testů MeSH
- předškolní dítě MeSH
- prospektivní studie MeSH
- reprodukovatelnost výsledků MeSH
- retrospektivní studie MeSH
- rizikové faktory MeSH
- rodokmen MeSH
- sekvenování exomu MeSH
- stanovení celkové genové exprese MeSH
- transkriptom MeSH
- zárodečné mutace * MeSH
- Check Tag
- dítě MeSH
- dospělí MeSH
- kojenec MeSH
- lidé MeSH
- mladiství MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- předškolní dítě MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- multicentrická studie MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- validační studie MeSH
BACKGROUND: Medulloblastoma is associated with rare hereditary cancer predisposition syndromes; however, consensus medulloblastoma predisposition genes have not been defined and screening guidelines for genetic counselling and testing for paediatric patients are not available. We aimed to assess and define these genes to provide evidence for future screening guidelines. METHODS: In this international, multicentre study, we analysed patients with medulloblastoma from retrospective cohorts (International Cancer Genome Consortium [ICGC] PedBrain, Medulloblastoma Advanced Genomics International Consortium [MAGIC], and the CEFALO series) and from prospective cohorts from four clinical studies (SJMB03, SJMB12, SJYC07, and I-HIT-MED). Whole-genome sequences and exome sequences from blood and tumour samples were analysed for rare damaging germline mutations in cancer predisposition genes. DNA methylation profiling was done to determine consensus molecular subgroups: WNT (MBWNT), SHH (MBSHH), group 3 (MBGroup3), and group 4 (MBGroup4). Medulloblastoma predisposition genes were predicted on the basis of rare variant burden tests against controls without a cancer diagnosis from the Exome Aggregation Consortium (ExAC). Previously defined somatic mutational signatures were used to further classify medulloblastoma genomes into two groups, a clock-like group (signatures 1 and 5) and a homologous recombination repair deficiency-like group (signatures 3 and 8), and chromothripsis was investigated using previously established criteria. Progression-free survival and overall survival were modelled for patients with a genetic predisposition to medulloblastoma. FINDINGS: We included a total of 1022 patients with medulloblastoma from the retrospective cohorts (n=673) and the four prospective studies (n=349), from whom blood samples (n=1022) and tumour samples (n=800) were analysed for germline mutations in 110 cancer predisposition genes. In our rare variant burden analysis, we compared these against 53 105 sequenced controls from ExAC and identified APC, BRCA2, PALB2, PTCH1, SUFU, and TP53 as consensus medulloblastoma predisposition genes according to our rare variant burden analysis and estimated that germline mutations accounted for 6% of medulloblastoma diagnoses in the retrospective cohort. The prevalence of genetic predispositions differed between molecular subgroups in the retrospective cohort and was highest for patients in the MBSHH subgroup (20% in the retrospective cohort). These estimates were replicated in the prospective clinical cohort (germline mutations accounted for 5% of medulloblastoma diagnoses, with the highest prevalence [14%] in the MBSHH subgroup). Patients with germline APC mutations developed MBWNT and accounted for most (five [71%] of seven) cases of MBWNT that had no somatic CTNNB1 exon 3 mutations. Patients with germline mutations in SUFU and PTCH1 mostly developed infant MBSHH. Germline TP53 mutations presented only in childhood patients in the MBSHH subgroup and explained more than half (eight [57%] of 14) of all chromothripsis events in this subgroup. Germline mutations in PALB2 and BRCA2 were observed across the MBSHH, MBGroup3, and MBGroup4 molecular subgroups and were associated with mutational signatures typical of homologous recombination repair deficiency. In patients with a genetic predisposition to medulloblastoma, 5-year progression-free survival was 52% (95% CI 40-69) and 5-year overall survival was 65% (95% CI 52-81); these survival estimates differed significantly across patients with germline mutations in different medulloblastoma predisposition genes. INTERPRETATION: Genetic counselling and testing should be used