The genomic landscape of Waldenström macroglobulinemia is characterized by highly recurring MYD88 and WHIM-like CXCR4 mutations, and small somatic deletions associated with B-cell lymphomagenesis

Blood

Volumn 123, Issue 11, 2014, Pages 1637-1646

  Hunter, Zachary R ^a,b   Xu, Lian ^a   Yang, Guang ^a   Zhou, Yangsheng ^a   Liu, Xia ^a   Cao, Yang ^a   Manning, Robert J ^a   Tripsas, Christina ^a   Patterson, Christopher J ^a   Sheehy, Patricia ^a   Treon, Steven P ^a,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MYELOID DIFFERENTIATION FACTOR 88; RETINOBLASTOMA BINDING PROTEIN 2; ARID1A PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; MYD88 PROTEIN, HUMAN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR;

ARID1A GENE; ARID1B GENE; ARTICLE; B LYMPHOCYTE; BCLAF1 GENE; BTG1 GENE; CARCINOGENESIS; CHROMOSOME 3P; CHROMOSOME 6Q; CHROMOSOME DELETION; CHROMOSOME TRANSLOCATION; CLINICAL ARTICLE; COHORT ANALYSIS; COPY NUMBER VARIATION; CXCR4 GENE; FOXP1 GENE; GENE; GENE LOSS; GENE SEQUENCE; GENETIC VARIABILITY; HIVEP2 GENE; HUMAN; IMMUNOGLOBULIN DEFICIENCY; INFECTION; LYN GENE; MKLN1 GENE; MYD88 GENE; PLEKHG1 GENE; PRDM2 GENE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SOMATIC MUTATION; VERRUCA VULGARIS; WALDENSTROEM MACROGLOBULINEMIA; ZYGOSITY; AMINO ACID SEQUENCE; B CELL LYMPHOMA; BONE MARROW; CHROMOSOME 6; CHROMOSOME MAP; COMPARATIVE GENOMIC HYBRIDIZATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DELETION; GENE TRANSLOCATION; GENETICS; GENOMICS; IMMUNE DEFICIENCY; MOLECULAR GENETICS; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION; WHIM SYNDROME;

AMINO ACID SEQUENCE; BONE MARROW; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 6; COMPARATIVE GENOMIC HYBRIDIZATION; DNA COPY NUMBER VARIATIONS; GENE DELETION; GENOMICS; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPHOMA, B-CELL; MOLECULAR SEQUENCE DATA; MUTATION; MYELOID DIFFERENTIATION FACTOR 88; NUCLEAR PROTEINS; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSLOCATION, GENETIC; WALDENSTROM MACROGLOBULINEMIA; WARTS;

EID: 84897511040     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-09-525808     Document Type: Article

References (69)

