Starting and stopping SUMOylation: What regulates the regulator?

Chromosoma

Volumn 122, Issue 6, 2013, Pages 451-463

  Watts, Felicity Z ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

DNA damage; Oxidative stress; PIAS; SENP; Ubc9; Ubiquitin

Indexed keywords

MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO 4 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; CANCER CELL; CELL STRESS; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

ACETYLATION; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; PHOSPHORYLATION; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84889078990     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-013-0422-0     Document Type: Review

References (116)

1. Albor A, El-Hizawi S, Horn EJ, Laederich M, Frosk P, Wrogemann K, Kulesz-Martin M (2006) The interaction of Piasy with Trim32, an E3-ubiquitin ligase mutated in limb-girdle muscular dystrophy type 2H, promotes Piasy degradation and regulates UVB-induced keratinocyte apoptosis through NFkappaB. J Biol Chem 281:25850-25866
2. Amente S, Lavadera ML, Palo GD, Majello B (2012) SUMO-activating SAE1 transcription is positively regulated by Myc. Am J Cancer Res 2:330-334
3. Azuma Y, Tan SH, Cavenagh MM, Ainsztein AM, Saitoh H, Dasso M (2001) Expression and regulation of the mammalian SUMO-1 E1 enzyme. FASEB J 15:1825-1827
4. Bailey D, O'Hare P (2002) Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. J Gen Virol 83:2951-2964
5. Bailey D, O'Hare P (2004) Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J Biol Chem 279:692-703
6. Bawa-Khalfe T, Cheng J, Lin SH, Ittmann MM, Yeh ET (2010) SENP1 induces prostatic intraepithelial neoplasia through multiple mechanisms. J Biol Chem 285:25859-25866
7. Becker J, Barysch SV, Karaca S, Dittner C, Hsiao HH, Diaz MB, Herzig S, Urlaub H, Melchior F (2013) Detecting endogenous SUMO targets in mammalian cells and tissues. Nat Struct Mol Biol 20:525-531
8. Bettermann K, Benesch M, Weis S, Haybaeck J (2012) SUMOylation in carcinogenesis. Cancer Lett 316:113-125
9. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, Kuo WP, Weber G, Lee K, Fraioli RE, Cho SH, Yung R, Asch E, Ohno-Machado L, Wong WH, Cepko CL (2004) Genomic analysis of mouse retinal development. PLoS Biology 2:E247
10. Boggio R, Colombo R, Hay RT, Draetta GF, Chiocca S (2004) A mechanism for inhibiting the SUMO pathway. Molecular cell 16:549-561
11. Bossis G, Melchior F (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol Cell 21:349-357
12. Bruderer R, Tatham MH, Plechanovova A, Matic I, Garg AK, Hay RT (2011) Purification and identification of endogenous polySUMO conjugates. EMBO Rep 12:142-148
13. Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell 131:309-323
14. Chen R, Dioum EM, Hogg RT, Gerard RD, Garcia JA (2011a) Hypoxia increases sirtuin 1 expression in a hypoxia-inducible factor-dependent manner. J Biol Chem 286:13869-13878
15. Chen SF, Gong C, Luo M, Yao HR, Zeng YJ, Su FX (2011b) Ubc9 expression predicts chemoresistance in breast cancer. Chin J Cancer 30:638-644
16. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF (2006a) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067-2081
17. Cheng J, Bawa T, Lee P, Gong L, Yeh ET (2006b) Role of desumoylation in the development of prostate cancer. Neoplasia 8:667-676
18. Chiocca S (2007) Viral control of the SUMO pathway: Gaml, a model system. Biochem Soc Trans 35:1419-1421
19. Chow KH, Elgort S, Dasso M, Ullman KS (2012) Two distinct sites in Nup153 mediate interaction with the SUMO proteases SENP1 and SENP2. Nucleus 3:349-358
20. Comerford KM, Leonard MO, Karhausen J, Carey R, Colgan SP, Taylor CT (2003) Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc Natl Acad Sci U S A 100:986-991
