Mechanisms, regulation and consequences of protein SUMOylation

Biochemical Journal

Volumn 428, Issue 2, 2010, Pages 133-145

  Wilkinson, Kevin A ^a   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Post translational modification; Sentrin small ubiquitin like modifier specific protease (SENP); Small ubiquitin like modifier (SUMO); Small ubiquitin like modifier activating enzyme (SAE); Ubiquitin; Ubiquitin conjugating 9 (Ubc9); Ubiquitin like modifiers

Indexed keywords

POST-TRANSLATIONAL MODIFICATIONS; SMALL UBIQUITIN-LIKE MODIFIERS; UBIQUITIN; UBIQUITIN-LIKE; UBIQUITIN-LIKE MODIFIERS;

AMINO ACIDS; MACHINERY; SUBSTRATES;

ENZYMES;

PROTEIN UBC9; SUMO PROTEIN; PROTEINASE;

ACETYLATION; AMINO ACID SEQUENCE; CELL STRESS; CONJUGATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; SUMOYLATION; UBIQUITINATION; ANIMAL; BIOLOGICAL MODEL; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; ENDOPEPTIDASES; HUMANS; MODELS, BIOLOGICAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 77952566949     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100158     Document Type: Review

References (164)

1. Tanaka, K., Nishide, J., Okazaki, K., Kato, H., Niwa, O., Nakagawa, T., Matsuda, H., Kawamukai, M. and Murakami, Y. (1999) Characterization of a fission yeast SUMO-1 homologue, pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol. Cell. Biol. 19, 8660-8672
2. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B. et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391
3. Meluh, P. B. and Koshland, D. (1995) Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol. Biol. Cell 6, 793-807
4. Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K. and Chen, D. J. (1996) UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics 36, 271-279 (Pubitemid 26307489)
5. Boddy, M. N., Howe, K., Etkin, L. D., Solomon, E. and Freemont, P. S. (1996) PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene 13, 971-982 (Pubitemid 26329084)
6. Okura, T., Gong, L., Kamitani, T., Wada, T., Okura, I., Wei, C. F., Chang, H. M. and Yeh, E. T. (1996) Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J. Immunol. 157, 4277-4281 (Pubitemid 126449343)
7. Matunis, M. J., Coutavas, E. and Blobel, G. (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135, 1457-1470 (Pubitemid 26427644)
8. Lapenta, V., Chiurazzi, P., van der Spek, P., Pizzuti, A., Hanaoka, F. and Brahe, C. (1997) SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family. Genomics 40, 362-366 (Pubitemid 27124102)
9. Mahajan, R., Delphin, C., Guan, T., Gerace, L. and Melchior, F. (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107 (Pubitemid 27180334)
10. Kamitani, T., Kito, K., Nguyen, H. P., Fukuda-Kamitani, T. and Yeh, E. T. (1998) Characterization of a second member of the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273, 11349-11353
11. Kamitani, T., Nguyen, H. P., Kito, K., Fukuda-Kamitani, T. and Yeh, E. T. (1998) Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273, 3117-3120
12. 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
13. Yang, M., Hsu, C. T., Ting, C. Y., Liu, L. F. and Hwang, J. (2006) Assembly of a polymeric chain of SUMO1 on human topoisomerase I in vitro. J. Biol. Chem. 281, 8264-8274
14. Matic, I., van Hagen, M., Schimmel, J., Macek, B., Ogg, S. C., Tatham, M. H., Hay, R. T., Lamond, A. I., Mann, M. and Vertegaal, A. C. (2008) In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol. Cell. Proteomics 7, 132-144
15. Wei, W., Yang, P., Pang, J., Zhang, S., Wang, Y., Wang, M. H., Dong, Z., She, J. X. and Wang, C. Y. (2008) A stress-dependent SUMO4 sumoylation of its substrate proteins. Biochem. Biophys. Res. Commun. 375, 454-459
16. Bohren, K. M., Nadkarni, V., Song, J. H., Gabbay, K. H. and Owerbach, D. (2004) 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. 279, 27233-27238
17. Guo, D., Li, M., Zhang, Y., Yang, P., Eckenrode, S., Hopkins, D., Zheng, W., Purohit, S., Podolsky, R. H., Muir, A. et al. (2004) A functional variant of SUMO4, a new IκBα modifier, is associated with type 1 diabetes. Nat. Genet. 36, 837-841
