SUMOylation attenuates c-Maf-dependent IL-4 expression

European Journal of Immunology

Volumn 40, Issue 4, 2010, Pages 1174-1184

  Lin, Bo Shiou ^a   Tsai, Pei Yun ^a   Hsieh, Wan Yun ^a   Tsao, Hsiao Wei ^a   Liu, Meng Wei ^a   Grenningloh, Roland ^b   Wang, Li Fang ^c   Ho, I Cheng ^b   Miaw, Shi Chuen ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

c Maf; Il4 gene regulation; SUMOylation

Indexed keywords

INTERLEUKIN 4; LYSINE; LYSINE 33; PIAS1 PROTEIN; PROTEIN UBC9; SUMO PROTEIN; TRANSCRIPTION FACTOR C MAF; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SUMOYLATION; TH2 CELL; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELLS, CULTURED; HUMANS; INTERLEUKIN-4; KIDNEY; LYSINE; MICE; MOLECULAR SEQUENCE DATA; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-MAF; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TH2 CELLS; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 77951068773     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939788     Document Type: Article

References (44)

1. Glimcher, L. H. and Murphy, K. M., Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 2000. 14: 1693-1711.
2. Ho, I. C. and Glimcher, L. H., Transcription: tantalizing times for T cells. Cell 2002. 109: S109-120.
3. Kataoka, K., Nishizawa, M. and Kawai, S., Structure-function analysis of the maf oncogene product, a member of the b-Zip protein family. J. Virol. 1993. 67: 2133-2141. (Pubitemid 23088388)
4. Nishizawa, M., Kataoka, K., Goto, N., Fujiwara, K. T. and Kawai, S., v-maf, a viral oncogene that encodes a "leucine zipper" motif. Proc. Natl. Acad. Sci. USA 1989. 86: 7711-7715.
5. Tanaka, Y., So, T., Lebedeva, S., Croft, M. and Altman, A., Impaired IL-4 and c-Maf expression and enhanced Th1-cell development in Vav1- deficient mice. Blood 2005. 106: 1286-1295. (Pubitemid 41129592)
6. 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.
7. 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.
8. 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.
9. Rocques, N., Abou Zeid, N., Sii-Felice, K., Lecoin, L., Felder-Schmittbuhl, M. P., Eychene, A. and Pouponnot, C., GSK-3-mediated phosphorylation enhances Maf-transforming activity. Mol. Cell 2007. 28: 584-597. (Pubitemid 350137803)
10. Melchior, F., SUMO - nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 2000. 16: 591-626.
11. Muller, S., Hoege, C., Pyrowolakis, G. and Jentsch, S., SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2001. 2: 202-210.
12. Seeler, J. S. and Dejean, A., Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 2003. 4: 690-699.
13. Saitoh, H. and Hinchey, J., Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 2000. 275: 6252-6258.
14. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R. and Becker, J., Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 1998. 280: 275-286.
15. Zhao, J., Sumoylation regulates diverse biological processes. Cell Mol. Life Sci. 2007. 64: 3017-3033.
16. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H. and Hay, R. T., Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 2001. 276: 35368-35374.
17. Bohren, K. M., Nadkarni, V., Song, J. H., Gabbay, K. H. and Owerbach, D., A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 2004. 279: 27233-27238.
18. Johnson, E. S., Protein modification by SUMO. Annu. Rev. Biochem. 2004. 73: 355-382.
19. Dohmen, R. J., SUMO protein modification. Biochim. Biophys. Acta 2004. 1695: 113-131.
20. Muller, S., Ledl, A. and Schmidt, D., SUMO: a regulator of gene expression and genome integrity. Oncogene 2004. 23: 1998-2008. (Pubitemid 38496729)
21. Liu, B. and Shuai, K., Regulation of the sumoylation system in gene expression. Curr. Opin. Cell Biol. 2008. 20: 288-293.
22. Tillmanns, S., Otto, C., Jaffray, E., Du Roure, C., Bakri, Y., Vanhille, L. et al., SUMO modification regulates MafB-driven macrophage differentiation by enabling Myb-dependent transcriptional repression. Mol. Cell Biol. 2007. 27: 5554-5564.
23. Shao, C. and Cobb, M. H., Sumoylation regulates the transcriptional activity of MafA in pancreatic beta cells. J. Biol. Chem. 2009. 284: 3117-3124.
