c-Maf interacts with c-Myb to down-regulate Bcl-2 expression and increase apoptosis in peripheral CD4 cells

European Journal of Immunology

Volumn 37, Issue 10, 2007, Pages 2868-2880

  Peng, Siying ^a   Lalani, Saif ^a   Leavenworth, Jianmei W ^a   Ho, I Cheng ^b   Pauza, Mary E ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Apoptosis; CD4 T cells; Transcription factors

Indexed keywords

DEXAMETHASONE; FAS ANTIGEN; GROWTH FACTOR; PROTEIN BCL 2; PROTEIN C MYB; PROTEIN P53; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR C MAF;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL STIMULATION; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; HUMORAL IMMUNITY; IRRADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; TRANSGENE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; CELLS, CULTURED; DOWN-REGULATION; HUMANS; MICE; MICE, TRANSGENIC; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MAF; PROTO-ONCOGENE PROTEINS C-MYB; RECEPTORS, ANTIGEN, T-CELL;

EID: 35348834173     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636979     Document Type: Article

References (72)

1. Kerppola, T. K. and Curran, T., A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins. Oncogene 1994. 9: 3149-3158.
2. Ho, I. C., Hodge, M. R., Rooney, J. W. and Glimcher, L. H., The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 1996. 85: 973-983.
3. Hodge, M. R., Chun, H. J., Rengarajan, J., Alt, A., Lieberson, R. and Glimcher, L. H., NF-AT-driven interleukin-4 transcription potentiated by NIP45. Science 1996. 274: 1903-1905.
4. Li, B., Tournier, C., Davis, R. J. and Flavell, R. A., Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 1999. 18: 420-432.
5. Pauza, M. E., Nguyen, A., Wolfe, T., Ho, I. C., Glimcher, L. H., von Herrath, M. and Lo, D., Variable effects of transgenic c-Maf on autoimmune diabetes. Diabetes 2001. 50: 39-46.
6. Ho, I. C., Lo, D. and Glimcher, L. H., c-Maf promotes T helper cell type 2 (Th2) and attenuates Th1 differentiation by both interleukin 4-dependent and -independent mechanisms. J. Exp. Med. 1998. 188: 1859-1866.
7. Kim, J. I., Ho, I. C., Grusby, M. J. and Glimcher, L. H., The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity 1999. 10: 745-751.
8. Sakai, M., Imaki, J., Yoshida, K., Ogata, A., Matsushima-Hibaya, Y., Kuboki, Y., Nishizawa, M. and Nishi, S., Rat maf related genes: Specific expression in chondrocytes, lens and spinal cord. Oncogene 1997. 14: 745-750.
9. Kawauchi, S., Takahashi, S., Nakajima, O., Ogino, H., Morita, M., Nishizawa, M., Yasuda, K. and Yamamoto, M., Regulation of lens fiber cell differentiation by transcription factor c-Maf. J. Biol. Chem. 1999. 274: 19254-19260.
10. Ogata, A., Shimizu, T., Abe, R., Shimizu, H. and Sakai, M., Expression of c-maf and mafB genes in the skin during rat embryonic development. Acta Histochem. 2004. 106: 65-67.
11. Huang, W., Lu, N., Eberspaecher, H. and De Crombrugghe, B., A new long form of c-Maf cooperates with Sox9 to activate the type II collagen gene. J. Biol. Chem. 2002. 277: 50668-50675.
12. MacLean, H. E., Kim, J. I., Glimcher, M. J., Wang, J., Kronenberg, H. M. and Glimcher, L. H., Absence of transcription factor c-Maf causes abnormal terminal differentiation of hypertrophic chondrocytes during endochondral bone development. Dev. Biol. 2003. 262: 51-63.
13. Li, M. Z., Wang, J. S., Jiang, D. J., Xiang, C. X., Wang, F. Y., Zhang, K H., Williams, P. R., and Chen, Z. F., Molecular mapping of developing dorsal horn-enriched genes by microarray and dorsal/ventral subtractive screening. Dev. Biol. 2006. 292: 555-564.
