Inherited GATA3 variants are associated with Ph-like childhood acute lymphoblastic leukemia and risk of relapse (original) (raw)
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- Pui, C.H. & Evans, W.E. Treatment of acute lymphoblastic leukemia. N. Engl. J. Med. 354, 166–178 (2006).
Article CAS PubMed Google Scholar - Pui, C.H., Mullighan, C.G., Evans, W.E. & Relling, M.V. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there? Blood 120, 1165–1174 (2012).
Article CAS PubMed PubMed Central Google Scholar - Hunger, S.P. et al. Improved survival for children and adolescents with acute lymphoblastic leukemia between 1990 and 2005: a report from the Children's Oncology Group. J. Clin. Oncol. 30, 1663–1669 (2012).
Article PubMed PubMed Central Google Scholar - Stanulla, M. et al. Integrating molecular information into treatment of childhood acute lymphoblastic leukemia—a perspective from the BFM Study Group. Blood Cells Mol. Dis. 39, 160–163 (2007).
Article PubMed Google Scholar - Biondi, A. et al. Imatinib after induction for treatment of children and adolescents with Philadelphia-chromosome-positive acute lymphoblastic leukaemia (EsPhALL): a randomised, open-label, intergroup study. Lancet Oncol. 13, 936–945 (2012).
Article CAS PubMed PubMed Central Google Scholar - Den Boer, M.L. et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 10, 125–134 (2009).
Article CAS PubMed PubMed Central Google Scholar - Roberts, K.G. et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 22, 153–166 (2012).
Article CAS PubMed PubMed Central Google Scholar - Harvey, R.C. et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome. Blood 116, 4874–4884 (2010).
Article CAS PubMed PubMed Central Google Scholar - Mullighan, C.G. et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N. Engl. J. Med. 360, 470–480 (2009).
Article CAS PubMed PubMed Central Google Scholar - Harvey, R.C. et al. Rearrangement of CRLF2 is associated with mutation of JAK kinases, alteration of IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia. Blood 115, 5312–5321 (2010).
Article CAS PubMed PubMed Central Google Scholar - Loh, M.L. et al. Tyrosine kinome sequencing of pediatric acute lymphoblastic leukemia: a report from the Children's Oncology Group TARGET Project. Blood 121, 485–488 (2013).
Article CAS PubMed PubMed Central Google Scholar - Papaemmanuil, E. et al. Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukemia. Nat. Genet. 41, 1006–1010 (2009).
Article CAS PubMed PubMed Central Google Scholar - Sherborne, A.L. et al. Variation in CDKN2A at 9p21.3 influences childhood acute lymphoblastic leukemia risk. Nat. Genet. 42, 492–494 (2010).
Article CAS PubMed PubMed Central Google Scholar - Treviño, L.R. et al. Germline genomic variants associated with childhood acute lymphoblastic leukemia. Nat. Genet. 41, 1001–1005 (2009).
Article PubMed PubMed Central Google Scholar - Xu, H. et al. Novel susceptibility variants at 10p12.31-12.2 for childhood acute lymphoblastic leukemia in ethnically diverse populations. J. Natl. Cancer Inst. 105, 733–742 (2013).
Article CAS PubMed PubMed Central Google Scholar - Xu, H. et al. ARID5B genetic polymorphisms contribute to racial disparities in the incidence and treatment outcome of childhood acute lymphoblastic leukemia. J. Clin. Oncol. 30, 751–757 (2012).
Article CAS PubMed PubMed Central Google Scholar - Paulsson, K. et al. Genetic landscape of high hyperdiploid childhood acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 107, 21719–21724 (2010).
Article CAS PubMed PubMed Central Google Scholar - Jones, A.V. et al. JAK2 haplotype is a major risk factor for the development of myeloproliferative neoplasms. Nat. Genet. 41, 446–449 (2009).
Article CAS PubMed PubMed Central Google Scholar - Olcaydu, D. et al. A common JAK2 haplotype confers susceptibility to myeloproliferative neoplasms. Nat. Genet. 41, 450–454 (2009).
