Sumoylation regulates diverse biological processes

Cellular and Molecular Life Sciences

Volumn 64, Issue 23, 2007, Pages 3017-3033

  Zhao, J ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Desumoylation; Gene expression; Genomic and chromosomal integrity; Loss of function of SUMO pathway; Signal transduction; SUMO; SUMO associated disease; Sumoylation cycle

Indexed keywords

DESUMOYLASE; ENZYME; GLYCOPROTEIN E1; GLYCOPROTEIN E2; NUCLEAR PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; SUMO PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ACETYLATION; CELL FUNCTION; CELL MEMBRANE; DEACETYLATION; DEGENERATIVE DISEASE; DEVELOPMENTAL DISORDER; DIABETES MELLITUS; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; HUMAN; NEOPLASM; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; PROTEIN PHOSPHORYLATION; REVIEW; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION; VIRUS INFECTION;

EID: 38549181148     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7137-4     Document Type: Review

References (168)

1. Saitoh, H., Pu, R. T. and Dasso, M. (1997)SUMO-1: wrestling with a new ubiquitin-related modifier. Trends Biochem. Sci. 22, 374-376.
2. Chen, A., Mannen, H. and Li, S. S. (1998) Characterization of mouse ubiquitin-like SMT3A and SMT3B cDNAs and gene/pseudogenes. Biochem. Mol. Biol. Int. 46, 1161-1174.
3. Mannen, H., Tseng, H. M., Cho, C. L. and Li, S. S. (1996) Cloning and expression of human homolog HSMT3 to yeast SMT3 suppressor of MIF2 mutations in a centromere protein gene. Biochem. Biophys. Res. Commun. 222, 178-180.
4. 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.
5. Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K. and Chen, D. J. (1996) UBL1, a human ubiquitinlike protein associating with human RAD51/RAD52 proteins. Genomics 36, 271-279.
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.
7. 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.
8. 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, 1457-70.
9. 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.
10. 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, 27233-27738.
11. 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. (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat. Genet. 36, 837-841.
12. Jin, J., Li, X., Gygi, S. P. and Harper, J.W. (2007) Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447, 1135-1138.
13. Bailey, D. and OHare, P. (2002) Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. J. Gen. Virol. 83, 2951-2964.
14. 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.
15. Hang, J. and Dasso, M. (2002) Association of the human SUMO-1 protease SENP2 with the nuclear pore. J. Biol. Chem. 277, 19961-1996.
16. Kagey, M. H., Melhuish, T. A. and Wotton, D. (2003) The polycomb protein Pc2 is a SUMO E3. Cell 113, 127-137.
17. 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. (2000)Anew SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. J. Biol. Chem. 275, 14102-14106.
18. 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.
19. Seeler, J. S. and Dejean, A. (2001) SUMO: of branched proteins and nuclear bodies. Oncogene 20, 7243-7249.
20. 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.
21. Dohmen, R. J., Stappen, R., McGrath, J. P., Forrova, H., Kolarov, J., Goffeau, A. and Varshavsky, A. (1995) An essential yeast gene encoding a homolog of ubiquitin-activating enzyme. J. Biol. Chem. 270, 18099-18109.
22. Johnson, E. S., Schwienhorst, I., Dohmen, R. J. and Blobel, G. (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16, 5509-5519.
23. Shayeghi, M., Doe, C. L., Tavassoli, M. and Watts, F. Z. (1997) Characterisation of Schizosaccharomyces pombe rad31, a UBA-related gene required for DNA damage tolerance. Nucleic Acids Res. 25, 1162-1169.
24. Jones, D., Crowe, E., Stevens, T. and Candido, E. (2002) Functional and phynogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol. 3(1): Research 0002.
25. 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.
26. 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.
27. Hochstrasser, M. (2001) SP-RING for SUMO: new functions bloom for a ubiquitin-like protein. Cell 107, 5-8.
28. Hari, K. L., Cook, K. R. and Karpen, G. H. (2001) The Drosophila Su(var)2 - 10 locus regulates chromosome structure and function and encodes a member of the PIAS protein family. Genes Dev. 15, 1334-1348.