21. Depaux A, Regnier-Ricard F, Germani A, Varin-Blank N (2007) A crosstalk between hSiah2 and Pias E3-ligases modulates Pias-dependent activation. Oncogene 26:6665-6676
22. Desterro JM, Rodriguez MS, Hay RT (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2:233-239
23. Deyrieux AF, Rosas-Acosta G, Ozbun MA, Wilson VG (2007) Sumoylation dynamics during keratinocyte differentiation. Journal of cell science 120:125-136
24. Dohmen RJ, Stappen R, McGrath JP, Forrova H, Kolarov J, Goffeau A, Varshavsky A (1995) An essential yeast gene encoding a homolog of ubiquitin-activating enzyme. J Biol Chem 270:18099-18109
25. Donaghue C, Bates H, Cotterill S (2001) Identification and characterisation of the Drosophila homologue of the yeast Uba2 gene. Biochim Biophys Acta 1518:210-214
26. Driscoll JJ, Pelluru D, Lefkimmiatis K, Fulciniti M, Prabhala RH, Greipp PR, Barlogie B, Tai YT, Anderson KC, Shaughnessy JD Jr, Annunziata CM, Munshi NC (2010) The sumoylation pathway is dysregulated in multiple myeloma and is associated with adverse patient outcome. Blood 115:2827-2834
27. Elmore ZC, Donaher M, Matson BC, Murphy H, Westerbeck JW, Kerscher O (2011) Sumo-dependent substrate targeting of the SUMO protease Ulp1. BMC Biol 9:74
28. Erker Y, Neyret-Kahn H, Seeler JS, Dejean A, Atfi A, Levy L (2013) Arkadia, a novel SUMO-targeted ubiquitin ligase involved in PML degradation. Mol Cell Biol 33:2163-2177
29. Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15:247-254
30. Flick K, Kaiser P (2009) Proteomic revelation: SUMO changes partners when the heat is on. Sci Signal 2
31. Goeres J, Chan PK, Mukhopadhyay D, Zhang H, Raught B, Matunis MJ (2011) The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup107-160 nucleoporin subcomplex. Molecular Biology of the Cell 22:4868-4882
32. Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, Cox J, Barton GJ, Mann M, Hay RT (2009) System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2:ra24
33. Golebiowski F, Szulc A, Sakowicz M, Szutowicz A, Pawelczyk T (2003) Expression level of Ubc9 protein in rat tissues. Acta Biochim Pol 50:1065-1073
34. Gong L, Millas S, Maul GG, Yeh ET (2000) Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J Biol Chem 275:3355-3359
35. Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, Emili A, Hochstrasser M (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280:4102-4110
36. Hay RT (2005) SUMO: a history of modification. Mol Cell 18:1-12
37. Heaton PR, Deyrieux AF, Bian XL, Wilson VG (2011) HPV E6 proteins target Ubc9, the SUMO conjugating enzyme. Virus Res 158:199-208
38. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I (2006) Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281:16117-16127
39. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425-479
40. Hickey CM, Wilson NR, Hochstrasser M (2012) Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 13:755-766
41. Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A, Sistonen L (2006) PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci U S A 103:45-50
42. Ho CW, Chen HT, Hwang J (2011) UBC9 autosumoylation negatively regulates sumoylation of septins in Saccharomyces cerevisiae. J Biol Chem 286:21826-21834
43. Hoefer J, Schafer G, Klocker H, Erb HH, Mills IG, Hengst L, Puhr M, Culig Z (2012) PIAS1 is increased in human prostate cancer and enhances proliferation through inhibition of p21. Am J Pathol 180:2097-2107
44. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141
45. Hsieh YL, Kuo HY, Chang CC, Naik MT, Liao PH, Ho CC, Huang TC, Jeng JC, Hsu PH, Tsai MD, Huang TH, Shih HM (2013) Ubc9 acetylation modulates distinct SUMO target modification and hypoxia response. EMBO J 32:791-804