1. Kyle RA, Therneau TM, Rajkumar SV, et al. Long-term follow-up of IgM monoclonal gammopathy of undetermined significance. Blood. 2003;102(10):3759- 3764. (Pubitemid 37409398)
2. Baldini L, Goldaniga M, Guffanti A, et al. Immunoglobulin M monoclonal gammopathies of undetermined significance and indolent Waldenstrom's macroglobulinemia recognize the same determinants of evolution into symptomatic lymphoid disorders: proposal for a common prognostic scoring system. J Clin Oncol. 2005;23(21):4662-4668. (Pubitemid 46224068)
3. Morra E, Cesana C, Klersy C, et al. Clinical characteristics and factors predicting evolution of asymptomatic IgM monoclonal gammopathies and IgM-related disorders. Leukemia. 2004;18(9):1512-1517. (Pubitemid 39264074)
4. Treon SP, Xu L, Yang G, et al. MYD88 L265P somatic mutation in Waldenström's macroglobulinemia. N Engl J Med. 2012;367(9):826-833.
5. Chapman MA, Lawrence MS, Keats JJ, et al. Initial genome sequencing and analysis of multiple myeloma. Nature. 2011;471(7339):467-472.
6. Puente XS, Pinyol M, Quesada V, et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature. 2011;475(7354):101-105.
7. Montesinos-Rongen M, Godlewska E, Brunn A, Wiestler OD, Siebert R, Deckert M. Activating L265P mutations of the MYD88 gene are common in primary central nervous system lymphoma. Acta Neuropathol. 2011;122(6):791-792.
8. Ngo VN, Young RM, Schmitz R, et al. Oncogenically active MYD88 mutations in human lymphoma. Nature. 2011;470(7332):115-119.
9. Pasqualucci L, Trifonov V, Fabbri G, et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet. 2011;43(9):830-837.
10. Jiménez C, Sebastián E, Chillón MC, et al. MYD88 L265P is a marker highly characteristic of, but not restricted to, Waldenström's macroglobulinemia. Leukemia. 2013;27(8):1722-1728.
11. Treon SP, Hunter ZR, Aggarwal A, et al. Characterization of familial Waldenstrom's macroglobulinemia. Ann Oncol. 2006;17(3):488-494.
12. Braggio E, Keats JJ, Leleu X, et al. Identification of copy number abnormalities and inactivating mutations in two negative regulators of nuclear factor-kappaB signaling pathways in Waldenstrom's macroglobulinemia. Cancer Res. 2009;69(8):3579-3588.
13. Schop RFJ, Van Wier SA, Xu R, et al. 6q deletion discriminates Waldenström macroglobulinemia from IgM monoclonal gammopathy of undetermined significance. Cancer Genet Cytogenet. 2006;169(2):150-153. (Pubitemid 44382607)
14. Braggio E, Keats JJ, Leleu X, et al. High-resolution genomic analysis in Waldenström's macroglobulinemia identifies disease-specific and common abnormalities with marginal zone lymphomas. Clin Lymphoma Myeloma. 2009;9(1):39-42.
15. Nguyen-Khac F, Lambert J, Chapiro E, et al; Groupe Français d'Etude de la Leucémie Lymphoïde Chronique et Maladie de Waldenström (GFCLL/MW); Groupe Ouest-Est d' étude des Leucémie Aiguës et Autres Maladies du Sang (GOELAMS); Groupe d'Etude des Lymphomes de l'Adulte (GELA). Chromosomal aberrations and their prognostic value in a series of 174 untreated patients with Waldenström's macroglobulinemia. Haematologica. 2013;98(4):649-654.
16. Owen RG, Treon SP, Al-Katib A, et al. Clinicopathological definition of Waldenstrom's macroglobulinemia: consensus panel recommendations from the Second International Workshop on Waldenstrom's Macroglobulinemia. Semin Oncol. 2003;30(2):110-115.
17. Futreal PA, Coin L, Marshall M, et al. A census of human cancer genes. Nat Rev Cancer. 2004;4(3):177-183. (Pubitemid 38337497)
18. Morin RD, Mendez-Lago M, Mungall AJ, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature. 2011;476(7360):298-303.
19. Ngo HT, Leleu X, Lee J, et al. SDF-1/CXCR4 and VLA-4 interaction regulates homing in Waldenstrom macroglobulinemia. Blood. 2008;112(1):150-158.
20. Hernandez PA, Gorlin RJ, Lukens JN, et al. Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat Genet. 2003;34(1):70-74. (Pubitemid 36548793)
21. Balabanian K, Lagane B, Pablos JL, et al. WHIM syndromes with different genetic anomalies are accounted for by impaired CXCR4 desensitization to CXCL12. Blood. 2005;105(6):2449-2457. (Pubitemid 40387045)
22. Wu B, Chien EYT, Mol CD, et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science. 2010;330(6007):1066-1071.