as a standard-of-care procedure in patients with MBWNT and MBSHH because these patients have the highest prevalence of damaging germline mutations in known cancer predisposition genes. We propose criteria for routine genetic screening for patients with medulloblastoma based on clinical and molecular tumour characteristics. FUNDING: German Cancer Aid; German Federal Ministry of Education and Research; German Childhood Cancer Foundation (Deutsche Kinderkrebsstiftung); European Research Council; National Institutes of Health; Canadian Institutes for Health Research; German Cancer Research Center; St Jude Comprehensive Cancer Center; American Lebanese Syrian Associated Charities; Swiss National Science Foundation; European Molecular Biology Organization; Cancer Research UK; Hertie Foundation; Alexander and Margaret Stewart Trust; V Foundation for Cancer Research; Sontag Foundation; Musicians Against Childhood Cancer; BC Cancer Foundation; Swedish Council for Health, Working Life and Welfare; Swedish Research Council; Swedish Cancer Society; the Swedish Radiation Protection Authority; Danish Strategic Research Council; Swiss Federal Office of Public Health; Swiss Research Foundation on Mobile Communication; Masaryk University; Ministry of Health of the Czech Republic; Research Council of Norway; Genome Canada; Genome BC; Terry Fox Research Institute; Ontario Institute for Cancer Research; Pediatric Oncology Group of Ontario; The Family of Kathleen Lorette and the Clark H Smith Brain Tumour Centre; Montreal Children's Hospital Foundation; The Hospital for Sick Children: Sonia and Arthur Labatt Brain Tumour Research Centre, Chief of Research Fund, Cancer Genetics Program, Garron Family Cancer Centre, MDT's Garron Family Endowment; BC Childhood Cancer Parents Association; Cure Search Foundation; Pediatric Brain Tumor Foundation; Brainchild; and the Government of Ontario.
2nd Department of Pediatrics Semmelweis University Budapest Hungary
Biotech Research and Innovation Centre Copenhagen Denmark
Broad Institute of Harvard and Massachusetts Institute of Technology Cambridge MA USA
Cancer Registry of Norway Oslo Norway
Clinical Cooperation Unit Neuropathology German Cancer Research Center Heidelberg Germany
Clinical Cooperation Unit Pediatric Oncology German Cancer Consortium Heidelberg Germany
Cnopf'sche Kinderklinik Nuremberg Germany
Comprehensive Cancer Center Mainfranken Würzburg Germany
Danish Cancer Society Research Center Copenhagen Denmark
Data Management Facility German Cancer Research Center Heidelberg Germany
Department of Children and Adolescents Oncology Gustave Roussy Cancer Campus Villejuif France
Department of Computational Biology St Jude Children's Research Hospital Memphis TN USA
Department of Developmental Neurobiology St Jude Children's Research Hospital Memphis TN USA
Department of Neurology Boston Children's Hospital and Harvard Medical School Boston MA USA
Department of Neuropathology Burdenko Neurosurgical Institute Moscow Russia
Department of Neuropathology Heidelberg University Hospital Heidelberg Germany
Department of Neuropathology Institute of Pathology University of Würzburg Würzburg Germany
Department of Neuropathology Sainte Anne Hospital Paris France
Department of Neurosurgery Asan Medical Center Seoul South Korea
Department of Neurosurgery University of Utah School of Medicine Salt Lake City UT USA
Department of Oncology St Jude Children's Research Hospital Memphis TN USA
Department of Paediatric Oncology Lady Cilento Children's Hospital South Brisbane QLD Australia
Department of Paediatric Oncology Sydney Children's Hospital Sydney NSW Australia
Department of Paediatric Oncology The Children's Hospital at Westmead Sydney NSW Australia
Department of Pathology Children's Memorial Health Institute Warsaw Poland
Department of Pediatric Hematology and Oncology Heidelberg University Hospital Heidelberg Germany
Department of Pediatric Hematology and Oncology Texas Children's Hospital Houston TX USA
Department of Pediatric Medicine Oslo University Hospital Oslo Norway
Department of Pediatrics McGill University Montreal QC Canada
Department of Pediatrics University of Toronto Toronto ON Canada
Developmental and Stem Cell Biology Program The Hospital for Sick Children Toronto ON Canada