46. Itahana Y, Yeh ET, Zhang Y (2006) Nucleocytoplasmic shuttling modulates activity and ubiquitination-dependent turnover of SUMO-specific protease 2. Mol Cell Biol 26:4675-4689
47. Jackson SP, Durocher D (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Molecular cell 49:795-807
48. Jacques C, Baris O, Prunier-Mirebeau D, Savagner F, Rodien P, Rohmer V, Franc B, Guyetant S, Malthiery Y, Reynier P (2005) Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J Clin Endocrinol Metab 90:2314-2320
49. Johnson ES, Gupta AA (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735-744
50. Kessler JD, Kahle KT, Sun T, Meerbrey KL, Schlabach MR, Schmitt EM, Skinner SO, Xu Q, Li MZ, Hartman ZC, Rao M, Yu P, Dominguez-Vidana R, Liang AC, Solimini NL, Bernardi RJ, Yu B, Hsu T, Golding I, Luo J, Osborne CK, Creighton CJ, Hilsenbeck SG, Schiff R, Shaw CA, Elledge SJ, Westbrook TF (2012) A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science 335:348-353
51. Kim YH, Sung KS, Lee SJ, Kim YO, Choi CY, Kim Y (2005) Desumoylation of homeodomain-interacting protein kinase 2 (HIPK2) through the cytoplasmic-nuclear shuttling of the SUMO-specific protease SENP1. FEBS Lett 579:6272-6278
52. Klug H, Xaver M, Chaugule VK, Koidl S, Mittler G, Klein F, Pichler A (2013) Ubc9 sumoylation controls SUMO chain formation and meiotic synapsis in Saccharomyces cerevisiae. Molecular Cell
53. Knipscheer P, Flotho A, Klug H, Olsen JV, van Dijk WJ, Fish A, Johnson ES, Mann M, Sixma TK, Pichler A (2008) Ubc9 sumoylation regulates SUMO target discrimination. Mol Cell 31:371-382
54. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI (1996) Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci U S A 93:2958-2963
55. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (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
56. Ledl A, Schmidt D, Muller S (2005) Viral oncoproteins E1A and E7 and cellular LxCxE proteins repress SUMO modification of the retinoblastoma tumor suppressor. Oncogene 24:3810-3818
57. Lee JS, Thorgeirsson SS (2004) Genome-scale profiling of gene expression in hepatocellular carcinoma: classification, survival prediction, and identification of therapeutic targets. Gastroenterology 127:S51-S55
58. Lee MH, Mabb AM, Gill GB, Yeh ET, Miyamoto S (2011) NF-kappaB induction of the SUMO protease SENP2: a negative feedback loop to attenuate cell survival response to genotoxic stress. Molecular cell 43:180-191
59. Li SJ, Hochstrasser M (2003) The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J Cell Biol 160:1069-1081
60. Li X, Luo Y, Yu L, Lin Y, Luo D, Zhang H, He Y, Kim YO, Kim Y, Tang S, Min W (2008) SENP1 mediates TNF-induced desumoylation and cytoplasmic translocation of HIPK1 to enhance ASK1-dependent apoptosis. Cell Death Differ 15:739-750
61. Liu B, Yang Y, Chernishof V, Loo RR, Jang H, Tahk S, Yang R, Mink S, Shultz D, Bellone CJ, Loo JA, Shuai K (2007) Proinflammatory stimuli induce IKKalpha-mediated phosphorylation of PIAS1 to restrict inflammation and immunity. Cell 129:903-914
62. Lois LM, Lima CD (2005) Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J 24:439-451
63. Makhnevych T, Ptak C, Lusk CP, Aitchison JD, Wozniak RW (2007) The role of karyopherins in the regulated sumoylation of septins. The Journal of Cell Biology 177:39-49
64. Manza LL, Codreanu SG, Stamer SL, Smith DL, Wells KS, Roberts RL, Liebler DC (2004) Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem Res Toxicol 17:1706-1715
65. Matic I, Macek B, Hilger M, Walther TC, Mann M (2008) Phosphorylation of SUMO-1 occurs in vivo and is conserved through evolution. J Proteome Res 7:4050-4057
66. Matic I, Schimmel J, Hendriks IA, van Santen MA, van de Rijke F, van Dam H, Gnad F, Mann M, Vertegaal AC (2010) Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol Cell 39:641-652
