SUMO2 and SUMO3 transcription is differentially regulated by oxidative stress in an Sp1-dependent manner

Biochemical Journal

Volumn 435, Issue 2, 2011, Pages 489-498

  Sang, Jing ^a   Yang, Kai ^a   Sun, Yueping ^a   Han, Yan ^a   Cang, Hui ^a   Chen, Yuying ^a   Shi, Guiying ^a   Wang, Kangmin ^a   Zhou, Jie ^b   Wang, Xiangrui ^b   Yi, Jing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Promoter analysis; Reactive oxygen species (ROS); Small ubiquitin related modifier 2 3 (SUMO2 3); Specificity protein 1 (Sp1); Transcription

Indexed keywords

DNA; HYDROGEN PEROXIDE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SUMO 2 PROTEIN; SUMO 3 PROTEIN; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SUMOYLATION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; UBIQUITINS;

EID: 79953196109     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101474     Document Type: Article

References (51)

1. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12
2. Ayaydin, F. and Dasso, M. (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15, 5208-5218
3. Yeh, E. T. (2009) SUMOylation and de-SUMOylation: wrestling with life's processes. J. Biol. Chem. 284, 8223-8227
4. Liu, B. and Shuai, K. (2008) Regulation of the sumoylation system in gene expression. Curr. Opin. Cell Biol. 20, 288-293
5. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H. and Hay, R. T. (2001) Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368-35374
6. Tempe, D., Piechaczyk, M. and Bossis, G. (2008) SUMO under stress. Biochem. Soc. Trans. 36, 874-878
7. Mukhopadhyay, D. and Dasso, M. (2007) Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286-295
8. Manza, L. L., Codreanu, S. G., Stamer, S. L., Smith, D. L., Wells, K. S., Roberts, R. L. and Liebler, D. C. (2004) Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem. Res. Toxicol. 17, 1706-1715
9. Saitoh, H. and Hinchey, J. (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258
10. Fu, C., Ahmed, K., Ding, H., Ding, X., Lan, J., Yang, Z., Miao, Y., Zhu, Y., Shi, Y., Zhu, J. et al. (2005) Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 24, 5401-5413 (Pubitemid 43080084)
11. Dorval, V., Mazzella, M. J., Mathews, P. M., Hay, R. T. and Fraser, P. E. (2007) Modulation of Aβ generation by small ubiquitin-like modifiers does not require conjugation to target proteins. Biochem. J. 404, 309-316
12. Liu, G. and Warbrick, E. (2006) The p66 and p12 subunits of DNA polymerase delta are modified by ubiquitin and ubiquitin-like proteins. Biochem. Biophys. Res. Commun. 349, 360-366
13. Guo, W. Z., Sugaya, S., Satoh, M., Tomonaga, T., Nomura, F., Hiwasa, T., Takiguchi, M., Kita, K. and Suzuki, N. (2009) Nm23-H1 is responsible for SUMO-2-involved DNA synthesis induction after X-ray irradiation in human cells. Arch. Biochem. Biophys. 486, 81-87
14. Galanty, Y., Belotserkovskaya, R., Coates, J., Polo, S., Miller, K. M. and Jackson, S. P. (2009) Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939
15. Han, Y., Huang, C., Sun, X., Xiang, B., Wang, M., Yeh, E. T., Chen, Y., Li, H., Shi, G., Cang, H. et al. (2010) SENP3-mediated de-conjugation of SUMO2/3 from promyelocytic leukemia is correlated with accelerated cell proliferation under mild oxidative stress. J. Biol. Chem. 285, 12906-12915
16. Carbia-Nagashima, A., Gerez, J., Perez-Castro, C., Paez-Pereda, M., Silberstein, S., Stalla, G. K., Holsboer, F. and Arzt, E. (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1α during hypoxia. Cell 131, 309-323 (Pubitemid 47592916)