Division of Applied Bioinformatics German Cancer Research Center Heidelberg Germany
Division of Haematology Oncology The Hospital for Sick Children Toronto ON Canada
Division of Molecular Genetics German Cancer Consortium Heidelberg Germany
Division of Molecular Genetics German Cancer Research Center Heidelberg Germany
Division of Neurosurgery The Hospital for Sick Children Toronto ON Canada
Division of Pediatric Neurooncology German Cancer Consortium Heidelberg Germany
Division of Theoretical Bioinformatics German Cancer Research Center Heidelberg Germany
European Molecular Biology Laboratory Genome Biology Unit Heidelberg Germany
Finsen Laboratory Rigshospitalet University of Copenhagen Copenhagen Denmark
Hopp Children's Cancer Center at the NCT Heidelberg Heidelberg Germany
Institute of Clinical Medicine University of Oslo Oslo Norway
Institute of Environmental Medicine Karolinska Institutet Stockholm Sweden
Institute of Human Genetics Heidelberg University Heidelberg Germany
Institute of Neuropathology University Hospital Basel Basel Switzerland
Michael Smith Genome Sciences Centre BC Cancer Agency Vancouver BC Canada
Oncology Clinic Finsen Centre Rigshospitalet University of Copenhagen Copenhagen Denmark
Pediatric Hematology and Oncology Hannover Medical School Hannover Germany
Pediatric Oncology and Hematology Pediatrics 3 University Hospital of Essen Essen Germany
Regional Centre for Applied Molecular Oncology Masaryk Memorial Cancer Institute Brno Czech Republic
Section of Environment and Radiation International Agency for Research on Cancer Lyon France
Swiss Tropical and Public Health Institute University of Basel Basel Switzerland
Unit of Survivorship Copenhagen Denmark
University Health Network Toronto General Hospital Toronto ON Canada
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- 520 9_
- $a BACKGROUND: Medulloblastoma is associated with rare hereditary cancer predisposition syndromes; however, consensus medulloblastoma predisposition genes have not been defined and screening guidelines for genetic counselling and testing for paediatric patients are not available. We aimed to assess and define these genes to provide evidence for future screening guidelines. METHODS: In this international, multicentre study, we analysed patients with medulloblastoma from retrospective cohorts (International Cancer Genome Consortium [ICGC] PedBrain, Medulloblastoma Advanced Genomics International Consortium [MAGIC], and the CEFALO series) and from prospective cohorts from four clinical studies (SJMB03, SJMB12, SJYC07, and I-HIT-MED). Whole-genome sequences and exome sequences from blood and tumour samples were analysed for rare damaging germline mutations in cancer predisposition genes. DNA methylation profiling was done to determine consensus molecular subgroups: WNT (MBWNT), SHH (MBSHH), group 3 (MBGroup3), and group 4 (MBGroup4). Medulloblastoma predisposition genes were predicted on the basis of rare variant burden tests against controls without a cancer diagnosis from the Exome Aggregation Consortium (ExAC). Previously defined somatic mutational signatures were used to further classify medulloblastoma genomes into two groups, a clock-like group (signatures 1 and 5) and a homologous recombination repair deficiency-like group (signatures 3 and 8), and chromothripsis was investigated using previously established criteria. Progression-free survival and overall survival were modelled for patients with a genetic predisposition to medulloblastoma. FINDINGS: We included a total of 1022 patients with medulloblastoma from the retrospective cohorts (n=673) and the four prospective studies (n=349), from whom blood samples (n=1022) and tumour samples (n=800) were analysed for germline mutations in 110 cancer predisposition genes. In our rare variant burden analysis, we compared these against 53 105 sequenced controls from ExAC and identified APC, BRCA2, PALB2, PTCH1, SUFU, and TP53 as consensus medulloblastoma predisposition genes according to our rare variant burden analysis and estimated that germline mutations accounted for 6% of medulloblastoma diagnoses in the retrospective cohort. The prevalence of genetic predispositions differed between molecular subgroups in the retrospective cohort and was highest for patients in