IFN regulatory factor 8 regulates MDM2 in germinal center B cells

Journal of Immunology

Volumn 183, Issue 5, 2009, Pages 3188-3194

  Zhou, Jeff X ^a   Lee, Chang Hoon ^a   Qi, Chen Feng ^a   Wang, Hongsheng ^a   Naghashfar, Zohreh ^a   Abbasi, Sadia ^a   Morse III, Herbert C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERLEUKIN 21; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; SMALL INTERFERING RNA; BCL6 PROTEIN, MOUSE; DNA BINDING PROTEIN; EPITOPE; INTERFERON REGULATORY FACTOR; MDM2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER CELL CULTURE; CONTROLLED STUDY; DNA STRAND BREAKAGE; DOWN REGULATION; GERMINAL CENTER; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; B CELL LYMPHOMA; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DRUG ANTAGONISM; GENE TARGETING; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; B-LYMPHOCYTE SUBSETS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA BREAKS; DNA-BINDING PROTEINS; EPITOPES, B-LYMPHOCYTE; GENE TARGETING; GERMINAL CENTER; INTERFERON REGULATORY FACTORS; LYMPHOMA, B-CELL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-MDM2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 70349251460     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803693     Document Type: Article

References (46)

1. Maizels, N. 2005. Immunoglobulin gene diversification. Annu. Rev. Genet. 39: 23-46.
2. Brugarolas, J., C. Chandrasekaran, J. I. Gordon, D. Beach, T. Jacks, and G. J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377: 552-557.
3. Deng, C., P. Zhang, J. W. Harper, S. J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82: 675-684.
4. Dulic, V., W. K. Kaufmann, S. J. Wilson, T. D. Tlsty, E. Lees, J. W. Harper, S. J. Elledge, and S. I. Reed. 1994. p53-Dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76: 1013-1023.
5. Shen, Y., and E. White. 2001. p53-Dependent apoptosis pathways. Adv. Cancer Res. 82: 55-84.
6. Phan, R. T., and R. Dalla-Favera. 2004. The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature 432: 635-639.
7. Baron, B. W., J. Anastasi, M. J. Thirman, Y. Furukawa, S. Fears, D. C. Kim, F. Simone, M. Birkenbach, A. Montag, A. Sadhu, et al. 2002. The human programmed cell death-2 (PDCD2) gene is a target of BCL6 repression: implications for a role of BCL6 in the down-regulation of apoptosis. Proc. Natl. Acad. Sci. USA 99: 2860-2865.
8. Phan, R. T., M. Saito, K. Basso, H. Niu, and R. Dalla-Favera. 2005. BCL6 interacts with the transcription factor Miz-1 to suppress the cyclin-dependent kinase inhibitor p21 and cell cycle arrest in germinal center B cells. Nat. Immunol. 6: 1054-1060.
9. Lee, C. H., M. Melchers, H. Wang, T. A. Torrey, R. Slota, C. F. Qi, J. Y. Kim, P. Lugar, H. J. Kong, L. Farrington, et al. 2006. Regulation of the germinal center gene program by IFN regulatory factor 8/IFN consensus sequence binding protein. J. Exp. Med. 203: 63-72.
10. Huang, W., G. Saberwal, E. Horvath, C. Zhu, S. Lindsey, and E. A. Eklund. 2006. Leukemia-associated, constitutively active mutants of SHP2 protein tyrosine phosphatase inhibit NF1 transcriptional activation by the interferon consensus sequence binding protein. Mol. Cell. Biol. 26: 6311-6332.
11. Unlu, S., A. Kumar, W. R. Waterman, J. Tsukada, K. Z. Wang, D. L. Galson, and P. E. Auron. 2007. Phosphorylation of IRF8 in a pre-associated complex with Spi-1/PU.1 and non-phosphorylated Stat1 is critical for LPS induction of the IL1B gene. Mol. Immunol. 44: 3364-3379.
