Emerging roles of desumoylating enzymes

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 3, 2009, Pages 155-162

  Kim, Jung Hwa ^a   Baek, Sung Hee ^b  

^a Inha University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Desumoylation enzyme; SENP; SUMO; SUMO isoform; Ulp

Indexed keywords

PROTEINASE; SENP1 ENZYME; SENP2 ENZYME; SENP3 ENZYME; SENP4 ENZYME; SENP5 ENZYME; SENP6 ENZYME; SENP7 ENZYME; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO PROTEIN; SUMO SPECIFIC PROTEINASE; UBIQUITIN; UBIQUITIN LIKE PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; CARCINOGENESIS; CATALYSIS; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL GROWTH; CELL STRAIN LNCAP; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; FIBROBLAST; HUMAN; MEDICAGO; MOUTH CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTOZOON; REVIEW; RHEUMATOID ARTHRITIS; RICE; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; SACROCOCCYX TERATOMA; SUMOYLATION; TOMATO; TRANSCRIPTION REGULATION;

ANIMALS; HUMANS; PLANT PROTEINS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTOZOAN PROTEINS; PYRUVATES; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 61349180289     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2008.12.008     Document Type: Review

References (134)

1. Kerscher O., Felberbaum R., and Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell. Dev. Biol. 22 (2006) 159-180
2. Jentsch S., and Pyrowolakis G. Ubiquitin and its kin: how close are the family ties?. Trends Cell Biol. 10 (2000) 335-342
3. 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. 280 (1998) 275-286
4. Bernier-Villamor V., Sampson D.A., Matunis M.J., and Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108 (2002) 345-356
5. Mossessova E., and Lima C.D. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5 (2000) 865-876
6. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 73 (2004) 355-382
7. Zhao J. Sumoylation regulates diverse biological processes. Cell Mol. Life Sci. 64 (2007) 3017-3033
8. Geiss-Friedlander R., and Melchior F. Concepts in sumoylation: a decade on. Nat. Rev., Mol. Cell Biol. 8 (2007) 947-956
9. Li S.J., and Hochstrasser M. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20 (2000) 2367-2377
10. Li S.J., and Hochstrasser M. A new protease required for cell-cycle progression in yeast. Nature 398 (1999) 246-251
11. Mukhopadhyay D., and Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32 (2007) 286-295
12. Hay R.T. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 17 (2007) 370-376
13. Gong L., Millas S., Maul G.G., and Yeh E.T. Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J. Biol. Chem. 275 (2000) 3355-3359
14. Drag M., Mikolajczyk J., Krishnakumar I.M., Huang Z., and Salvesen G.S. Activity profiling of human deSUMOylating enzymes (SENPs) with synthetic substrates suggests an unexpected specificity of two newly characterized members of the family. Biochem. J. 409 (2008) 461-469
15. Meluh P.B., and Koshland D. 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 (1995) 793-807
16. Melchior F. SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16 (2000) 591-626
17. Su H.L., and Li S.S. Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 296 (2002) 65-73
18. Guo D., Li M., Zhang Y., Yang P., Eckenrode S., Hopkins D., Zheng W., Purohit S., Podolsky R.H., Muir A., Wang J., Dong Z., Brusko T., Atkinson M., Pozzilli P., Zeidler A., Raffel L.J., Jacob C.O., Park Y., Serrano-Rios M., Larrad M.T., Zhang Z., Garchon H.J., Bach J.F., Rotter J.I., She J.X., and Wang C.Y. A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat. Genet. 36 (2004) 837-841
19. Owerbach D., McKay E.M., Yeh E.T., Gabbay K.H., and Bohren K.M. A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337 (2005) 517-520
20. Desterro J.M., Rodriguez M.S., Kemp G.D., and Hay R.T. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274 (1999) 10618-10624
