Reactive oxygen species-mediated p53 core-domain modifications determine apoptotic or necrotic death in cancer cells

Antioxidants and Redox Signaling

Volumn 16, Issue 5, 2012, Pages 400-412

  Gogna, Rajan ^a   Madan, Esha ^a   Kuppusamy, Periannan ^b   Pati, Uttam ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; DNA; GOLD NANOPARTICLE; GOLD NANOPARTICLE 10; GOLD NANOPARTICLE 80; PHOSPHOTRANSFERASE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ACETYLATION; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CONTROLLED STUDY; DNA BINDING; DRUG MECHANISM; ENZYME ACTIVATION; GENE ACTIVATION; GENE CLUSTER; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUMOR REGRESSION;

APOPTOSIS; GOLD; HUMANS; METAL NANOPARTICLES; NECROSIS; NEOPLASMS; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

MUS;

EID: 84855865827     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4103     Document Type: Article

References (50)

1. Appella E and Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 268: 2764-2772, 2001. (Pubitemid 32862957)
2. Bhabra G, Sood A, Fisher B, Cartwright L, Saunders M, Evans WH, Surprenant A, Lopez-Castejon G, Mann S, Davis SA, Hails LA, Ingham E, Verkade P, Lane J, Heesom K, Newson R, and Case CP. Nanoparticles can cause DNA damage across a cellular barrier. Nat Nanotechnol 4: 876-883, 2009.
3. Bhattacharya R, Mukherjee P, Xiong Z, Atala A, Soker S, and Mukhopadhyay D. Gold nanoparticles inhibit VEGF165-induced proliferation of HUVEC cells. Nano Lett 4: 2479-2481, 2004. (Pubitemid 40002388)
4. Bode AM and Dong Z. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 4: 793-805, 2004. (Pubitemid 39331151)
5. Bragado P, Armesilla A, Silva A, and Porras A. Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 12: 1733-1742, 2007. (Pubitemid 47106882)
6. Chao C, Hergenhahn M, Kaeser MD, Wu Z, Saito S, Iggo R, Hollstein M, Appella E, and Xu Y. Cell type-and promoterspecific roles of Ser18 phosphorylation in regulating p53 responses. J Biol Chem 278: 41028-41033, 2003. (Pubitemid 37280926)
7. Cheng Y, C Samia A, Meyers JD, Panagopoulos I, Fei B, and Burda C. Highly efficient drug delivery with gold nanoparticle vectors for in vivo photodynamic therapy of cancer. J Am Chem Soc 130: 10643-10647, 2008.
8. El-Sayed IH, Huang X, and El-Sayed MA. Surface plasmon resonance scattering and absorption of anti-EGFR antibody conjugated gold nanoparticles in cancer diagnostics: applications in oral cancer. Nano Lett 5: 829-834, 2005. (Pubitemid 40749040)
9. El-Sayed IH, Huang X, and El-Sayed MA. Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles. Cancer Lett 239: 129-135, 2006. (Pubitemid 43946581)
10. Fogal V, Hsieh JK, Royer C, Zhong S, and Lu X. Cell cycledependent nuclear retention of p53 by E2F1 requires phosphorylation of p53 at Ser315. EMBO J 24: 2768-2782, 2005. (Pubitemid 41170026)
11. Gannon CJ, Patra CR, Bhattacharya R, Mukherjee P, and Curley SA. Intracellular gold nanoparticles enhance noninvasive radiofrequency thermal destruction of human gastrointestinal cancer cells. J Nanobiotechnol 6: 2, 2008.
12. Gottifredi V and Prives C. Molecular biology. Getting p53 out of the nucleus. Science 292: 1851-1852, 2001. (Pubitemid 32538354)
13. Hao M, Lowy AM, Kapoor M, Deffie A, Liu G, and Lozano G. Mutation of phosphoserine 389 affects p53 function in vivo. J Biol Chem 271: 29380-29385, 1996. (Pubitemid 26382655)
