Hypermethylation of the tumor suppressor gene PRDM1/Blimp-1 supports a pathogenetic role in EBV-positive Burkitt lymphom

Blood Cancer Journal

Volumn 4, Issue 11, 2014, Pages

  Zhang, T ^a   Ma, J ^a   Nie, K ^a   Yan, J ^a,d   Liu, Y ^a   Bacchi, C E ^b   Queiroga, E M ^b   Gualco, G ^b   Sample, J T ^c   Orazi, A ^a   Knowles, D M ^a   Tam, W ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Consultoria em Patologia ^*  (Brazil)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE ACTIVATION; BURKITT LYMPHOMA; CARCINOGENESIS; CELL CYCLE ARREST; CELL DIFFERENTIATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; EPIGENETIC REPRESSION; EPSTEIN BARR VIRUS; EXON; G1 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHOBLASTOID CELL LINE; NONHUMAN; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; S PHASE CELL CYCLE CHECKPOINT; TRANSIENT TRANSFECTION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; FEMALE; GENETICS; MALE; METABOLISM; PATHOLOGY; TUMOR CELL LINE; VIROLOGY;

BURKITT LYMPHOMA; CELL LINE, TUMOR; DNA METHYLATION; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; MALE; REPRESSOR PROTEINS; TUMOR SUPPRESSOR PROTEINS;

EID: 84927948951     PISSN: None     EISSN: 20445385     Source Type: Journal    
DOI: 10.1038/bcj.2014.75     Document Type: Article

References (37)