21. Gong L., Li B., Millas S., and Yeh E.T. Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex. FEBS Lett. 448 (1999) 185-189
22. Johnson E.S., Schwienhorst I., Dohmen R.J., and Blobel G. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. Embo J. 16 (1997) 5509-5519
23. Okuma T., Honda R., Ichikawa G., Tsumagari N., and Yasuda H. In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem. Biophys. Res. Commun. 254 (1999) 693-698
24. Desterro J.M., Thomson J., and Hay R.T. Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417 (1997) 297-300
25. Johnson E.S., and Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272 (1997) 26799-26802
26. Lee G.W., Melchior F., Matunis M.J., Mahajan R., Tian Q., and Anderson P. 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 (1998) 6503-6507
27. Saitoh H., Sparrow D.B., Shiomi T., Pu R.T., Nishimoto T., Mohun T.J., and Dasso M. Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2. Curr. Biol. 8 (1998) 121-124
28. Rodriguez M.S., Dargemont C., and Hay R.T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276 (2001) 12654-12659
29. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
30. Pichler A., Knipscheer P., Oberhofer E., van Dijk W.J., Korner R., Olsen J.V., Jentsch S., Melchior F., and Sixma T.K. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12 (2005) 264-269
31. Johnson E.S., and Gupta A.A. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106 (2001) 735-744
32. Kahyo T., Nishida T., and Yasuda H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell. 8 (2001) 713-718
33. Nakagawa K., and Yokosawa H. PIAS3 induces SUMO-1 modification and transcriptional repression of IRF-1. FEBS Lett. 530 (2002) 204-208
34. Nishida T., and Yasuda H. PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J. Biol. Chem. 277 (2002) 41311-41317
35. Sachdev S., Bruhn L., Sieber H., Pichler A., Melchior F., and Grosschedl R. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15 (2001) 3088-3103
36. Takahashi Y., Kahyo T., Toh E.A., Yasuda H., and Kikuchi Y. 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 (2001) 48973-48977
37. Kagey M.H., Melhuish T.A., Powers S.E., and Wotton D. Multiple activities contribute to Pc2 E3 function. Embo J. 24 (2005) 108-119
38. Kagey M.H., Melhuish T.A., and Wotton D. The polycomb protein Pc2 is a SUMO E3. Cell 113 (2003) 127-137
39. 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. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. Embo J. 21 (2002) 2682-2691
40. Pichler A., Gast A., Seeler J.S., Dejean A., and Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108 (2002) 109-120
41. Saitoh H., and Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275 (2000) 6252-6258
42. 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. 276 (2001) 35368-35374
43. Bencsath K.P., Podgorski M.S., Pagala V.R., Slaughter C.A., and Schulman B.A. Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J. Biol. Chem. 277 (2002) 47938-47945
44. Bylebyl G.R., Belichenko I., and Johnson E.S. The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278 (2003) 44113-44120
45. Fu C., Ahmed K., Ding H., Ding X., Lan J., Yang Z., Miao Y., Zhu Y., Shi Y., Zhu J., Huang H., and Yao X. Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 24 (2005) 5401-5413
46. Bae S.H., Jeong J.W., Park J.A., Kim S.H., Bae M.K., Choi S.J., and Kim K.W. Sumoylation increases HIF-1alpha stability and its transcriptional activity. Biochem. Biophys. Res. Commun. 324 (2004) 394-400
47. Desterro J.M., Rodriguez M.S., and Hay R.T. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2 (1998) 233-239
48. Lee M.H., Lee S.W., Lee E.J., Choi S.J., Chung S.S., Lee J.I., Cho J.M., Seol J.H., Baek S.H., Kim K.I., Chiba T., Tanaka K., Bang O.S., and Chung C.H. SUMO-specific protease SUSP4 positively regulates p53 by promoting Mdm2 self-ubiquitination. Nat. Cell Biol. 8 (2006) 1424-1431