14. Kurschner, C. and Morgan, J. I., The maf proto-oncogene stimulates transcription from multiple sites in a promoter that directs Purkinje neuron-specific gene expression. Mol. Cell. Biol. 1995. 15: 246-254.
15. Dhakshinamoorthy, S. and Jaiswal, A. K., c-Maf negatively regulates ARE-mediated detoxifying enzyme genes expression and anti-oxidant induction. Oncogene 2002. 21: 5301-5312.
16. Hurt, E. M., Wiestner, A., Rosenwald, A., Shaffer, A. L., Campo, E., Grogan, T., Bergsagel, P. L. et al., Overexpression of c-maf is a frequent oncogenic event in multiple myeloma that promotes proliferation and pathological interactions with bone marrow stroma. Cancer Cell 2004. 5: 191-199.
17. Civil, A., van Genesen, S. T. and Lubsen, N. H., c-Maf, the gammaD-crystallin Maf-responsive element and growth factor regulation. Nucleic Acids Res. 2002. 30: 975-982.
18. Hale, T. K., Myers, C., Maitra, R., Kolzau, T., Nishizawa, M. and Braithwaite, A. W., Maf transcriptionally activates the mouse p53 promoter and causes a p53-dependent cell death. J. Biol. Chem. 2000. 275: 17991-17999.
19. Hwang, E. S., White, I. A. and Ho, I. C., An IL-4-independent and CD25-mediated function of c-maf in promoting the production of Th2 cytokines. Proc. Natl. Acad. Sci. USA 2002. 99: 13026-13030.
20. Khaled, A. R. and Durum, S. K., Death and Baxes: Mechanisms of lymphotrophic cytokines. Immunol. Rev. 2003. 193: 48-57.
21. Schluns, K. S. and Lefrancois, L., Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 2003. 3: 269-279.
22. Sprent, J. and Surh, C. D., Cytokines and T cell homeostasis. Immunol. Lett. 2003. 85: 145-149.
23. Di Santo, J. P., Colucci, F. and Guy-Grand, D., Natural killer and T cells of innate and adaptive immunity: Lymphoid compartments with different requirements for common gamma chain-dependent cytokines. Immunol Rev. 1998. 165: 29-38.
24. Li, X. C., Demirci, G., Ferrari-Lacraz, S., Groves, C., Coyle, A., Malek, T. R. and Strom, T. B., IL-15 and IL-2: A matter of life and death for T cells in vivo. Nat. Med. 2001. 7: 114-118.
25. Mor, F. and Cohen, I. R., IL-2 rescues antigen-specific T cells from radiation or dexamethasone-induced apoptosis. Correlation with induction of Bcl-2. J. Immunol. 1996. 156: 515-522.
26. + helper T cells. A model for the long-term survival of memory cells. J. Immunol. 1996. 156: 1764-1771.
27. Smith, K. A., Interleukin-2: Inception, impact, and implications. Science 1988. 240: 1169-1176.
28. Tan, J. T., Dudl, E., LeRoy, E., Murray, R., Sprent, J., Weinberg, K. I. and Surh, C. D., IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. USA 2001. 98: 8732-8737.
29. He, Y. W. and Malek, T. R., The structure and function of gamma c-dependent cytokines and receptors: Regulation of T lymphocyte development and homeostasis. Crit. Rev. Immunol. 1998. 18: 503-524.
30. Duke, R. C. and Cohen, J. J., IL-2 addiction: Withdrawal of growth factor activates a suicide program in dependent T cells. Lymphokine Res. 1986. 5: 289-299.
31. Szczylik, C. and Wiktor-Jedrzejczak, W., The effects of X-irradiation in vitro on subpopulations of human lymphocytes. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1981. 39: 253-263.
32. Anderson, R. E., Olson, G. B., Autry, J. R., Howarth, J. L., Troup, G. M. and Bartels, P. H., Radiosensitivity of T and B lymphocytes. IV. Effect of whole body irradiation upon various lymphoid tissues and numbers of recirculating lymphocytes. J. Immunol. 1977. 118: 1191-1200.
