High resolution analysis of follicular lymphoma genomes reveals somatic recurrent sites of copy-neutral loss of heterozygosity and copy number alterations that target single genes

Genes Chromosomes and Cancer

Volumn 49, Issue 8, 2010, Pages 669-681

  Cheung, K John J ^a   Delaney, Allen ^b   Ben Neriah, Susana ^a   Schein, Jacquie ^b   Lee, Tang ^a   Shah, Sohrab P ^a   Cheung, Dorothy ^b   Johnson, Nathalie A ^a   Mungall, Andrew J ^b   Telenius, Adele ^a   Lai, Betty ^a   Boyle, Merrill ^a   Connors, Joseph M ^a   Gascoyne, Randy D ^a   Marra, Marco A ^b   Horsman, Douglas E ^a  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; DNA; FRAGILE HISTIDINE TRIAD PROTEIN; MEMBRANE PROTEIN; PEROXIN 14; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CARCINOGENESIS; CHROMOSOME 10Q; CHROMOSOME 12; CHROMOSOME 18; CHROMOSOME 1P; CHROMOSOME 1Q; CHROMOSOME 6P; CHROMOSOME 6Q; CHROMOSOME 7; CLINICAL ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; CYTOGENETICS; FEMALE; FOLLICULAR LYMPHOMA; GENE TARGETING; GENE TRANSLOCATION; GENOME; HETEROZYGOSITY LOSS; HUMAN; HUMAN TISSUE; MALE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; X CHROMOSOME;

CHROMOSOMES, ARTIFICIAL, BACTERIAL; CHROMOSOMES, HUMAN, PAIR 12; COMPUTATIONAL BIOLOGY; CYTOGENETIC ANALYSIS; FEMALE; GENE DOSAGE; GENE EXPRESSION PROFILING; GENOME, HUMAN; HUMANS; LOSS OF HETEROZYGOSITY; LYMPHOMA, FOLLICULAR; MALE; MIDDLE AGED; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSPECTIVE STUDIES;

EID: 77953526533     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.20780     Document Type: Article

References (56)

