SUMOylation and cell signalling

Biotechnology Journal

Volumn 4, Issue 12, 2009, Pages 1740-1752

  Andreou, Artemisia M ^a   Tavernarakis, Nektarios ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Post translational modification; Signalling pathways; Stress; SUMOylation

Indexed keywords

APOPTOSIS; CANCER METASTASIS; CELL SIGNALLING; CELLULAR PROCESS; HUMAN DISEASE; IN-CELL; LOCALISATION; MITOCHONDRIAL ACTIVITY; NEURODEGENERATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN MODIFICATIONS; RAPID RESPONSE; SIGNALLING PATHWAYS; STRESS RESPONSE; SUB-CELLULAR; SUBSTRATE COMPLEXES; SUMOYLATION; TARGET GENES; TARGET PROTEINS; TRANSIENT STATE; UBIQUITINATION;

ACETYLATION; CELL DEATH; COMPLEXATION; PHOSPHORYLATION; TARGETS;

PROTEINS;

CELL PROTEIN; HUNTINGTIN; PARKIN; PROTEIN SENP; PROTEIN SENP 5; PROTEINASE; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO 4 PROTEIN; SUMO PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; BINDING AFFINITY; CELL AGING; CELL COMMUNICATION; CELL DIVISION; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; ENZYME LOCALIZATION; ENZYME MODIFICATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GENE CONTROL; GENE MUTATION; GENE SILENCING; HUMAN; HUNTINGTON CHOREA; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

ACETYLATION; CELL AGING; CELL COMMUNICATION; DISEASE; MITOCHONDRIA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITINATION;

EID: 73849105365     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.200900219     Document Type: Review

References (135)

