C-Myc overexpression promotes a germinal center-like program in Burkitt's lymphoma

Oncogene

Volumn 29, Issue 6, 2010, Pages 888-897

  Scheller, H ^a   Tobollik, S ^a   Kutzera, A ^a   Eder, M ^a   Unterlehberg, J ^a   Pfeil, I ^a   Jungnickel, B ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Burkitt's lymphoma; C Myc; Germinal center; Somatic hypermutation

Indexed keywords

CYTIDINE DEAMINASE; PROTEIN BCL 6; TRANSCRIPTION FACTOR E2A;

ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; BURKITT LYMPHOMA; CARCINOGENESIS; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE OVEREXPRESSION; GERMINAL CENTER; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; ONCOGENE C MYC; PRIORITY JOURNAL; SOMATIC HYPERMUTATION;

ANIMALS; B-LYMPHOCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BURKITT LYMPHOMA; CELL LINE, TUMOR; CYTIDINE DEAMINASE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GERMINAL CENTER; HUMANS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-MYC; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 76849112497     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.377     Document Type: Article

References (51)

1. Adams JM, Gerondakis S, Webb E, Corcoran LM, Cory S. (1983). Cellular myc oncogene is altered by chromosome translocation to an immunoglobulin locus in murine plasmacytomas and is rearranged similarly in human Burkitt lymphomas. Proc Natl Acad Sci USA 80: 1982-1986.
2. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S et al. (1985). The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
3. Aiello A, Delia D, Fontanella E, Giardini R, Rilke F, Della Porta G. (1990). Expression of differentiation and adhesion molecules in sporadic Burkitt's lymphoma. Hematol Oncol 8: 229-238.
4. Bachl J, Olsson C. (1999). Hypermutation targets a green fluorescent protein-encoding transgene in the presence of immunoglobulin enhancers. Eur J Immunol 29: 1383-1389.
5. Cattoretti G, Pasqualucci L, Ballon G, Tam W, Nandula SV, Shen Q et al. (2005). Deregulated BCL6 expression recapitulates the pathogenesis of human diffuse large B cell lymphomas in mice. Cancer Cell 7: 445-455.
6. Chapman CJ, Wright D, Stevenson FK. (1998). Insight into Burkitt's lymphoma from immunoglobulin variable region gene analysis. Leuk Lymphoma 30: 257-267. (Pubitemid 28391042)
7. Chesi M, Robbiani DF, Sebag M, Chng WJ, Affer M, Tiedemann R et al. (2008). AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell 13: 167-180.
8. Cole MD, Cowling VH. (2008). Transcription-independent functions of MYC: regulation of translation and DNA replication. Nat Rev Mol Cell Biol 9: 810-815.
9. Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallo RC, Croce CM. (1982). Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci USA 79: 7824-7827.
10. Dedeoglu F, Horwitz B, Chaudhuri J, Alt FW, Geha RS. (2004). Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NFkappaB. Int Immunol 16: 395-404.
11. Di Noia JM, Neuberger MS. (2007). Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 76: 1-22.
12. Faili A, Aoufouchi S, Gueranger Q, Zober C, Leon A, Bertocci B et al. (2002). AID-dependent somatic hypermutation occurs as a DNA single-strand event in the BL2 cell line. Nat Immunol 3: 815-821.
13. Gavioli R, Frisan T, Vertuani S, Bornkamm GW, Masucci MG. (2001). c-myc overexpression activates alternative pathways for intracellular proteolysis in lymphoma cells. Nat Cell Biol 3: 283-288.
14. Honjo T, Kinoshita K, Muramatsu M. (2002). Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu Rev Immunol 20: 165-196.
15. Johnston JM, Yu MT, Carroll WL. (1991). c-myc hypermutation is ongoing in endemic, but not all Burkitt's lymphoma. Blood 78: 2419-2425.
16. Khuda SE, Loo WM, Janz S, Van Ness B, Erickson LD. (2008). Deregulation of c-Myc confers distinct survival requirements for memory B cells, plasma cells, and their progenitors. J Immunol 181: 7537-7549.
17. Klein U, Goossens T, Fischer M, Kanzler H, Braeuninger A, Rajewsky K et al. (1998). Somatic hypermutation in normal and transformed human B cells. Immunol Rev 162: 261-280.
18. Klein U, Klein G, Ehlin-Henriksson B, Rajewsky K, Kuppers R. (1995). Burkitt's lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol Med 1: 495-505.
19. Klein U, Tu Y, Stolovitzky GA, Keller JL, Haddad Jr J, Miljkovic V et al. (2003). Transcriptional analysis of the B cell germinal center reaction. Proc Natl Acad Sci USA 100: 2639-2644.
20. Kovalchuk AL, Qi CF, Torrey TA, Taddesse-Heath L, Feigenbaum L, Park SS et al. (2000). Burkitt lymphoma in the mouse. J Exp Med 192: 1183-1190.
21. Kuppers R, Dalla-Favera R. (2001). Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene 20: 5580-5594.
22. Kuppers R, Klein U, Hansmann ML, Rajewsky K. (1999). Cellular origin of human B-cell lymphomas. N Engl J Med 341: 1520-1529.