1. Al Kuraya K, Siraj AK, Bavi P, Al-Jomah N, El-Solh H, Ezzat A, Al-Dayel F, Belgaumi A, Al-Kofide A, Sabbah R, Sheikh S, Amr S, Simon R, Sauter G. 2006. High throughput tissue microarray analysis of FHIT expression in diffuse large cell B-cell lymphoma from Saudi Arabia. Mod Pathol 19:1124-1129.
2. Au WY, Gascoyne RD, Viswanatha DS, Skinnider BF, Connors JM, Klasa RJ, Horsman DE. 1999. Concurrent chromosomal alterations at 3q27, 8q24 and 18q21 in B-cell lymphomas. Br J Haematol 105:437-440.
3. Barbieri D, Michaux JL, Bosly A, van Hove W, Noens L, Drochmans A, Louwagie A, Tricot G, Boogaerts M, Vermaelen K. 1984. Cytogenetic evaluation of bone marrow involvement in non-Hodgkin's lymphomas. A survey of 94 cases. Haematologica 69:285-296.
4. Bende RJ, Smit LA, van Noesel CJ. 2007. Molecular pathways in follicular lymphoma. Leukemia 21:18-29.
5. Benjamini Y, Liu W. 1999. A step-down multiple hypotheses testing procedure that controls the false discovery rate under independence. J Stat Plan Inference 82:163-170.
6. Chen PM, Yang MH, Hsiao LT, Yu IT, Chu CJ, Chao TC, Yen CC, Wang WS, Chiou TJ, Liu JH. 2004. Decreased FHIT protein expression correlates with a worse prognosis in patients with diffuse large B-cell lymphoma. Oncol Rep 11: 349-356.
7. Cheung KJ, Shah SP, Steidl C, Johnson N, Relander T, Telenius A, Lai B, Murphy KP, Lam W, Al-Tourah AJ, Connors JM, Ng RT, Gascoyne RD, Horsman DE. 2009. Genome-wide profiling of follicular lymphoma by array comparative genomic hybridization reveals prognostically significant DNA copy number imbalances. Blood 113:137-148.
8. Davies AJ, Lee AM, Taylor C, Clear AJ, Goff LK, Iqbal S, Cuthbert- Heavens D, Calaminici M, Norton AJ, Lister TA, Fitzgibbon J. 2005. A limited role for TP53 mutation in the transformation of follicular lymphoma to diffuse large B-cell lymphoma. Leukemia 19:1459-1465.
9. de Leeuw RJ, Davies JJ, Rosenwald A, Bebb G, Gascoyne RD, Dyer MJ, Staudt LM, Martinez-Climent JA, Lam WL. 2004. Comprehensive whole genome array CGH profiling of mantle cell lymphoma model genomes. Hum Mol Genet 13:1827-1837. (Pubitemid 39214331)
10. Dolken G, Illerhaus G, Hirt C, Mertelsmann R. 1996. BCL-2/JH rearrangements in circulating B cells of healthy blood donors and patients with nonmalignant diseases. J Clin Oncol 14:1333-1344.
11. Fitzgibbon J, Iqbal S, Davies A, O'shea D, Carlotti E, Chaplin T, Matthews J, Raghavan M, Norton A, Lister TA, Young BD. 2007. Genome-wide detection of recurring sites of uniparental disomy in follicular and transformed follicular lymphoma. Leukemia 21:1514-1520.
12. Gavva NR, Wen SC, Daftari P, Moniwa M, Yang WM, Yang- Feng LP, Seto E, Davie JR, Shen CK. 2002. NAPP2, a peroxisomal membrane protein, is also a transcriptional corepressor. Genomics 79:423-431. (Pubitemid 34211950)
13. Hayslip J, Montero A. 2006. Tumor suppressor gene methylation in follicular lymphoma: A comprehensive review. Mol Cancer 5:44.
14. Herman JG, Civin CI, Issa JP, Collector MI, Sharkis SJ, Baylin SB. 1997. Distinct patterns of inactivation of p15INK4B and p16INK4A characterize the major types of hematological malignancies. Cancer Res 57:837-841.
15. Horsman DE, Connors JM, Pantzar T, Gascoyne RD. 2001. Analysis of secondary chromosomal alterations in 165 cases of follicular lymphoma with t(14;18). Genes Chromosomes Cancer 30: 375-382. (Pubitemid 32216328)
16. Ichikawa A, Kinoshita T, Watanabe T, Kato H, Nagai H, Tsushita K, Saito H, Hotta T. 1997. Mutations of the p53 gene as a prognostic factor in aggressive B-cell lymphoma. N Engl J Med 337:529-534. (Pubitemid 27352019)
17. Ishkanian AS, Malloff CA, Watson SK, DeLeeuw RJ, Chi B, Coe BP, Snijders A, Albertson DG, Pinkel D, Marra MA, Ling V, MacAulay C, Lam WL. 2004. A tiling resolution DNA microarray with complete coverage of the human genome. Nat Genet 36:299-303.
18. Johnson NA, Al-Tourah A, Brown CJ, Connors JM, Gascoyne RD, Horsman DE. 2008. Prognostic significance of secondary cytogenetic alterations in follicular lymphomas. Genes Chromosomes Cancer 47:1038-1048.
19. Johnson NA, Boyle M, Bashashati A, Leach S, Brooks-Wilson A, Sehn LH, Chhanabhai M, Brinkman RR, Connors JM, Weng AP, Gascoyne RD. 2009. Diffuse large B-cell lymphoma: Reduced CD20 expression is associated with an inferior survival. Blood 113:3773-3780.