18. Owerbach, D., McKay, E. M., Yeh, E. T., Gabbay, K. H. and Bohren, K. M. (2005) A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337, 517-520
19. Gong, L., Li, B., Millas, S. and Yeh, E. T. (1999) Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex. FEBS Lett. 448, 185-189 (Pubitemid 29151657)
20. Johnson, E. S. and Blobel, G. (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272, 26799-26802
21. Gong, L., Kamitani, T., Fujise, K., Caskey, L. S. and Yeh, E. T. (1997) Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem. 272, 28198-28201 (Pubitemid 27517756)
22. Desterro, J. M., Thomson, J. and Hay, R. T. (1997) Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417, 297-300 (Pubitemid 27511608)
23. Schwarz, S. E., Matuschewski, K., Liakopoulos, D., Scheffner, M. and Jentsch, S. (1998) The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme. Proc. Natl. Acad. Sci. U.S.A. 95, 560-564
24. Saitoh, H., Sparrow, D. B., Shiomi, T., Pu, R. T., Nishimoto, T., Mohun, T. J. and Dasso, M. (1998) Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2. Curr. Biol. 8, 121-124
25. Lee, G. W., Melchior, F., Matunis, M. J., Mahajan, R., Tian, Q. and Anderson, P. (1998) Modification of Ran GTPase-activating protein by the small ubiquitin-related modifier SUMO-1 requires Ubc9, an E2-type ubiquitin- conjugating enzyme homologue. J. Biol. Chem. 273, 6503-6507
26. Rodriguez, M. S., Dargemont, C. and Hay, R. T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659
27. Sampson, D. A., Wang, M. and Matunis, M. J. (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21664-21669
28. Xu, J., He, Y., Qiang, B., Yuan, J., Peng, X. and Pan, X. M. (2008) A novel method for high accuracy sumoylation site prediction from protein sequences. BMC Bioinformatics 9, 8
29. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
30. Johnson, E. S. and Gupta, A. A. (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106, 735-744
31. Kahyo, T., Nishida, T. and Yasuda, H. (2001) Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell 8, 713-718
32. Schmidt, D. and Muller, S. (2002) Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. U.S.A. 99, 2872-2877
33. Kotaja, N., Karvonen, U., Janne, O. A. and Palvimo, J. J. (2002) PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22, 5222-5234
34. Nishida, T. and Yasuda, H. (2002) PIAS1 and PIASxα function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J. Biol. Chem. 277, 41311-41317
35. Sachdev, S., Bruhn, L., Sieber, H., Pichler, A., Melchior, F. and Grosschedl, R. (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15, 3088-3103
36. Weger, S., Hammer, E. and Heilbronn, R. (2005) Topors acts as a SUMO-1 E3 ligase for p53 in vitroand in vivo. FEBS Lett. 579, 5007-5012
37. Braschi, E., Zunino, R. and McBride, H. M. (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 10, 748-754
38. Zhao, X. and Blobel, G. (2005) A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. U.S.A. 102, 4777-4782
39. Andrews, E. A., Palecek, J., Sergeant, J., Taylor, E., Lehmann, A. R. and Watts, F. Z. (2005) Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25, 185-196
40. Potts, P. R. and Yu, H. (2005) Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25, 7021-7032
41. Rajendra, R., Malegaonkar, D., Pungaliya, P., Marshall, H., Rasheed, Z., Brownell, J., Liu, L. F., Lutzker, S., Saleem, A. and Rubin, E. H. (2004) Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J. Biol. Chem. 279, 36440-36444
42. Kagey, M. H., Melhuish, T. A. and Wotton, D. (2003) The polycomb protein Pc2 is a SUMO E3. Cell 113, 127-137
43. Yang, S. H. and Sharrocks, A. D. (2010) The SUMO E3 ligase activity of Pc2 is coordinated through a SUMO-interaction motif, Mol. Cell Biol., doi:10.1128/MCB.01510-09
44. Merrill, J. C., Melhuish, T. A., Kagey, M. H., Yang, S. H., Sharrocks, A. D. and Wotton, D. A role for non-covalent SUMO interaction motifs in Pc2/CBX4 E3 activity. PLoS One 5, e8794