1. Geiss-Friedlander, R., Melchior, F., Concepts in sumoylation: A decade on. Nat. Rev. Mol. Cell Biol. 2007, 8, 947-956.
2. Bayer, P., Arndt, A., Metzger, S., Mahajan, R. et al., Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 1998, 280, 275-286.
3. Jin, C., Shiyanova, T., Shen, Z., Liao, X., Heteronuclear nuclear magnetic resonance assignments, structure and dynamics of SUMO-1, a human ubiquitin-like protein. Int. J. Biol. Macromol. 2001, 28, 227-234.
4. Johnson, E. S., Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73, 355-382.
5. Johnson, E. S., Schwienhorst, I., Dohmen, R. J., Blobel, G., The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 1997, 16, 5509-5519.
6. Huang, H.W.,Tsoi,S.C., Sun,Y. H., Li,S.S., Identification and characterization of the SMT3 cDNA and gene encoding ubiquitin-like protein from Drosophila melanogaster. Biochem. Mol. Biol. Int. 1998, 46, 775-785.
7. Choudhury, B. K., Li, S. S., Identification and characterization of the SMT3 cDNA and gene from nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 1997, 234, 788-791.
8. Bohren, K. M., Nadkarni,V., Song, J. H., Gabbay, K. H., Owerbach, D., A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 2004, 279, 27233-27238.
9. Chen, A., Mannen, H., Li, S. S., Characterization of mouse ubiquitin-like SMT3A and SMT3B cDNAs and gene/ pseudogenes. Biochem. Mol. Biol. Int. 1998, 46, 1161-1174.
10. Lapenta,V., Chiurazzi, P., van der Spek, P., Pizzuti, A. et al., SMT3A,a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family. Genomics 1997, 40, 362-366.
11. Matunis,M. J., Coutavas, E., Blobel,G.,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. 1996, 135, 1457-1470.
12. 2+-charged talon resin. Protein Expr. Purif. 2007, 54, 289-294.
13. Owerbach,D.,McKay, E. M.,Yeh, E.T.,Gabbay, K. H., Bohren, K. M., A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 2005, 337, 517-520.
14. Tatham,M.H., Jaffray, E.,Vaughan,O.A., Desterro, J.M. et al., Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 2001, 276, 35368-35374.
15. Chupreta, S., Holmstrom, S., Subramanian, L., Iniguez-Lluhi, J. A., A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 2005, 25, 4272-4282.
16. Song, J., Durrin, L. K.,Wilkinson,T. A., Krontiris,T.G., Chen, Y., Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 2004, 101, 14373-14378.
17. Saitoh, H., Hinchey, J., Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 2000, 275, 6252-6258.
18. Hay, R. T., SUMO: A history of modification. Mol. Cell 2005, 18, 1-12.
19. Desterro, J. M., Rodriguez, M. S.,Kemp,G.D.,Hay, R.T., Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 1999, 274, 10618-10624.
20. Okuma, T., Honda, R., Ichikawa, G., Tsumagari, N., Yasuda, H., In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem. Biophys. Res. Commun. 1999, 254, 693-698.
21. Schwienhorst, I., Johnson, E. S., Dohmen, R. J., SUMO conjugation and deconjugation. Mol. Gen. Genet. 2000, 263, 771-786.
22. Johnson, E. S., Gupta, A. A., An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 2001, 106, 735-744.
23. Takahashi,Y.,Toh-e, A., Kikuchi,Y.,A novel factor required for the SUMO1/Smt3 conjugation of yeast septins. Gene 2001, 275, 223-231.
24. Melchior, F., Schergaut, M., Pichler, A., SUMO: Ligases, isopeptidases and nuclear pores. Trends Biochem. Sci. 2003, 28, 612-618.
25. Mikolajczyk, J., Drag, M., Bekes, M., Cao, J. T. et al., Small ubiquitin-related modifier (SUMO)-specific proteases: Profiling the specificities and activities of human SENPs. J. Biol. Chem. 2007, 282, 26217-26224.
26. Azuma,Y.,Tan, S. H., Cavenagh, M. M.,Ainsztein,A. M. et al., Expression and regulation of the mammalian SUMO-1 E1 enzyme. FASEB J. 2001, 15, 1825-1827.
27. Bailey,D.,O'Hare,P., Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 2004, 279, 692-703.
28. Mukhopadhyay, D., Dasso, M., Modification in reverse: The SUMO proteases. Trends Biochem. Sci. 2007, 32, 286-295.
29. Bailey, D., O'Hare, P., Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. J. Gen. Virol. 2002, 83, 2951-2964.
