Low-frequency variation near common germline susceptibility loci are associated with risk of Ewing sarcoma.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2020
Historique:
received: 24 02 2020
accepted: 03 08 2020
entrez: 4 9 2020
pubmed: 4 9 2020
medline: 21 10 2020
Statut: epublish

Résumé

Ewing sarcoma (EwS) is a rare, aggressive solid tumor of childhood, adolescence and young adulthood associated with pathognomonic EWSR1-ETS fusion oncoproteins altering transcriptional regulation. Genome-wide association studies (GWAS) have identified 6 common germline susceptibility loci but have not investigated low-frequency inherited variants with minor allele frequencies below 5% due to limited genotyped cases of this rare tumor. We investigated the contribution of rare and low-frequency variation to EwS susceptibility in the largest EwS genome-wide association study to date (733 EwS cases and 1,346 unaffected controls of European ancestry). We identified two low-frequency variants, rs112837127 and rs2296730, on chromosome 20 that were associated with EwS risk (OR = 0.186 and 2.038, respectively; P-value < 5×10-8) and located near previously reported common susceptibility loci. After adjusting for the most associated common variant at the locus, only rs112837127 remained a statistically significant independent signal (OR = 0.200, P-value = 5.84×10-8). These findings suggest rare variation residing on common haplotypes are important contributors to EwS risk. Motivate future targeted sequencing studies for a comprehensive evaluation of low-frequency and rare variation around common EwS susceptibility loci.

Sections du résumé

BACKGROUND
Ewing sarcoma (EwS) is a rare, aggressive solid tumor of childhood, adolescence and young adulthood associated with pathognomonic EWSR1-ETS fusion oncoproteins altering transcriptional regulation. Genome-wide association studies (GWAS) have identified 6 common germline susceptibility loci but have not investigated low-frequency inherited variants with minor allele frequencies below 5% due to limited genotyped cases of this rare tumor.
METHODS
We investigated the contribution of rare and low-frequency variation to EwS susceptibility in the largest EwS genome-wide association study to date (733 EwS cases and 1,346 unaffected controls of European ancestry).
RESULTS
We identified two low-frequency variants, rs112837127 and rs2296730, on chromosome 20 that were associated with EwS risk (OR = 0.186 and 2.038, respectively; P-value < 5×10-8) and located near previously reported common susceptibility loci. After adjusting for the most associated common variant at the locus, only rs112837127 remained a statistically significant independent signal (OR = 0.200, P-value = 5.84×10-8).
CONCLUSIONS
These findings suggest rare variation residing on common haplotypes are important contributors to EwS risk.
IMPACT
Motivate future targeted sequencing studies for a comprehensive evaluation of low-frequency and rare variation around common EwS susceptibility loci.

Identifiants

pubmed: 32881892
doi: 10.1371/journal.pone.0237792
pii: PONE-D-20-05330
pmc: PMC7470401
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0237792

Subventions

Organisme : NCI NIH HHS
ID : U24 CA055727
Pays : United States

Déclaration de conflit d'intérêts

The authors have read the journal's policy and the authors of this manuscript have the following competing interests: Leidos Biomedical Research Inc. and Information Management Services, Inc. provided salaries for authors J.M., E.K., C.L.D., L.B., K.J., M.M., K.W., and W.Z. This does not alter our adherence to PLOS ONE policies on sharing data and materials. There are no patents, products in development or marketed products to declare.

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Auteurs

Shu-Hong Lin (SH)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Joshua N Sampson (JN)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Thomas G P Grünewald (TGP)

Max-Eder Research Group for Pediatric Sarcoma Biology, Ludwig Maximilians Universität (LMU), Munich, Germany.
Division of Translational Pediatric Sarcoma Research, German Cancer Research Center (DKFZ), German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Pathology, Heidelberg University Hospital, Heidelberg, Germany.

Didier Surdez (D)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.

Stephanie Reynaud (S)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Olivier Mirabeau (O)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.
SIREDO Oncology Centre, Institut Curie, Paris, France.

Eric Karlins (E)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Rebeca Alba Rubio (RA)

Max-Eder Research Group for Pediatric Sarcoma Biology, Ludwig Maximilians Universität (LMU), Munich, Germany.

Sakina Zaidi (S)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.
SIREDO Oncology Centre, Institut Curie, Paris, France.

Sandrine Grossetête-Lalami (S)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.
SIREDO Oncology Centre, Institut Curie, Paris, France.

Stelly Ballet (S)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Eve Lapouble (E)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Valérie Laurence (V)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Jean Michon (J)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Gaelle Pierron (G)

SIREDO Oncology Centre, Institut Curie, Paris, France.