29. Roth, W., Sustmann, C., Kieslinger, M., Gilmozzi, A., Irmer, D., Kremmer, E., Turck, C. and Grosschedl, R. (2004) PIASy-deficient mice display modest defects in IFN and Wnt signaling. J. Immunol. 173, 6189-6199.
30. Santti, H., Mikkonen, L., Anand, A., Hirvonen-Santti, S., Toppari, J., Panhuysen, M., Vauti, F., Perera, M., Corte, G., Wurst, W., Janne, O. A. and Palvimo, J. J. (2005) Disruption of the murine PIASx gene results in reduced testis weight. J. Mol. Endocrinol. 34, 645-654.
31. 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.
32. McDonald, W. H., Pavlova, Y., Yates, J. R., 3rd and Boddy, M. N. (2003) Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem. 278, 45460-45467.
33. 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. USA 102, 4777-4782.
34. Xhemalce, B., Seeler, J. S., Thon, G., Dejean, A. and Arcangioli, B. (2004) Role of the fission yeast SUMO E3 ligase Pli1p in centromere and telomere maintenance. EMBO J. 23, 3844-3853.
35. Xhemalce, B., Riising, E. M., Baumann, P., Dejean, A., Arcangioli, B. and Seeler, J. S. (2007) Role of SUMO in the dynamics of telomere maintenance in fission yeast. Proc. Natl. Acad. Sci. USA 104, 893-898.
36. Johnson, E. S. and Gupta, A. A. (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106, 735-744.
37. Chen, X. L., Reindle, A. and Johnson, E. S. (2005) Misregulation of 2 micronm circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25, 4311-4320.
38. Takahashi, Y., Yong-Gonzalez, V., Kikuchi, Y. and Strunnikov, A. (2006) SIZ1/SIZ2 control of chromosome transmission fidelity is mediated by the sumoylation of topoisomerase II. Genetics 172, 783-794.
39. Reindle, A., Belichenko, I., Bylebyl, G. R., Chen, X. L., Gandhi, N. and Johnson, E. S. (2006) Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J. Cell. Sci. 119, 4749-4757.
40. Takahashi, Y., Toh, E. A. and Kikuchi, Y. (2003) Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. J. Biochem. (Tokyo) 133, 415-422.
41. Huang, R. Y., Kowalski, D., Minderman, H., Gandhi, N. and Johnson, E. S. (2007) Small ubiquitin-related modifier pathway is a major determinant of doxorubicin cytotoxicity in Saccharomyces cerevisiae. Cancer Res. 67, 765-772.
42. Cheng, J., Bawa, T., Lee, P., Gong, L. and Yeh, E. T. (2006) Role of desumoylation in the development of prostate cancer. Neoplasia 8, 667-676.
43. Yamaguchi, T., Sharma, P., Athanasiou, M., Kumar, A., Yamada, S. and Kuehn, M. R. (2005) Mutation of SENP1/SuPr-2 reveals an essential role for desumoylation in mouse development. Mol. Cell. Biol. 25, 5171-5182.
44. Veltman, I. M., Vreede, L. A., Cheng, J., Looijenga, L. H., Janssen, B., Schoenmakers, E. F., Yeh, E. T. and van Kessel, A. G. (2005) 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, 1955-63.
45. Tagawa, H., Miura, I., Suzuki, R., Suzuki, H., Hosokawa, Y. and Seto, M. (2002) Molecular cytogenetic analysis of the breakpoint region at 6q21-22 in T-cell lymphoma/leukemia cell lines. Genes Chromosomes Cancer 34, 175-185.
46. 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. Proteom. 5, 2298-2310.
47. 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.
48. Verger, A., Perdomo, J. and Crossley, M. (2003) Modification with SUMO: a role in transcriptional regulation. EMBO Rep. 4, 137-142.
49. Yang, X. J. and Gregoire, S. (2006) A recurrent phosphosumoyl switch in transcriptional repression and beyond. Mol. Cell 23, 779-786.
50. Gill, G. (2005) Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 15, 536-541.
51. Hay, R. T. (2006) Role of ubiquitin-like proteins in transcriptional regulation. Ernst Schering Res. Found. Workshop, 173-192.