14. Haupt Y, Rowan S, Shaulian E, Kazaz A, Vousden K, and Oren M. p53 mediated apoptosis in HeLa cells: transcription dependent and independent mechanisms. Leukemia 11(Suppl 3): 337-339, 1997.
15. Hoh J, Jin S, Parrado T, Edington J, Levine AJ, and Ott J. The p53MH algorithm and its application in detecting p53-responsive genes. Proc Natl Acad Sci USA 99: 8467-8472, 2002. (Pubitemid 34693586)
16. Jiang W, Kim BY, Rutka JT, and Chan WC. Nanoparticlemediated cellular response is size-dependent. Nat Nanotechnol 3: 145-150, 2008.
17. Jimenez GS, Khan SH, Stommel JM, and Wahl GM. p53 regulation by post-translational modification and nuclear retention in response to diverse stresses. Oncogene 18: 7656-7665, 1999. (Pubitemid 30052692)
18. Kaeser MD and Iggo RD. Chromatin immunoprecipitation analysis fails to support the latency model for regulation of p53 DNA binding activity in vivo. Proc Natl Acad Sci USA 99: 95-100, 2002. (Pubitemid 34060322)
19. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, Quong AA, Zhang X, Beerman T, Pestell RG, and Avantaggiati ML. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 173: 533-544, 2006. (Pubitemid 43765200)
20. Li AG, Piluso LG, Cai X, Gadd BJ, Ladurner AG, and Liu X. An acetylation switch in p53 mediates holo-TFIID recruitment. Mol Cell 28: 408-421, 2007. (Pubitemid 350030559)
21. Liu B, Chen Y, and St Clair DK. ROS and p53: a versatile partnership. Free Radic Biol Med 44: 1529-1535, 2008.
22. Luo J, Su F, Chen D, Shiloh A, and Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408: 377-381, 2000.
23. Macip S, IgarashiM, Berggren P, Yu J, Lee SW, and Aaronson SA. Influence of induced reactive oxygen species in p53-mediated cell fate decisions. Mol Cell Biol 23: 8576-8585, 2003. (Pubitemid 37433363)
24. MacLaine NJ and Hupp TR. How phosphorylation controls p53. Cell Cycle 10: 916-921, 2011.
25. Mayo LD, Seo YR, Jackson MW, Smith ML, Rivera Guzman J, Korgaonkar CK, and Donner DB. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. J Biol Chem 280: 25953-25959, 2005. (Pubitemid 41022185)
26. Mukherjee P, Bhattacharya R, Bone N, Lee YK, Patra CR, Wang S, Lu L, Secreto C, Banerjee PC, Yaszemski MJ, Kay NE, and Mukhopadhyay D. Potential therapeutic application of gold nanoparticles in B-chronic lymphocytic leukemia (BCLL): enhancing apoptosis. J Nanobiotechnol 5: 4, 2007.
27. Mukherjee P, Bhattacharya R, Wang P, Wang L, Basu S, Nagy JA, Atala A, Mukhopadhyay D, and Soker S. Antiangiogenic properties of gold nanoparticles. Clin Cancer Res 11: 3530-3534, 2005. (Pubitemid 40627908)
28. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, and Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102: 849-862, 2000.
29. Omata Y, Lewis JB, Lockwood PE, Tseng WY, Messer RL, Bouillaguet S, and Wataha JC. Gold-induced reactive oxygen species (ROS) do not mediate suppression of monocytic mitochondrial or secretory function. Toxicol In Vitro 20: 625-633, 2006. (Pubitemid 43816260)
30. Pan Y,Neuss S, LeifertA, FischlerM,Wen F, Simon U, Schmid G, Brandau W, and Jahnen-Dechent W. Size-dependent cytotoxicity of gold nanoparticles. Small 3: 1941-1949, 2007. (Pubitemid 350099867)
31. Polley S, Guha S, Roy NS, Kar S, Sakaguchi K, Chuman Y, Swaminathan V, Kundu T, and Roy S. Differential recognition of phosphorylated transactivation domains of p53 by different p300 domains. J Mol Biol 376: 8-12, 2008.
32. Saito S, Yamaguchi H, Higashimoto Y, Chao C, Xu Y, Fornace AJ, Jr., Appella E, and Anderson CW. Phosphorylation site interdependence of human p53 post-translational modifications in response to stress. J Biol Chem 278: 37536-37544, 2003. (Pubitemid 37175275)