45. Gregoire, S. and Yang, X. J. (2005) Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell. Biol. 25, 2273-2287
46. Lee, J. H., Park, S. M., Kim, O. S., Lee, C. S., Woo, J. H., Park, S. J., Joe, E. H. and Jou, I. (2009) Differential SUMOylation of LXRα and LXRβ mediates transrepression of STAT1 inflammatory signaling in IFN-γ -stimulated brain astrocytes. Mol. Cell 35, 806-817
47. Gao, C., Ho, C. C., Reineke, E., Lam, M., Cheng, X., Stanya, K. J., Liu, Y., Chakraborty, S., Shih, H. M. and Kao, H. Y. (2008) Histone deacetylase 7 promotes PML sumoylation and is essential for PML nuclear body formation. Mol. Cell. Biol. 28, 5658-5667
48. Subramaniam, S., Sixt, K. M., Barrow, R. and Snyder, S. H. (2009) Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 324, 1327-1330
49. Oh, S. M., Liu, Z., Okada, M., Jang, S. W., Liu, X., Chan, C. B., Luo, H. and Ye, K. (2010) Ebp1 sumoylation, regulated by TLS/FUS E3 ligase, is required for its anti-proliferative activity. Oncogene 29, 1017-1030
50. Morita, Y., Kanei-Ishii, C., Nomura, T. and Ishii, S. (2005) TRAF7 sequesters c-Myb to the cytoplasm by stimulating its sumoylation. Mol. Biol. Cell 16, 5433-5444
51. Pichler, A., Gast, A., Seeler, J. S., Dejean, A. and Melchior, F. (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109-120
52. Tatham, M. H., Kim, S., Jaffray, E., Song, J., Chen, Y. and Hay, R. T. (2005) Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat. Struct. Mol. Biol. 12, 67-74
53. Kirsh, O., Seeler, J. S., Pichler, A., Gast, A., Muller, S., Miska, E., Mathieu, M., Harel-Bellan, A., Kouzarides, T., Melchior, F. and Dejean, A. (2002) The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21, 2682-2691
54. Pichler, A., Knipscheer, P., Saitoh, H., Sixma, T. K. and Melchior, F. (2004) The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type. Nat. Struct. Mol. Biol. 11, 984-991
55. Reverter, D. and Lima, C. D. (2005) Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687-692
56. Li, S. J. and Hochstrasser, M. (1999) A new protease required for cell-cycle progression in yeast. Nature 398, 246-251
57. Li, S. J. and Hochstrasser, M. (2000) The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20, 2367-2377
58. Bylebyl, G. R., Belichenko, I. and Johnson, E. S. (2003) The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278, 44113-44120
59. Yeh, E. T. (2009) SUMOylation and De-SUMOylation: wrestling with life's processes. J. Biol. Chem. 284, 8223-8227
60. Mukhopadhyay, D. and Dasso, M. (2007) Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286-295
61. Gong, L., Millas, S., Maul, G. G. and Yeh, E. T. (2000) Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J. Biol. Chem. 275, 3355-3359
62. Hang, J. and Dasso, M. (2002) Association of the human SUMO-1 protease SENP2 with the nuclear pore. J. Biol. Chem. 277, 19961-19966
63. Zhang, H., Saitoh, H. and Matunis, M. J. (2002) Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol. Cell. Biol. 22, 6498-6508
64. Nishida, T., Tanaka, H. and Yasuda, H. (2000) A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur. J. Biochem. 267, 6423-6427
65. Di Bacco, A., Ouyang, J., Lee, H. Y., Catic, A., Ploegh, H. and Gill, G. (2006) The SUMO-specific protease SENP5 is required for cell division. Mol. Cell. Biol. 26, 4489-4498
66. Gong, L. and Yeh, E. T. (2006) Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J. Biol. Chem. 281, 15869-15877
67. Mukhopadhyay, D., Ayaydin, F., Kolli, N., Tan, S. H., Anan, T., Kametaka, A., Azuma, Y., Wilkinson, K. D. and Dasso, M. (2006) SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J. Cell Biol. 174, 939-949 (Pubitemid 44455183)
68. Shen, L. N., Geoffroy, M. C., Jaffray, E. G. and Hay, R. T. (2009) Characterization of SENP7, a SUMO-2/3-specific isopeptidase. Biochem. J. 421, 223-230
69. Bailey, D. and O'Hare, P. (2004) Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 279, 692-703 (Pubitemid 38044874)