52. Schmidt, D. and Muller, S. (2003) PIAS/SUMO: new partners in transcriptional regulation. Cell. Mol. Life Sci. 60, 2561-2574.
53. Sharrocks, A. D. (2006) PIAS proteins and transcriptional regulation-more than just SUMO E3 ligases? Genes Dev. 20, 754-758.
54. Maul, G. G., Negorev, D., Bell, P. and Ishov, A. M. (2000) Properties and assembly mechanisms of ND10, PML bodies, or PODs. J. Struct. Biol. 129, 278-287.
55. Melnick, A. and Licht, J. D. (1999) Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 93, 3167-3215.
56. Ishov, A. M., Sotnikov, A. G., Negorev, D., Vladimirova, O. V., Neff, N., Kamitani, T., Yeh, E. T., Strauss, J. F., 3rd and Maul, G. G. (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell. Biol. 147, 221-234.
57. Zhong, S., Muller, S., Ronchetti, S., Freemont, P. S., Dejean, A. and Pandolfi, P. P. (2000) Role of SUMO-1-modified PML in nuclear body formation. Blood 95, 2748-2752.
58. Boggio, R., Colombo, R., Hay, R. T., Draetta, G. F. and Chiocca, S. (2004) A mechanism for inhibiting the SUMO pathway. Mol. Cell 16, 549-561.
59. Potts, P. R. and Yu, H. (2005) Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25, 7021-7032.
60. Ulrich, H. D., Vogel, S. and Davies, A. A. (2005) SUMO keeps a check on recombination during DNA replication. Cell Cycle 4, 1699-1702.
61. Watts, F. Z. (2006) Sumoylation of PCNA: wrestling with recombination at stalled replication forks. DNA Repair (Amst.) 5, 399-403.
62. Papouli, E., Chen, S., Davies, A. A., Huttner, D., Krejci, L., Sung, P. and Ulrich, H. D. (2005) Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell. 19, 123-133.
63. Pfander, B., Moldovan, G. L., Sacher, M., Hoege, C. and Jentsch, S. (2005) SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436, 428-433.
64. 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.
65. 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.
66. Steinacher, R. and Schar, P. (2005) Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15, 616-623.
67. 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.
68. Apionishev, S., Malhotra, D., Raghavachari, S., Tanda, S. and Rasooly, R. S. (2001) The Drosophila UBC9 homologue lesswright mediates the disjunction of homologues in meiosis I. Genes Cells 6, 215-224.
69. Strunnikov, A. V., Aravind, L. and Koonin, E. V. (2001) Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158, 95-107.
70. 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.
71. Chung, T. L., Hsiao, H. H., Yeh, Y. Y., Shia, H. L., Chen, Y. L., Liang, P. H., Wang, A. H., Khoo, K. H. and Shoei-Lung Li, S. (2004) In vitro modification of human centromere protein CENP-C fragments by small ubiquitin-like modifier (SUMO) protein: definitive identification of the modification sites by tandem mass spectrometry analysis of the isopeptides. J. Biol. Chem. 279, 39653-39662.
72. Everett, R. D., Earnshaw, W. C., Findlay, J. and Lomonte, P. (1999) Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18, 1526-1538.
73. Bachant, J., Alcasabas, A., Blat, Y., Kleckner, N. and Elledge, S. J. (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9, 1169-1182.
74. Stead, K., Aguilar, C., Hartman, T., Drexel, M., Meluh, P. and Guacci, V. (2003) Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J. Cell. Biol. 163, 729-741.
75. Joseph, J., Liu, S. T., Jablonski, S. A., Yen, T. J. and Dasso, M. (2004) The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr. Biol. 14, 611-617.
76. Joseph, J., Tan, S. H., Karpova, T. S., McNally, J. G. and Dasso, M. (2002) SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J. Cell. Biol. 156, 595-602.
77. Desterro, J. M., Keegan, L. P., Jaffray, E., Hay, R. T., O'Connell, M. A. and Carmo-Fonseca, M. (2005) SUMO-1 modification alters ADAR1 editing activity. Mol. Biol. Cell 16, 5115-5126.