the MBSHH subgroup (20% in the retrospective cohort). These estimates were replicated in the prospective clinical cohort (germline mutations accounted for 5% of medulloblastoma diagnoses, with the highest prevalence [14%] in the MBSHH subgroup). Patients with germline APC mutations developed MBWNT and accounted for most (five [71%] of seven) cases of MBWNT that had no somatic CTNNB1 exon 3 mutations. Patients with germline mutations in SUFU and PTCH1 mostly developed infant MBSHH. Germline TP53 mutations presented only in childhood patients in the MBSHH subgroup and explained more than half (eight [57%] of 14) of all chromothripsis events in this subgroup. Germline mutations in PALB2 and BRCA2 were observed across the MBSHH, MBGroup3, and MBGroup4 molecular subgroups and were associated with mutational signatures typical of homologous recombination repair deficiency. In patients with a genetic predisposition to medulloblastoma, 5-year progression-free survival was 52% (95% CI 40-69) and 5-year overall survival was 65% (95% CI 52-81); these survival estimates differed significantly across patients with germline mutations in different medulloblastoma predisposition genes. INTERPRETATION: Genetic counselling and testing should be used as a standard-of-care procedure in patients with MBWNT and MBSHH because these patients have the highest prevalence of damaging germline mutations in known cancer predisposition genes. We propose criteria for routine genetic screening for patients with medulloblastoma based on clinical and molecular tumour characteristics. FUNDING: German Cancer Aid; German Federal Ministry of Education and Research; German Childhood Cancer Foundation (Deutsche Kinderkrebsstiftung); European Research Council; National Institutes of Health; Canadian Institutes for Health Research; German Cancer Research Center; St Jude Comprehensive Cancer Center; American Lebanese Syrian Associated Charities; Swiss National Science Foundation; European Molecular Biology Organization; Cancer Research UK; Hertie Foundation; Alexander and Margaret Stewart Trust; V Foundation for Cancer Research; Sontag Foundation; Musicians Against Childhood Cancer; BC Cancer Foundation; Swedish Council for Health, Working Life and Welfare; Swedish Research Council; Swedish Cancer Society; the Swedish Radiation Protection Authority; Danish Strategic Research Council; Swiss Federal Office of Public Health; Swiss Research Foundation on Mobile Communication; Masaryk University; Ministry of Health of the Czech Republic; Research Council of Norway; Genome Canada; Genome BC; Terry Fox Research Institute; Ontario Institute for Cancer Research; Pediatric Oncology Group of Ontario; The Family of Kathleen Lorette and the Clark H Smith Brain Tumour Centre; Montreal Children's Hospital Foundation; The Hospital for Sick Children: Sonia and Arthur Labatt Brain Tumour Research Centre, Chief of Research Fund, Cancer Genetics Program, Garron Family Cancer Centre, MDT's Garron Family Endowment; BC Childhood Cancer Parents Association; Cure Search Foundation; Pediatric Brain Tumor Foundation; Brainchild; and the Government of Ontario.
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
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- 700 1_
- $a Lannering, Birgitta $u Department of Pediatrics, University of Gothenburg, The Queen Silvia Children's Hospital, Gothenburg, Sweden.
- 700 1_
- $a Schüz, Joachim $u Section of Environment and Radiation, International Agency for Research on Cancer, Lyon, France.
- 700 1_
- $a Johansen, Christoffer $u Oncology Clinic, Finsen Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark; Unit of Survivorship, Copenhagen, Denmark.
- 700 1_
- $a Andersen, Tina V $u Danish Cancer Society Research Center, Copenhagen, Denmark.
- 700 1_
- $a Röösli, Martin $u Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland; Swiss Tropical and Public Health Institute, University of Basel, Basel, Switzerland.
- 700 1_
- $a Kuehni, Claudia E $u Swiss Childhood Cancer Registry, Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland.
- 700 1_
- $a Grotzer, Michael $u Department of Pediatric Oncology, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.
- 700 1_
- $a Kjaerheim, Kristina $u Cancer Registry of Norway, Oslo, Norway.