70. Kuo, M. L., den Besten, W., Thomas, M. C. and Sherr, C. J. (2008) Arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease Senp3. Cell Cycle 7, 3378-3387
71. 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
72. Hayashi, T., Seki, M., Maeda, D., Wang, W., Kawabe, Y., Seki, T., Saitoh, H., Fukagawa, T., Yagi, H. and Enomoto, T. (2002) Ubc9 is essential for viability of higher eukaryotic cells. Exp. Cell Res. 280, 212-221
73. Nacerddine, K., Lehembre, F., Bhaumik, M., Artus, J., Cohen-Tannoudji, M., Babinet, C., Pandolfi, P. P. and Dejean, A. (2005) The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9, 769-779 (Pubitemid 41724105)
74. Alkuraya, F. S., Saadi, I., Lund, J. J., Turbe-Doan, A., Morton, C. C. and Maas, R. L. (2006) SUMO1 haploinsufficiency leads to cleft lip and palate. Science 313, 1751
75. Zhang, F. P., Mikkonen, L., Toppari, J., Palvimo, J. J., Thesleff, I. and Janne, O. A. (2008) Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 28, 5381-5390
76. Evdokimov, E., Sharma, P., Lockett, S. J., Lualdi, M. and Kuehn, M. R. (2008) Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J. Cell Sci. 121, 4106-4113
77. 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
78. Vertegaal, A. C., Andersen, J. S., Ogg, S. C., Hay, R. T., Mann, M. and Lamond, A. I. (2006) Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 5, 2298-2310
79. Ayaydin, F. and Dasso, M. (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15, 5208-5218
80. Bossis, G. and Melchior, F. (2006) SUMO: regulating the regulator. Cell Div. 1, 13
81. Agbor, T. A. and Taylor, C. T. (2008) SUMO, hypoxia and the regulation of metabolism. Biochem. Soc. Trans. 36, 445-448
82. Cimarosti, H. and Henley, J. M. (2008) Investigating the mechanisms underlying neuronal death in ischemia using in vitro oxygen-glucose deprivation: potential involvement of protein SUMOylation. Neuroscientist 14, 626-636
83. Tempe, D., Piechaczyk, M. and Bossis, G. (2008) SUMO under stress. Biochem. Soc. Trans. 36, 874-878
84. Yang, W., Sheng, H., Homi, H. M., Warner, D. S. and Paschen, W. (2008) Cerebral ischemia/stroke and small ubiquitin-like modifier (SUMO) conjugation - a new target for therapeutic intervention? J. Neurochem. 106, 989-999
85. Martin, S., Wilkinson, K. A., Nishimune, A. and Henley, J. M. (2007) Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction. Nat. Rev. Neurosci. 8, 948-959
86. Perry, J. J., Tainer, J. A. and Boddy, M. N. (2008) A SIM-ultaneous role for SUMO and ubiquitin. Trends. Biochem. Sci. 33, 201-208
87. Geoffroy, M. C. and Hay, R. T. (2009) An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 10, 564-568
88. Finley, D. and Chau, V. (1991) Ubiquitination. Annu. Rev. Cell Biol. 7, 25-69
89. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479
90. Hicke, L. and Dunn, R. (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172
91. Muller, S., Matunis, M. J. and Dejean, A. (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17, 61-70 (Pubitemid 28041048)
92. Lallemand-Breitenbach, V., Jeanne, M., Benhenda, S., Nasr, R., Lei, M., Peres, L., Zhou, J., Zhu, J., Raught, B. and de The, H. (2008) Arsenic degrades PML or PML-RARα through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10, 547-555
93. Tatham, M. H., Geoffroy, M. C., Shen, L., Plechanovova, A., Hattersley, N., Jaffray, E. G., Palvimo, J. J. and Hay, R. T. (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546
94. Weisshaar, S. R., Keusekotten, K., Krause, A., Horst, C., Springer, H. M., Gottsche, K., Dohmen, R. J. and Praefcke, G. J. (2008) Arsenic trioxide stimulates SUMO-2/3 modification leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett. 582, 3174-3178
95. Kerscher, O. (2007) SUMO junction - what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555
96. Dikic, I., Wakatsuki, S. and Walters, K. J. (2009) Ubiquitin-binding domains - from structures to functions. Nat. Rev. Mol. Cell. Biol. 10, 659-671