17. Huang, C., Han, Y., Wang, Y., Sun, X., Yan, S., Yeh, E. T., Chen, Y., Cang, H., Li, H., Shi, G. et al. (2009) SENP3 is responsible for HIF-1 transactivation under mild oxidative stress via p300 de-SUMOylation. EMBO J. 28, 2748-2762
18. Bossis, G. and Melchior, F. (2006) SUMO: regulating the regulator. Cell Div. 1, 13
19. Kurepa, J., Walker, J. M., Smalle, J., Gosink, M. M., Davis, S. J., Durham, T. L., Sung, D. Y. and Vierstra, R. D. (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J. Biol. Chem. 278, 6862-6872
20. Hay, R. T. (2007) SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 17, 370-376
21. Yang, W., Sheng, H., Warner, D. S. and Paschen, W. (2008) Transient focal cerebral ischemia induces a dramatic activation of small ubiquitin-like modifier conjugation. J. Cereb. Blood Flow Metab. 28, 892-896
22. Bossis, G. and Melchior, F. (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21, 349-357 (Pubitemid 43163530)
23. Xu, Z., Chan, H. Y., Lam, W. L., Lam, K. H., Lam, L. S., Ng, T. B. and Au, S. W. (2009) SUMO proteases: redox regulation and biological consequences. Antioxid. Redox Signaling 11, 1453-1484
24. Cheng, J., Kang, X., Zhang, S. and Yeh, E. T. (2007) SUMO-specific protease 1 is essential for stabilization of HIF1α during hypoxia. Cell 131, 584-595
25. Xu, Z., Lam, L. S., Lam, L. H., Chau, S. F., Ng, T. B. and Au, S. W. (2008) Molecular basis of the redox regulation of SUMO proteases: a protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation. FASEB J. 22, 127-137
26. Wang, Y., Mukhopadhyay, D., Mathew, S., Hasebe, T., Heimeier, R. A., Azuma, Y., Kolli, N., Shi, Y. B., Wilkinson, K. D. and Dasso, M. (2009) Identification and developmental expression of Xenopus laevis SUMO proteases. PLoS ONE 4, e8462
27. Sugaya, S., Nakanishi, H., Tanzawa, H., Sugita, K., Kita, K. and Suzuki, N. (2005) Down-regulation of SMT3A gene expression in association with DNA synthesis induction after X-ray irradiation in nevoid basal cell carcinoma syndrome (NBCCS) cells. Mutat. Res. 578, 327-332
28. Deyrieux, A. F., Rosas-Acosta, G., Ozbun, M. A. and Wilson, V. G. (2007) Sumoylation dynamics during keratinocyte differentiation. J. Cell Sci. 120, 125-136
29. Halliwell, B. (2007) Biochemistry of oxidative stress. Biochem. Soc. Trans. 35, 1147-1150
30. Halliwell, B. (2007) Oxidative stress and cancer: have we moved forward? Biochem. J. 401, 1-11
31. Loftus, L. T., Gala, R., Yang, T., Jessick, V. J., Ashley, M. D., Ordonez, A. N., Thompson, S. J., Simon, R. P. and Meller, R. (2009) Sumo-2/3-ylation following in vitro modeled ischemia is reduced in delayed ischemic tolerance. Brain Res. 1272, 71-80
32. Ueta, E., Yoneda, K., Kimura, T., Tatemoto, Y., Doi, S., Yamamoto, T. and Osaki, T. (2001) Mn-SOD antisense upregulates in vivo apoptosis of squamous cell carcinoma cells by anticancer drugs and γ-rays regulating expression of the BCL-2 family proteins, COX-2 and p21. Int. J. Cancer 94, 545-550
33. Wang, Y., Huang, X., Cang, H., Gao, F., Yamamoto, T., Osaki, T. and Yi, J. (2007) The endogenous reactive oxygen species promote NF-κB activation by targeting on activation of NF-κB-inducing kinase in oral squamous carcinoma cells. Free Radical Res. 41, 963-971 (Pubitemid 47343400)
34. Arnold, R. S., Shi, J., Murad, E., Whalen, A. M., Sun, C. Q., Polavarapu, R., Parthasarathy, S., Petros, J. A. and Lambeth, J. D. (2001) Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci. U.S.A. 98, 5550-5555