Heinrich Kovar (H)

Children's Cancer Research Institute, St. Anna Kinderkrebsforschung, Vienna, Austria.

Udo Kontny (U)

Division of Pediatric Hematology, Oncology and Stem Cell Transplantation, Uniklinik RWTH Aachen, Aachen, Germany.

Anna González-Neira (A)

Human Genotyping Unit-CeGen, Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain.

Javier Alonso (J)

Unidad de Tumores Solidos Infantiles (IIER-ISCIII) & Centro de Investigación Biomédica en Red de Enfermedades Raras (CB06/07/1009; CIBERER-ISCIII), Instituto de Salud Carlos III, Majadahonda, Spain.

Ana Patino-Garcia (A)

Laboratory of Pediatrics, University Clinic of Navarra, Program in Solid Tumors, Center for Applied Medical Research (CIMA) and Navarra's Health Research Institute (IdiSNA), Pamplona, Spain.

Nadège Corradini (N)

Institute for Paediatric Haematology and Oncology, Leon Bérard Cancer Centre, University of Lyon, Lyon, France.

Perrine Marec Bérard (PM)

Institute for Paediatric Haematology and Oncology, Leon Bérard Cancer Centre, University of Lyon, Lyon, France.

Jeremy Miller (J)

Information Management Services, Inc., Calverton, MD, United States of America.

Neal D Freedman (ND)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Nathaniel Rothman (N)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Brian D Carter (BD)

Behavioral and Epidemiology Research Group, American Cancer Society, Atlanta, GA, United States of America.

Casey L Dagnall (CL)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Laurie Burdett (L)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Kristine Jones (K)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Michelle Manning (M)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Kathleen Wyatt (K)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Weiyin Zhou (W)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

Meredith Yeager (M)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, United States of America.

David G Cox (DG)

Institut National de la Santé et de la Recherche Médicale (INSERM), Paris, France.

Robert N Hoover (RN)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Javed Khan (J)

Genetics Branch, Center for Cancer Research, National Cancer Institute, Bethesda, MD, United States of America.

Gregory T Armstrong (GT)

Department of Epidemiology and Cancer Control, St. Jude Children's Research Hospital, Memphis, TN, United States of America.

Wendy M Leisenring (WM)

Cancer Prevention and Clinical Statistics Programs, Fred Hutchinson Cancer Research Center, Seattle, WA, United States of America.

Smita Bhatia (S)

Institute for Cancer Outcomes and Survivorship, University of Alabama at Birmingham, Birmingham, AL, United States of America.

Leslie L Robison (LL)

Department of Epidemiology and Cancer Control, St. Jude Children's Research Hospital, Memphis, TN, United States of America.

Andreas E Kulozik (AE)

Department of Pediatric Oncology, Hematology and Immunology and Hopp Children Cancer Center, University of Heidelberg, Heidelberg, Germany.

Jennifer Kriebel (J)

Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.
Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.
German Center for Diabetes Research (DZD), München, Neuherberg, Germany.

Thomas Meitinger (T)

German Research Center for Environmental Health, Institute of Human Genetics, Helmholtz Zentrum München, Neuherberg, Germany.
Institute of Human Genetics, Technische Universität München, Munich, Germany.

Markus Metzler (M)

Department of Paediatrics and Adolescent Medicine, University Hospital of Erlangen, Erlangen, Germany.

Manuela Krumbholz (M)

Department of Paediatrics and Adolescent Medicine, University Hospital of Erlangen, Erlangen, Germany.

Wolfgang Hartmann (W)

Division of Translational Pathology, Gerhard-Domagk Institute of Pathology, University Hospital of Münster, Münster, Germany.

Konstantin Strauch (K)

Institute of Genetic Epidemiology, LMU Munich, Munich, Germany.

Thomas Kirchner (T)

Institute of Pathology, Faculty of Medicine, LMU Munich, Munich, Germany.

Uta Dirksen (U)

Pediatrics III, West German Cancer Centre, University Hospital Essen, Essen, Germany.
German Cancer Consortium (DKTK), Center Essen, Heidelberg, Germany.

Lisa Mirabello (L)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Margaret A Tucker (MA)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Franck Tirode (F)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.
SIREDO Oncology Centre, Institut Curie, Paris, France.

Lindsay M Morton (LM)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Stephen J Chanock (SJ)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

Olivier Delattre (O)

Inserm U830, Équipe Labellisés LNCC, PSL Université, Institut Curie, Paris, France.
SIREDO Oncology Centre, Institut Curie, Paris, France.

Mitchell J Machiela (MJ)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America.

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