Article CAS PubMed Google Scholar - Kilpivaara, O. et al. A germline JAK2 SNP is associated with predisposition to the development of JAK2V617F-positive myeloproliferative neoplasms. Nat. Genet. 41, 455–459 (2009).
Article CAS PubMed PubMed Central Google Scholar - Yang, J.J. et al. Ancestry and pharmacogenomics of relapse in acute lymphoblastic leukemia. Nat. Genet. 43, 237–241 (2011).
Article CAS PubMed PubMed Central Google Scholar - Fujiwara, T. et al. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol. Cell 36, 667–681 (2009).
Article CAS PubMed PubMed Central Google Scholar - Wei, G. et al. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity 35, 299–311 (2011).
Article CAS PubMed PubMed Central Google Scholar - Yagi, R., Zhu, J. & Paul, W.E. An updated view on transcription factor GATA3-mediated regulation of Th1 and Th2 cell differentiation. Int. Immunol. 23, 415–420 (2011).
Article CAS PubMed PubMed Central Google Scholar - Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157–163 (2012).
Article CAS PubMed PubMed Central Google Scholar - Enciso-Mora, V. et al. A genome-wide association study of Hodgkin's lymphoma identifies new susceptibility loci at 2p16.1 (REL), 8q24.21 and 10p14 (GATA3). Nat. Genet. 42, 1126–1130 (2010).
Article CAS PubMed PubMed Central Google Scholar - Pasquet, M. et al. High frequency of GATA2 mutations in patients with mild chronic neutropenia evolving to MonoMac syndrome, myelodysplasia, and acute myeloid leukemia. Blood 121, 822–829 (2013).
Article CAS PubMed PubMed Central Google Scholar - Hahn, C.N. et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat. Genet. 43, 1012–1017 (2011).
Article CAS PubMed PubMed Central Google Scholar - Davies, S.M. et al. Pharmacogenetics of minimal residual disease response in children with B-precursor acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood 111, 2984–2990 (2008).
Article CAS PubMed PubMed Central Google Scholar - Huang, R.S. et al. A genome-wide approach to identify genetic variants that contribute to etoposide-induced cytotoxicity. Proc. Natl. Acad. Sci. USA 104, 9758–9763 (2007).
Article CAS PubMed PubMed Central Google Scholar - Degner, J.F. et al. DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482, 390–394 (2012).
Article CAS PubMed PubMed Central Google Scholar - Borowitz, M.J. et al. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia and its relationship to other prognostic factors: a Children's Oncology Group study. Blood 111, 5477–5485 (2008).
Article CAS PubMed PubMed Central Google Scholar - Shi, J. et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460, 753–757 (2009).
Article CAS PubMed PubMed Central Google Scholar - Purcell, S.M. et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460, 748–752 (2009).
Article CAS PubMed Google Scholar - Troyer, J.L. et al. Genome-wide association study implicates _PARD3B_-based AIDS restriction. J. Infect. Dis. 203, 1491–1502 (2011).
Article CAS PubMed PubMed Central Google Scholar - Burchard, E.G. et al. Lower bronchodilator responsiveness in Puerto Rican than in Mexican subjects with asthma. Am. J. Respir. Crit. Care Med. 169, 386–392 (2004).
Article PubMed Google Scholar - Korn, J.M. et al. Integrated genotype calling and association analysis of SNPs, common copy number polymorphisms and rare CNVs. Nat. Genet. 40, 1253–1260 (2008).
Article CAS PubMed PubMed Central Google Scholar - Pritchard, J.K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
CAS PubMed PubMed Central Google Scholar - Mao, X. et al. A genomewide admixture mapping panel for Hispanic/Latino populations. Am. J. Hum. Genet. 80, 1171–1178 (2007).
Article CAS PubMed PubMed Central Google Scholar - Tibshirani, R., Hastie, T., Narasimhan, B. & Chu, G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc. Natl. Acad. Sci. USA 99, 6567–6572 (2002).