- 700 1_
- $a Monoranu, Camelia M $u Comprehensive Cancer Center Mainfranken, Würzburg, Germany; Department of Neuropathology, Institute of Pathology, University of Würzburg, Würzburg, Germany.
- 700 1_
- $a Archer, Tenley C $u Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Neurology, Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.
- 700 1_
- $a Duke, Elizabeth $u Department of Neurology, Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.
- 700 1_
- $a Pomeroy, Scott L $u Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Neurology, Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.
- 700 1_
- $a Shelagh, Redmond $u Swiss Childhood Cancer Registry, Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland.
- 700 1_
- $a Frank, Stephan $u Institute of Neuropathology, University Hospital Basel, Basel, Switzerland.
- 700 1_
- $a Sumerauer, David $u Department of Pediatric Hematology and Oncology, 2nd Faculty of Medicine, University Hospital Motol, Charles University, Prague, Czech Republic.
- 700 1_
- $a Scheurlen, Wolfram $u Cnopf'sche Kinderklinik, Nuremberg, Germany.
- 700 1_
- $a Ryzhova, Marina V $u Department of Neuropathology, Burdenko Neurosurgical Institute, Moscow, Russia.
- 700 1_
- $a Milde, Till $u Department of Pediatric Hematology and Oncology, Heidelberg University Hospital, Heidelberg, Germany; Clinical Cooperation Unit Pediatric Oncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany; Hopp Children's Cancer Center at the NCT Heidelberg, Heidelberg, Germany.
- 700 1_
- $a Kratz, Christian P $u Pediatric Hematology and Oncology, Hannover Medical School, Hannover, Germany.
- 700 1_
- $a Samuel, David $u Valley Children's Hospital, Madera, CA, USA.
- 700 1_
- $a Zhang, Jinghui $u Department of Computational Biology, St Jude Children's Research Hospital, Memphis, TN, USA.
- 700 1_
- $a Solomon, David A $u Division of Neuropathology, Department of Pathology and Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, CA, USA.
- 700 1_
- $a Marra, Marco $u Michael Smith Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada.
- 700 1_
- $a Eils, Roland $u Division of Theoretical Bioinformatics, German Cancer Research Center, Heidelberg, Germany.
- 700 1_
- $a Bartram, Claus R $u Institute of Human Genetics, Heidelberg University, Heidelberg, Germany.
- 700 1_
- $a von Hoff, Katja $u Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Klinik für Pädiatrie mS Onkologie und Hämatologie, Charité, Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, Berlin, Germany.
- 700 1_
- $a Rutkowski, Stefan $u Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
- 700 1_
- $a Ramaswamy, Vijay $u Division of Haematology/Oncology, The Hospital for Sick Children, Toronto, ON, Canada; Department of Pediatrics, University of Toronto, Toronto, ON, Canada.
- 700 1_
- $a Gilbertson, Richard J $u Department of Oncology and Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, UK.
- 700 1_
- $a Korshunov, Andrey $u Department of Neuropathology, Heidelberg University Hospital, Heidelberg, Germany; Clinical Cooperation Unit Neuropathology, German Cancer Research Center, Heidelberg, Germany.
- 700 1_
- $a Taylor, Michael D $u Division of Neurosurgery, The Hospital for Sick Children, Toronto, ON, Canada.
- 700 1_
- $a Lichter, Peter $u Division of Molecular Genetics, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
- 700 1_
- $a Malkin, David $u Division of Haematology/Oncology, The Hospital for Sick Children, Toronto, ON, Canada; Department of Pediatrics, University of Toronto, Toronto, ON, Canada.
- 700 1_
- $a Gajjar, Amar $u Department of Oncology, St Jude Children's Research Hospital, Memphis, TN, USA.
- 700 1_
- $a Korbel, Jan O $u European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany.
- 700 1_
- $a Pfister, Stefan M $u Department of Pediatric Hematology and Oncology, Heidelberg University Hospital, Heidelberg, Germany; Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany; Hopp Children's Cancer Center at the NCT Heidelberg, Heidelberg, Germany. Electronic address: s.pfister@kitz-heidelberg.de.
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