30. Gong, L., Millas, S., Maul, G. G.,Yeh, E.T., Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J. Biol. Chem. 2000, 275, 3355-3359.
31. Hang, J., Dasso, M., Association of the human SUMO-1 protease SENP2 with the nuclear pore. J. Biol. Chem. 2002, 277, 19961-19966.
32. Gong, L.,Yeh, E.T., Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J. Biol. Chem. 2006, 281, 15869-15877.
33. Kim, K. I., Baek, S. H., Jeon,Y. J., Nishimori, S. et al., A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. J. Biol. Chem. 2000, 275, 14102-14106.
34. Mukhopadhyay, D., Ayaydin, F., Kolli, N., Tan, S. H. et al., SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J. Cell Biol. 2006, 174, 939-949.
35. Braschi, E., Zunino, R., McBride, H. M., MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 2009, 10, 748-754.
36. Martin, S., Wilkinson, K. A., Nishimune, A., Henley, J. M., Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction. Nat. Rev. Neurosci. 2007, 8, 948-959.
37. Benson, M.D., Li,Q. J., Kieckhafer, K., Dudek,D. et al., SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc. Natl. Acad. Sci. USA 2007, 104, 1805-1810.
38. Ayaydin, F., Dasso, M., Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 2004, 15, 5208-5218.
39. Minty, A., Dumont, X., Kaghad, M., Caput,D., Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 2000, 275, 36316-36323.
40. Rodriguez, M. S., Dargemont, C., Hay, R. T., SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 2001, 276, 12654-12659.
41. Iniguez-Lluhi, J. A., Pearce, D., A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol. Cell. Biol. 2000, 20, 6040-6050.
42. Poukka, H., Karvonen, U., Yoshikawa, N., Tanaka, H. et al., The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor. J. Cell Sci. 2000, 113, 2991-3001.
43. Yang, S. H., Galanis,A.,Witty, J., Sharrocks,A.D.,An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J. 2006, 25, 5083-5093.
44. Gupta, V., Bei, M., Modification of Msx1 by SUMO-1. Biochem. Biophys. Res. Commun. 2006, 345, 74-77.
45. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P., Dikic, I., Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 2006, 281, 16117-16127.
46. Rosendorff, A., Sakakibara, S., Lu, S., Kieff, E. et al., NXP-2 association with SUMO-2 depends on lysines required for transcriptional repression. Proc. Natl. Acad. Sci. USA 2006, 103, 5308-5313.
47. Hilgarth, R. S., Hong, Y., Park-Sarge, O. K., Sarge, K. D., Insights into the regulation of heat shock transcription factor 1 SUMO-1 modification. Biochem. Biophys. Res. Commun. 2003, 303, 196-200.
48. Hietakangas,V.,Ahlskog, J. K., Jakobsson,A. M., Hellesuo,M. et al., Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 2003, 23, 2953-2968.
49. Hietakangas,V.,Anckar, J., Blomster,H.A., Fujimoto,M. et al., PDSM,a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 2006, 103, 45-50.
50. Girdwood, D., Bumpass, D., Vaughan, O. A., Thain, A. et al., P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 2003, 11, 1043-1054.
51. Yang, S. H., Sharrocks,A. D., SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 2004, 13, 611-617.
52. Gill,G., Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15, 536-541.
53. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S. et al., An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell. Biol. 2007, 27, 2661-2675.
54. Shiio,Y., Eisenman, R.N., Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 2003, 100, 13225-13230.
55. Ghioni, P., D'Alessandra, Y., Mansueto, G., Jaffray, E. et al., The protein stability and transcriptional activity of p63alpha are regulated by SUMO-1 conjugation. Cell Cycle 2005, 4, 183-190.
56. Huang,Y. P.,Wu,G., Guo, Z., Osada, M. et al., Altered sumoylation of p63alpha contributes to the split-hand/foot malformation phenotype. Cell Cycle 2004, 3, 1587-1596.
57. Long, J.,Wang, G., He, D., Liu, F., Repression of Smad4 transcriptional activity by SUMO modification. Biochem. J. 2004, 379, 23-29.