12. Kong, H. J., D. E. Anderson, C. H. Lee, M. K. Jang, T. Tamura, P. Tailor, H. K. Cho, J. Cheong, H. Xiong, H. C. Morse III, and K. Ozato. 2007. Cutting edge: autoantigen Ro52 is an interferon inducible E3 ligase that ubiquitinates IRF-8 and enhances cytokine expression in macrophages. J. Immunol. 179: 26-30.
13. Xiong, H., H. Li, H. J. Kong, Y. Chen, J. Zhao, S. Xiong, B. Huang, H. Gu, L. Mayer, K. Ozato, and J. C. Unkeless. 2005. Ubiquitin-dependent degradation of interferon regulatory factor-8 mediated by Cbl down-regulates interleukin-12 expression. J. Biol. Chem. 280: 23531-23539.
14. Tamura, T., and K. Ozato. 2002. ICSBP/IRF-8: its regulatory roles in the development of myeloid cells. J. Interferon Cytokine Res. 22: 145-152.
15. Tamura, T., P. Thotakura, T. S. Tanaka, M. S. Ko, and K. Ozato. 2005. Identification of target genes and a unique cis element regulated by IRF-8 in developing macrophages. Blood 106: 1938-1947.
16. Wang, H., C. H. Lee, C. Qi, P. Tailor, J. Feng, S. Abbasi, T. Atsumi, and H. C. Morse III. 2008. IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood 112: 4028-4038.
17. Cattoretti, G., R. Shaknovich, P. M. Smith, H. M. Jack, V. V. Murty, and B. Alobeid. 2006. Stages of germinal center transit are defined by B cell transcription factor coexpression and relative abundance. J. Immunol. 177: 6930-6939.
18. Martinez, A., S. Pittaluga, M. Rudelius, T. Davies-Hill, D. Sebasigari, T. J. Fountaine, S. Hewitt, E. S. Jaffe, and M. Raffeld. 2008. Expression of the interferon regulatory factor 8/ICSBP-1 in human reactive lymphoid tissues and B-cell lymphomas: a novel germinal center marker. Am. J. Surg. Pathol. 32: 1190-1200.
19. Momand, J., G. P. Zambetti, D. C. Olson, D. George, and A. J. Levine. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69: 1237-1245.
20. Toledo, F., and G. M. Wahl. 2006. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 6: 909-923. (Pubitemid 44862676)
21. Brooks, C. L., and W. Gu. 2004. Dynamics in the p53-Mdm2 ubiquitination pathway. Cell Cycle 3: 895-899.
22. Roth, J., M. Dobbelstein, D. A. Freedman, T. Shenk, and A. J. Levine. 1998. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17: 554-564.
23. waf1/cip1 proteasomal turnover independently of ubiquitylation. EMBO J. 22: 6365-6377.
24. Bueso-Ramos, C. E., Y. Yang, E. deLeon, P. McCown, S. A. Stass, and M. Albitar. 1993. The human MDM-2 oncogene is overexpressed in leukemias. Blood 82: 2617-2623.
25. Cordon-Cardo, C., E. Latres, M. Drobnjak, M. R. Oliva, D. Pollack, J. M. Woodruff, V. Marechal, J. Chen, M. F. Brennan, and A. J. Levine. 1994. Molecular abnormalities of mdm2 and p53 genes in adult soft tissue sarcomas. Cancer Res. 54: 794-799. (Pubitemid 24068339)
26. Ladanyi, M., C. Cha, R. Lewis, S. C. Jhanwar, A. G. Huvos, and J. H. Healey. 1993. MDM2 gene amplification in metastatic osteosarcoma. Cancer Res. 53: 16-18. (Pubitemid 23019370)
27. Oliner, J. D., K. W. Kinzler, P. S. Meltzer, D. L. George, and B. Vogelstein. 1992. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358: 80-83.
28. Mehta, D. S., A. L. Wurster, M. J. Whitters, D. A. Young, M. Collins, and M. J. Grusby. 2003. IL-21 induces the apoptosis of resting and activated primary B cells. J. Immunol. 170: 4111-4118.
29. Ozaki, K., R. Spolski, C. G. Feng, C. F. Qi, J. Cheng, A. Sher, H. C. Morse III, C. Liu, P. L. Schwartzberg, and W. J. Leonard. 2002. A critical role for IL-21 in regulating immunoglobulin production. Science 298: 1630-1634.