78. Panse, V. G., Kressler, D., Pauli, A., Petfalski, E., Gnadig, M., Tollervey, D. and Hurt, E. (2006) Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7, 1311-1321.
79. 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. (2006) SUMOspecific protease SUSP4 positively regulates p53 by promoting Mdm2 self-ubiquitination. Nat. Cell Biol. 8, 1424-1431.
80. Mahajan, R., Gerace, L. and Melchior, F. (1998) Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell. Biol. 140, 259-270.
81. Matunis, M. J., Wu, J. and Blobel, G. (1998) SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell. Biol. 140, 499-509.
82. 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.
83. Dadke, S., Cotteret, S., Yip, S. C., Jaffer, Z. M., Haj, F., Ivanov, A., Rauscher, F., 3rd, 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.
84. + channel K2P1. Cell 121, 37-47.
85. Desterro, J. M., Rodriguez, M. S. and Hay, R. T. (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2, 233-239.
86. Klenk, C., Humrich, J., Quitterer, U. and Lohse, M. J. (2006) SUMO-1 controls the protein stability and the biological function of phosducin. J. Biol. Chem. 281, 8357-8364.
87. Harder, Z., Zunino, R. and McBride, H. (2004) Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14, 340-345.
88. Giorgino, F., de Robertis, O., Laviola, L., Montrone, C., Perrini, S., McCowen, K. C. and Smith, R. J. (2000) The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells. Proc. Natl. Acad. Sci. USA 97, 1125-1130.
89. Sobko, A., Ma, H. and Firtel, R. A. (2002) Regulated SUMOylation and ubiquitination of DdMEK1 is required for proper chemotaxis. Dev. Cell 2, 745-756.
90. Fei, E., Jia, N., Yan, M., Ying, Z., Sun, Q., Wang, H., Zhang, T., Ma, X., Ding, H., Yao, X., Shi, Y. and Wang, G. (2006) SUMO-1 modification increases human SOD1 stability and aggregation. Biochem. Biophys. Res. Commun. 347, 406-412.
91. Lalioti, V. S., Vergarajauregui, S., Pulido, D. and Sandoval, I. V. (2002)The insulin-sensitive glucose transporter, GLUT4, interacts physically with Daxx: two proteins with capacity to bind Ubc9 and conjugated to SUMO1. J. Biol. Chem. 277, 19783-19791.
92. Cheng, T. S., Chang, L. K., Howng, S. L., Lu, P. J., Lee, C. I. and Hong, Y. R. (2006) SUMO-1modification of centrosomal protein hNinein promotes hNinein nuclear localization. Life Sci. 78, 1114-1120.
93. Hayashi, N., Shirakura, H., Uehara, T. and Nomura, Y. (2006) Relationship between SUMO-1 modification of caspase-7 and its nuclear localization in human neuronal cells. Neurosci. Lett. 397, 5-9.
94. Boggio, R. and Chiocca, S. (2005) Gam1 and the SUMO pathway. Cell Cycle 4, 533-535.
95. 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.
96. Boggio, R. and Chiocca, S. (2006) Viruses and sumoylation: recent highlights. Curr. Opin. Microbiol. 9, 430-436.
97. Lin, X., Liang, M., Liang, Y. Y., Brunicardi, F. C. and Feng, X. H. (2003) SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J. Biol. Chem. 278, 31043-31048.
98. 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. (2004) SUMO modification of Huntingtin and Huntington's disease pathology. Science 304, 100-104.
99. Sacher, M., Pfander, B., Hoege, C. and Jentsch, S. (2006) Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8, 1284-1290.
100. Benanti, J. A., Williams, D. K., Robinson, K. L., Ozer, H. L. and Galloway, D. A. (2002) Induction of extracellular matrix-remodeling genes by the senescence-associated protein APA-1. Mol. Cell. Biol. 22, 7385-7397.
101. Bae, S. H., Jeong, J. W., Park, J. A., Kim, S. H., Bae, M. K., Choi, S. J. and Kim, K. W. (2004) Sumoylation increases HIF-1alpha stability and its transcriptional activity. Biochem. Biophys. Res. Commun. 324, 394-400.