35. Zhao, J., Chen, J., Lu, B., Dong, L., Wang, H., Bi, C., Wu, G., Guo, H., Wu, M. and Guo, Y. (2008) TIP30 induces apoptosis under oxidative stress through stabilization of p53 messenger RNA in human hepatocellular carcinoma. Cancer Res. 68, 4133-4141
36. Donato, M. T., Lahoz, A., Castell, J. V. and Gomez-Lechon, M. J. (2008) Cell lines: a tool for in vitro drug metabolism studies. Curr. Drug Metab. 9, 1-11
37. Pan, X., Wang, Y., Zhang, M., Pan, W., Qi, Z. T. and Cao, G. W. (2004) Effects of endostatin-vascular endothelial growth inhibitor chimeric recombinant adenoviruses on antiangiogenesis. World J. Gastroenterol. 10, 1409-1414
38. Yu, Y., Wei, S. G., Zhang, Z. H., Gomez-Sanchez, E., Weiss, R. M. and Felder, R. B. (2008) Does aldosterone upregulate the brain renin-angiotensin system in rats with heart failure? Hypertension 51, 727-733
39. Zuo, Y., Xiang, B., Yang, J., Sun, X., Wang, Y., Cang, H. and Yi, J. (2009) Oxidative modification of caspase-9 facilitates its activation via disulfide-mediated interaction with Apaf-1. Cell Res. 19, 449-457
40. Philipsen, S. and Suske, G. (1999) A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res. 27, 2991-3000 (Pubitemid 29355710)
41. Ding, H., Benotmane, A. M., Suske, G., Collen, D. and Belayew, A. (1999) Functional interactions between Sp1 or Sp3 and the helicase-like transcription factor mediate basal expression from the human plasminogen activator inhibitor-1 gene. J. Biol. Chem. 274, 19573-19580
42. 41a Yan, S., Sun, X., Xiang, B., Cang, H., Kang, X., Chen, Y., Li, H., Shi, G., Yeh, E. T., Wang, B., Wang, X. and Yi, J. (2010) Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J. 29, 3773-3786
43. Morel, Y. and Barouki, R. (1999) Repression of gene expression by oxidative stress. Biochem. J. 342, 481-496 (Pubitemid 29452631)
44. Posewitz, M. C. and Wilcox, D. E. (1995) Properties of the Sp1 zinc finger 3 peptide: coordination chemistry, redox reactions, and metal binding competition with metallothionein. Chem. Res. Toxicol. 8, 1020-1028
45. Wu, X., Bishopric, N. H., Discher, D. J., Murphy, B. J. and Webster, K. A. (1996) Physical and functional sensitivity of zinc finger transcription factors to redox change. Mol. Cell. Biol. 16, 1035-1046
46. Dynan, W. S. and Tjian, R. (1983) Isolation of transcription factors that discriminate between different promoters recognized by RNA polymerase II. Cell 32, 669-680 (Pubitemid 13087925)
47. Schafer, G., Cramer, T., Suske, G., Kemmner, W., Wiedenmann, B. and Hocker, M. (2003) Oxidative stress regulates vascular endothelial growth factor-A gene transcription through Sp1- and Sp3-dependent activation of two proximal GC-rich promoter elements. J. Biol. Chem. 278, 8190-8198
48. Chou, W. C., Chen, H. Y., Yu, S. L., Cheng, L., Yang, P. C. and Dang, C. V. (2005) Arsenic suppresses gene expression in promyelocytic leukemia cells partly through Sp1 oxidation. Blood 106, 304-310
49. Su, K., Yang, X., Roos, M. D., Paterson, A. J. and Kudlow, J. E. (2000) Human Sug1/p45 is involved in the proteasome-dependent degradation of Sp1. Biochem. J. 348, 281-289
50. Wang, Y. T., Chuang, J. Y., Shen, M. R., Yang, W. B., Chang, W. C. and Hung, J. J. (2008) Sumoylation of specificity protein 1 augments its degradation by changing the localization and increasing the specificity protein 1 proteolytic process. J. Mol. Biol. 380, 869-885
51. Bouwman, P. and Philipsen, S. (2002) Regulation of the activity of Sp1-related transcription factors. Mol. Cell. Endocrinol. 195, 27-38