Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1

EMBO Journal

Volumn 18, Issue 22, 1999, Pages 6462-6471

  Gostissa, Monica ^a   Hengstermann, Arnd ^b   Fogal, Valentina ^a   Sandy, Peter ^a   Schwarz, Sylvia E ^b   Scheffner, Martin ^b   Del Sal, Giannino ^a,c  

^a Laboratorio Nazionale CIB   (Italy)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF TRIESTE   (Italy)

Author keywords

p53; Regulation; SUMO 1; Transactivation; Ubc9

Indexed keywords

CELL PROTEIN; LYSINE; PROTEIN P53; UBIQUITIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CELL LINE; HUMANS; KINETICS; LYSINE; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; RECOMBINANT PROTEINS; SUMO-1 PROTEIN; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINS;

ANIMALIA;

EID: 0033570892     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.22.6462     Document Type: Article

References (44)

1. Baldwin, A.S. (1996) The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol., 14, 649-693.
2. 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.
3. Chelbi-Alix, M.K. and de The, H. (1999) Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene, 18, 935-941.
4. 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.
5. 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.
6. el-Deiry, W.S. et al. (1993) WAF-1, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
7. Giaccia, A.J. and Kastan, M.B. (1998) The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev., 12, 2973-2983.
8. Gu, W. and Roeder, R.G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell, 90, 595-606.
9. 1 and S phase protein that associates with Cdk2. Cell, 75, 791-803.
10. Haupt, Y., Maya, R., Kazaz, A. and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-299.
11. Hodges, M., Tissot, C. and Freemont, P.S. (1998) Protein regulation: Tag wrestling with relatives of ubiquitin. Curr. Biol., 8, R749-R752.
12. Hollstein, M., Shomer, B., Greenblatt, M., Soussi, T., Hovig, E., Montesano, R. and Harris, C.C. (1996) Somatic point mutations in the p53 gene of human tumors and cell lines: updated compilation. Nucleic Acids Res., 24, 141-146.
13. Honda, R., Tanaka, H. and Yasuda, H. (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett., 420, 25-27.
14. Hupp, T.R. and Lane, D.P. (1994) Allosteric activation of latent p53 tetramers. Curr. Biol., 4, 865-875.
15. Hupp, T.R., Meek, D.W., Midgley, C.A. and Lane, D.P. (1992) Regulation of the specific DNA-binding function of p53. Cell, 83, 875-886.
16. Hupp, T.R., Sparks, A. and Lane, D.P. (1995) Small peptides activate the latent sequence-specific DNA binding function of p53. Cell, 83, 237-245.
17. Khanna, K.K. et al. (1998) ATM associates with and phosphorylates p53: mapping the region of interaction. Nature Genet., 20, 398-400.
18. Ko, L.J. and Prives, C. (1996) p53: puzzle and paradigm. Genes Dev., 10, 1054-1072.
19. Kubbutat, M.H.G., Jones, S.N. and Vousden, K.H. (1997) Regulation of p53 stability by mdm2. Nature, 387, 299-303.
20. Kubbutat, M.H.G., Ludwig, R.L., Ashcroft, M. and Vousden, K.H. (1998) Regulation of Mdm2-directed degradation by the C terminus of p53. Mol. Cell. Biol., 18, 5690-5698.
21. Kussie, P.H., Gorina, S., Marechal, V., Elenbaas, B., Moreau, J., Levine, A.J. and Pavletich, N.P. (1996) Crystal structure of the MDM2 oncoprotein bound to the transactivation domain of the p53 tumor suppressor. Science, 274, 948-953.
22. Lain, S., Midgley, C., Sparks, A., Lane, E.B. and Lane, D.P. (1999) An inhibitor of nuclear export activates the p53 response and induces the localization of HDM2 and p53 to U1A-positive nuclear bodies associated with the PODs. Exp. Cell Res., 248, 457-472.
23. Lee, G.W., Melchior, F., Matunis, 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, 6503-7.
24. Levine, A.J. (1997) p53, the cellular gatekeeper for growth and division. Cell, 88, 323-331.
25. Li, S.J. and Hochstrasser, M. (1999) A new protease required for cell-cycle progression in yeast. Nature, 398, 246-251.
26. Lu, H. and Levine, A.J. (1995) Human TAF-31 is a transcriptional coactivator of the p53 protein. Proc. Natl Acad. Sci. USA, 92, 5154-5158.
27. 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.
28. 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.
29. Masutani, C. et al. (1994) Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J., 13, 1831-1843.
30. 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.
31. Momand, J., Zambetti, G.P., Olson, D.C., George, D. and Levine, A.J. (1992) The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell, 69, 1237-1245.
32. Muller, S. and Dejean, A. (1999) Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol., 73, 5139-5143.
33. Okuma, J., 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, 693-698.
34. Prives, C. (1998) Signaling to p53: Breaking the MDM2-p53 circuit Cell, 95, 5-8.
35. Saitoh, H., Pu, R.T. and Dasso, M. (1997) SUMO-1: wrestling with a new ubiquitin-related modifier. Trends Biochem. Sci., 22, 374-376.
36. 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. USA, 95, 560-564.
37. Shaw, P., Freeman, J., Bovey, R. and Iggo, R. (1996) Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus. Oncogene, 12, 921-930.
38. Shen, Z., Pardington-Purtymun, P.E., Comeaux, J.C., Moyzis, R.K. and Chen, D.J. (1996) Association of UBE21 with RAD52, UBL1, p53 and RAD51 proteins in a yeast two-hybrid system. Genomics, 37, 183-186.
39. Shieh, S.Y., Ikeda, M., Taya, Y. and Prives, C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell, 91, 325-334.
40. Sternsdorf, T., Jensen, K. and Will, H. (1997) Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1. J. Cell Biol., 139, 1621-1634.
41. Thut, C.J., Chen, J.L., Klemin, R. and Tijan, R. (1995) p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science, 267, 100-104.
42. Unger, T., Sionov, R.V., Moallem, E., Yee, C.L., Howley, P.M., Oren, M. and Haupt, Y. (1999) Mutations in serines 15 and 20 of human p53 impair its apoptotic activity. Oncogene, 18, 3205-3212.
43. Waterman, M.J., Stavridi, E.S., Waterman, J.L. and Halazonetis, T.D. (1998) ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nature Genet., 19, 175-178.
44. Zhang, Y. and Xiong, Y. (1999) Mutations in human ARF exon 2 disrupt its nucleolar localization and impairs its ability to block nuclear export of MDM2 and p53. Mol. Cell, 3, 579-591.