49. Lin X., Liang M., Liang Y.Y., Brunicardi F.C., and Feng X.H. SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J. Biol. Chem. 278 (2003) 31043-31048
50. Sacher M., Pfander B., Hoege C., and Jentsch S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8 (2006) 1284-1290
51. Steffan J.S., Agrawal N., Pallos J., Rockabrand E., Trotman L.C., Slepko N., Illes K., Lukacsovich T., Zhu Y.Z., Cattaneo E., Pandolfi P.P., Thompson L.M., and Marsh J.L. SUMO modification of Huntingtin and Huntington's disease pathology. Science 304 (2004) 100-104
52. Ulrich H.D., Vogel S., and Davies A.A. SUMO keeps a check on recombination during DNA replication. Cell Cycle 4 (2005) 1699-1702
53. Watts F.Z. Sumoylation of PCNA: wrestling with recombination at stalled replication forks. DNA Repair. (Amst) 5 (2006) 399-403
54. Xie Y., Kerscher O., Kroetz M.B., McConchie H.F., Sung P., and Hochstrasser M. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 282 (2007) 34176-34184
55. Uzunova K., Gottsche K., Miteva M., Weisshaar S.R., Glanemann C., Schnellhardt M., Niessen M., Scheel H., Hofmann K., Johnson E.S., Praefcke G.J., and Dohmen R.J. Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282 (2007) 34167-34175
56. Tatham M.H., Geoffroy M.C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., Palvimo J.J., and Hay R.T. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10 (2008) 538-546
57. Lallemand-Breitenbach V., Jeanne M., Benhenda S., Nasr R., Lei M., Peres L., Zhou J., Zhu J., Raught B., and de The H. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10 (2008) 547-555
58. Lee J., Lee Y., Lee M.J., Park E., Kang S.H., Chung C.H., Lee K.H., and Kim K. Dual Modification of BMAL1 by SUMO2/3 and Ubiquitin Promotes Circadian Activation of the CLOCK/BMAL1 Complex. Mol. Cell. Biol. 28 (2008) 6056-6065
59. Yeh E.T., Gong L., and Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 248 (2000) 1-14
60. Mendoza H.M., Shen L.N., Botting C., Lewis A., Chen J., Ink B., and Hay R.T. NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem. 278 (2003) 25637-25643
61. Wu K., Yamoah K., Dolios G., Gan-Erdene T., Tan P., Chen A., Lee C.G., Wei N., Wilkinson K.D., Wang R., and Pan Z.Q. DEN1 is a dual function protease capable of processing the C terminus of Nedd8 and deconjugating hyper-neddylated CUL1. J. Biol. Chem. 278 (2003) 28882-28891
62. Mukhopadhyay D., Ayaydin F., Kolli N., Tan S.H., Anan T., Kametaka A., Azuma Y., Wilkinson K.D., and Dasso M. SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J. Cell. Biol. 174 (2006) 939-949
63. Kim K.I., Baek S.H., and Chung C.H. Versatile protein tag, SUMO: its enzymology and biological function. J. Cell. Physiol. 191 (2002) 257-268
64. Drag M., and Salvesen G.S. DeSUMOylating enzymes-SENPs. IUBMB Life 60 (2008) 734-742
65. Nicholson B., Leach C.A., Goldenberg S.J., Francis D.M., Kodrasov M.P., Tian X., Shanks J., Sterner D.E., Bernal A., Mattern M.R., Wilkinson K.D., and Butt T.R. Characterization of ubiquitin and ubiquitin-like-protein isopeptidase activities. Protein Sci. 17 (2008) 1035-1043
66. Lindner H.A., Fotouhi-Ardakani N., Lytvyn V., Lachance P., Sulea T., and Menard R. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J. Virol. 79 (2005) 15199-15208
67. Horton R.A., Strachan E.A., Vogel K.W., and Riddle S.M. A substrate for deubiquitinating enzymes based on time-resolved fluorescence resonance energy transfer between terbium and yellow fluorescent protein. Anal. Biochem. 360 (2007) 138-143
68. Gan-Erdene T., Nagamalleswari K., Yin L., Wu K., Pan Z.Q., and Wilkinson K.D. Identification and characterization of DEN1, a deneddylase of the ULP family. J. Biol. Chem. 278 (2003) 28892-28900
69. Dang L.C., Melandri F.D., and Stein R.L. Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes. Biochemistry 37 (1998) 1868-1879
