250K single nucleotide polymorphism array karyotyping identifies acquired uniparental disomy and homozygous mutations, including novel missense substitutions of c-Cbl, in myeloid malignancies.

Two types of acquired loss of heterozygosity are possible in cancer: deletions and copy-neutral uniparental disomy (UPD). Conventionally, copy number losses are identified using metaphase cytogenetics, whereas detection of UPD is accomplished by microsatellite and copy number analysis and as such, is not often used clinically. Recently, introduction of single nucleotide polymorphism (SNP) microarrays has allowed for the systematic and sensitive detection of UPD in hematologic malignancies and other cancers. In this study, we have applied 250K SNP array technology to detect previously cryptic chromosomal changes, particularly UPD, in a cohort of 301 patients with myelodysplastic syndromes (MDS), overlap MDS/myeloproliferative disorders (MPD), MPD, and acute myeloid leukemia. We show that UPD is a common chromosomal defect in myeloid malignancies, particularly in chronic myelomonocytic leukemia (CMML; 48%) and MDS/MPD-unclassifiable (38%). Furthermore, we show that mapping minimally overlapping segmental UPD regions can help target the search for both known and unknown pathogenic mutations, including newly identified missense mutations in the proto-oncogene c-Cbl in 7 of 12 patients with UPD11q. Acquired mutations of c-Cbl E3 ubiquitin ligase may explain the pathogenesis of a clonal process in a subset of MDS/MPD, including CMML.

[1]  G. Mufti,et al.  Whole genome scanning as a cytogenetic tool in hematologic malignancies. , 2008, Blood.

[2]  J. Maciejewski,et al.  Phospho-STAT5 expression pattern with the MPL W515L mutation is similar to that seen in chronic myeloproliferative disorders with JAK2 V617F. , 2008, Human pathology.

[3]  C. Preudhomme,et al.  Cooperating gene mutations in acute myeloid leukemia: a review of the literature , 2008, Leukemia.

[4]  C. O'keefe,et al.  Chromosomal lesions and uniparental disomy detected by SNP arrays in MDS, MDS/MPD, and MDS-derived AML. , 2008, Blood.

[5]  M. McDevitt,et al.  SNP Array Karyotyping Allows for the Detection of Uniparental Disomy and Cryptic Chromosomal Abnormalities in MDS/MPD-U and MPD , 2007, PloS one.

[6]  L. Rönnstrand,et al.  Grb2 mediates negative regulation of stem cell factor receptor/c-Kit signaling by recruitment of Cbl. , 2007, Experimental cell research.

[7]  G. Mufti,et al.  Prevalence and prognostic significance of allelic imbalance by single-nucleotide polymorphism analysis in low-risk myelodysplastic syndromes. , 2007, Blood.

[8]  Bas J. Wouters,et al.  Segmental uniparental disomy as a recurrent mechanism for homozygous CEBPA mutations in acute myeloid leukemia , 2007, Leukemia.

[9]  J. Downing,et al.  Genome-wide single-nucleotide polymorphism analysis in juvenile myelomonocytic leukemia identifies uniparental disomy surrounding the NF1 locus in cases associated with neurofibromatosis but not in cases with mutant RAS or PTPN11 , 2007, Oncogene.

[10]  M. Caligiuri,et al.  Novel c-CBL and CBL-b ubiquitin ligase mutations in human acute myeloid leukemia. , 2007, Blood.

[11]  Chunaram Choudhary,et al.  Flt3-dependent transformation by inactivating c-Cbl mutations in AML. , 2007, Blood.

[12]  Motohiro Kato,et al.  Highly sensitive method for genomewide detection of allelic composition in nonpaired, primary tumor specimens by use of affymetrix single-nucleotide-polymorphism genotyping microarrays. , 2007, American journal of human genetics.

[13]  A. Tsygankov,et al.  The Cbl family proteins: Ring leaders in regulation of cell signaling , 2006, Journal of cellular physiology.

[14]  Johan Eide,et al.  Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. , 2006, Clinical cancer research : an official journal of the American Association for Cancer Research.

[15]  Jason C. Ting,et al.  Analysis and visualization of chromosomal abnormalities in SNP data with SNPscan , 2006, BMC Bioinformatics.

[16]  S. Akiki,et al.  Acquired Isodisomy for chromosome 13 is common in AML, and associated with FLT3-itd mutations , 2005, Leukemia.