24. Sii-Felice, K., Pouponnot, C., Gillet, S., Lecoin, L., Girault, J. A., Eychene, A. and Felder-Schmittbuhl, M. P., MafA transcription factor is phosphorylated by p38 MAP kinase. FEBS Lett. 2005. 579: 3547-3554. (Pubitemid 40897689)
25. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guerardel, C., Dejean, A. and Leprince, D., An acetylation/deacetylation- SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell Biol. 2007. 27: 2661-2675.
26. Wang, J. M., Ko, C. Y., Chen, L. C., Wang, W. L. and Chang, W. C., Functional role of NF-IL6beta and its sumoylation and acetylation modifications in promoter activation of cyclooxygenase 2 gene. Nucleic Acids Res. 2006. 34: 217-231.
27. Gregoire, S., Tremblay, A. M., Xiao, L., Yang, Q., Ma, K., Nie, J., Mao, Z. et al., Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J. Biol. Chem. 2006. 281: 4423-4433.
28. Gregoire, S. and Yang, X. J., Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell Biol. 2005. 25: 2273-2287.
29. Friedman, J. S., Khanna, H., Swain, P. K., Denicola, R., Cheng, H., Mitton, K. P., Weber, C. H. et al., The minimal transactivation domain of the basic motif-leucine zipper transcription factor NRL interacts with TATA-binding protein. J. Biol. Chem. 2004. 279: 47233-47241.
30. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P. and Dikic, I., Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 2006. 281: 16117-16127.
31. Garaude, J., Farras, R., Bossis, G., Charni, S., Piechaczyk, M., Hipskind, R. A. and Villalba, M., SUMOylation regulates the transcriptional activity of JunB in T lymphocytes. J. Immunol. 2008. 180: 5983-5990.
32. Berberich-Siebelt, F., Berberich, I., Andrulis, M., Santner-Nanan, B., Jha, M. K., Klein-Hessling, S., Schimpl, A. and Serfling, E., SUMOylation interferes with CCAAT/enhancer-binding protein beta-mediated c-myc repression, but not IL-4 activation in T cells. J. Immunol. 2006. 176: 4843-4851.
33. Zhao, X., Zheng, B., Huang, Y., Yang, D., Katzman, S., Chang, C., Fowell, D. and Zeng, W. P., Interaction between GATA-3 and the transcriptional coregulator Pias1 is important for the regulation of Th2 immune responses. J. Immunol. 2007. 179: 8297-8304.
34. Terui, Y., Saad, N., Jia, S., McKeon, F. and Yuan, J., Dual role of sumoylation in the nuclear localization and transcriptional activation of NFAT1. J. Biol. Chem. 2004. 279: 28257-28265.
35. Deng, Z., Wan, M. and Sui, G., PIASy-mediated sumoylation of Yin Yang 1 depends on their interaction but not the RING finger. Mol. Cell Biol. 2007. 27: 3780-3792.
36. Leavenworth, J.W., Ma, X., Mo, Y. Y. and Pauza, M. E., SUMO conjugation contributes to immune deviation in nonobese diabetic mice by suppressing c-Maf transactivation of IL-4. J. Immunol. 2009. 183: 1110-1119.
37. 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.
38. Bauquet, A. T., Jin, H., Paterson, A. M., Mitsdoerffer, M., Ho, I. C., Sharpe, A. H. and Kuchroo, V. K., The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat. Immunol. 2009. 10: 167-175.
39. Cao, S., Liu, J., Chesi, M., Bergsagel, P. L., Ho, I. C., Donnelly, R. P. and Ma, X., Differential regulation of IL-12 and IL-10 gene expression in macrophages by the basic leucine zipper transcription factor c-Maf fibrosarcoma. J. Immunol. 2002. 169: 5715-5725. (Pubitemid 35291673)
40. Homma, Y., Cao, S., Shi, X. and Ma, X., The Th2 transcription factor c-Maf inhibits IL-12p35 gene expression in activated macrophages by targeting NF-kappaB nuclear translocation. J. Interferon Cytokine Res. 2007. 27: 799-808. (Pubitemid 47479864)
41. Hurt, E. M., Wiestner, A., Rosenwald, A., Shaffer, A. L., Campo, E., Grogan, T. 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. (Pubitemid 38283804)
42. Morito, N., Yoh, K., Fujioka, Y., Nakano, T., Shimohata, H., Hashimoto, Y., Yamada, A. et al., Overexpression of c-Maf contributes to T-cell lymphoma in both mice and human. Cancer Res. 2006. 66: 812-819. (Pubitemid 43165946)
43. Kim, J. I., Li, T., Ho, I. C., Grusby, M. J. and Glimcher, L. H., Requirement for the c-Maf transcription factor in crystallin gene regulation and lens development. Proc. Natl. Acad. Sci. USA 1999. 96: 3781-3785.
44. Miaw, S. C., Choi, A., Yu, E., Kishikawa, H. and Ho, I. C., ROG, repressor of GATA, regulates the expression of cytokine genes. Immunity 2000. 12: 323-333.