23. Lee SC, Bottaro A, Chen L, Insel RA. (2006). Mad1 is a transcriptional repressor of Bcl-6. Mol Immunol 43: 1965-1971.
24. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, Kleinstein SH et al. (2008). Two levels of protection for the B cell genome during somatic hypermutation. Nature 451: 841-845.
25. Martinez-Valdez H, Guret C, de Bouteiller O, Fugier I, Banchereau J, Liu YJ. (1996). Human germinal center B cells express the apoptosis-inducing genes Fas, c-myc, P53, and Bax but not the survival gene bcl-2. J Exp Med 183: 971-977.
26. Mierau M, Drexler GA, Kutzera A, Braunschmidt K, Ellwart J, Eckardt-Schupp F et al. (2008). Non-conservative homologous recombination in human B lymphocytes is promoted by activation-induced cytidine deaminase and transcription. Nucleic Acids Res 36: 5591-5601.
27. Niu H, Ye BH, Dalla-Favera R. (1998). Antigen receptor signaling induces MAP kinase-mediated phosphorylation and degradation of the BCL-6 transcription factor. Genes Dev 12: 1953-1961.
28. Pajic A, Staege MS, Dudziak D, Schuhmacher M, Spitkovsky D, Eissner G et al. (2001). Antagonistic effects of c-myc and Epstein-Barr virus latent genes on the phenotype of human B cells. Int J Cancer 93: 810-816.
29. Pasqualucci L, Migliazza A, Basso K, Houldsworth J, Chaganti RS, Dalla-Favera R. (2003). Mutations of the BCL6 proto-oncogene disrupt its negative autoregulation in diffuse large B-cell lymphoma. Blood 101: 2914-2923. (Pubitemid 36857975)
30. Pasqualucci L, Migliazza A, Fracchiolla N, William C, Neri A, Baldini L et al. (1998). BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc Natl Acad Sci USA 95: 11816-11821.
31. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, Kuppers R et al. (2001). Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412: 341-346.
32. Polack A, Feederle R, Klobeck G, Hortnagel K. (1993). Regulatory elements in the immunoglobulin kappa locus induce c-myc activation and the promoter shift in Burkitt's lymphoma cells. EMBO J 12: 3913-3920.
33. Polack A, Hortnagel K, Pajic A, Christoph B, Baier B, Falk M et al. (1996). c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc Natl Acad Sci USA 93: 10411-10416.
34. Rajewsky K. (1996). Clonal selection and learning in the antibody system. Nature 381: 751-758. (Pubitemid 26243107)
35. Refaeli Y, Young RM, Turner BC, Duda J, Field KA, Bishop JM. (2008). The B cell antigen receptor and overexpression of MYC can cooperate in the genesis of B cell lymphomas. PLoS Biol 6: e152.
36. Ruckerl F, Busse B, Bachl J. (2006). Episomal vectors to monitor and induce somatic hypermutation in human Burkitt-Lymphoma cell lines. Mol Immunol 43: 1645-1652.
37. Rutherford MN, LeBrun DP. (1998). Restricted expression of E2A protein in primary human tissues correlates with proliferation and differentiation. Am J Pathol 153: 165-173.
38. Saito M, Gao J, Basso K, Kitagawa Y, Smith PM, Bhagat G et al. (2007). A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 12: 280-292. (Pubitemid 47333420)
39. Sayegh CE, Quong MW, Agata Y, Murre C. (2003). E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nat Immunol 4: 586-593.
40. Schoetz U, Cervelli M, Wang YD, Fiedler P, Buerstedde JM. (2006). E2A expression stimulates Ig hypermutation. J Immunol 177: 395-400.
41. Schuhmacher M, Kohlhuber F, Holzel M, Kaiser C, Burtscher H, Jarsch M et al. (2001). The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res 29: 397-406.
42. Shaffer AL, Rosenwald A, Hurt EM, Giltnane JM, Lam LT, Pickeral OK et al. (2001). Signatures of the immune response. Immunity 15: 375-385.
43. Shen HM, Peters A, Baron B, Zhu X, Storb U. (1998). Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280: 1750-1752.
44. Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T, Casellas R et al. (2008). MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28: 621-629.
45. Thorley-Lawson DA, Allday MJ. (2008). The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 6: 913-924.
46. Toyama H, Okada S, Hatano M, Takahashi Y, Takeda N, Ichii H et al. (2002). Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity 17: 329-339.
47. Wagner SD, Amen F, Trivedi PS, Horncastle D, Elderfield K, Naresh KN. (2007). Bcl-6 and c-Myc are rarely co-expressed in adult diffuse large B-cell lymphoma. Leuk Lymphoma 48: 1510-1513.
48. Wang CL, Wabl M. (2005). Hypermutation rate normalized by chronological time. J Immunol 174: 5650-5654.
49. Yin X, Giap C, Lazo JS, Prochownik EV. (2003). Low molecular weight inhibitors of Myc-Max interaction and function. Oncogene 22: 6151-6159.
50. Yoshikawa K, Okazaki IM, Eto T, Kinoshita K, Muramatsu M, Nagaoka H et al. (2002). AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 296: 2033-2036.
51. Zhang W, Bardwell PD, Woo CJ, Poltoratsky V, Scharff MD, Martin A. (2001). Clonal instability of V region hypermutation in the Ramos Burkitt's lymphoma cell line. Int Immunol 13: 1175-1184.