[17]  Gudmundur A. Thorisson,et al.  The International HapMap Project Web site. , 2005, Genome research.

[18]  T. A. Lister,et al.  Association between acquired uniparental disomy and homozygous gene mutation in acute myeloid leukemias. , 2005, Cancer research.

[19]  Shigeru Chiba,et al.  A robust algorithm for copy number detection using high-density oligonucleotide single nucleotide polymorphism genotyping arrays. , 2005, Cancer research.

[20]  Mario Cazzola,et al.  A gain-of-function mutation of JAK2 in myeloproliferative disorders. , 2005, The New England journal of medicine.

[21]  Sandra A. Moore,et al.  Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. , 2005, Cancer cell.

[22]  P. Campbell,et al.  Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders , 2005, The Lancet.

[23]  松山 智洋 What's going on 造血器腫瘍 A gain-of-function mutation of JAK2 in myeloproliferative disorders. Kralovics R, Passamonti F, Buser AS, Teo SS, Tiedt R, Passweg JR, Tichelli A, Cazzola M, Skoda RC. N Engl J Med. 2005; 352: 1779-90. PMID:15858187.--慢性骨髄増殖性疾患においてJAK2遺伝子の変異が高頻度にみられることを示した論文 , 2005 .

[24]  Jan Bressler,et al.  Epigenetics and human disease. , 2004, Annual review of genomics and human genetics.

[25]  M. Lohuizen,et al.  Stem Cells and Cancer The Polycomb Connection , 2004, Cell.

[26]  P. Kosarev,et al.  Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome , 2002, Genome Biology.

[27]  R. Kralovics,et al.  Acquired uniparental disomy of chromosome 9p is a frequent stem cell defect in polycythemia vera. , 2002, Experimental hematology.

[28]  M. Caligiuri,et al.  Absence of the wild-type allele predicts poor prognosis in adult de novo acute myeloid leukemia with normal cytogenetics and the internal tandem duplication of FLT3: a cancer and leukemia group B study. , 2001, Cancer research.

[29]  I. Day,et al.  An efficient procedure for genotyping single nucleotide polymorphisms. , 2001, Nucleic acids research.

[30]  F. Walker,et al.  RING finger mutations that abolish c-Cbl-directed polyubiquitination and downregulation of the EGF receptor are insufficient for cell transformation. , 2001, Molecular cell.

[31]  Ping Wang,et al.  Structure of a c-Cbl–UbcH7 Complex RING Domain Function in Ubiquitin-Protein Ligases , 2000, Cell.

[32]  W P Robinson,et al.  Mechanisms leading to uniparental disomy and their clinical consequences , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[33]  T. Hunter,et al.  The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. , 1999, Science.

[34]  D. Bowtell,et al.  The Cbl protooncoprotein stimulates CSF‐1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation , 1999, The EMBO journal.

[35]  Z. Kam,et al.  c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. , 1998, Genes & development.

[36]  L. Moretta,et al.  Regulation of KIR expression in human T cells: a safety mechanism that may impair protective T-cell responses. , 1998, Immunology today.

[37]  W. Langdon,et al.  Tyrosine kinase activity of the EGF receptor is enhanced by the expression of oncogenic 70Z-Cbl , 1997, Oncogene.

[38]  H. Band,et al.  Phosphotyrosine binding domain-dependent upregulation of the platelet-derived growth factor receptor alpha signaling cascade by transforming mutants of Cbl: implications for Cbl's function and oncogenicity , 1997, Molecular and cellular biology.

[39]  J. Ferrara,et al.  The Immunopathophysiology of Acute Graft‐Versus‐Host‐Disease , 1996, Stem cells.

[40]  H. Kaneko,et al.  TP53 mutations emerge at early phase of myelodysplastic syndrome and are associated with complex chromosomal abnormalities. , 1995, Blood.

[41]  W. Langdon,et al.  Tumour induction by activated abl involves tyrosine phosphorylation of the product of the cbl oncogene. , 1994, The EMBO journal.

[42]  H. Gralnick,et al.  The chronic myeloid leukaemias: guidelines for distinguishing chronic granulocytic, atypical chronic myeloid, and chronic myelomonocytic leukaemia: Proposals by the French ‐ American ‐ British Cooperative Leukaemia Group , 1994, British journal of haematology.