102. Floyd, Z. E. and Stephens, J. M. (2004) Control of peroxisome proliferator-activated receptor gamma2 stability and activity by SUMOylation. Obes. Res. 12, 921-928.
103. Dorval, V. and Fraser, P. E. (2006) Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. J. Biol. Chem. 281, 9919-9924.
104. 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.
105. Gutierrez, G. J. and Ronai, Z. (2006) Ubiquitin and SUMO systems in the regulation of mitotic checkpoints. Trends Biochem. Sci. 31, 324-332.
106. Kirkin, V. and Dikic, I. (2007) Role of ubiquitin- and Ubl-binding proteins in cell signaling. Curr. Opin. Cell Biol. 19, 199-205.
107. 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.
108. Zhao, X., Sternsdorf, T., Bolger, T. A., Evans, R. M. and Yao, T. P. (2005) Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol. Cell. Biol. 25, 8456-8464.
109. Zheng, G. and Yang, Y. C. (2005) Sumoylation and acetylation play opposite roles in the transactivation of PLAG1 and PLAGL2. J. Biol. Chem. 280, 40773-40781.
110. Wang, J. M., Ko, C. Y., Chen, L. C., Wang, W. L. and Chang, W. C. (2006) Functional role of NF-IL6beta and its sumoylation and acetylation modifications in promoter activation of cyclooxygenase 2 gene. Nucleic Acids Res. 34, 217-231.
111. Yang, S. H. and Sharrocks, A. D. (2004) SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell. 13, 611-617.
112. Nathan, D., Ingvarsdottir, K., Sterner, D. E., Bylebyl, G. R., Dokmanovic, M., Dorsey, J. A., Whelan, K. A., Krsmanovic, M., Lane, W. S., Meluh, P. B., Johnson, E. S. and Berger, S. L. (2006) Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev 20, 966-976.
113. Shiio, Y. and Eisenman, R. N. (2003) Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 100, 13225-13230.
114. Nathan, D., Sterner, D. E. and Berger, S. L. (2003) Histone modifications: now summoning sumoylation. Proc. Natl. Acad. Sci. USA 100, 13118-13120.
115. Wu, H., Sun, L., Zhang, Y., Chen, Y., Shi, B., Li, R., Wang, Y., Liang, J., Fan, D., Wu, G., Wang, D., Li, S. and Shang, Y. (2006) Coordinated regulation of AIB1 transcriptional activity by sumoylation and phosphorylation. J. Biol. Chem. 281, 21848-21856.
116. 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.
117. Kang, J., Gocke, C. B. and Yu, H. (2006) Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity. BMC Biochem. 7, 5.
118. 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.
119. Yamashita, D., Yamaguchi, T., Shimizu, M., Nakata, N., Hirose, F. and Osumi, T. (2004) The transactivating function of peroxisome proliferator- activated receptor gamma is negatively regulated by SUMO conjugation in the aminoterminal domain. Genes Cells 9, 1017-1029.
120. 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. USA 103, 45-50.
121. 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.
122. 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.
123. Minty, A., Dumont, X., Kaghad, M. and Caput, D. (2000) 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. 275, 36316-36323.
124. 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. USA 101, 14373-14378.
125. Jakobs, A., Koehnke, J., Himstedt, F., Funk, M., Korn, B., Gaestel, M. and Niedenthal, R. (2007) Ubc9 fusion-directed SUMOylation (UFDS): a method to analyze function of protein SUMOylation. Nat. Methods 4, 245-250.
126. Weis, K. (2003) Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112, 441-451.
127. Kadoya, T., Yamamoto, H., Suzuki, T., Yukita, A., Fukui, A., Michiue, T., Asahara, T., Tanaka, K., Asashima, M. and Kikuchi, A. (2002) Desumoylation activity of Axam, a novel Axin-binding protein, is involved in downregulation of beta-catenin. Mol. Cell. Biol. 22, 3803-3819.
128. Pichler, A. and Melchior, F. (2002) Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 3, 381-387.
129. 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.
130. Stade, K., Vogel, F., Schwienhorst, I., Meusser, B., Volkwein, C., Nentwig, B., Dohmen, R. J. and Sommer, T. (2002)A lack of SUMO conjugation affects cNLS-dependent nuclear protein import in yeast. J. Biol. Chem. 277, 49554-49561.