58. de The, H., Lavau, C., Marchio, A., Chomienne, C. et al., The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991, 66, 675-684.
59. Goddard,A.D., Borrow, J.,Freemont,P.S., Solomon, E., Characterization of a zinc finger gene disrupted by the t(15;17) in acute promyelocytic leukemia. Science 1991, 254, 1371-1374.
60. Kakizuka, A., Miller,W. H., Jr., Umesono, K.,Warrell, R. P. Jr. et al., Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 1991, 66, 663-674.
61. Kastner,P.,Perez,A., Lutz,Y., Rochette-Egly,C. et al., [Fusion proteins between PML and alpha-RAR in acute promyelocytic leukemia]. C. R. Seances Soc. Biol. Fil. 1991, 185, 391-401.
62. Lallemand-Breitenbach,V., Jeanne, M., Benhenda, S., Nasr, R. et al., Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 2008, 10, 547-555.
63. Tatham, M. H., Geoffroy, M. C., Shen, L., Plechanovova,A. et al., RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 2008, 10, 538-546.
64. Schmidt, D., Muller, S., Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. USA 2002, 99, 2872-2877.
65. Garcia-Dominguez, M., Reyes, J. C., SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim. Biophys. Acta 2009, 1789, 451-459.
66. Butt, T. R., Edavettal, S. C., Hall, J. P., Mattern, M. R., SUMO fusion technology for difficult-to-express proteins. Protein Expr. Purif. 2005, 43, 1-9.
67. Malakhov,M.P., Mattern,M. R.,Malakhova,O.A., Drinker,M. et al., SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J. Struct. Funct. Genomics 2004, 5, 75-86.
68. Marblestone, J.G., Edavettal, S.C., Lim,Y., Lim,P. et al., Comparison of SUMO fusion technology with traditional gene fusion systems: Enhanced expression and solubility with SUMO. Protein Sci. 2006, 15, 182-189.
69. Zuo, X., Li, S., Hall, J., Mattern, M. R. et al., Enhanced expression and purification of membrane proteins by SUMO fusion in Escherichia coli. J. Struct. Funct. Genomics 2005, 6, 103-111.
70. Lee, C.D., Sun, H. C., Hu, S. M., Chiu, C. F. et al.,An improved SUMO fusion protein system for effective production of native proteins. Protein Sci. 2008, 17, 1241-1248.
71. Liu, L., Spurrier, J., Butt,T. R., Strickler, J. E., Enhanced protein expression in the baculovirus/insect cell system using engineered SUMO fusions. Protein Expr. Purif. 2008, 62, 21-28.
72. Peroutka, R. J., Elshourbagy, N., Piech, T., Butt, T. R., Enhanced protein expression in mammalian cells using engineered SUMO fusions: Secreted phospholipase A2. Protein Sci. 2008, 17, 1586-1595.
73. Leavenworth, J.W., Ma, X.,Mo,Y.Y.,Pauza, M. E., SUMO conjugation contributes to immune deviation in nonobese diabetic mice by suppressing c-Maf transactivation of IL-4. J. Immunol. 2009, 183, 1110-1119.
74. Wang, C.Y., She, J. X., SUMO4 and its role in type 1 diabetes pathogenesis. Diabetes Metab. Res. Rev. 2008, 24, 93-102.
75. Woo, C. H., Shishido, T., McClain, C., Lim, J. H. et al., Extracellular signal-regulated kinase 5 SUMOylation antagonizes shear stress-induced antiinflammatory response and endothelial nitric oxide synthase expression in endothelial cells. Circ. Res. 2008, 102, 538-545.
76. Dorval,V., Fraser, P. E., SUMO on the road to neurodegeneration. Biochim. Biophys. Acta 2007, 1773, 694-706.
77. Ehninger, A., Mziaut, H., Solimena, M., Emerging role of SUMO in pancreatic beta-cells. Horm. Metab. Res. 2007, 39, 658-664.
78. Kim, K. I., Baek, S. H., Small ubiquitin-like modifiers in cellular malignancy and metastasis. Int. Rev. Cell Mol. Biol. 2009, 273, 265-311.
79. Li, M., Guo, D., Isales, C. M., Eizirik, D. L. et al., SUMO wrestling with type 1 diabetes. J. Mol. Med. 2005, 83, 504-513.
80. Dimmer, K. S., Scorrano, L., (De)constructing mitochondria: What for? Physiology (Bethesda) 2006, 21, 233-241.
81. Bossy-Wetzel, E., Barsoum, M. J., Godzik, A., Schwarzenbacher, R., Lipton, S. A., Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr. Opin. Cell Biol. 2003, 15, 706-716.
82. Hales, K. G., Fuller, M. T., Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 1997, 90, 121-129.