Article CAS PubMed PubMed Central Google Scholar - Liu, E.Y., Li, M., Wang, W. & Li, Y. MaCH-admix: genotype imputation for admixed populations. Genet. Epidemiol. 37, 25–37 (2013).
Article CAS PubMed Google Scholar - Pruim, R.J. et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26, 2336–2337 (2010).
Article CAS PubMed PubMed Central Google Scholar - Chen, I.M. et al. Outcome modeling with CRLF2, IKZF1, JAK, and minimal residual disease in pediatric acute lymphoblastic leukemia: a Children's Oncology Group study. Blood 119, 3512–3522 (2012).
Article CAS PubMed PubMed Central Google Scholar - Andersen, P.K. & Perme, M.P. Pseudo-observations in survival analysis. Stat. Methods Med. Res. 19, 71–99 (2010).
Article PubMed Google Scholar - Duan, S. et al. Genetic architecture of transcript-level variation in humans. Am. J. Hum. Genet. 82, 1101–1113 (2008).
Article CAS PubMed PubMed Central Google Scholar - Spielman, R.S. et al. Common genetic variants account for differences in gene expression among ethnic groups. Nat. Genet. 39, 226–231 (2007).
Article CAS PubMed PubMed Central Google Scholar - Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).
Article CAS PubMed PubMed Central Google Scholar - Zhou, X. et al. The Human Epigenome Browser at Washington University. Nat. Methods 8, 989–990 (2011).
Article CAS PubMed PubMed Central Google Scholar
Acknowledgements
We thank the patients and parents who participated in the COG protocols included in this study, the clinicians and research staff at COG institutions and J. Pullen (University of Mississippi at Jackson) for assistance in the classification of patients with ALL. Genome-wide genotyping of COG P9905 samples was performed by the Center for Molecular Medicine with generous financial support from the Jeffrey Pride Foundation and the National Childhood Cancer Foundation. V.P.-A. is supported by a Spanish Ministry of Education Fellowship Grant and by a St. Jude Children's Research Hospital Academic Programs Special Fellowship. J.J.Y. is supported by an American Society of Hematology Scholar Award, an Alex Lemonade Stand Foundation for Childhood Cancer Young Investigator Grant and by the Order of St. Francis Foundation. K.G.R. is supported by a National Health and Medical Research Council (Australia) Overseas Training Fellowship and by a Haematology Society of Australia and New Zealand Novartis New Investigator Scholarship. C.G.M. is a Pew Scholar in the Biomedical Sciences and a St. Baldrick's Scholar. We thank M. Shriver (Pennsylvania State University) for sharing SNP genotype data for the Native American references, J. Pritchard and J. Degner (University of Chicago) for sharing DNase I hypersensitivity data for HapMap YRI cell lines, R.C. Ribeiro (St. Jude Children's Research Hospital) and P. De Alarcon (University of Illinois College of Medicine at Peoria) for coordinating collaborations in Guatemala and S. Naron for her editorial assistance. This work was supported by the US National Institutes of Health (grant numbers CA156449, CA21765, CA36401, CA98543, CA114766, CA98413, CA140729 and GM92666), in part by the intramural Program of the National Cancer Institute and by the American Lebanese Syrian Associated Charities (ALSAC). Study sponsors were not directly involved in the design of the study, the collection, analysis and interpretation of data, the writing of the manuscript or the decision to submit the manuscript. Detailed acknowledgments for the dbGaP data sets are provided in the Supplementary Note.
