SUMO/sentrin: Protein modifiers regulating important cellular functions

Biochemistry and Cell Biology

Volumn 77, Issue 4, 1999, Pages 299-309

  Kretz Remy, Carole ^a   Tanguay, Robert M ^b  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

I B; NF B; Nucleus; PML; Protein modification; Protein transport; RanGAP1

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR FACTOR I; UBIQUITIN;

CONFERENCE PAPER; CONFORMATIONAL TRANSITION; DROSOPHILA; INTRACELLULAR TRANSPORT; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN CONFORMATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN TRANSPORT;

EUKARYOTA;

EID: 0032738332     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o99-029     Document Type: Conference Paper

References (77)

1. Arenzana-Seisdedos, F., Thompson, J., Rodriguez, M.S., Bachelerie, F., Thomas, D., and Hay, R.T. 1995. Inducible nuclear expression of newly synthesized IκB alpha negatively regulates DNA-binding and transcriptional activities of NF-κB. Mol. Cell. Biol. 15: 2689-2696.
2. Arrigo, P., and Kretz-Remy, C. 1998. Regulation of mammalian gene expression by free radicals. In Molecular biology of free radicals in human diseases. Edited by O.I. Aruoma and B. Halliwell, OICA International. pp. 183-223.
3. Baeuerle, P.A., and Baltimore, D. 1996. NF-κB: ten years after. Cell, 87: 13-20.
4. Baldwin, Jr., A.S. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14: 649-683.
5. Ball, E., Karlik, C.C., Beall, C.J., Saville, D.L., Sparrow, J.C., Bullard, B., and Fyrberg, E.A. 1987. Arthrin, a myofibrillar protein of insect flight muscle, is an actin-ubiquitin conjugate. Cell, 51: 221-228.
6. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R., and Becker, J. 1998. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280: 275-286.
7. Biggins, S., Ivanovska, I., and Rose, M.D. 1996. Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. J. Cell Biol. 133: 1331-1346.
8. 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.
9. Campbell, I. G., Nicolai, H.M., Foulkes, W.D., Senger, G., Stamp, G.W., Allan, G., Boyer, C., Jones, K., Bast, R. C., Jr., and Solomon, E. 1994. A novel gene encoding a B-box protein within the BRCA1 region at 17q21.1. Hum. Mol. Genet. 3: 589-594.
10. Chelbi-Alix, M.K., Quignon, F., Pelicano, L., Koken, M.H., and de The, H. 1998. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein. J. Virol. 72: 1043-1051.
11. Chen, Z.J., Hagler, J., Palombella, V.J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9: 1586-1597.
12. Dasso, M., and Pu, R.T. 1998. Nuclear structure '98. Nuclear transport: run by Ran? Am. J. Hum. Genet. 63: 311-316.
13. de The, H., Lavau, C., Marchio, A., Chomienne, C., Degos, L., and Dejean, A. 1991. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell, 66: 675-684.
14. Desterro, J.M., Thomson, J., and Hay, R.T. 1997. Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417: 297-300.
15. Desterro, J.M., Rodriguez, M.S., and Hay, R.T. 1998. SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell, 2: 233-239.
16. Desterro, J.M., Rodriguez, M.S., Kemp, G.D., and Hay, R.T. 1999. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274: 10618-10624.
17. 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.
18. Dyck, J.A., Maul, G.G., Miller, Jr., W.H., Chen, J.D., Kakizuka, A., and Evans, R. M. 1994. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell, 76: 333-343.
19. Epps, J.L., and Tanda, S. 1998 The Drosophila semushi mutation blocks nuclear import of Bicoid during embryogenesis. Curr. Biol. 8: 1277-1280.
20. Everett, R.D., Meredith, M, Orr, A., Cross, A., Kathoria, M., and Parkinson, J. 1997. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpes virus regulatory protein. EMBO J. 16: 1519-1530.
21. 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.
22. Goldknopf, I.L., and Busch, H. 1977. Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24. Proc. Natl. Acad. Sci. U.S.A. 74: 864-868.
23. Gong, L., Kamitani, T., Fujise, K., Caskey, L.S., and Yeh, E.T. 1997. Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem. 272: 28198-28201.
24. Haas, A.L., and Siepmann, T.J. 1997. Pathways of ubiquitin conjugation. FASEB J. 11: 1257-1268.
25. Hicke, L., and Riezman, H. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand- stimulated endocytosis. Cell, 84: 277-287.
