c-MYC activation impairs the NF-κB and the interferon response: Implications for the pathogenesis of Burkitt's lymphoma

International Journal of Cancer

Volumn 120, Issue 7, 2007, Pages 1387-1395

  Schlee, Martin ^a   Hölzel, Michael ^a   Bernard, Sandra ^b   Mailhammer, Reinhard ^a   Schuhmacher, Marino ^c   Reschke, Judith ^a   Eick, Dirk ^a   Marinkovic, Dragan ^d   Wirth, Thomas ^d   Rosenwald, Andreas ^e   Staudt, Louis M ^e   Eilers, Martin ^b   Baran Marszak, Fanny ^f   Fagard, Remi ^g   Feuillard, Jean ^g   Laux, Gerhard ^a   Bornkamm, Georg W ^a,h  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c GPC Biotech AG   (Germany)

^d UNIVERSITY OF ULM   (Germany)

^e NATIONAL CANCER INSTITUTE   (United States)

^f UNIVERSITÉ PARIS 13   (France)

^g CNRS   (France)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Antigen presentation; Burkitt's lymphoma; c myc; Interferon; NF B; STAT1

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; DOXYCYCLINE; EPSTEIN BARR VIRUS ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; RNA; STAT1 PROTEIN; STAT2 PROTEIN; TETRACYCLINE;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE ACTIVATION; GENE OVEREXPRESSION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE C MYC; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; VERO CELL;

BLOTTING, WESTERN; BURKITT LYMPHOMA; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; HUMANS; INTERFERON-BETA; MICROARRAY ANALYSIS; NEOPLASM PROTEINS; NF-KAPPA B; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 33847662881     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22372     Document Type: Article

References (57)