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Authors and Affiliations
- Department of Pharmaceutical Sciences, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Virginia Perez-Andreu, Wenjian Yang, Heng Xu, Shuyu E, Joshua Yew-Suang Lim, Colton Smith, William E Evans, Mary V Relling & Jun J Yang - Department of Pathology, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Kathryn G Roberts & Charles G Mullighan - Cancer Center, University of New Mexico, Albuquerque, New Mexico, USA
Richard C Harvey, I-Ming Chen & Cheryl L Willman - Department of Biostatistics, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Cheng Cheng & Deqing Pei - Department of Pathology and Laboratory Medicine, Nationwide Children's Hospital, Columbus, Ohio, USA
Julie Gastier-Foster - Department of Pediatrics, Ohio State University School of Medicine, Columbus, Ohio, USA
Julie Gastier-Foster - Department of Pediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Joshua Yew-Suang Lim - Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Yiping Fan - Department of Epidemiology and Health Policy Research, University of Florida, Gainesville, Florida, USA
Meenakshi Devidas - Johns Hopkins Medical Institute, Baltimore, Maryland, USA
Michael J Borowitz - Hartwell Center for Bioinformatics & Biotechnology, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Geoffrey Neale - Department of Bioengineering & Therapeutic Science and Medicine, University of California, San Francisco, San Francisco, California, USA
Esteban G Burchard & Dara G Torgerson - Unidad Nacional de Oncología Pediátrica, Guatemala City, Guatemala
Federico Antillon Klussmann & Cesar Rolando Najera Villagran - Department of Pediatric Hematology/Oncology, University of Texas Southwestern Medical Center, Dallas, Texas, USA
Naomi J Winick - Department of Pediatrics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
Bruce M Camitta - New York University Cancer Institute, New York, New York, USA
Elizabeth Raetz & William L Carroll - Department of Laboratory Medicine, University of Washington, Seattle, Washington, USA
Brent Wood - Department of Biochemistry and Molecular Biology, Pennsylvania State University College of Medicine, Hershey, Pennsylvania, USA
Feng Yue - Maine Children's Cancer Program, Scarborough, Maine, USA
Eric Larsen - Department of Hematology and Oncology, Cook Children's Medical Center, Fort Worth, Texas, USA
W Paul Bowman - Department of Pediatrics, University of California, San Francisco, San Francisco, California, USA
Mignon L Loh - Laboratory of Experimental Immunology, National Cancer Institute, Frederick, Maryland, USA
Michael Dean - Department of Oncology, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
Deepa Bhojwani & Ching-Hon Pui - Department of Hematology and Oncology, Children's Hospital Colorado, University of Colorado, Aurora, Colorado, USA
Stephen P Hunger
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Contributions
J.J.Y. supervised the research. V.P.-A., S.P.H., C.L.W., C.G.M. and J.J.Y. conceived and designed the experiments. V.P.-A., K.G.R., R.C.H., J.G.-F., S.E., I.-M.C., G.N., E.G.B., D.G.T. and C.R.N.V. performed the experiments. V.P.-A., J.J.Y., R.C.H., W.Y., C.C., D.P., Y.F., M. Devidas, C.S. and G.N. performed statistical analysis. V.P.-A., K.G.R., R.C.H., W.Y., H.X., S.E., J.Y.-S.L., I.-M.C., Y.F., M.J.B., C.S., G.N., E.G.B., D.G.T., F.A.K., C.R.N.V., M.L.L., M. Devidas, D.B., C.-H.P., W.E.E., M.V.R., S.P.H., C.L.W. and C.G.M. analyzed the data. R.C.H., J.G.-F., J.Y.-S.L., Y.F., E.G.B., F.A.K., C.R.N.V., N.J.W., B.M.C., E.R., B.W., F.Y., W.L.C., E.L., W.P.B., M.L.L., M. Dean, S.P.H., C.L.W. and C.G.M. contributed reagents, materials and/or analysis tools. V.P.-A. and J.J.Y. wrote the manuscript.
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Correspondence toJun J Yang.
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Perez-Andreu, V., Roberts, K., Harvey, R. et al. Inherited GATA3 variants are associated with Ph-like childhood acute lymphoblastic leukemia and risk of relapse.Nat Genet 45, 1494–1498 (2013). https://doi.org/10.1038/ng.2803
- Received: 25 May 2013
- Accepted: 27 September 2013
- Published: 20 October 2013
- Issue Date: December 2013
- DOI: https://doi.org/10.1038/ng.2803