26. Hodges, M., Tissot, C., Howe, K., Grimwade, D., and Freemont, P.S. 1998. Structure, organization, and dynamics of promyelocytic leukemia protein nuclear bodies. Am. J. Hum. Genet. 63: 297-304.
27. Joanisse, D.R., Inaguma, Y., and Tanguay, R.M. 1998. Cloning and developmental expression of a Nuclear ubiquitin-conjugating enzyme (DmUbc9) that interacts with small heat shock proteins in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 244: 102-109.
28. Johnson, E.S., and Blobel, G. 1997. Ubc9 is the conjugating enzyme for the Ubiquitin-like protein Smt3p. J. Biol. Chem. 272: 26799-26802.
29. Johnson, P.R., and Hochstrasser, M. 1997. SUMO-1: ubiquitin gains weight. Trends Cell Biol. 7: 408-413.
30. 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 Aoslp/Uba2p heterodimer. EMBO J. 16: 5509-5519.
31. Kakizuka, A., Miller, Jr., W.H., Umesono, K., Warrell, R.P., Jr., Frankel, S.R., Murty, V.V., Dmitrovsky, E., and Evans, R.M. 1991. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor. PML. Cell, 66: 663-674.
32. Kamitani, T., Nguyen, H. P., and Yeh, E. T. 1997. Preferential modification of nuclear proteins by a novel ubiquitin-like molecule. J. Biol. Chem. 272: 14001-14004.
33. Kamitani, T., Kito, K, Nguyen, H.P., Fukada-Kamitami, T., and Yeh, E.T. 1998a. Characterization of a second member of the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273: 11349-11353.
34. Kamitani, T., Kito, K., Nguyen, H.P., Wada, H., Fukuda-Kamitani, T., and Yeh, E.T. 1998b. Identification of three major sentrinization sites in PML. J. Biol. Chem. 273: 26675-26682.
35. Kamitani, T., Nguyen, H.P., Kito, K., Fukuda-Kamitani, T., and Yeh, E.T. 1998c. Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273: 3117-3120.
36. Koken, M.H., Puvion-Dutilleul, F., Guillemin, M.C., Viron, A., Linares-Cruz, G., Stuurman, N., de Jong, L., Szostecki, C., Calvo, F., Chomienne, C., Degos, L., Puvion, E., and de Thé, H. 1994. The t(15:17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13: 1073-1083.
37. Korioth, F., Gieffers, C., Maul, G.G., and Frey, J. 1995. Molecular characterization of NDP52, a novel protein of the nuclear domain 10, which is redistributed upon virus infection and interferon treatment. J. Cell Biol. 130: 1-13.
38. Kretz-Remy, C., Mehlen, P., Mirault, M.E., and Arrigo, A.P. 1996. Inhibition of IκB-alpha phosphorylation and degradation and subsequent NF-κB activation by glutathiore peroxidase over-expression. J. Cell Biol. 133: 1083-1093.
39. Lee. G.W., Melchior, F., Mtunis, M.J., Mahajan, R., Tian, Q., and Anderson, P. 1998. Modification of Ran GTPase activating protein by the small ubiquitin-related modifier SUMO-1 requires Ubc9, an E2-type ubiquitin-conjugating enzyme homologue. J. Biol. Chem. 273: 6503-6507.
40. Li, S.J., and Hochstrasser, M. 1999. A new protease required for cell-cycle progression in yeast. Nature (London), 398: 246-251.
41. Loeb, K.R., and Haas, A.L. 1992. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267: 7806-7813.
42. Loeb, K. R., and Haas, A.L. 1994. Conjugates of ubiquitin cross-reactive protein distribute in a cytoskeletal pattern. Mol. Cell. Biol. 14: 8408-8419.
43. 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.
44. 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.
45. Matunis, M. J., Coutavas, E., and Blobel, G. 1996. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135: 1457-1470.
46. 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.
47. 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.
48. Muller, S., Matunis, M.J., and Dejean, A. 1998. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17: 61-70.
49. Naumann. M., and Scheidereit, C. 1994. Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J. 13: 4597-4607.
50. Okuma, T., Honda, R., Ichikawa, G., Tsumagari, N., and Yasuda, H. 1999. In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem. Biophys. Res. Commun. 254: 603-698.
51. 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.
52. Pickart, C.M. 1997. Targeting of substrates to the 26S proteasome. FASEB J. 11: 1055-1066.
53. Regnier, C.H., Song, H.Y., Gao, X., Goeddel, D.V., Cao, Z., and Rothe, M. 1997. Identification and characterization of an IκB kinase. Cell. 90: 373-383.