70. Li S.J., and Hochstrasser M. The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J. Cell. Biol. 160 (2003) 1069-1081
71. Panse V.G., Kuster B., Gerstberger T., and Hurt E. Unconventional tethering of Ulp1 to the transport channel of the nuclear pore complex by karyopherins. Nat. Cell Biol. 5 (2003) 21-27
72. Bailey D., and O'Hare P. Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 279 (2004) 692-703
73. Bailey D., and O'Hare P. Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. J. Gen. Virol. 83 (2002) 2951-2964
74. Kim Y.H., Sung K.S., Lee S.J., Kim Y.O., Choi C.Y., and Kim Y. Desumoylation of homeodomain-interacting protein kinase 2 (HIPK2) through the cytoplasmic-nuclear shuttling of the SUMO-specific protease SENP1. FEBS Lett. 579 (2005) 6272-6278
75. Hang J., and Dasso M. Association of the human SUMO-1 protease SENP2 with the nuclear pore. J. Biol. Chem. 277 (2002) 19961-19966
76. Zhang H., Saitoh H., and Matunis M.J. Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol. Cell. Biol. 22 (2002) 6498-6508
77. Ross S., Best J.L., Zon L.I., and Gill G. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 10 (2002) 831-842
78. Itahana Y., Yeh E.T., and Zhang Y. Nucleocytoplasmic shuttling modulates activity and ubiquitination-dependent turnover of SUMO-specific protease 2. Mol. Cell. Biol. 26 (2006) 4675-4689
79. Nishida T., Kaneko F., Kitagawa M., and Yasuda H. Characterization of a novel mammalian SUMO-1/Smt3-specific isopeptidase, a homologue of rat axam, which is an axin-binding protein promoting beta-catenin degradation. J. Biol. Chem. 276 (2001) 39060-39066
80. Best J.L., Ganiatsas S., Agarwal S., Changou A., Salomoni P., Shirihai O., Meluh P.B., Pandolfi P.P., and Zon L.I. SUMO-1 protease-1 regulates gene transcription through PML. Mol. Cell 10 (2002) 843-855
81. Nishida T., Tanaka H., and Yasuda H. A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur J. Biochem. 267 (2000) 6423-6427
82. Gong L., and Yeh E.T. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J. Biol. Chem. 281 (2006) 15869-15877
83. Kuo M.L., den Besten W., Thomas M.C., and Sherr C.J. Arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease Senp3. Cell Cycle 7 (2008) 3378-3387
84. Kim K.I., Baek S.H., Jeon Y.J., Nishimori S., Suzuki T., Uchida S., Shimbara N., Saitoh H., Tanaka K., and Chung C.H. A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. J. Biol. Chem. 275 (2000) 14102-14106
85. Choi S.J., Chung S.S., Rho E.J., Lee H.W., Lee M.H., Choi H.S., Seol J.H., Baek S.H., Bang O.S., and Chung C.H. Negative modulation of RXRalpha transcriptional activity by small ubiquitin-related modifier (SUMO) modification and its reversal by SUMO-specific protease SUSP1. J. Biol. Chem. 281 (2006) 30669-30677
86. Shen L.N., Dong C., Liu H., Naismith J.H., and Hay R.T. The structure of SENP1-SUMO-2 complex suggests a structural basis for discrimination between SUMO paralogues during processing. Biochem. J. 397 (2006) 279-288
87. Reverter D., and Lima C.D. A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex. Structure 12 (2004) 1519-1531
88. Renatus M., Parrado S.G., D'Arcy A., Eidhoff U., Gerhartz B., Hassiepen U., Pierrat B., Riedl R., Vinzenz D., Worpenberg S., and Kroemer M. Structural basis of ubiquitin recognition by the deubiquitinating protease USP2. Structure 14 (2006) 1293-1302
89. Hu M., Li P., Li M., Li W., Yao T., Wu J.W., Gu W., Cohen R.E., and Shi Y. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111 (2002) 1041-1054
90. Drag M., Mikolajczyk J., Bekes M., Reyes-Turcu F.E., Ellman J.A., Wilkinson K.D., and Salvesen G.S. Positional-scanning fluorigenic substrate libraries reveal unexpected specificity determinants of DUBs (deubiquitinating enzymes). Biochem. J. 415 (2008) 367-375
91. Shen L., Tatham M.H., Dong C., Zagorska A., Naismith J.H., and Hay R.T. SUMO protease SENP1 induces isomerization of the scissile peptide bond. Nat. Struct. Mol. Biol. 13 (2006) 1069-1077