97. Minty, A., Dumont, X., Kaghad, M. and Caput, D. (2000) Covalent modification of p73α by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275, 36316-36323
98. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G. and Chen, Y. (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 14373-14378
99. Hannich, J. T., Lewis, A., Kroetz, M. B., Li, S. J., Heide, H., Emili, A. and Hochstrasser, M. (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102-4110
100. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P. and Dikic, I. (2006) Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127
101. Andres, M. E., Burger, C., Peral-Rubio, M. J., Battaglioli, E., Anderson, M. E., Grimes, J., Dallman, J., Ballas, N. and Mandel, G. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl. Acad. Sci. U.S.A. 96, 9873-9878
102. Ballas, N., Battaglioli, E., Atouf, F., Andres, M. E., Chenoweth, J., Anderson, M. E., Burger, C., Moniwa, M., Davie, J. R., Bowers, W. J. et al. (2001) Regulation of neuronal traits by a novel transcriptional complex. Neuron 31, 353-365
103. Hakimi, M. A., Bochar, D. A., Chenoweth, J., Lane, W. S., Mandel, G. and Shiekhattar, R. (2002) A core-BRAF35 complex containing histone deacetylase mediates repression of neuronal-specific genes. Proc. Natl. Acad. Sci. U.S.A. 99, 7420-7425
104. Ballas, N., Grunseich, C., Lu, D. D., Speh, J. C. and Mandel, G. (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121, 645-657 (Pubitemid 40720016)
105. Ouyang, J., Shi, Y., Valin, A., Xuan, Y. and Gill, G. (2009) Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. Mol. Cell 34, 145-154
106. Geiss-Friedlander, R. and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956
107. Pichler, A., Knipscheer, P., Oberhofer, E., van Dijk, W. J., Korner, R., Olsen, J. V., Jentsch, S., Melchior, F. and Sixma, T. K. (2005) SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12, 264-269
108. Yang, S. H. and Sharrocks, A. D. (2004) SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13, 611-617 (Pubitemid 38299387)
109. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12
110. Martin, S., Nishimune, A., Mellor, J. R. and Henley, J. M. (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447, 321-325 (Pubitemid 46788827)
111. Verger, A., Perdomo, J. and Crossley, M. (2003) Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4, 137-142
112. Gill, G. (2005) Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 15, 536-541
113. Ross, S., Best, J. L., Zon, L. I. and Gill, G. (2002) SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 10, 831-842 (Pubitemid 35335638)
114. Girdwood, D., Bumpass, D., Vaughan, O. A., Thain, A., Anderson, L. A., Snowden, A. W., Garcia-Wilson, E., Perkins, N. D. and Hay, R. T. (2003) P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11, 1043-1054 (Pubitemid 36566325)
115. Kuo, H. Y., Chang, C. C., Jeng, J. C., Hu, H. M., Lin, D. Y., Maul, G. G., Kwok, R. P. and Shih, H. M. (2005) SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc. Natl. Acad. Sci. U.S.A. 102, 16973-16978
116. Hardeland, U., Steinacher, R., Jiricny, J. and Schar, P. (2002) Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456-1464 (Pubitemid 34246524)
117. Baba, D., Maita, N., Jee, J. G., Uchimura, Y., Saitoh, H., Sugasawa, K., Hanaoka, F., Tochio, H., Hiroaki, H. and Shirakawa, M. (2005) Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435, 979-982
118. 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
119. Yang, W., Sheng, H., Warner, D. S. and Paschen, W. (2008) Transient global cerebral ischemia induces a massive increase in protein sumoylation. J. Cereb. Blood Flow Metab. 28, 269-279
120. 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 vitromodeled ischemia is reduced in delayed ischemic tolerance. Brain Res. 1272, 71-80
121. Cimarosti, H., Lindberg, C., Bomholt, S. F., Ronn, L. C. and Henley, J. M. (2008) Increased protein SUMOylation following focal cerebral ischemia. Neuropharmacology 54, 280-289