20. Kameoka Y, Tagawa H, Tsuzuki S, Karnan S, Ota A, Suguro M, Suzuki R, Yamaguchi M, Morishima Y, Nakamura S, Seto M. 2004. Contig array CGH at 3p14.2 points to the FRA3B/FHIT common fragile region as the target gene in diffuse large B-cell lymphoma. Oncogene 23:9148-9154.
21. Koduru PR, Raju K, Vadmal V, Menezes G, Shah S, Susin M, Kolitz J, Broome JD. 1997. Correlation between mutation in P53, p53 expression, cytogenetics, histologic type, and survival in patients with B-cell non-Hodgkin's lymphoma. Blood 90: 4078-4091. (Pubitemid 27484063)
22. Koduru PR, Zariwala M, Soni M, Gong JZ, Xiong Y, Broome JD. 1995. Deletion of cyclin-dependent kinase 4 inhibitor genes P15 and P16 in non-Hodgkin's lymphoma. Blood 86:2900-2905.
23. Krug U, Ganser A, Koeffler HP. 2002. Tumor suppressor genes in normal and malignant hematopoiesis. Oncogene 21:3475-3495.
24. Krzywinski M, Bosdet I, Smailus D, Chiu R, Mathewson C, Wye N, Barber S, Brown-John M, Chan S, Chand S, Cloutier A, Girn N, Lee D, Masson A, Mayo M, Olson T, Pandoh P, Prabhu AL, Schoenmakers E, Tsai M, Albertson D, Lam W, Choy CO, Osoegawa K, Zhao S, de Jong PJ, Schein J, Jones S, Marra MA. 2004. A set of BAC clones spanning the human genome. Nucleic Acids Res 32:3651-3660.
25. Lasota J, Miettinen M. 2008. Clinical significance of oncogenic KIT and PDGFRA mutations in gastrointestinal stromal tumours. Histopathology 53:245-266.
26. Limpens J, Stad R, Vos C, de Vlaam C, de Jong D, van Ommen GJ, Schuuring E, Kluin PM. 1995. Lymphoma-associated translocation t(14;18) in blood B cells of normal individuals. Blood 85:2528-2536.
27. Lo Coco F, Gaidano G, Louie DC, Offit K, Chaganti RS, Dalla- Favera R. 1993. P53 Mutations are associated with histologic transformation of follicular lymphoma. Blood 82:2289-2295. (Pubitemid 23304250)
28. Lossos IS. 2005. Higher-grade transformation of follicular lymphoma - A continuous enigma. Leukemia 19:1331-1333. (Pubitemid 41136323)
29. Lu D, Zhao Y, Tawatao R, Cottam HB, Sen M, Leoni LM, Kipps TJ, Corr M, Carson DA. 2004. Activation of the Wnt signaling pathway in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 101:3118-3123. (Pubitemid 38327744)
30. Martinez-Climent JA, Alizadeh AA, Segraves R, Blesa D, Rubio- Moscardo F, Albertson DG, Garcia-Conde J, Dyer MJ, Levy R, Pinkel D, Lossos IS. 2003. Transformation of follicular lymphoma to diffuse large cell lymphoma is associated with a heterogeneous set of DNA copy number and gene expression alterations. Blood 101:3109-3117.
31. McDonnell TJ, Deane N, Platt FM, Nunez G, Jaeger U, McKearn JP, Korsmeyer SJ. 1989. bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57:79-88. (Pubitemid 19098870)
32. McDonnell TJ, Korsmeyer SJ. 1991. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature 349:254-256.
33. Mecucci C, Vermaelen K, Tricot G, Louwagie A, Michaux JL, Bosly A, Thomas J, Barbieri D, Van den Berghe H. 1983. 3q-, 3q+ Anomaly in malignant proliferations in humans. Cancer Genet Cytogenet 9:376-381.
34. Nemeth MJ, Bodine DM. 2007. Regulation of hematopoiesis and the hematopoietic stem cell niche by Wnt signaling pathways. Cell Res 17:746-758.
35. Ogawa S, Hangaishi A, Miyawaki S, Hirosawa S, Miura Y, Takeyama K, Kamada N, Ohtake S, Uike N, Shimazaki C. 1995. Loss of the cyclin-dependent kinase 4-inhibitor (p16; MTS1) gene is frequent in and highly specific to lymphoid tumors in primary human hematopoietic malignancies. Blood 86:1548-1556.
36. O'shea D, O'Riain C, Gupta M, Waters R, Yang Y, Wrench D, Gribben J, Rosenwald A, Ott G, Rimsza LM, Holte H, Cazier JB, Johnson NA, Campo E, Chan WC, Gascoyne RD, Young BD, Staudt LM, Lister TA, Fitzgibbon J. 2009. Regions of acquired uniparental disomy at diagnosis of follicular lymphoma are associated with both overall survival and risk of transformation. Blood 113:2298-2301.
37. Pekarsky Y, Zanesi N, Palamarchuk A, Huebner K, Croce CM. 2002. FHIT: From gene discovery to cancer treatment and prevention. Lancet Oncol 3:748-754. (Pubitemid 35446744)
38. Pinyol M, Cobo F, Bea S, Jares P, Nayach I, Fernandez PL, Montserrat E, Cardesa A, Campo E. 1998. p16(INK4a) gene inactivation by deletions, mutations, and hypermethylation is associated with transformed and aggressive variants of non- Hodgkin's lymphomas. Blood 91:2977-2984. (Pubitemid 28227549)