83. Desagher, S., Martinou, J. C., Mitochondria as the central control point of apoptosis. Trends Cell Biol. 2000, 10, 369-377.
84. Harder, Z., Zunino, R., McBride, H., Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 2004, 14, 340-345.
85. Figueroa-Romero, C., Iniguez-Lluh, J. A., Stadler, J., Chang, C. R. et al., SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. FASEB J. 2009.
86. Zunino, R., Schauss, A., Rippstein, P., Andrade-Navarro, M., McBride, H. M., The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell Sci. 2007, 120, 1178-1188.
87. Neuspiel, M., Schauss, A. C., Braschi, E., Zunino, R. et al., Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18, 102-108.
88. Bossis, G., Melchior, F., Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 2006, 21, 349-357.
89. Boggio, R., Chiocca, S., Viruses and sumoylation: Recent highlights. Curr. Opin. Microbiol. 2006, 9, 430-436.
90. Kurepa, J.,Walker, J. M., Smalle, J., Gosink, M. M. et al., The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis.Accumulation of SUMO1 and -2 conjugates is increased by stress. J. Biol. Chem. 2003, 278, 6862-6872.
91. Sramko, M., Markus, J., Kabat, J.,Wolff, L., Bies, J., Stress-induced inactivation of the c-Myb transcription factor through conjugation of SUMO-2/3 proteins. J. Biol. Chem. 2006, 281, 40065-40075.
92. Zhou,W.,Ryan, J. J., Zhou, H., Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 2004, 279, 32262-32268.
93. Hong,Y., Rogers, R., Matunis,M. J.,Mayhew,C.N. et al., Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J. Biol. Chem. 2001, 276, 40263-40267.
94. Manza, L. L., Codreanu, S. G., Stamer, S. L., Smith, D. L. et al., Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem. Res.Toxicol. 2004, 17, 1706-1715.
95. Golebiowski, F., Matic, I.,Tatham, M. H., Cole, C. et al., System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2009, 2, ra24.
96. Comerford, K. M., Leonard, M. O., Karhausen, J., Carey, R. et al., Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc. Natl. Acad. Sci. USA 2003, 100, 986-991.
97. Bossis, G., Melchior, F., SUMO: Regulating the regulator. Cell Div. 2006, 1, 13.
98. Li,T., Santockyte, R., Shen, R.F.,Teckle, E. et al., Expression of SUMO-2/3 induced senescence through p53- and pRB-mediated pathways. J. Biol. Chem. 2006, 281, 36221-36227.
99. Finkel,T., Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 2003, 15, 247-254.
100. Boggio, R., Colombo, R.,Hay, R.T., Draetta,G. F., Chiocca, S., A mechanism for inhibiting the SUMO pathway. Mol. Cell 2004, 16, 549-561.
101. Muller, S., Dejean,A.,Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 1999, 73, 5137-5143.
102. Li, S. J., Hochstrasser, M.,A new protease required for cell-cycle progression in yeast. Nature 1999, 398, 246-251.
103. Bischof, O., and DEjean, A., SUMO is growing senescent. Cell Cycle 2007, 6, 677-681.
104. Akar, C. A., Feinstein, D. L., Modulation of inducible nitric oxide synthase expression by sumoylation. J. Neuroinflammation 2009, 6, 12.
105. Li,T., Evdokimov, E., Shen, R. F., Chao, C. C. et al., Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins:A proteomic analysis. Proc. Natl. Acad. Sci. USA 2004, 101, 8551-8556.
106. Campisi, J., Senescent cells, tumor supression and organismal aging: Good citizens, bad neighbors. Cell 2005, 120, 513-522.
107. Okada, H., Mak, T. W., Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer 2004, 4, 592-603.
108. Ben-Porath, I., Weinberg, R.A., When cells get stressed: An integrative view of cellular senescence. J. Clin. Invest. 2004, 113, 8-13.
109. Hickman, E. S., Moroni, M.C., Helin, K.,The role of p53 and pRB in apoptosis and cancer. Curr. Opin. Genet. Dev. 2002, 12, 60-66.
110. Gostissa, M., Hengstermann, A., Fogal, V., Sandy, P. et al., Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 1999, 18, 6462-6471.
111. Ledl,A., Schmidt,D., and Muller,S.,Viral oncoproteins E1A and E7 and cellular LxCxE proeins repress SUMO modification of the retinoblastoma tumor supressor. Oncogene 2005, 24, 3810-3818.