54. Rothwarf, D.M., Zandi, E., Natoli, G., and Karin, M. 1998. IKK-g is an essential regulatory subunit of the IκB kinase complex. Nature (London), 395: 297-300.
55. Saitoh, H., Pu, R., Cavenagh, M., and Dasso, M. 1997. RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc. Natl. Acad. Sci. U.S.A. 94: 3736-3741.
56. Saltzman, A., Searfoss, G., Marcireau, C., Stone. M., Ressner, R., Munro, R., Franks, C., D'Alonzo, J., Tocque, B., Jaye, M., and Ivashchenko, Y. 1998. hUBC9 associates with MEKK1 and type I TNF-alpha receptor and stimulates NFkB activity. FEBS Lett. 425: 431-435.
57. Scheidereit, C. 1998. Signal transduction. Docking IκB kinases. Nature (London), 395: 225-226.
58. Schwarz, S. E., Matuschewski, K., Liakopoulos, D., Scheffner, M., and Jentsch, S. 1998. The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme. Proc. Natl. Acad. Sci. U.S.A. 95: 560-564.
59. Seufert, W., Futcher, B., and Jentsch, S. 1995. Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature (London), 373: 78-81.
60. Shen, Z., Pardington-Purtymun, P.E., Comeaux, J.C., Moyzis, R. K., and Chen, D.J. 1996. Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system. Genomics, 37: 183-186.
61. Stemsdorf, T., Grotzinger, T., Jensen, K., and Will, H. 1997. Nuclear dots: actors on many stages. Immunobiology, 198: 307-331.
62. Szostecki, C., Guldner, H.H., Netter, H.J., and Will, H. 1990, Isolation and characterization of cDNA encoding a human nuclear antigen predominantly recognized by autoantibodies from patients with primary biliary cirrhosis. J. Immunol. 145: 4338-4347.
63. Tanguay, R.M., Joanisse, D., Inaguma, Y., and Michaud, S. 1999. Small heat shock proteins: in search of functions in vivo. In Environmental stress and gene regulation. Edited by K.B. Storey, BIOS Sci. Pub., Washington, D.C. pp. 125-138.
64. Tashiro, K., Pando, M. P., Kanegae, Y., Wamsley, P.M., Inoue, S., and Verma, I. M. 1997. Direct involvement of the ubiquitin-conjugating enzyme Ubc9/Hus5 in the degradation of IκBalpha. Proc. Natl. Acad. Sci. U.S.A. 94: 7862-7867.
65. Tsytsykova, A.V., Tsisikov, E.N., Wright, D.A., Futcher, B., and Geha, R.S. 1998. The mouse genome contains two expressed intronless retroposed pseudogenes for the sentrin/sumo-I/PIC1 conjugating enzyme Ubc9. Mol. Immunol. 35: 1057-1067.
66. Varshavsky, A. 1997. The ubiquitin system. Trends Biochem. Sci. 22: 383-387.
67. Verma, I.M., Stevenson, J.K., Schwarz, E.M., Vanantwerp, D., and Miyamoto, S. 1995. ReI/NF-κB/I κB family: Intimate tales of association and dissociation. Genes Dev. 9: 2723-2735.
68. Walking, J.F., Sung, P., Prakash, L., and Prakash, S. 1993. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol. Cell. Biol. 13: 7757-7765.
69. Weis, K., Rambaud, S., Lavau, C., Jansen, J., Carvalho, T., Carmo-Fonseca, M., Lamond, A., and Dejean, A. 1994. Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell, 76: 345-356.
70. Whiteside, S.T., and Israel, A. 1997. IκB proteins: structure, function and regulation. Semin. Cancer Biol. 8: 75-82.
71. Whiteside, S.T., Epinat, J.C., Rice, N.R., and Israel, A. 1997. IκB epsilon, a novel member of the IκB family, controls RelA and cRel NF-κB activity. EMBO J. 16: 1413-1426.
72. Wilkinson, K.D. 1995. Roles of ubiquitinylation in proteolysis and cellular regulation. Annu. Rev. Nutr. 15: 161-189.
73. Wilkinson, K.D. 1997. Regulation of ubiquitin-dependent processes by deubiquinating enzymes. FASEB J. 11: 1245-1256.
74. Yaron, A., Gonen, H., Alkalay, I., Hatzubai, A., Jung, S., Beyth, S., Mercurio, F., Manning, A. M., Ciechanover, A., and Ben-Neriah, Y. 1997. Inhibition of NF-κB cellular function via specific targeting of the IκB-ubiquitin ligase. EMBO J. 16: 6486-6494.
75. Yaron, A., Hatzubai, A., Davis, M., Lavon, I., Amit, S., Manning, A.M., Andersen, J. S., Mann, M., Mercurio, F., and Ben-Neriah, Y. 1998. Identification of the receptor component of the IκBα-ubiquitin ligase. Nature (London), 396: 590-594.
76. Zandi, E., Rothwarf, D.M., Delhase, M., Hayakawa, M., and Karin, M. 1997. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell. 91: 243-252.
77. Zhong, H., Su Yang, H., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. 1997. The transcriptional activity of NF-κB is regulated by the IκB- associated PKAc subunit through a cyclic AMP-independent mechanism. Cell, 89: 413-424.