122. Ja Lee, Y., Castri, P., Bembry, J., Maric, D., Auh, S. and Hallenbeck, J. M. (2009) SUMOylation participates in induction of ischemic tolerance. J. Neurochem. 109, 257-267
123. Golebiowski, F., Matic, I., Tatham, M. H., Cole, C., Yin, Y., Nakamura, A., Cox, J., Barton, G. J., Mann, M. and Hay, R. T. (2009) System-wide changes to SUMO modifications in response to heat shock. Sci. Signaling 2, ra24
124. Ulrich, H. D. (2005) Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 15, 525-532
125. Desterro, J. M., Rodriguez, M. S. and Hay, R. T. (1998) SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell 2, 233-239
126. Huang, E. J. and Reichardt, L. F. (2003) Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642
127. Carter, S., Bischof, O., Dejean, A. and Vousden, K. H. (2007) C-terminal modifications regulate MDM2 dissociation and nuclear export of p53. Nat. Cell Biol. 9, 428-435
128. Chiocca, S., Baker, A. and Cotten, M. (1997) Identification of a novel antiapoptotic protein, GAM-1, encoded by the CELO adenovirus. J. Virol. 71, 3168-3177
129. Glotzer, J. B., Saltik, M., Chiocca, S., Michou, A. I., Moseley, P. and Cotten, M. (2000) Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407, 207-211
130. Boggio, R., Passafaro, A. and Chiocca, S. (2007) Targeting SUMO E1 to ubiquitin ligases: a viral strategy to counteract sumoylation. J. Biol. Chem. 282, 15376-15382
131. Um, J. W., Min, D. S., Rhim, H., Kim, J., Paik, S. R. and Chung, K. C. (2006) Parkin ubiquitinates and promotes the degradation of RanBP2. J. Biol. Chem. 281, 3595-3603
132. Um, J. W. and Chung, K. C. (2006) Functional modulation of parkin through physical interaction with SUMO-1. J. Neurosci. Res. 84, 1543-1554
133. Kurdistani, S. K. and Grunstein, M. (2003) Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 4, 276-284
134. Sapetschnig, A., Rischitor, G., Braun, H., Doll, A., Schergaut, M., Melchior, F. and Suske, G. (2002) Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J. 21, 5206-5215
135. Bouras, T., Fu, M., Sauve, A. A., Wang, F., Quong, A. A., Perkins, N. D., Hay, R. T., Gu, W. and Pestell, R. G. (2005) SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1. J. Biol. Chem. 280, 10264-10276
136. Shalizi, A., Gaudilliere, B., Yuan, Z., Stegmuller, J., Shirogane, T., Ge, Q., Tan, Y., Schulman, B., Harper, J. W. and Bonni, A. (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017
137. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guerardel, C., Dejean, A. and Leprince, D. (2007) An acetylation/deacetylation- SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell. Biol. 27, 2661-2675
138. David, G., Neptune, M. A. and DePinho, R. A. (2002) SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J. Biol. Chem. 277, 23658-23663
139. Cheng, J., Wang, D., Wang, Z. and Yeh, E. T. (2004) SENP1 enhances androgen receptor-dependent transcription through desumoylation of histone deacetylase 1. Mol. Cell. Biol. 24, 6021-6028
140. Yang, S. H., Jaffray, E., Senthinathan, B., Hay, R. T. and Sharrocks, A. D. (2003) SUMO and transcriptional repression: dynamic interactions between the MAP kinase and SUMO pathways. Cell Cycle 2, 528-530
141. Hietakangas, V., Ahlskog, J. K., Jakobsson, A. M., Hellesuo, M., Sahlberg, N. M., Holmberg, C. I., Mikhailov, A., Palvimo, J. J., Pirkkala, L. and Sistonen, L. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953-2968
142. Gregoire, S., Tremblay, A. M., Xiao, L., Yang, Q., Ma, K., Nie, J., Mao, Z., Wu, Z., Giguere, V. and Yang, X. J. (2006) Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J. Biol. Chem. 281, 4423-4433
143. Hietakangas, V., Anckar, J., Blomster, H. A., Fujimoto, M., Palvimo, J. J., Nakai, A. and Sistonen, L. (2006) PDSM, a motif for phosphorylation- dependent SUMO modification. Proc. Natl. Acad. Sci. U.S.A. 103, 45-50
144. Yang, S. H., Galanis, A., Witty, J. and Sharrocks, A. D. (2006) An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J. 25, 5083-5093
145. Mohideen, F., Capili, A. D., Bilimoria, P. M., Yamada, T., Bonni, A. and Lima, C. D. (2009) A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 16, 945-952