33. Zacharchuk, C. M., Mercep, M., Chakraborti, P. K., Simons, S. S., Jr. and Ashwell, J. D., Programmed T lymphocyte death. Cell activation- and steroid-induced pathways are mutually antagonistic. J. Immunol. 1990. 145: 4037-4045.
34. Lenardo, M., Chan, K. M., Hornung, F., McFarland, H., Siegel, R., Wang, J. and Zheng, L., Mature T lymphocyte apoptosis - immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 1999. 17: 221-253.
35. Strasser, A., Harris, A. W., Jacks, T. and Cory, S., DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 1994. 79: 329-339.
36. Lowe, S. W., Schmitt, E. M., Smith, S. W., Osborne, B. A. and Jacks, T., p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 1993. 362: 847-849.
37. Lowe, S. W., Ruley, H. E., Jacks, T. and Housman, D. E., p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993. 74: 957-967.
38. Hegde, S. P., Zhao, J., Ashmun, R. A. and Shapiro, L. H., c-Maf induces monocytic differentiation and apoptosis in bipotent myeloid progenitors. Blood 1999. 94: 1578-1589.
39. Hedge, S. P., Kumar, A., Kurschner, C. and Shapiro, L. H., c-Maf interacts with c-Myb to regulate transcription of an early myeloid gene during differentiation. Mol. Cell. Biol. 1998. 18: 2729-2737.
40. Badiani, P., Corbella, P., Kioussis, D., Marvel, J. and Weston, K., Dominant interfering alleles define a role for c-Myb in T-cell development. Genes Dev. 1994. 8: 770-782.
41. Taylor, D., Badiani, P. and Weston, K., A dominant interfering Myb mutant causes apoptosis in T cells. Genes Dev. 1996. 10: 2732-2744.
42. Frampton, J., Ramqvist, T. and Graf, T., v-Myb of E26 leukemia virus upregulates bcl-2 and suppresses apoptosis in myeloid cells. Genes Dev. 1996. 10: 2720-2731.
43. Cory, S., Huang, D. C. and Adams, J. M., The Bcl-2 family: Roles in cell survival and oncogenesis. Oncogene 2003. 22: 8590-8607.
44. Kluck, R. M., Bossy-Wetzel, E., Green, D. R. and Newmeyer, D. D., The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 1997. 275: 1132-1136.
45. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I. et al., Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997. 275: 1129-1132.
46. Zou, H., Li, Y., Liu, X. and Wang, X., An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999. 274: 11549-11556.
47. Young, R. L. and Korsmeyer, S. J., A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol. 1993. 13: 3686-3697.
48. Wilson, B. E., Mochon, E. and Boxer, L. M., Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 1996. 16: 5546-5556.
49. Chen, H. M. and Boxer, L. M., Pi 1 binding sites are negative regulators of bcl-2 expression in pre-B cells. Mol. Cell. Biol. 1995. 15: 3840-3847.
50. Smith, M. D., Ensor, E. A., Coffin, R. S., Boxer, L. M. and Latchman, D. S., Bcl-2 transcription from the proximal P2 promoter is activated in neuronal cells by the Brn-3a POU family transcription factor. J. Biol. Chem. 1998. 273: 16715-16722.
51. Salomoni, P., Perrotti, D., Martinez, R., Franceschi, C. and Calabretta, B., Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of Bcl-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc. Natl. Acad. Sci. USA 1997. 94: 3296-3301.
52. Biedenkapp, H., Borgmeyer, U., Sippel, A. E. and Klempnauer, K. H., Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 1988. 335: 835-837.
53. Ness, S. A., Marknell, A. and Graf, T., The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell 1989. 59: 1115-1125.