67. McDoniels-Silvers AL, Nimri CF, Stoner GD, Lubet RA, You M (2002) Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clin Cancer Res 8:1127-1138
68. Mo YY, Moschos SJ (2005) Targeting Ubc9 for cancer therapy. Expert Opin Ther Targets 9:1203-1216
69. Mo YY, Yu Y, Theodosiou E, Ee PL, Beck WT (2005) A role for Ubc9 in tumorigenesis. Oncogene 24:2677-2683
70. Moschos SJ, Jukic DM, Athanassiou C, Bhargava R, Dacic S, Wang X, Kuan SF, Fayewicz SL, Galambos C, Acquafondata M, Dhir R, Becker D (2010) Expression analysis of Ubc9, the single small ubiquitin-like modifier (SUMO) E2 conjugating enzyme, in normal and malignant tissues. Hum Pathol 41:1286-1298
71. Moutty MC, Sakin V, Melchior F (2011) Importin alpha/beta mediates nuclear import of individual SUMO E1 subunits and of the holo-enzyme. Molecular Biology of the Cell 22:652-660
72. Mukhopadhyay D, Dasso M (2007) Modification in reverse: the SUMO proteases. Trends Biochem Sci 32:286-295
73. Muller S, Dejean A (1999) Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J Virol 73:5137-5143
74. Nigam N, Singh A, Sahi C, Chandramouli A, Grover A (2008) SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Mol Genet Genomics 279:371-383
75. Panse VG, Kuster B, Gerstberger T, Hurt E (2003) Unconventional tethering of Ulp1 to the transport channel of the nuclear pore complex by karyopherins. Nat Cell Biol 5:21-27
76. Parkinson J, Everett RD (2000) Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins. J Virol 74:10006-10017
77. Pinto MP, Carvalho AF, Grou CP, Rodriguez-Borges JE, Sa-Miranda C, Azevedo JE (2012) Heat shock induces a massive but differential inactivation of SUMO-specific proteases. Biochim Biophys Acta 1823:1958-1966
78. Roscic A, Moller A, Calzado MA, Renner F, Wimmer VC, Gresko E, Ludi KS, Schmitz ML (2006) Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Molecular cell 24:77-89
79. Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275:6252-6258
80. Saitoh H, Sparrow DB, Shiomi T, Pu RT, Nishimoto T, Mohun TJ, Dasso M (1998) Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2. Curr Biol 8:121-124
81. Sang J, Yang K, Sun Y, Han Y, Cang H, Chen Y, Shi G, Wang K, Zhou J, Wang X, Yi J (2011) SUMO2 and SUMO3 transcription is differentially regulated by oxidative stress in an Sp1-dependent manner. Biochem J 435:489-498
82. Schwienhorst I, Johnson ES, Dohmen RJ (2000) SUMO conjugation and deconjugation. Mol Gen Genet 263:771-786
83. Shao R, Zhang FP, Tian F, Anders Friberg P, Wang X, Sjoland H, Billig H (2004) Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF-1alpha in adult mouse brain and heart in vivo. FEBS Lett 569:293-300
84. Skilton A, Ho JC, Mercer B, Outwin E, Watts FZ (2009) SUMO chain formation is required for response to replication arrest in S. pombe. PLoS One 4:e6750
85. Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci U S A 101:14373-14378
86. Song J, Zhang Z, Hu W, Chen Y (2005) Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J Biol Chem 280:40122-40129
87. Stelter P, Ulrich HD (2003) Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425:188-191
88. Su YF, Yang T, Huang H, Liu LF, Hwang J (2012) Phosphorylation of Ubc9 by Cdk1 enhances SUMOylation activity. PLoS One 7:e34250
89. Subramaniam S, Mealer RG, Sixt KM, Barrow RK, Usiello A, Snyder SH (2010) Rhes, a physiologic regulator of sumoylation, enhances cross-sumoylation between the basic sumoylation enzymes E1 and Ubc9. J Biol Chem 285:20428-20432
90. Sun H, Hunter T (2012) Poly-small ubiquitin-like modifier (PolySUMO)-binding proteins identified through a string search. J Biol Chem 287:42071-42083
91. Sydorskyy Y, Srikumar T, Jeram SM, Wheaton S, Vizeacoumar FJ, Makhnevych T, Chong YT, Gingras AC, Raught B (2010) A novel mechanism for SUMO system control: regulated Ulp1 nucleolar sequestration. Mol Cell Biol 30:4452-4462