131. Duprez, E., Saurin, A. J., Desterro, J. M., Lallemand-Breitenbach, V., Howe, K., Boddy, M. N., Solomon, E., de The, H., Hay, R. T. and Freemont, P. S. (1999) SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J. Cell Sci. 112, 381-393.
132. Kamitani, T., Kito, K., Nguyen, H. P., Wada, H., Fukuda-Kamitani, T. and Yeh, E. T. (1998) Identification of three major sentrinization sites in PML. J. Biol. Chem. 273, 26675-26682.
133. Sternsdorf, T., Jensen, K., Reich, B. and Will, H. (1999) The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization, and modification by small ubiquitin-like modifiers. J. Biol. Chem. 274, 12555-12566.
134. Besnault-Mascard, L., Leprince, C., Auffredou, M. T., Meunier, B., Bourgeade, M. F., Camonis, J., Lorenzo, H. K. and Vazquez, A. (2005) Caspase-8 sumoylation is associated with nuclear localization. Oncogene 24, 3268-3273.
135. Shirakura, H., Hayashi, N., Ogino, S., Tsuruma, K., Uehara, T. and Nomura, Y. (2005) Caspase recruitment domain of procaspase-2 could be a target for SUMO-1 modification through Ubc9. Biochem. Biophys. Res. Commun. 331, 1007-1015.
136. Lin, X., Sun, B., Liang, M., Liang, Y. Y., Gast, A., Hildebrand, J., Brunicardi, F. C., Melchior, F. and Feng, X. H. (2003) Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol. Cell 11, 1389-1396.
137. Orlando, V. (2003) Polycomb, epigenomes, and control of cell identity. Cell 112, 599-606.
138. Muller, S., Ledl, A. and Schmidt, D. (2004) SUMO: a regulator of gene expression and genome integrity. Oncogene 23, 1998-2008.
139. Watts, F. Z. (2007) The role of SUMO in chromosome segregation. Chromosoma 116, 15-20.
140. Wood, L. D., Irvin, B. J., Nucifora, G., Luce, K. S. and Hiebert, S. W. (2003) Small ubiquitin-like modifier conjugation regulates nuclear export of TEL, a putative tumor suppressor. Proc. Natl. Acad. Sci. USA 100, 3257-3262.
141. James, D. E., Brown, R., Navarro, J. and Pilch, P. F. (1988) Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 333, 183-185.
142. Lee, J. S. and Thorgeirsson, S. S. (2004) Genome-scale profiling of gene expression in hepatocellular carcinoma: classification, survival prediction, and identification of therapeutic targets. Gastroenterology 127, S51-S55.
143. McDoniels-Silvers, A. L., Nimri, C. F., Stoner, G. D., Lubet, R. A. and You, M. (2002) Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clin. Cancer Res. 8, 1127-1138.
144. Mo, Y. Y., Yu, Y., Theodosiou, E., Rachel Ee, P. L. and Beck, W. T. (2005) A role for Ubc9 in tumorigenesis. Oncogene 24, 2677-2683.
145. Wang, L. and Banerjee, S. (2004) Differential PIAS3 expression in human malignancy. Oncol. Rep. 11, 1319-1324.
146. Jacques, C., Baris, O., Prunier-Mirebeau, D., Savagner, F., Rodien, P., Rohmer, V., Franc, B., Guyetant, S., Malthiery, Y. and 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.
147. Deyrieux, A. F., Rosas-Acosta, G., Ozbun, M. A. and Wilson, V. G. (2007) Sumoylation dynamics during keratinocyte differentiation. J. Cell. Sci. 120, 125-136.
148. Bischof, O., Schwamborn, K., Martin, N., Werner, A., Sustmann, C., Grosschedl, R. and Dejean, A. (2006) The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol. Cell 22, 783-794.
149. 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. (2006) Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat. Cell Biol.8, 631-639.
150. Wei, H., Wang, X., Gan, B., Urvalek, A. M., Melkoumian, Z. K., Guan, J. L. and Zhao, J. (2006) Sumoylation delimits KLF8 transcriptional activity associated with the cell cycle regulation. J. Biol. Chem. 281, 16664-16671.