30. Holtschke, T., J. Lohler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K. P. Knobeloch, L. Gabriele, J. F. Waring, et al. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 87: 307-317.
31. Zhang, J. Q., C. Okumura, T. McCarty, M. S. Shin, P. Mukhopadhyay, M. Hori, T. A. Torrey, Z. Naghashfar, J. X. Zhou, C. H. Lee, et al. 2004. Evidence for selective transformation of autoreactive immature plasma cells in mice deficient in Fasl. J. Exp. Med. 200: 1467-1478.
32. Qi, C. F., S. Xiang, M. S. Shin, X. Hao, C. H. Lee, J. X. Zhou, T. A. Torrey, J. W. Hartley, T. N. Fredrickson, and H. C. Morse III. 2006. Expression of the cyclin-dependent kinase inhibitor p27 and its deregulation in mouse B cell lymphomas. Leuk. Res. 30: 153-163.
33. Slack, A., Z. Chen, R. Tonelli, M. Pule, L. Hunt, A. Pession, and J. M. Shohet. 2005. The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc. Natl. Acad. Sci. USA 102: 731-736.
34. Kanno, Y., B. Z. Levi, T. Tamura, and K. Ozato. 2005. Immune cell-specific amplification of interferon signaling by the IRF-4/8-PU.1 complex. J. Interferon Cytokine Res. 25: 770-779.
35. Lee, T. I., S. E. Johnstone, and R. A. Young. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1: 729-748.
36. Chang, C. J., D. J. Freeman, and H. Wu. 2004. PTEN regulates Mdm2 expression through the P1 promoter. J. Biol. Chem. 279: 29841-29848.
37. Smith, G. P. 1978. Sequence of the full-length immunoglobulin κ-chain of mouse myeloma MPC11. Biochem. J. 171: 337-347. (Pubitemid 8332710)
38. Zhang, Z., H. Wang, M. Li, S. Agrawal, X. Chen, and R. Zhang. 2004. MDM2 is a negative regulator of p21WAF1/CIP1, independent of p53. J. Biol. Chem. 279: 16000-16006.
39. Chtanova, T., S. G. Tangye, R. Newton, N. Frank, M. R. Hodge, M. S. Rolph, and C. R. Mackay. 2004. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J. Immunol. 173: 68-78.
40. Vinuesa, C. G., S. G. Tangye, B. Moser, and C. R. Mackay. 2005. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 5: 853-865.
41. Klein, U., Y. Tu, G. A. Stolovitzky, J. L. Keller, J. Haddad, Jr., V. Miljkovic, G. Cattoretti, A. Califano, and R. Dalla-Favera. 2003. Transcriptional analysis of the B cell germinal center reaction. Proc. Natl. Acad. Sci. USA 100: 2639-2644.
42. Bettess, M. D., N. Dubois, M. J. Murphy, C. Dubey, C. Roger, S. Robine, and A. Trumpp. 2005. c-Myc is required for the formation of intestinal crypts but dispensable for homeostasis of the adult intestinal epithelium. Mol. Cell. Biol. 25: 7868-7878.
43. Pasqualucci, L., A. Migliazza, K. Basso, J. Houldsworth, R. S. Chaganti, and R. Dalla-Favera. 2003. Mutations of the BCL6 proto-oncogene disrupt its negative autoregulation in diffuse large B-cell lymphoma. Blood 101: 2914-2923. (Pubitemid 36857975)
44. Ye, B. H., F. Lista, F. Lo Coco, D. M. Knowles, K. Offit, R. S. Chaganti, and R. Dalla-Favera. 1993. Alterations of a zinc finger-encoding gene, BCL-6, in diffuse large-cell lymphoma. Science 262: 747-750.
45. Toney, L. M., G. Cattoretti, J. A. Graf, T. Merghoub, P. P. Pandolfi, R. Dalla-Favera, B. H. Ye, and A. L. Dent. 2000. BCL-6 regulates chemokine gene transcription in macrophages. Nat. Immunol. 1: 214-220.
46. Pantano, S., D. Jarrossay, S. Saccani, D. Bosisio, and G. Natoli. 2006. Plastic downregulation of the transcriptional repressor BCL6 during maturation of human dendritic cells. Exp. Cell Res. 312: 1312-1322.