92. Takahashi Y, Kahyo T, Toh EA, Yasuda H, Kikuchi Y (2001) Yeast Ull1/Siz1 is a novel SUMO1/Smt3 ligase for septin components and functions as an adaptor between conjugating enzyme and substrates. J Biol Chem 276:48973-48977
93. Takahashi Y, Toh EA, Kikuchi Y (2003) Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. J Biochem (Tokyo) 133:415-422
94. Talamillo A, Sanchez J, Barrio R (2008) Functional analysis of the SUMOylation pathway in Drosophila. Biochem Soc Trans 36:868-873
95. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10:538-546
96. Tatham MH, Matic I, Mann M, Hay RT (2011) Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal 4:rs4
97. Tatham MH, Plechanovova A, Jaffray EG, Salmen H, Hay RT (2013) Ube2W conjugates ubiquitin to alpha-amino groups of protein N-termini. The Biochemical journal
98. Taylor DL, Ho JC, Oliver A, Watts FZ (2002) Cell-cycle-dependent localisation of Ulp1, a Schizosaccharomyces pombe Pmt3 (SUMO)-specific protease. J Cell Sci 115:1113-1122
99. Truong K, Lee TD, Chen Y (2012a) Small ubiquitin-like modifier (SUMO) modification of E1 Cys domain inhibits E1 Cys domain enzymatic activity. J Biol Chem 287:15154-15163
100. Truong K, Lee TD, Li B, Chen Y (2012b) Sumoylation of SAE2 C-terminus regulates SAE nuclear localization. J Biol Chem 287:42611-42619
101. Ullmann R, Chien CD, Avantaggiati ML, Muller S (2012) An acetylation switch regulates SUMO-dependent protein interaction networks. Molecular cell 46:759-770
102. Um JW, Chung KC (2006) Functional modulation of parkin through physical interaction with SUMO-1. J Neurosci Res 84:1543-1554
103. Wang L, Banerjee S (2004) Differential PIAS3 expression in human malignancy. Oncol Rep 11:1319-1324
104. Wang Y, Mukhopadhyay D, Mathew S, Hasebe T, Heimeier RA, Azuma Y, Kolli N, Shi YB, Wilkinson KD, Dasso M (2009) Identification and developmental expression of Xenopus laevis SUMO proteases. PLoS One 4:e8462
105. Wang Z, Prelich G (2009) Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol Cell Biol 29:1694-1706
106. Wang ZY, Qiu QQ, Seufert W, Taguchi T, Testa JR, Whitmore SA, Callen DF, Welsh D, Shenk T, Deuel TF (1996) Molecular cloning of the cDNA and chromosome localization of the gene for human ubiquitin-conjugating enzyme 9. J Biol Chem 271:24811-24816
107. Wohlschlegel JA, Johnson ES, Reed SI, Yates JR 3rd (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279:45662-45668
108. Xu Z, Lam LS, Lam LH, Chau SF, Ng TB, Au SW (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
109. Yan S, Sun X, Xiang B, Cang H, Kang X, Chen Y, Li H, Shi G, Yeh ET, Wang B, Wang X, Yi J (2010) Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J 29:3773-3786
110. Yan W, Santti H, Janne OA, Palvimo JJ, Toppari J (2003) Expression of the E3 SUMO-1 ligases PIASx and PIAS1 during spermatogenesis in the rat. Gene Expr Patterns 3:301-308
111. Yang SH, Galanis A, Witty J, Sharrocks AD (2006) An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J 25:5083-5093
112. Yeh ET (2009) SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem 284:8223-8227
113. Yun C, Wang Y, Mukhopadhyay D, Backlund P, Kolli N, Yergey A, Wilkinson KD, Dasso M (2008) Nucleolar protein B23/nucleophosmin regulates the vertebrate SUMO pathway through SENP3 and SENP5 proteases. J Cell Biol 183:589-595
114. Zhao Y, Kwon SW, Anselmo A, Kaur K, White MA (2004) Broad spectrum identification of cellular small ubiquitin-related modifier (SUMO) substrate proteins. J Biol Chem 279:20999-21002
115. Zhou W, Ryan JJ, Zhou H (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 279:32262-32268
116. Zunino R, Braschi E, Xu L, McBride HM (2009) Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem 284:17783-17795