112. Muller, S., Berger, M., Lehembre, F., Seeler, J. S. et al., c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 2000, 275, 13321-13329.
113. Rodriguez, M., Desterro, J.M., Lain, S., Midgley, C.A. et al., SUMO-1 modification activates the transcriptional response of p53. EMBO J. 1999, 18, 6455-6461.
114. Bischof, O., Schwamborn, K., Martin, N.,Werner, A. et al., The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol. Cell 2006, 22, 783-794.
115. Sugrue, M. M., Shin, D.Y., Lee, S.W., Aaronson, S.A.,Wildtype p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc. Natl. Acad. Sci. USA 1997, 97, 9648-9653.
116. Schmidt,D., Müller, S., PIAS/SUMO: New partners in transcriptional regulation. Cell. Mol. Life Sci. 2003, 60, 2561-2574.
117. Uchimura,Y., Ichimura,T.,Uwada, J.,Tachibana,T. et al., Involvement of SUMO modification in MBD1- and MCAF1-mediated heterochromatin formation. J. Biol. Chem. 2006, 281, 23180-23190.
118. Nathan,D., Ingvarsdottir, K., Sterner,D. E., Bylebyl,G. R. et al., Histone sumoylation is a negative regulator in Saccharomyces serevisiae and shown dynamic interplay with positive-acting histone modifications. Genes Dev. 2006, 20, 966-976.
119. Yates,K. E.,Korbel,G. A., Shtutman, M., Roninson, I.B.,Di-Maio, D., Repression of the SUMO-specific protease Senp1 induces p53-dependent premature senescence in normal human fibroblasts. Aging Cell 2008, 7, 609-621.
120. Yang,W., Sheng, H.,Warner, D. S., Paschen,W., Transient global cerebral ischemia induces a massive increase in protein sumoylation. J. Cereb. Blood Flow Metab. 2008, 28, 269-279.
121. Subramaniam, S., Sixt, K. M., Barrow, R., Snyder, S. H., Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 2009, 324, 1327-1330.
122. Falk, J. D.,Vargiu, P., Foye, P. E., Usui, H. et al., Rhes: A striatal-specific Ras homolog related to Dexras1. J. Neurosci. Res. 1999, 57, 782-788.
123. Mukherjee, S., Thomas, M., Dadgar, N., Lieberman, A. P., Iniguez-Lluhi, J. A., Small ubiquitin-like modifier (SUMO) modification of the androgen receptor attenuates polyglutamine-mediated aggregation. J. Biol. Chem. 2009, 284, 21296-21306.
124. Um, J.W., Chung, K. C., Functional modulation of parkin through physical interaction with SUMO-1. J. Neurosci. Res. 2006, 84, 1543-1554.
125. Wu, F., Mo, Y., Ubiquitin-like protein modifications in prostate and breast cancer. Front. Biosci. 2007, 12, 700-711.
126. Baek, S. H., Ohgi, K. A., Rose, D.W., Koo, E. H. et al., Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 2002, 110, 55-67.
127. Kim, J. H., Choi, H. J., Kim, B., Kim, M. H. et al., Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat. Cell Biol. 2006, 8, 631-639.
128. Andreou, A. M., Pauws, E., Jones, M. C., Singh, M. K. et al., TBX22 missense mutations found in patients with X-linked cleft palate affect DNA binding, sumoylation, and transcriptional repression. Am. J. Hum. Genet. 2007, 81, 700-712.
129. Dobreva, G., Dambacher, J., Grosschedl, R., SUMO modification of a novel MAR-binding protein, SATB2, modulates immunoglobulin mu gene expression. Genes Dev. 2003, 17, 3048-3061.
130. Lee,M. H., Lee, S.W., Lee, E. J., Choi, S. J. et al., SUMO-specific protease SUSP4 positively regulates p53 by promoting Mdm2 self-ubiquitination. Nat. Cell Biol. 2006, 8, 1424-1431.
131. Rogers, R. S., Horvath, C. M., Matunis,M. J., SUMO modification of STAT1 and its role in PIAS-mediated inhibition of gene activation. J. Biol. Chem. 2003, 278, 30091-30097.
132. Sachdev, S., Bruhn, L., Sieber, H., Pichler,A. et al., PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 2001, 15, 3088-3103.
133. Lee, H., Quinn, J.C., Prasanth, K.V., Swiss,V.A. et al., PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev. 2006, 20, 784-794.
134. Mahajan, R., Delphin, C., Guan,T., Gerace, L., Melchior, F., A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997, 88, 97-107.
135. Hardeland,U., Steinacher, R., Jiricny, J., Schar, P., Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002, 21, 1456-1464.