23. Orsini MJ, Parent JL, Mundell SJ, Marchese A, Benovic JL. Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization [published correction appears in J Biol Chem. 2000;275(33):25876]. J Biol Chem. 1999;274(43):31076- 31086.
24. Haribabu B, Richardson RM, Fisher I, et al. Regulation of human chemokine receptors CXCR4. Role of phosphorylation in desensitization and internalization. J Biol Chem. 1997;272(45):28726-28731. (Pubitemid 27517830)
25. Lagane B, Chow KYC, Balabanian K, et al. CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood. 2008;112(1):34-44.
26. Poulain S, Roumier C, Decambron A, et al. MYD88 L265P mutation in Waldenstrom macroglobulinemia. Blood. 2013;121(22):4504-4511.
27. Leleu X, Eeckhoute J, Jia X, et al. Targeting NF-kappaB in Waldenstrom macroglobulinemia. Blood. 2008;111(10):5068-5077.
28. Yang G, Zhou Y, Liu X, et al. A mutation in MYD88 (L265P) supports the survival of lymphoplasmacytic cells by activation of Bruton tyrosine kinase in Waldenström macroglobulinemia. Blood. 2013;122(7):1222-1232.
29. Dale DC, Bolyard AA, Kelley ML, et al. The CXCR4 antagonist plerixafor is a potential therapy for myelokathexis, WHIM syndrome. Blood. 2011;118(18):4963-4966.
30. Poulain S, Ertault M, Leleu X, et al. SDF1/CXCL12 (-801GA) polymorphism is a prognostic factor aftertreatment initiation in Waldenstrom macroglobulinemia. Leuk Res. 2009;33(9):1204-1207.
31. Hooks SB, Callihan P, Altman MK, Hurst JH, Ali MW, Murph MM. Regulators of G-Protein signaling RGS10 and RGS17 regulate chemoresistance in ovarian cancer cells. Mol Cancer. 2010;9:289.
32. Busillo JM, Benovic JL. Regulation of CXCR4 signaling. Biochim Biophys Acta. 2007;1768(4):952-963. (Pubitemid 46452548)
33. Nagl NG Jr, Wang X, Patsialou A, Van Scoy M, Moran E. Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. EMBO J. 2007;26(3):752-763.
34. Choi J, Ko M, Jeon S, et al. The SWI/SNF-like BAF complex is essential for early B cell development. J Immunol. 2012;188(8):3791-3803.
35. Heltemes-Harris LM, Willette MJL, Ramsey LB, et al. Ebf1 or Pax5 haploinsufficiency synergizes with STAT5 activation to initiate acute lymphoblastic leukemia. J Exp Med. 2011;208(6):1135-1149.
36. Jones S, Li M, Parsons DW, et al. Somatic mutations in the chromatin remodeling gene ARID1A occur in several tumor types. Hum Mutat. 2012;33(1):100-103.
37. Guan B, Wang T-L, Shih IM. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 2011;71(21):6718-6727.
38. Inoue H, Giannakopoulos S, Parkhurst CN, et al. Target genes of the largest human SWI/SNF complex subunit control cell growth. Biochem J. 2011;434(1):83-92.
39. Humbert N, Martien S, Augert A, et al. A genetic screen identifies topoisomerase 1 as a regulator of senescence. Cancer Res. 2009;69(10):4101-4106.
40. Shadat NMA, Koide N, Khuda II-EI-E, et al. Retinoblastoma protein-interacting zinc finger 1 (RIZ1) regulates the proliferation of monocytic leukemia cells via activation of p53. Cancer Invest. 2010;28(8):806-812.
41. Wall M, Rayeroux KC, MacKinnon RN, Zordan A, Campbell LJ. ETV6 deletion is a common additional abnormality in patients with myelodysplastic syndromes or acute myeloid leukemia and monosomy 7. Haematologica. 2012;97(12):1933-1936.
42. Stegmaier K, Pendse S, Barker GF, et al. Frequent loss of heterozygosity at the TEL gene locus in acute lymphoblastic leukemia of childhood. Blood. 1995;86(1):38-44.
43. Kuiper RP, Schoenmakers EF, van Reijmersdal SV, et al. High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression. Leukemia. 2007;21(6):1258-1266. (Pubitemid 46831815)
44. Bohlander SK. ETV6: a versatile player in leukemogenesis. Semin Cancer Biol. 2005;15(3):162-174.
45. Obrador-Hevia A, Serra-Sitjar M, Rodríguez J, Villalonga P, Fernández de Mattos S. The tumour suppressor FOXO3 is a key regulator of mantle cell lymphoma proliferation and survival. Br J Haematol. 2012;156(3):334-345.
46. Ticchioni M, Essafi M, Jeandel PY, et al. Homeostatic chemokines increase survival of B-chronic lymphocytic leukemia cells through inactivation of transcription factor FOXO3a. Oncogene. 2007;26(50):7081-7091. (Pubitemid 350064189)
47. Karube K, Nakagawa M, Tsuzuki S, et al. Identification of FOXO3 and PRDM1 as tumor-suppressor gene candidates in NK-cell neoplasms by genomic and functional analyses. Blood. 2011;118(12):3195-3204.