1. Nalesnik MA, Starzl TE. Epstein-Barr virus, infectious mononucleosis, and posttransplant lymphoproliferative disorders. Transplant Sci 1994;4:61-79.
2. Young L, Alfieri C, Hennessy K, Evans H, O'Hara C, Anderson KC, Ritz J, Shapiro RS, Rickinson A, Kieff E, Cohen JI. Expression of Epstein-Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease. N Engl J Med 1989;321:1080-5.
3. Delecluse HJ, Kremmer E, Rouault JP, Cour C, Bornkamm G, Berger F. The expression of Epstein-Barr virus latent proteins is related to the pathological features of post-transplant lymphoproliferative disorders. Am J Pathol 1995;146:1113-20.
4. Rooney CM, Smith CA, Ng CY, Loftin S, Li C, Krance RA, Brenner MK, Heslop HE. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 1995;345:9-13.
5. Haque T, Wilkie GM, Taylor C, Amlot PL, Murad P, Iley A, Dombagoda D, Britton KM, Swerdlow AJ, Crawford DH. Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 2002;360:436-42.
6. Lenoir GM, Bornkamm GW. Burkitt's lymphoma, a human cancer model for the study of the multistep development of cancer: proposal of a new scenario. In: Klein G, ed. Advances in viral oncology, vol.7. New York: Raven, 1987:173-206.
7. Magrath I. The pathogenesis of Burkitt's lymphoma. Adv Cancer Res 1990;55:133-270.
8. Rooney CM, Gregory CD, Rowe M, Finerty S, Edwards C, Rupani H, Rickinson AB. Endemic Burkitt's lymphoma: phenotypic analysis of tumor biopsy cells and of derived tumor cell lines. J Natl Cancer Inst 1986;77:681-7.
9. Avila-Carino J, Torsteinsdottir S, Ehlin-Henriksson B, Lenoir G, Klein G, Klein E, Masucci MG. Paired Epstein-Barr virus (EBV)-negative and EBV-converted Burkitt lymphoma lines: stimulatory capacity in allogeneic mixed lymphocyte cultures. Int J Cancer 1987;40:691-7.
10. Khanna R, Burrows SR, Argaet V, Moss DJ. Endoplasmic reticulum signal sequence facilitated transport of peptide epitopes restores immunogenicity of an antigen processing defective tumour cell line. Int Immunol 1994;6:639-45.
11. Rowe M, Khanna R, Jacob CA, Argaet V, Kelly A, Powis S, Belich M, Croom-Carter D, Lee S, Burrows SR, Trowsdale J, Moss DJ et al. Restoration of endogenous antigen processing in Burkitt's lymphoma cells by Epstein-Barr virus latent membrane protein-1: coordinate up-regulation of peptide transporters and HLA-class I antigen expression. Eur J Immunol 1995;25:1374-84.
12. Frisan T, Zhang QJ, Levitskaya J, Coram M, Kurilla MG, Masucci MG. Defective presentation of MHC class I-restricted cytotoxic T-cell epitopes in Burkitt's lymphoma cells. Int J Cancer 1996;68:251-8.
13. Frisan T, Levitsky V, Polack A, Masucci MG. Phenotype-dependent differences in proteasome subunit composition and cleavage specificity in B cell lines. J Immunol 1998;160:3281-9.
14. Gavioli R, Frisan T, Vertuani S, Bornkamm GW, Masucci MG. c-myc overexpression activates alternative pathways for intracellular proteolysis in lymphoma cells. Nat Cell Biol 2001;3:283-8.
15. Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G, Kurilla MG, Masucci MG. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 1995;375:685-8.
16. Lee SP, Brooks JM, Al-Jarrah H, Thomas WA, Haigh TA, Taylor GS, Humme S, Schepers A, Hammerschmidt W, Yates JL, Rickinson AB, Blake NW. CD8 T cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J Exp Med 2004;199:1409-20.
17. Tellam J, Connolly G, Green KJ, Miles JJ, Moss DJ, Burrows SR, Khanna R. Endogenous presentation of CD8+ T cell epitopes from Epstein-Barr virus-encoded nuclear antigen 1. J Exp Med 2004;199:1421-31.
18. Kelly G, Bell A, Rickinson A. Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat Med 2002;8:1098-104.
19. Kempkes B, Spitkovsky D, Jansen-Durr P, Ellwart JW, Kremmer E, Delecluse HJ, Rottenberger C, Bornkamm GW, Hammerschmidt W. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J 1995;14:88-96.
20. Polack A, Hortnagel K, Pajic A, Christoph B, Baier B, Falk M, Mautner J, Geltinger C, Bornkamm GW, Kempkes B. 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 1996;93:10411-16.
21. Schuhmacher M, Kohlhuber F, Holzel M, Kaiser C, Burtscher H, Jarsch M, Bornkamm GW, Laux G, Polack A, Weidle UH, Eick D. The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res 2001;29:397-406.
22. Pajic A, Staege MS, Dudziak D, Schuhmacher M, Spitkovsky D, Eissner G, Brielmeier M, Polack A, Bornkamm GW. Antagonistic effects of c-myc and Epstein-Barr virus latent genes on the phenotype of human B cells. Int J Cancer 2001;93:810-16.
23. Staege MS, Lee SP, Frisan T, Mautner J, Scholz S, Pajic A, Rickinson AB, Masucci MG, Polack A, Bornkamm GW. MYC overexpression imposes a nonimmunogenic phenotype on Epstein-Barr virus-infected B cells. Proc Natl Acad Sci USA 2002;99:4550-5.
24. Diaz MO, Ziemin S, Le Beau MM, Pitha P, Smith SD, Chilcote RR, Rowley JD. Homozygous deletion of the α- and β 1-interferon genes in human leukemia and derived cell lines. Proc Natl Acad Sci USA 1988;85:5259-63.
25. Marinkovic D, Marinkovic T, Mahr B, Hess J, Wirth T. Reversible lymphomagenesis in conditionally c-MYC expressing mice. Int J Cancer 2004;110:336-42.
26. Schuhmacher M, Staege MS, Pajic A, Polack A, Weidle UH, Bornkamm GW, Eick D, Kohlhuber F. Control of cell growth by c-Myc in the absence of cell division. Curr Biol 1999;9:1255-8.
27. Alizadeh AA, Eisen MB, Davis RE, Ma C, Losses IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000;403:503-11.
28. Najjar I, Baran-Marszak F, Le Clorennec C, Laguillier C, Schischmanoff O, Youlyouz-Marfak I, Schlee M, Bornkamm GW, Raphael M, Feuillard J, Fagard R. Latent membrane protein 1 regulates STAT1 through NF-κB-dependent interferon secretion in Epstein-Barr virus-immortalized B cells. J Virol 2005;79:4936-43.