92. Reverter D., and Lima C.D. Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates. Nat. Struct. Mol. Biol. 13 (2006) 1060-1068
93. Xu Z., and Au S.W. Mapping residues of SUMO precursors essential in differential maturation by SUMO-specific protease, SENP1. Biochem. J. 386 (2005) 325-330
94. Di Bacco A., Ouyang J., Lee H.Y., Catic A., Ploegh H., and Gill G. The SUMO-specific protease SENP5 is required for cell division. Mol. Cell. Biol. 26 (2006) 4489-4498
95. Lima C.D., and Reverter D. Structure of the human SENP7 catalytic domain and poly-SUMO deconjugation activities for SENP6 and SENP7. J. Biol. Chem. 283 (2008) 32045-32055
96. Mikolajczyk J., Drag M., Bekes M., Cao J.T., Ronai Z., and Salvesen G.S. Small ubiquitin-related modifier (SUMO)-specific proteases: profiling the specificities and activities of human SENPs. J. Biol. Chem. 282 (2007) 26217-26224
97. Miura K., Jin J.B., and Hasegawa P.M. Sumoylation, a post-translational regulatory process in plants. Curr. Opin. Plant Biol. 10 (2007) 495-502
98. Colby T., Matthai A., Boeckelmann A., and Stuible H.P. SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol. 142 (2006) 318-332
99. Ponder E.L., and Bogyo M. Ubiquitin-like modifiers and their deconjugating enzymes in medically important parasitic protozoa. Eukaryot. Cell 6 (2007) 1943-1952
100. Dohmen R.J. SUMO protein modification. Biochim. Biophys. Acta 1695 (2004) 113-131
101. Li X., Lee Y.K., Jeng J.C., Yen Y., Schultz D.C., Shih H.M., and Ann D.K. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 282 (2007) 36177-36189
102. Kim J.H., Choi H.J., Kim B., Kim M.H., Lee J.M., Kim I.S., Lee M.H., Choi S.J., Kim K.I., Kim S.I., Chung C.H., and Baek S.H. Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat. Cell. Biol. 8 (2006) 631-639
103. Ji Z., Degerny C., Vintonenko N., Deheuninck J., Foveau B., Leroy C., Coll J., Tulasne D., Baert J.L., and Fafeur V. Regulation of the Ets-1 transcription factor by sumoylation and ubiquitinylation. Oncogene 26 (2007) 395-406
104. Cheng J., Wang D., Wang Z., and Yeh E.T. SENP1 enhances androgen receptor-dependent transcription through desumoylation of histone deacetylase 1. Mol. Cell. Biol. 24 (2004) 6021-6028
105. Cheng J., Perkins N.D., and Yeh E.T. Differential regulation of c-Jun-dependent transcription by SUMO-specific proteases. J. Biol. Chem. 280 (2005) 14492-14498
106. Gregoire S., and Yang X.J. Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell. Biol. 25 (2005) 2273-2287
107. Yamaguchi T., Sharma P., Athanasiou M., Kumar A., Yamada S., and Kuehn M.R. Mutation of SENP1/SuPr-2 reveals an essential role for desumoylation in mouse development. Mol. Cell. Biol. 25 (2005) 5171-5182
108. Strunnikov A.V., Aravind L., and Koonin E.V. Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158 (2001) 95-107
109. Felberbaum R., and Hochstrasser M. Ulp2 and the DNA damage response: desumoylation enables safe passage through mitosis. Cell Cycle 7 (2008) 52-56
110. Taylor D.L., Ho J.C., Oliver A., and Watts F.Z. Cell-cycle-dependent localisation of Ulp1, a Schizosaccharomyces pombe Pmt3 (SUMO)-specific protease. J. Cell. Sci. 115 (2002) 1113-1122
111. Meinecke I., Cinski A., Baier A., Peters M.A., Dankbar B., Wille A., Drynda A., Mendoza H., Gay R.E., Hay R.T., Ink B., Gay S., and Pap T. Modification of nuclear PML protein by SUMO-1 regulates Fas-induced apoptosis in rheumatoid arthritis synovial fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5073-5078
112. Yang Y., Fu W., Chen J., Olashaw N., Zhang X., Nicosia S.V., Bhalla K., and Bai W. SIRT1 sumoylation regulates its deacetylase activity and cellular response to genotoxic stress. Nat. Cell. Biol. 9 (2007) 1253-1262
113. Li X., Luo Y., Yu L., Lin Y., Luo D., Zhang H., He Y., Kim Y.O., Kim Y., Tang S., and Min W. SENP1 mediates TNF-induced desumoylation and cytoplasmic translocation of HIPK1 to enhance ASK1-dependent apoptosis. Cell Death Differ. 15 (2008) 739-750