151. Alarcon-Vargas, D. and Ronai, Z. (2002) SUMO in cancer - wrestlers wanted. Cancer Biol. Ther. 1, 237-242.
152. Kikuchi, A., Kishida, S. and Yamamoto, H. (2006) Regulation of Wnt signaling by protein-protein interaction and posttranslational modifications. Exp. Mol. Med. 38, 1-10.
153. Kim, K. I. and Baek, S. H. (2006) SUMOylation code in cancer development and metastasis. Mol. Cells 22, 247-253.
154. Kracklauer, M. P. and Schmidt, C. (2003) At the crossroads of SUMO and NF-kappaB. Mol. Cancer 2, 39.
155. Seeler, J. S., Bischof, O., Nacerddine, K. and Dejean, A. (2007) SUMO, the three Rs and cancer. Curr. Top. Microbiol. Immunol. 313, 49-71.
156. Watson, I. R. and Irwin, M. S. (2006) Ubiquitin and ubiquitinlike modifications of the p53 family. Neoplasia 8, 655-666.
157. Wu, F. and Mo, Y. Y. (2007) Ubiquitin-like protein modifications in prostate and breast cancer. Front. Biosci. 12, 700-711.
158. Bischof, O. and Dejean, A. (2007) SUMO is growing senescent. Cell Cycle 6, 677-681.
159. Pountney, D. L., Chegini, F., Shen, X., Blumbergs, P. C. and Gai, W. P. (2005) SUMO-1 marks subdomains within glial cytoplasmic inclusions of multiple system atrophy. Neurosci. Lett. 381, 74-79.
160. Pountney, D. L., Huang, Y., Burns, R. J., Haan, E., Thompson, P. D., Blumbergs, P. C. and Gai, W. P. (2003) SUMO-1 marks the nuclear inclusions in familial neuronal intranuclear inclusion disease. Exp. Neurol. 184, 436-446.
161. Li, Y., Wang, H., Wang, S., Quon, D., Liu, Y. W. and Cordell, B. (2003) Positive and negative regulation of APP amyloidogenesis by sumoylation. Proc. Natl. Acad. Sci. USA 100, 259-264.
162. Terashima, T., Kawai, H., Fujitani, M., Maeda, K. and Yasuda, H. (2002) SUMO-1 co-localized with mutant atrophin-1 with expanded polyglutamines accelerates intranuclear aggregation and cell death. Neuroreport 13, 2359-2364.
163. Chan, H. Y., Warrick, J. M., Andriola, I., Merry, D. and Bonini, N. M. (2002) Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila. Hum. Mol. Genet. 11, 2895-2904.
164. Li, M., Guo, D., Isales, C. M., Eizirik, D. L., Atkinson, M., She, J. X. and Wang, C. Y. (2005) SUMO wrestling with type 1 diabetes. J. Mol. Med. 83, 504-513.
165. Wang, C. Y., Podolsky, R. and She, J. X. (2006) Genetic and functional evidence supporting SUMO4 as a type 1 diabetes susceptibility gene. Ann. NY Acad. Sci. 1079, 257-267.
166. Lin, H.-Y., Wang, C.-L., Hsiao, P.-J., Lu, Y.-C., Chen, S.-Y., Lin, K.-D., Hsin, S.-C., Hsieh, M.-C. and Hsin, S.-J. (2007) SUMO4 M55V variant iIs aAssociated with diabetic nephropathy in type 2 diabetes. Diabetes 56, 1177-1180.
167. Guo, D., Han, J., Adam, B. L., Colburn, N. H., Wang, M. H., Dong, Z., Eizirik, D. L., She, J. X. and Wang, C. Y. (2005) Proteomic analysis of SUMO4 substrates in HEK293 cells under serum starvation-induced stress. Biochem. Biophys. Res. Commun. 337, 1308-1318.
168. Jiang, R., Bush, J. O. and Lidral, A. C. (2006) Development of the upper lip: morphogenetic and molecular mechanisms. Dev. Dyn. 235, 1152-1166.