Oncotarget

Research Papers:

Recurrent genetic defects on chromosome 5q in myeloid neoplasms

Naoko Hosono, Hideki Makishima, Reda Mahfouz, Bartlomiej Przychodzen, Kenichi Yoshida, Andres Jerez, Thomas LaFramboise, Chantana Polprasert, Michael J. Clemente, Yuichi Shiraishi, Kenichi Chiba, Hiroko Tanaka, Satoru Miyano, Masashi Sanada, Edward Cui, Amit K. Verma, Michael A. McDevit, Alan F. List, Yogen Saunthararajah, Mikkael A. Sekeres, Jacqueline Boultwood, Seishi Ogawa and Jaroslaw P. Maciejewski _

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Oncotarget. 2017; 8:6483-6495. https://doi.org/10.18632/oncotarget.14130

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Abstract

Naoko Hosono1,2, Hideki Makishima1,*, Reda Mahfouz1, Bartlomiej Przychodzen1, Kenichi Yoshida3,4, Andres Jerez1, Thomas LaFramboise5, Chantana Polprasert1, Michael J. Clemente1, Yuichi Shiraishi6, Kenichi Chiba6, Hiroko Tanaka7, Satoru Miyano6,7, Masashi Sanada3,4, Edward Cui5, Amit K. Verma8, Michael A. McDevitt9, Alan F. List10, Yogen Saunthararajah1, Mikkael A. Sekeres1,12,13, Jacqueline Boultwood13, Seishi Ogawa3,4, Jaroslaw P. Maciejewski1,11,*

1Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland, OH, USA

2First Department of Internal Medicine, Faculty of Medical Sciences, University of Fukui, Fukui, Japan

3Cancer Genomics Project, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

4Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan

5Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH, USA

6Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, The University of Tokyo, Tokyo, Japan

7Laboratory of Sequence Analysis, Human Genome Center, Institute of Medical Science, The University of Tokyo, Tokyo, Japan

8Department of Oncology, Albert Einstein College of Medicine, Bronx, NY, USA

9Division of Hematology and Hematological Malignancy, Department of Internal Medicine and Oncology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

10H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA

11Leukemia Program, Cleveland Clinic, Taussig Cancer Institute, Cleveland, OH, USA

12Department of Hematology and Medical Oncology, Taussig Cancer Institute, Cleveland Clinic, Cleveland, OH, USA

13LLR Molecular Haematology Unit, Nuffield Division of Clinical Laboratory Sciences, Radcliffe Department of Medicine, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom

*These authors contributed equally to this work

Correspondence to:

Jaroslaw P. Maciejewski, email: [email protected]

Keywords: MDS, del(5q), TP53, G3BP1

Received: June 20, 2016     Accepted: December 16, 2016     Published: December 23, 2016

ABSTRACT

Background: Deletion of chromosome 5q (del(5q)) is the most common karyotypic abnormality in myeloid neoplasms.

Materials and Methods: To define the pathogenic molecular features associated with del(5q), next–generation sequencing was applied to 133 patients with myeloid neoplasms (MDS; N = 69, MDS/MPN; N = 5, sAML; N = 29, pAML; N = 30) with del(5q) as a sole abnormally or a part of complex karyotype and results were compared to molecular features of patients diploid for chr5.

Findings: A number of 5q genes with haploinsufficient expression and/or recurrent somatic mutations were identified; for these genes, CSNK1A1 and G3BP1 within the commonly deleted 5q region and DDX41 within a commonly retained region were most commonly affected by somatic mutations. These genes showed consistent haploinsufficiency in deleted cases; low expression/mutations of G3BP1 or DDX41 were associated with poor survival, likely due to decreased cellular function. The most common mutations on other chromosomes in patients with del(5q) included TP53, and mutations of FLT3 (ITD or TKD), NPM1 or TET2 and were mutually exclusive. Serial sequencing allowed for definition of clonal architecture and dynamics, in patients with exome sequencing allelic imbalance for informative SNPs facilitated simultaneous approximation of clonal size of del(5q) and clonal burden for somatic mutations.

Interpretation: Our results illuminate the spectrum of molecular defects characteristic of del(5q), their clinical impact and succession of stepwise evolution.


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