Phosphorylation regulates the interaction and complex formation between wt p53 protein and PARP-1

Journal of Cellular Biochemistry

Volumn 89, Issue 6, 2003, Pages 1260-1248

  Wȩsierska Ga̧dek, Józefa ^a   Wojciechowski, Jacek ^a   Schmid, Gerald ^a,b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Inst für Molekulare Onkologie   (Germany)

Author keywords

2D PAGE; Cell cycle arrest, FACS analysis; NES; Nucleocytoplasmic shuttling; p53 isomers; p53 nuclear export; p53 phosphorylation; p53 pull down assay; p53 stability

Indexed keywords

BACULOVIRUS VECTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; SERINE; UNCLASSIFIED DRUG; VIRUS VECTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACULOVIRUS; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; COMPLEX FORMATION; CONTROLLED STUDY; DEPHOSPHORYLATION; GENE OVEREXPRESSION; IMMUNOBLOTTING; INSECT CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TUMOR SUPPRESSOR GENE;

INSECTA;

EID: 0043125662     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.10569     Document Type: Article

References (65)

1. Adachi Y, Yanagida M. 1989. Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kDa protein preferentially localized in the nucleus and its periphery. J Cell Biol 108:1195-1207.
2. Appella E, Anderson CW. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 268:2764-2772.
3. Bargonetti J, Manfredi JJn. 2002. Multiple roles of the tumor suppressor p53. Curr Opin Oncol 14:86-91.
4. Blagosklonny M. 2002a. p53: An ubiquitous target of anticancer drugs. Int J Cancer 98:161-166.
5. Blagosklonny MV, Demidenko ZN, Fojo T. 2002b. Inhibition of transcription results in accumulation of wt p53 followed by delayed outburst of p53-inducible proteins: p53 as a sensor of transcriptional integrity. Cell Cycle 1:67-74.
6. Bothner B, Lewis WS, Di Giammmarino LE, Weber DJ, Bothner JS, Kriwacki WR. 2001. Defining the molecular basis of Arf and Hdm 2 interactions. J Mol Biol 314:263-277.
7. David-Pfeuty T, Chakrani F, Ory K, Nouvian-Doughe Y. 1996. Cell cycle-dependent regulation of nuclear traffic occurs one subclass of human tumor cells and in untransformed cells. Cell Growth Differ 7:1211-1225.
8. Eliyahu D, Michalovitz D, Oren M. 1985. Overproduction of p53 antigen makes established cells highly tumorigenic. Nature 316:158-160.
9. Freedman DA, Levine AJ. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol 18:7288-7293.
10. Fritsche M, Haessler C, Brandner G. 1993. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8:307-318.
11. Fuchs B, Hecker D, Scheidtmann KH. 1995. Phosphorylation studies on rat p53 using the baculovirus expression system. Manipulation of the phosphorylation state with okadaic acid and influence on DNA binding. Eur J Biochem 228:625-639.
12. Geyer RK, Yu ZK, Maki CG. 2000. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat Cell Biol 2:569-573.
13. Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, Del Sal G. 1999. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 18:5462-5471.
14. Gu W, Roeder RG. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90:595-606.
15. Gu J, Nie L, Wiederschain D, Yuan ZM. 2001. Identification of p53 sequence elements that are required for MDM2-mediated nuclear export. Mol Cell Biol 21:8533-8546.
16. ARF) in activing p53. J Biol Chem 40:37765-37770.
17. Haupt Y, Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296-299.
18. Herceg Z, Wang ZQ. 1999. Failure of poly(ADP-ribose) polymerase cleavage by caspases leads to induction of necrosis and enhanced apoptosis. Mol Cell Biol 7:5124-5133.
19. Honda R, Yasuda H. 1999. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumour suppressor p53. EMBO J 18:22-27.
20. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, Grosveld G, Sherr CJ. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649-659.
21. Kessis TD, Slebos RJ, Nelson WG, Kastan MB, Plunkett BS, Han SM, Lorincz AT, Hedrick L, Cho KR. 1993. Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc Natl Acad Sci USA 90:3988-3992.
22. Kim IS, Kim DH, Han SM, Chin MU, Nam HJ, Cho HP, Choi SY, Song BJ, Kim ER, Bae YS, Moon YH. 2000. Truncated form of importin alpha identified in breast cancer cell inhibits nuclear import of p53. J Biol Chem 275:23139-23145.
23. Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387:299-303.
24. Kudo N, Wolff B, Sekimoto T, Schreiner EP, Yoner Yanagida M, Horinouchi S, Yoshida M. 1998. Leptomycin B inhibition of signal mediated nuclear export by direct bidning to CRM1. Exp Cell Res 242:540-547.
25. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S. 1999. Leptomycin B inactivated CRM1/exportin1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci USA 96:9112-9117.
26. Kumari SR, Mendoza-Alvarez H, Alvarez-Gonzalez R. 1998. Functional interactions of p53 with poly(ADP-ribose) polymerase (PARP) during apoptosis following DNA damage: Covalent poly(ADP-ribosyl)ation of p53 by exogenous PARP and noncovalent binding of p53 to the M(r) 85,000 proteolytic fragment. Cancer Res 58:5075-5078.
27. 4. Nature 227:680-685.
28. ARF without relocation of MDM 2 to the nucleolus: Nat Cell Biol 3:445-451.
29. Ljungman M, Zhang F, Chen F, Rainbow AJ, McKay BC. 1999. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene 18:583-592.