39. Purdie KJ, Lambert SR, Teh MT, Chaplin T, Molloy G, Raghavan M, Kelsell DP, Leigh IM, Harwood CA, Proby CM, Young BD. 2007. Allelic imbalances and microdeletions affecting the PTPRD gene in cutaneous squamous cell carcinomas detected using single nucleotide polymorphism microarray analysis. Genes Chromosomes Cancer 46:661-669.
40. Ross CW, Ouillette PD, Saddler CM, Shedden KA, Malek SN. 2007. Comprehensive analysis of copy number and allele status identifies multiple chromosome defects underlying follicular lymphoma pathogenesis. Clin Cancer Res 13:4777-4785.
41. Sanchez-Beato M, Saez AI, Navas IC, Algara P, Sol Mateo M, Villuendas R, Camacho F, Sanchez-Aguilera A, Sanchez E, Piris MA. 2001. Overall survival in aggressive B-cell lymphomas is dependent on the accumulation of alterations in p53, p16, and p27. Am J Pathol 159:205-213. (Pubitemid 33704205)
42. Sanchez-Beato M, Sanchez-Aguilera A, Piris MA. 2003. Cell cycle deregulation in B-cell lymphomas. Blood 101:1220-1235. (Pubitemid 36182489)
43. Sanchez-Izquierdo D, Siebert R, Harder L, Marugan I, Gozzetti A, Price HP, Gesk S, Hernandez-Rivas JM, Benet I, Sole F, Sonoki T, Le Beau MM, Schlegelberger B, Dyer MJ, Garcia- Conde J, Martinez-Climent JA. 2001. Detection of translocations affecting the BCL6 locus in B cell non-Hodgkin's lymphoma by interphase fluorescence in situ hybridization. Leukemia 15:1475-1484.
44. Sander CA, Yano T, Clark HM, Harris C, Longo DL, Jaffe ES, Raffeld M. 1993. P53 Mutation is associated with progression in follicular lymphomas. Blood 82:1994-2004.
45. Scheijen B, Griffin JD. 2002. Tyrosine kinase oncogenes in normal hematopoiesis and hematological disease. Oncogene 21:3314-3333.
46. Schmidt M, Sievers E, Endo T, Lu D, Carson D, Schmidt-Wolf IG. 2009. Targeting Wnt pathway in lymphoma and myeloma cells. Br J Haematol 144:796-798.
47. Schwaenen C, Viardot A, Berger H, Barth TF, Bentink S, Dohner H, Enz M, Feller AC, Hansmann ML, Hummel M, Kestler HA, Klapper W, Kreuz M, Lenze D, Loeffler M, Moller P, Muller- Hermelink HK, Ott G, Rosolowski M, Rosenwald A, Ruf S, Siebert R, Spang R, Stein H, Truemper L, Lichter P, Bentz M, Wessendorf S, Molecular Mechanisms in Malignant Lymphomas Network Project of the Deutsche Krebshilfe. 2009. Microarray-based genomic profiling reveals novel genomic aberrations in follicular lymphoma which associate with patient survival and gene expression status. Genes Chromosomes Cancer 48:39-54.
48. Shah SP, Lam WL, Ng RT, Murphy KP. 2007. Modeling recurrent DNA copy number alterations in array CGH data. Bioinformatics 23:i450-i458.
49. Shah SP, Xuan X, DeLeeuw RJ, Khojasteh M, Lam WL, Ng R, Murphy KP. 2006. Integrating copy number polymorphisms into array CGH analysis using a robust HMM. Bioinformatics 22:e431-e439.
50. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW, editors. 2008. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissue (IARC WHO Classification of Tumours), 4th ed. World Health Organization, Lyon, 439 p.
51. Tilly H, Rossi A, Stamatoullas A, Lenormand B, Bigorgne C, Kunlin A, Monconduit M, Bastard C. 1994. Prognostic value of chromosomal abnormalities in follicular lymphoma. Blood 84: 1043-1049. (Pubitemid 24245867)
52. Tyybakinoja A, Elonen E, Vauhkonen H, Saarela J, Knuutila S. 2008. Single nucleotide polymorphism microarray analysis of karyotypically normal acute myeloid leukemia reveals frequent copy number neutral loss of heterozygosity. Haematologica 93: 631-632. (Pubitemid 351536397)
53. Uchida T, Watanabe T, Kinoshita T, Murate T, Saito H, Hotta T. 1995. Mutational analysis of the CDKN2 (MTS1/p16ink4A) gene in primary B-cell lymphomas. Blood 86:2724-2731.
54. Zhao P, Lam AK, Lu YL, Zhong M, Chen LH, Pu XL. 2006. Aberrant FHIT protein expression in classical Hodgkin's lymphoma: A potential marker. Pathology 38:399-402. (Pubitemid 44477587)
55. Zimpfer A, Went P, Tzankov A, Pehrs AC, Lugli A, Maurer R, Terracciano L, Pileri S, Dirnhofer S. 2004. Rare expression of KIT (CD117) in lymphomas: A tissue microarray study of 1166 cases. Histopathology 45:398-404. (Pubitemid 39430645)
56. Zorn AM, Barish GD, Williams BO, Lavender P, Klymkowsky MW, Varmus HE. 1999. Regulation of Wnt signaling by Sox proteins: XSox17 alpha/beta and XSox3 physically interact with beta-catenin. Mol Cell 4:487-498.