54. Mizuguchi, G., Nakagoshi, H., Nagase, T., Nomura, N., Date, T., Ueno, Y. and Ishii, S., DNA binding activity and transcriptional activator function of the human B-Myb protein compared with c-Myb. J. Biol. Chem. 1990. 265: 9280-9284.
55. Howe, K. M. and Watson, R. J., Nucleotide preferences in sequence-specific recognition of DNA by c-Myb protein. Nucleic Acids Res. 1991. 19: 3913-3919.
56. Golay, J., Loffarelli, L., Luppi, M., Castellano, M. and Introna, M., The human A-Myb protein is a strong activator of transcription. Oncogene 1994. 9: 2469-2479.
57. Bergholtz, S., Andersen, T. O., Andersson, K. B., Borrebaek, J., Luscher, B. and Gabrielsen, O. S., The highly conserved DNA-binding domains of A-, B- and c-Myb differ with respect to DNA-binding, phosphorylation and redox properties. Nucleic Acids Res. 2001. 29: 3546-3556.
58. Yang, Y., Ochando, J., Yopp, A., Bromberg, J. S. and Ding, Y., IL-6 plays a unique role in initiating c-Maf expression during early stage of CD4 T cell activation. J. Immunol. 2005. 174: 2720-2729.
59. Mucenski, M. L., McLain, K., Kier, A. B., Swerdlow, S. H., Schreiner, C. M., Miller, T. A., Pietryga, D. W. et al., A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 1991. 65: 677-689.
60. Lei, W., Rushton, J. J., Davis, L. M., Liu, F. and Ness, S. A., Positive and negative determinants of target gene specificity in myb transcription factors. J. Biol. Chem. 2004. 279: 29519-29527.
61. Van Snick, J., Interleukin-6: An overview. Annu. Rev. Immunol. 1990. 8: 253-278.
62. Kamogawa, Y., Minasi, L. A., Carding, S. R., Bottomly, K. and Flavell, R. A., The relationship of IL-4- and IFN gamma-producing T cells studied by lineage ablation of IL-4-producing cells. Cell 1993. 75: 985-995.
63. Paul, W. E. and Seder, R. A., Lymphocyte responses and cytokines. Cell 1994. 76: 241-251.
64. Cao, Q., Batey, R., Pang, G., Russell, A. and Clancy, R., IL-6, IFN-gamma and TNF-alpha production by liver-associated T cells and acute liver injury in rats administered concanavalin A. Immunol. Cell. Biol. 1998. 76: 542-549.
65. Santana, M. A. and Rosenstein, Y., What it takes to become an effector T cell: The process, the cells involved, and the mechanisms. J. Cell Physiol. 2003 195: 392-401.
66. Diehl, S. and Rincon, M., The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 2002. 39: 531-536.
67. Zhang, X., Brunner, T., Carter, L., Dutton, R. W., Rogers, P., Bradley, L., Sato, T. et al., Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/ FasL-mediated apoptosis. J. Exp. Med. 1997. 185: 1837-1849.
68. Refaeli, Y., Van Parijs, L., London, C. A., Tschopp, J. and Abbas, A. K., Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 1998. 8: 615-623.
69. Pandiyan, P., Gartner, D., Soezeri, O., Radbruch, A., Schulze-Osthoff, K. and Brunner-Weinzierl, M. C., CD152 (CTLA-4) determines the unequal resistance of Th1 and Th2 cells against activation-induced cell death by a mechanism requiring PI3 kinase function. J. Exp. Med. 2004. 199: 831-842.
70. Ivanov, V. N., Lopez Bergami, P., Maulit, G., Sato, T. A., Sassoon, D. and Ronai, Z., FAP-1 association with Fas (Apo-1) inhibits Fas expression on the cell surface. Mol. Cell. Biol. 2003. 23: 3623-3635.
71. Winer, J., Jung, C. K., Shackel, I. and Williams, P. M., Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 1999. 270: 41-49.
72. Pfaffl, M. W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001. 29: E45.