30. Lorum MA, Ashkroft M, Kubbutat MH, Vousden KH. 2000. Identification of a cryptic nucleolar-localization signal in MDM2. Nat Cell Biol 2:179-181.
31. Maltzman W, Czyzyk L. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol 4:1689-1694.
32. Mao L, Merlo A, Bed G, Shapiro GI, Edwards CD, Rollins BJ, Sidransky D. 1995. A novel p16INK4A transcript. Cancer Res 55:2995-2997.
33. Moll UM, Riou G, Levine AJ. 1992. Two distinct mechanisms alter p53 in breast cancer: Mutation and nuclear exclusion. Proc Natl Acad Sci 89:7262-7266.
34. Moll UM, LaQuaglia M, Bernard J, Riou G. 1995. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc Natl Acad Sci USA 92:4407-4411.
35. Momand J, Zambetti G, Olson D, George D, Levine AJ. 1992. The Mdm2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69:1237-1245.
36. O'Farell PH. 1975. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007-4021.
37. Oliner JD, Pientenpol JA, Thiagalingman S, Gyuris J, Kinzler KW, Vogelstein B. 1993. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362:857-860.
38. Pomerantz J, Schreiber-Agus N. 1998. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92:713-723.
39. Prives C, Hall PA. 1999. The p53 pathway. J Pathol 187:112-126.
40. Quelle DE, Zindy F, Ashmun R, Sherr CJ. 1995. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83:993-1000.
41. Rodriguez MS, Desterro JMP, Lain S, Midgley CA, Lane DP, Hay RT. 1999. SUMO-1 modification activates the transcriptional response of p53. EMBO J 18:6455-6461.
42. Roser S, Pool-Zobel B-I, Rechkemmer G. 2001. Contribution of apoptosis to responses in the comet assay. Mut Res 497:169-175.
43. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
44. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
45. Shaulsky G, Ben-Ze'ev A, Rotter V. 1990. Subcellular distribution of the p53 protein during the cell cycle of Baalb/c 3T3 cells. Oncogene 5:1707-1711.
46. Simbulan-Rosenthal CM, Rosenthal DS, Iyer S, Boulares AH, Smulson ME. 1998. Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J Biol Chem 273:13703-13712.
47. Stommel JM, Marchenko ND, Jimenez GS, Moll UM, Hope TJ, Wahl GM. 1999. A leucine-rich nuclear export signal in the p53 tetramerization domain: Regulation of subcellular localization and p53 activity by NES masking. EMBO J 18:1660-1672.
48. Tao W, Levine AL. 1999. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53. Proc Natl Acad Sci USA 96:3077-3080.
49. Vaziri H, West MD, Allsopp RC, Davison TS, Wu YS, Arrowsmith CH, Poirier GG, Benchimol S. 1998. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J 17:6018-6033.
50. Vindelov LL, Christensen IJ, Nissen NI. 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 5:323-327.
51. Wang ZQ, Auer B, Stingl L, Berghammer H, Haidacher D, Schweiger M, Wagner EF. 1995. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev 9:509-20.
52. Weber DJ, Taylor JL, Roussel FM, Sherr JCh, Bar-Sagi D. 1999. Nucleolar Arf sequesters Mdm2 and activates p 53. Nat Cell Biol 1:20-26.
53. Wesierska-Gadek J, Schmid G. 2000a. Overexpressed poly(ADP-ribose) polymerase delays the release of rat cells from p53-mediated G(1) checkpoint. J Cell Biochem 80:85-103.
54. Wesierska-Gadek J, Schmid G. 2001. Poly(ADP-ribose) polymerase-1 regulates the stability of the wild-type p53 protein. Cell Mol Biol Lett 6:117-140.
55. Wesierska-Gadek J, Bugajska-Schretter A, Cerni C. 1996a. ADP-ribosylation of p53 tumor suppressor protein: Mutant but not wild-type p53 is modified. J Cell Biochem 62:90-101.
56. Wesierska-Gadek J, Hohenauer H, Hitchman E, Penner E. 1996b. Autoantibodies against nucleoporin p62 constitute a novel marker of primary biliary cirrhosis. Gastroenterology 110:840-847.
57. Wesierska-Gadek J, Schmid G, Cerni C. 1996c. ADP-ribosylation of wild-type p53 in vitro: Binding of p53 protein to specific p53 consensus sequence prevents its modification. Biochem Biophys Res Commun 224:96-102.
58. Wesierska-Gadek J, Wang ZQ, Schmid G. 1999. Reduced stability of regularly spliced but not alternatively spliced p53 protein in PARP-deficient mouse fibroblasts. Cancer Res 59:28-34.
59. Wesierska-Gadek J, Bohrn E, Herceg Z, Wang ZQ, Wurzer G. 2000b. Differential susceptibility of normal and PARP knock-out mouse fibroblasts to proteasome inhibitors. J Cell Biochem 78:681-696.
60. Wesierska-Gadek J, Schloffer D, Kotala V, Horky M. 2002. Escape of p53 protein from E6-mediated degradation in HeLa cells after cisplatin therapy. Int J Cancer 101:128-136.
61. Wesierska-Gadek J, Wojciechowski J, Schmid G. 2003. Central and carboxy-terminal regions of human p53 protein are essential for interaction and complex formation with PARP-1. J Cell Biochem 89:220-232.
62. Whitacre CM, Hashimoto H, Tsai ML, Chatterjee S, Berger SJ, Berger NA. 1995. Involvement of NAD-poly(ADP-ribose) metabolism in p53 regulation and its consequences. Cancer Res 55:3697-3701.
63. Wolff B, Sanglier JJ, Wang Y. 1997. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem Biol 2:139-147.
64. Wurzer G, Herceg Z, Wesierska-Gadek J. 2000. Increased resistance to anticancer therapy of mouse cells lacking the poly(ADP-ribose) polymerase attributable to up-regulation of the multidrug resistance gene product P-glycoprotein. Cancer Res 60:4238-4244.
65. Zhang Y, Xiong Y. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage induced phosphorylation. Science 292:1910-1915.