114. Di Bacco A., and Gill G. SUMO-specific proteases and the cell cycle. An essential role for SENP5 in cell proliferation. Cell. Cycle. 5 (2006) 2310-2313
115. Jacques C., Baris O., Prunier-Mirebeau D., Savagner F., Rodien P., Rohmer V., Franc B., Guyetant S., Malthiery Y., and Reynier P. Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J. Clin. Endocrinol. Metab. 90 (2005) 2314-2320
116. Cheng J., Bawa T., Lee P., Gong L., and Yeh E.T. Role of desumoylation in the development of prostate cancer. Neoplasia 8 (2006) 667-676
117. Kim K.I., and Baek S.H. SUMOylation code in cancer development and metastasis. Mol. Cells 22 (2006) 247-253
118. Veltman I.M., Vreede L.A., Cheng J., Looijenga L.H., Janssen B., Schoenmakers E.F., Yeh E.T., and van Kessel A.G. Fusion of the SUMO/Sentrin-specific protease 1 gene SENP1 and the embryonic polarity-related mesoderm development gene MESDC2 in a patient with an infantile teratoma and a constitutional t(12;15)(q13;q25). Hum. Mol. Genet. 14 (2005) 1955-1963
119. Tagawa H., Miura I., Suzuki R., Suzuki H., Hosokawa Y., and Seto M. Molecular cytogenetic analysis of the breakpoint region at 6q21-22 in T-cell lymphoma/leukemia cell lines. Genes Chromosomes Cancer 34 (2002) 175-185
120. Ding X., Sun J., Wang L., Li G., Shen Y., Zhou X., and Chen W. Overexpression of SENP5 in oral squamous cell carcinoma and its association with differentiation. Oncol. Rep. 20 (2008) 1041-1045
121. Panse V.G., Kressler D., Pauli A., Petfalski E., Gnadig M., Tollervey D., and Hurt E. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7 (2006) 1311-1321
122. Lewis A., Felberbaum R., and Hochstrasser M. A nuclear envelope protein linking nuclear pore basket assembly, SUMO protease regulation, and mRNA surveillance. J. Cell Biol. 178 (2007) 813-827
123. Zhao X., Wu C.Y., and Blobel G. Mlp-dependent anchorage and stabilization of a desumoylating enzyme is required to prevent clonal lethality. J. Cell Biol. 167 (2004) 605-611
124. Vethantham V., Rao N., and Manley J.L. Sumoylation modulates the assembly and activity of the pre-mRNA 3′ processing complex. Mol. Cell. Biol. 27 (2007) 8848-8858
125. Haindl M., Harasim T., Eick D., and Muller S. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep. 9 (2008) 273-279
126. Yun C., Wang Y., Mukhopadhyay D., Backlund P., Kolli N., Yergey A., Wilkinson K.D., and Dasso M. Nucleolar protein B23/nucleophosmin regulates the vertebrate SUMO pathway through SENP3 and SENP5 proteases. J. Cell Biol. 183 (2008) 589-595
127. Bachant J., Alcasabas A., Blat Y., Kleckner N., and Elledge S.J. The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9 (2002) 1169-1182
128. Stead K., Aguilar C., Hartman T., Drexel M., Meluh P., and Guacci V. Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J. Cell Biol. 163 (2003) 729-741
129. Bachellier-Bassi S., Gadal O., Bourout G., and Nehrbass U. Cell cycle-dependent kinetochore localization of condensin complex in Saccharomyces cerevisiae. J. Struct. Biol. 162 (2008) 248-259
130. Cheng J., Kang X., Zhang S., and Yeh E.T. SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131 (2007) 584-595
131. Zunino R., Schauss A., Rippstein P., Andrade-Navarro M., and McBride H.M. The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell. Sci. 120 (2007) 1178-1188
132. Benson M.D., Li Q.J., Kieckhafer K., Dudek D., Whorton M.R., Sunahara R.K., Iniguez-Lluhi J.A., and Martens J.R. SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 1805-1810
133. Rajan S., Plant L.D., Rabin M.L., Butler M.H., and Goldstein S.A. Sumoylation silences the plasma membrane leak K+ channel K2P1. Cell 121 (2005) 37-47
134. Nijman S.M., Luna-Vargas M.P., Velds A., Brummelkamp T.R., Dirac A.M., Sixma T.K., and Bernards R. A genomic and functional inventory of deubiquitinating enzymes. Cell 123 (2005) 773-786