1. Martins G, Calame K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu Rev Immunol 2008; 26: 133-169.
2. Tam W. PRDM1 (PR domain containing 1, with ZNF domain). Atlas Genet Cytogenet Oncol Haematol 16: 135-140.
3. Pasqualucci L, Compagno M, Houldsworth J, Monti S, Grunn A, Nandula SV et al. Inactivation of the PRDM1/BLIMP1 gene in diffuse large B cell lymphoma. J Exp Med 2006; 203: 311-317.
4. Tam W, Gomez M, Chadburn A, Lee JW, Chan WC, Knowles DM. Mutational analysis of PRDM1 indicates a tumor-suppressor role in diffuse large B-cell lymphomas. Blood 2006; 107: 4090-4100.
5. Calado DP, Zhang B, Srinivasan L, Sasaki Y, Seagal J, Unitt C et al. Constitutive canonical NF-kappaB activation cooperates with disruption of BLIMP1 in the pathogenesis of activated B cell-like diffuse large cell lymphoma. Cancer Cell 2010; 18: 580-589.
6. Mandelbaum J, Bhagat G, Tang H, Mo T, Brahmachary M, Shen Q et al. BLIMP1 is a tumor suppressor gene frequently disrupted in activated B cell-like diffuse large B cell lymphoma. Cancer Cell 2010; 18: 568-579.
7. Nie K, Zhang T, Allawi H, Gomez M, Liu Y, Chadburn A et al. Epigenetic downregulation of the tumor suppressor gene PRDM1/Blimp-1 in diffuse large B cell lymphomas: a potential role of the microRNA let-7. Am J Pathol 2010; 177: 1470-1479.
8. Shaffer AL, Young RM, Staudt LM. Pathogenesis of human B cell lymphomas. Annu Rev Immunol 2012; 30: 565-610.
9. Karube K, Nakagawa M, Tsuzuki S, Takeuchi I, Honma K, Nakashima Y et al. Identification of FOXO3 and PRDM1 as tumor-suppressor gene candidates in NK-cell neoplasms by genomic and functional analyses. Blood 2011; 118: 3195-3204.
10. Kucuk C, Iqbal J, Hu X, Gaulard P, De Leval L, Srivastava G et al. PRDM1 is a tumor suppressor gene in natural killer cell malignancies. Proc Natl Acad Sci USA 2011; 108: 20119-20124.
11. Boi M, Rinaldi A, Kwee I, Bonetti P, Todaro M, Tabbo F et al. PRDM1/BLIMP1 is commonly inactivated in anaplastic large T-cell lymphoma. Blood 2013; 122: 2683-2693.
12. Swerdlow SH, Campo E, Seto M, Muller-Hermelink HK. Mantle cell lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H et al. (eds) WHO Classification of Tumors of Haematopoietic and Lymphoid Tissues. IARC: Lyon, France, pp 229-232, 2008.
13. Piccaluga PP, De Falco G, Kustagi M, Gazzola A, Agostinelli C, Tripodo C et al. Gene expression analysis uncovers similarity and differences among Burkitt lymphoma subtypes. Blood 2011; 117: 3596-3608.
14. Bellan C, Lazzi S, Hummel M, Palummo N, de Santi M, Amato T et al. Immunoglobulin gene analysis reveals 2 distinct cells of origin for EBV-positive and EBVnegative Burkitt lymphomas. Blood 2005; 106: 1031-1036.
15. Cattoretti G. PRDM1/BLIMP-1 expression in lymphomas. Haematologica 2006; 91: 434-435.
16. Leucci E, Onnis A, Cocco M, De Falco G, Imperatore F, Giuseppina A et al. B-cell differentiation in EBV-positive Burkitt lymphoma is impaired at posttranscriptional level by miRNA-altered expression. Int J Cancer 2010; 126: 1316-1326.
17. Vrzalikova K, Vockerodt M, Leonard S, Bell A, Wei W, Schrader A et al. Downregulation of BLIMP1alpha by the EBV oncogene, LMP-1, disrupts the plasma cell differentiation program and prevents viral replication in B cells: implications for the pathogenesis of EBV-associated B-cell lymphomas. Blood 2011; 117: 5907-5917.
18. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002; 18: 1427-1431.
19. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T. BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 2005; 21: 4067-4068.
20. Nie K, Gomez M, Landgraf P, Garcia JF, Liu Y, Tan LH et al. MicroRNAmediated down-regulation of PRDM1/Blimp-1 in Hodgkin/Reed-Sternberg cells: a potential pathogenetic lesion in Hodgkin lymphomas. Am J Pathol 2008; 173: 242-252.
21. Speck SH. EBV framed in Burkitt lymphoma. Nat Med 2002; 8: 1086-1087.
22. Kluin PM, Harris NL, Stein H, Leoncini L, Raphael M, Campo E et al. B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma. WHO Classification of Tumors of Haematopoietic and Lymphoid Tissues. IARC: Lyon, France, pp 265-266, 2008.
23. Tunyaplin C, Shaffer AL, Angelin-Duclos CD, Yu X, Staudt LM, Calame KL. Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation. J Immunol 2004; 173: 1158-1165.
24. Masucci MG, Contreras-Salazar B, Ragnar E, Falk K, Minarovits J, Ernberg I et al. 5-Azacytidine up regulates the expression of Epstein-Barr virus nuclear antigen 2 (EBNA-2) through EBNA-6 and latent membrane protein in the Burkitt's lymphoma line rael. J Virol 1989; 63: 3135-3141.
25. Robertson KD, Hayward SD, Ling PD, Samid D, Ambinder RF. Transcriptional activation of the Epstein-Barr virus latency C promoter after 5-azacytidine treatment: evidence that demethylation at a single CpG site is crucial. Mol Cell Biol 1995; 15: 6150-6159.
26. Hangaishi A, Kurokawa M. Blimp-1 is a tumor suppressor gene in lymphoid malignancies. Int J Hematol 2010; 91: 46-53.
27. Iqbal J, Kucuk C, Deleeuw RJ, Srivastava G, Tam W, Geng H et al. Genomic analyses reveal global functional alterations that promote tumor growth and novel tumor suppressor genes in natural killer-cell malignancies. Leukemia 2009; 23: 1139-1151.
28. Cattoretti G, Angelin-Duclos C, Shaknovich R, Zhou H, Wang D, Alobeid B. PRDM1/ Blimp-1 is expressed in human B-lymphocytes committed to the plasma cell lineage. J Pathol 2005; 206: 76-86.
29. Paschos K, Smith P, Anderton E, Middeldorp JM, White RE, Allday MJ. Epstein-Barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim. PLoS Pathogen 2009; 5: e1000492.
30. Bell AI, Groves K, Kelly GL, Croom-Carter D, Hui E, Chan AT et al. Analysis of Epstein-Barr virus latent gene expression in endemic Burkitt's lymphoma and nasopharyngeal carcinoma tumour cells by using quantitative real-time PCR assays. J Gen Virol 2006; 87(Part 10): 2885-2890.
31. Tao Q, Robertson KD, Manns A, Hildesheim A, Ambinder RF. Epstein-Barr virus (EBV) in endemic Burkitt's lymphoma: molecular analysis of primary tumor tissue. Blood 1998; 91: 1373-1381.
32. Bieging KT, Swanson-Mungerson M, Amick AC, Longnecker R. Epstein-Barr virus in Burkitt's lymphoma: a role for latent membrane protein 2A. Cell Cycle 2010; 9: 901-908.
33. Wang H, Nicholas MW, Conway KL, Sen P, Diz R, Tisch RM et al. EBV latent membrane protein 2A induces autoreactive B cell activation and TLR hypersensitivity. J Immunol 2006; 177: 2793-2802.
34. Shore AM, White PC, Hui RC, Essafi A, Lam EW, Rowe M et al. Epstein-Barr virus represses the FoxO1 transcription factor through latent membrane protein 1 and latent membrane protein 2A. J Virol 2006; 80: 11191-11199.
35. Calame K. Activation-dependent induction of Blimp-1. Curr Opin Immunol 2008; 20: 259-264.
36. Laichalk LL, Thorley-Lawson DA. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol 2005; 79: 1296-1307.
37. Thorley-Lawson DA, Allday MJ. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 2008; 6: 913-924.