29. Staller P, Peukert K, Kiermaier A, Seoane J, Lukas J, Karsunky H, Moroy T, Bartek J, Massague J, Hanel F, Eilers M. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol 2001;3:392-9.
30. Pahl HL. Activators and target genes of Rel/NF-κB transcription factors. Oncogene 1999;18:6853-66.
31. Cahir-McFarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, Staudt LM, Kieff E. Role of NF-αB in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J Virol 2004;78:4108-19.
32. Dirmeier U, Hoffmann R, Kilger E, Schultheiss U, Briseno C, Gires O, Kieser A, Eick D, Sugden B, Hammerschmidt W. Latent membrane protein 1 of Epstein-Barr virus coordinately regulates proliferation with control of apoptosis. Oncogene 2005;24:1711-17.
33. You Z, Madrid LV, Saims D, Sedivy J, Wang CY. c-Myc sensitizes cells to tumor necrosis factor-mediated apoptosis by inhibiting nuclear factor κB transactivation. J Biol Chem 2002;277:36671-7.
34. Tanaka H, Matsumura I, Ezoe S, Satoh Y, Sakamaki T, Albanese C, Machii T, Pestell RG, Kanakura Y. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-κB activity that facilitates MnSOD-mediated ROS elimination. Mol Cell 2002;9:1017-29.
35. Eischen CM, Woo D, Roussel MF, Cleveland JL. Apoptosis triggered by Myc-induced suppression of Bc1-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol Cell Biol 2001;21:5063-70.
36. Keller U, Nilsson JA, Maclean KH, Old JB, Cleveland JL. Nfkb1 is dispensable for Myc-induced lymphomagenesis. Oncogene 2005;24:6231-40.
37. de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BR. Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol 2001;69:912-20.
38. Der SD, Zhou A, Williams BR, Silverman RH. Identification of genes differentially regulated by interferon α, β, or γ using oligonucleotide arrays. Proc Natl Acad Sci USA 1998;95:15623-8.
39. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998;67:227-64.
40. Richardson C, Fielding C, Rowe M, Brennan P. Epstein-Barr virus regulates STAT1 through latent membrane protein 1. J Virol 2003;77:4439-43.
41. Kaiser C, Laux G, Eick D, Jochner N, Bornkamm GW, Kempkes B. The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J Virol 1999;73:4481-4.
42. Bornkamm GW, Berens C, Kuklik-Roos C, Bechet JM, Laux G, Bachl J, Korndoerfer M, Schlee M, Holzel M, Malamoussi A, Chapman RD, Nimmerjahn F et al. Stringent doxycycline-dependent control of gene activities using an episomal one-vector system. Nucleic Acids Res 2005;33:e137.
43. Hiscott J, Grandvaux N, Sharma S, Tenoever BR, Servant MJ, Lin R. Convergence of the NF-κB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann NY Acad Sci 2003;1010:237-48.
44. Ramana CV, Grammatikakis N, Chernov M, Nguyen H, Goh KC, Williams BR, Stark GR. Regulation of c-myc expression by IFN-γ through Stat1-dependent and -independent pathways. EMBO J 2000;19:263-72.
45. Oberg F, Larsson LG, Anton R, Nilsson K. Interferon γ abrogates the differentiation block in v-myc-expressing U-937 monoblasts. Proc Natl Acad Sci USA 1991;88:5567-71.
46. Kirchhoff S, Schaper F, Hauser H. Interferon regulatory factor 1 (IRF-1) mediates cell growth inhibition by transactivation of downstream target genes. Nucleic Acids Res 1993;21:2881-9.
47. Tanaka N, Ishihara M, Taniguchi T. Suppression of c-myc or fosB-induced cell transformation by the transcription factor IRF-1. Cancer Lett 1994;83(1/2):191-6.
48. Kroger A, Dallugge A, Kirchhoff S, Hauser H. IRF-1 reverts the transformed phenotype of oncogenically transformed cells in vitro and in vivo. Oncogene 2003;22:1045-56.
49. Holtschke T, Lohler J, Kanno Y, Fehr T, Giese N, Rosenbauer F, Lou J, Knobeloch KP, Gabriele L, Waring JF, Bachmann MF, Zinkernagel RM et al. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 1996;87:307-17.
50. Tanaka N, Ishihara M, Kitagawa M, Harada H, Kimura T, Matsuyama T, Lamphier MS, Aizawa S, Mak TW, Taniguchi T. Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1. Cell 1994;77:829-39.
51. Nozawa H, Oda E, Nakao K, Ishihara M, Ueda S, Yokochi T, Ogasawara K, Nakatsuru Y, Shimizu S, Ohira Y, Hioki K, Aizawa S et al. Loss of transcription factor IRF-1 affects tumor susceptibility in mice carrying the Ha-ras transgene or nullizygosity for p53. Genes Dev 1999;13:1240-5.
52. Kaplan DH, Shankaran V, Dighe AS, Stocken E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 1998;95:7556-61.
53. Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H, Kikuchi H, Sasaki S, Imai K, Shibue T, Honda K, Taniguchi T. Integration of interferon-α/ β signalling to p53 responses in tumour suppression and antiviral defence. Nature 2003;424:516-23.
54. Baran-Marszak F, Feuillard J, Najjar I, Le Clorennec C, Bechet JM, Dusanter-Fourt I, Bornkamm GW, Raphael M, Fagard R. Differential roles of STAT1α and STAT1β in fludarabine-induced cell cycle arrest and apoptosis in human B cells. Blood 2004;104:2475-83.
55. Townsend PA, Cragg MS, Davidson SM, McCormick J, Barry S, Lawrence KM, Knight RA, Hubank M, Chen PL, Latchman DS, Stephanou A. STAT-1 facilitates the ATM activated checkpoint pathway following DNA damage. J Cell Sci 2005;118 (Part 8):1629-39.
56. Townsend PA, Scarabelli TM, Davidson SM, Knight RA, Latchman DS, Stephanou A. STAT-1 interacts with p53 to enhance DNA damage-induced apoptosis. J Biol Chem 2004;279:5811-20.
57. Ouchi T, Lee SW, Ouchi M, Aaronson SA, Horvath CM. Collaboration of signal transducer and activator of transcription 1 (STAT1) and BRCA1 in differential regulation of IFN-γ target genes. Proc Natl Acad Sci USA 2000;97:5208-13.