33. Sakaguchi K, Sakamoto H, Lewis MS, Anderson CW, Erickson JW, Appella E, and Xie D. Phosphorylation of serine 392 stabilizes the tetramer formation of tumor suppressor protein p53. Biochemistry 36: 10117-10124, 1997. (Pubitemid 27357721)
34. Shieh SY, Ikeda M, Taya Y, and Prives C. DNA damageinduced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334, 1997. (Pubitemid 27467963)
35. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS, and McMahon SB. Acetylation of the p53 DNAbinding domain regulates apoptosis induction. Mol Cell 24: 841-851, 2006. (Pubitemid 44960096)
36. Tang Y, Luo J, Zhang W, and Gu W. Tip60-dependent acetylation of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol Cell 24: 827-839, 2006. (Pubitemid 44960094)
37. Tang Y, Zhao W, Chen Y, Zhao Y, and Gu W. Acetylation is indispensable for p53 activation. Cell 133: 612-626, 2008. (Pubitemid 351636297)
38. Terui T, Murakami K, Takimoto R, Takahashi M, Takada K, Murakami T, Minami S, Matsunaga T, Takayama T, Kato J, and Niitsu Y. Induction of PIG3 and NOXA through acetylation of p53 at 320 and 373 lysine residues as a mechanism for apoptotic cell death by histone deacetylase inhibitors. Cancer Res 63: 8948-8954, 2003. (Pubitemid 38064075)
39. Thomas M and Klibanov AM. Conjugation to gold nanoparticles enhances polyethylenimine's transfer of plasmid DNA into mammalian cells. Proc Natl Acad Sci USA 100: 9138-9143, 2003. (Pubitemid 37033896)
40. Tu HC, Ren D, Wang GX, Chen DY, Westergard TD, Kim H, Sasagawa S, Hsieh JJ, and Cheng EH. The p53-cathepsin axis cooperates with ROS to activate programmed necrotic death upon DNA damage. Proc Natl Acad Sci USA 106: 1093-1098, 2009.
41. Vega FM, Sevilla A, and Lazo PA. p53 Stabilization and accumulation induced by human vaccinia-related kinase 1. Mol Cell Biol 24: 10366-10380, 2004. (Pubitemid 39507873)
42. Visaria RK, Griffin RJ, Williams BW, Ebbini ES, Paciotti GF, Song CW, and Bischof JC. Enhancement of tumor thermal therapy using gold nanoparticle-assisted tumor necrosis factor-alpha delivery. Mol Cancer Ther 5: 1014-1020, 2006. (Pubitemid 43724602)
43. Vogelstein B, Lane D, and Levine AJ. Surfing the p53 network. Nature 408: 307-310, 2000.
44. Vousden KH and Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 8: 275-283, 2007. (Pubitemid 46474662)
45. Vousden KH and Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2: 594-604, 2002. (Pubitemid 37328926)
46. Xie S, Wang Q, Wu H, Cogswell J, Lu L, Jhanwar-Uniyal M, and Dai W. Reactive oxygen species-induced phosphorylation of p53 on serine 20 is mediated in part by polo-like kinase-3. J Biol Chem 276: 36194-36199, 2001.
47. Yuan J, Lipinski M, and Degterev A. Diversity in the mechanisms of neuronal cell death. Neuron 40: 401-413, 2003. (Pubitemid 37244104)
48. Zacchi P, Gostissa M, Uchida T, Salvagno C, Avolio F, Volinia S, Ronai Z, Blandino G, Schneider C, and Del Sal G. The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 419: 853-857, 2002. (Pubitemid 35238573)
49. Zong WX and Thompson CB. Necrotic death as a cell fate. Genes Dev 20: 1-15, 2006. (Pubitemid 43042662)
50. He L, He X, Lim LP, de Stanchina E, Xuang Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson A, et al. A micro RNA component of the p53 tumour suppressor network. Nature 447: 1130-1134, 2007. (Pubitemid 47014436)