146. Kadare, G., Toutant, M., Formstecher, E., Corvol, J. C., Carnaud, M., Boutterin, M. C. and Girault, J. A. (2003) PIAS1-mediated sumoylation of focal adhesion kinase activates its autophosphorylation. J. Biol. Chem. 278, 47434-47440
147. Eun Jeoung, L., Sung Hee, H., Jaesun, C., Sung Hwa, S., Kwang Hum, Y., Min Kyoung, K., Tae Yoon, P. and Sang Sun, K. (2008) Regulation of glycogen synthase kinase 3β functions by modification of the small ubiquitin-like modifier. Open Biochem. J. 2, 67-76
148. Roscic, A., Moller, A., Calzado, M. A., Renner, F., Wimmer, V. C., Gresko, E., Ludi, K. S. and Schmitz, M. L. (2006) Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol. Cell 24, 77-89
149. Woo, C. H., Shishido, T., McClain, C., Lim, J. H., Li, J. D., Yang, J., Yan, C. and Abe, J. (2008) Extracellular signal-regulated kinase 5 SUMOylation antagonizes shear stress-induced antiinflammatory response and endothelial nitric oxide synthase expression in endothelial cells. Circ. Res. 102, 538-545
150. Dadke, S., Cotteret, S., Yip, S. C., Jaffer, Z. M., Haj, F., Ivanov, A., Rauscher, III, F., Shuai, K., Ng, T., Neel, B. G. and Chernoff, J. (2007) Regulation of protein tyrosine phosphatase 1B by sumoylation. Nat. Cell Biol. 9, 80-85
151. Favreau, C., Worman, H. J., Wozniak, R. W., Frappier, T. and Courvalin, J. C. (1996) Cell cycle-dependent phosphorylation of nucleoporins and nuclear pore membrane protein Gp210. Biochemistry 35, 8035-8044
152. Stehmeier, P. and Muller, S. (2009) Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol. Cell 33, 400-409
153. Liu, B., Yang, Y., Chernishof, V., Loo, R. R., Jang, H., Tahk, S., Yang, R., Mink, S., Shultz, D., Bellone, C. J. et al. (2007) Proinflammatory stimuli induce IKKα-mediated phosphorylation of PIAS1 to restrict inflammation and immunity. Cell 129, 903-914
154. Park, H. J., Zheng, H., Kulkarni, D., Kerrigan, J., Pungaliya, P., Saleem, A. and Rubin, E. H. (2008) Identification of phosphorylation sites of TOPORS and a role for serine 98 in the regulation of ubiquitin but not SUMO E3 ligase activity. Biochemistry 47, 13887-13896
155. Matic, I., Macek, B., Hilger, M., Walther, T. C. and Mann, M. (2008) Phosphorylation of SUMO-1 occurs in vivoand is conserved through evolution. J. Proteome Res. 7, 4050-4057
156. Bencsath, K. P., Podgorski, M. S., Pagala, V. R., Slaughter, C. A. and Schulman, B. A. (2002) Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J. Biol. Chem. 277, 47938-47945
157. Wohlschlegel, J. A., Johnson, E. S., Reed, S. I. and Yates, III, J. R. (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279, 45662-45668
158. Zhou, W., Ryan, J. J. and Zhou, H. (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 279, 32262-32268
159. Zhao, Y., Kwon, S. W., Anselmo, A., Kaur, K. and White, M. A. (2004) Broad spectrum identification of cellular small ubiquitin-related modifier (SUMO) substrate proteins. J. Biol. Chem. 279, 20999-21002
160. Knipscheer, P., Flotho, A., Klug, H., Olsen, J. V., van Dijk, W. J., Fish, A., Johnson, E. S., Mann, M., Sixma, T. K. and Pichler, A. (2008) Ubc9 sumoylation regulates SUMO target discrimination. Mol. Cell 31, 371-382
161. Weger, S., Hammer, E. and Engstler, M. (2003) The DNA topoisomerase I binding protein topors as a novel cellular target for SUMO-1 modification: characterization of domains necessary for subcellular localization and sumolation. Exp. Cell Res. 290, 13-27
162. Zhu, S., Goeres, J., Sixt, K. M., Bekes, M., Zhang, X. D., Salvesen, G. S. and Matunis, M. J. (2009) Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1. Mol. Cell 33, 570-580
163. Meulmeester, E., Kunze, M., Hsiao, H. H., Urlaub, H. and Melchior, F. (2008) Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell 30, 610-619
164. Zhu, J., Zhu, S., Guzzo, C. M., Ellis, N. A., Sung, K. S., Choi, C. Y. and Matunis, M. J. (2008) Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 283, 29405-29415