48. Bakker WJ, Blázquez-Domingo M, Kolbus A, et al. FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1. J Cell Biol. 2004;164(2):175-184. (Pubitemid 38133938)
49. Rouault JP, Rimokh R, Tessa C, et al. BTG1, a member of a new family of antiproliferative genes. EMBO J. 1992;11(4):1663-1670.
50. Lohr JG, Stojanov P, Lawrence MS, et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc Natl Acad Sci U S A. 2012;109(10):3879-3884.
51. Mullighan CG, Goorha S, Radtke I, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature. 2007;446(7137):758-764. (Pubitemid 46582031)
52. Waanders E, Scheijen B, van der Meer LT, et al. The origin and nature of tightly clustered BTG1 deletions in precursor B-cell acute lymphoblastic leukemia support a model of multiclonal evolution. PLoS Genet. 2012;8(2):e1002533.
53. van Galen JC, Kuiper RP, van Emst L, et al. BTG1 regulates glucocorticoid receptor autoinduction in acute lymphoblastic leukemia. Blood. 2010;115(23):4810-4819.
54. Treon SP. How I treat Waldenström macroglobulinemia. Blood. 2009;114(12):2375-2385.
55. Moritake H, Shimonodan H, Marutsuka K, Kamimura S, Kojima H, Nunoi H. C-MYC rearrangement may induce an aggressive phenotype in anaplastic lymphoma kinase positive anaplastic large cell lymphoma: identification of a novel fusion gene ALO17/CMYC. Am J Hematol. 2011;86(1):75-78.
56. Cools J, Wlodarska I, Somers R, et al. Identification of novel fusion partners of ALK, the anaplastic lymphoma kinase, in anaplastic large-cell lymphoma and inflammatory myofibroblastic tumor. Genes Chromosomes Cancer. 2002;34(4):354-362. (Pubitemid 34787456)
57. Owen HR, Elser M, Cheung E, Gersbach M, Kraus WL, Hottiger MO. MYBBP1a is a novel repressor of NF-kappaB. J Mol Biol. 2007;366(3):725-736.
58. Iwashita Y, Fukuchi N, Waki M, Hayashi K, Tahira T. Genome-wide repression of NF-κB target genes by transcription factor MIBP1 and its modulation by O-linked b-N-acetylglucosamine (O-GlcNAc) transferase. J Biol Chem. 2012;287(13):9887-9900.
59. Rossi D, Deaglio S, Dominguez-Sola D, et al. Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma. Blood. 2011;118(18):4930-4934.
60. Craxton A, Jiang A, Kurosaki T, Clark EA. Syk and Bruton's tyrosine kinase are required for B cell antigen receptor-mediated activation of the kinase Akt. J Biol Chem. 1999;274(43):30644-30650.
61. Niiro H, Allam A, Stoddart A, Brodsky FM, Marshall AJ, Clark EA. The B lymphocyte adaptor molecule of 32 kilodaltons (Bam32) regulates B cell antigen receptor internalization. J Immunol. 2004;173(9):5601-5609. (Pubitemid 39392147)
62. Gauld SB, Cambier JC. Src-family kinases in B-cell development and signaling. Oncogene. 2004;23(48):8001-8006. (Pubitemid 39468857)
63. Liu W, Quinto I, Chen X, et al. Direct inhibition of Bruton's tyrosine kinase by IBtk, a Btk-binding protein. Nat Immunol. 2001;2(10):939-946. (Pubitemid 32976166)
64. Jefferies CA, Doyle S, Brunner C, et al. Bruton's tyrosine kinase is a Toll/interleukin-1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J Biol Chem. 2003;278(28):26258-26264. (Pubitemid 36835395)
65. Liu X, Zhan Z, Li D, et al. Intracellular MHC class II molecules promote TLR-triggered innate immune responses by maintaining activation of the kinase Btk. Nat Immunol. 2011;12(5):416-424.
66. Makishima H, Jankowska AM, McDevitt MA, et al. CBL, CBLB, TET2, ASXL1, and IDH1/2 mutations and additional chromosomal aberrations constitute molecular events in chronic myelogenous leukemia. Blood. 2011;117(21):e198-e206.
67. Bachmaier K, Toya S, Gao X, et al. E3 ubiquitin ligase Cblb regulates the acute inflammatory response underlying lung injury. Nat Med. 2007;13(8):920-926. (Pubitemid 47222038)
68. Xu L, Hunter ZR, Yang G, et al. MYD88 L265P in Waldenstrom's macroglobulinemia, immunoglobulin M monoclonal gammopathy, and other B-cell lymphoproliferative disorders using conventional and quantitative allele-specific polymerase chain reaction [published correction appears in Blood. 2013;121(26):5259]. Blood. 2013;121(11):2051-2058.
69. Varettoni M, Arcaini L, Zibellini S, et al. Prevalence and clinical significance of the MYD88 (L265P) somatic mutation in Waldenstrom's macroglobulinemia and related lymphoid neoplasms. Blood. 2013;121(13):2522-2528.