Low-dose valproic acid enhances radiosensitivity of prostate cancer through acetylated p53-dependent modulation of mitochondrial membrane potential and apoptosis

Molecular Cancer Research

Volumn 9, Issue 4, 2011, Pages 448-461

  Chen, Xufeng ^a   Wong, Jeffrey Y C ^a   Wong, Patty ^a   Radany, Eric H ^a,b  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Hope Cancer Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; HISTONE ACETYLTRANSFERASE; PROTEIN BCL 2; PROTEIN P53; PROTEIN TIP60; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CYTOTOXICITY; DRUG EFFECT; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IONIZING RADIATION; LOW DRUG DOSE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN LOCALIZATION; RADIOSENSITIVITY;

ACETYLATION; APOPTOSIS; CELL LINE, TUMOR; HISTONE DEACETYLASE INHIBITORS; HUMANS; LYSINE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; PROSTATIC NEOPLASMS; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; TUMOR SUPPRESSOR PROTEIN P53; VALPROIC ACID;

EID: 79954488451     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0471     Document Type: Article

References (66)

1. Howell SB. Resistance to apoptosis in prostate cancer cells. Mol Urol 2000;4:225-9; discussion 231.
2. Zietman AL, DeSilvio ML, Slater JD, Rossi CJ Jr, Miller DW, Adams JA, et al. Comparison of conventional-dose vs high-dose conformal radiation therapy in clinically localized adenocarcinoma of the prostate: a randomized controlled trial. JAMA 2005;294:1233-9. (Pubitemid 41352111)
3. Pollack A, Zagars GK, Starkschall G, Antolak JA, Lee JJ, Huang E, et al. Prostate cancer radiation dose response: results of the M. D. Anderson phase III randomized trial. Int J Radiat Oncol Biol Phys 2002;53:1097-105. (Pubitemid 34787842)
4. Zelefsky MJ, Fuks Z, Hunt M, Lee HJ, Lombardi D, Ling CC, et al. High dose radiation delivered by intensity modulated conformal radiotherapy improves the outcome of localized prostate cancer. J Urol 2001;166:876-81. (Pubitemid 32750970)
5. Camphausen K, Tofilon PJ. Inhibition of histone deacetylation: a strategy for tumor radiosensitization. J Clin Oncol 2007;25:4051-6. (Pubitemid 47492949)
6. Baschnagel A, Russo A, Burgan WE, Carter D, Beam K, Palmieri D, et al. Vorinostat enhances the radiosensitivity of a breast cancer brain metastatic cell line grown in vitro and as intracranial xenografts. Mol Cancer Ther 2009;8:1589-95.
7. Camphausen K, Burgan W, Cerra M, Oswald KA, Trepel JB, Lee MJ, et al. Enhanced radiation-induced cell killing and prolongation of gammaH2AX foci expression by the histone deacetylase inhibitor MS-275. Cancer Res 2004;64:316-21. (Pubitemid 38114113)
8. Camphausen K, Cerna D, Scott T, Sproull M, Burgan WE, Cerra MA, et al. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer 2005;114:380-6. (Pubitemid 40279957)
9. Camphausen K, Scott T, Sproull M, Tofilon PJ. Enhancement of xenograft tumor radiosensitivity by the histone deacetylase inhibitor MS-275 and correlation with histone hyperacetylation. Clin Cancer Res 2004;10:6066-71. (Pubitemid 39302609)
10. Chinnaiyan P, Cerna D, Burgan WE, Beam K, Williams ES, Camphausen K, et al. Postradiation sensitization of the histone deacetylase inhibitor valproic acid. Clin Cancer Res 2008;14:5410-5.
11. Zhang Y, Jung M, Dritschilo A. Enhancement of radiation sensitivity of human squamous carcinoma cells by histone deacetylase inhibitors. Radiat Res 2004;161:667-74. (Pubitemid 39149575)
12. Florenes VA, Skrede M, Jorgensen K, Nesland JM. Deacetylase inhibition in malignant melanomas: impact on cell cycle regulation and survival. Melanoma Res 2004;14:173-81. (Pubitemid 38879578)
13. Bedford JS, Dewey WC. Radiation Research Society. 1952-2002. Historical and current highlights in radiation biology: has anything important been learned by irradiating cells?Radiat Res 2002;158:251-91. (Pubitemid 34924928)
14. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007;26:5541-52. (Pubitemid 47255934)
15. Zhang F, Zhang T, Teng ZH, Zhang R, Wang JB, Mei QB. Sensitization to gamma-irradiation-induced cell cycle arrest and apoptosis by the histone deacetylase inhibitor trichostatin A in nonsmall cell lung cancer (NSCLC) cells. Cancer Biol Ther 2009;8:823-31.
16. Zhang Y, Adachi M, Zhao X, Kawamura R, Imai K. Histone deacetylase inhibitors FK228, N-(2-aminophenyl)-4-[N-(pyridin-3-yl-methoxycarbonyl) amino-methyl]benzamide and m-carboxycinnamic acid bishydroxamide augment radiation-induced cell death in gastrointestinal adenocarcinoma cells. Int J Cancer 2004;110:301-8. (Pubitemid 38580407)
17. Munshi A, Kurland JF, Nishikawa T, Tanaka T, Hobbs ML, Tucker SL, et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 2005;11:4912-22. (Pubitemid 41557212)
18. Fertil B, Dertinger H, Courdi A, Malaise EP. Mean inactivation dose: a useful concept for intercomparison of human cell survival curves. Radiat Res 1984;99:73-84. (Pubitemid 14095136)
19. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 2004;6:443-50. (Pubitemid 38607505)
20. Sedelnikova OA, Pilch DR, Redon C, Bonner WM. Histone H2AX in DNA damage and repair. Cancer Biol Ther 2003;2:233-5.
21. Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem 2004;279:2273-80. (Pubitemid 38084500)
22. Bromfield GP, Meng A, Warde P, Bristow RG. Cell death in irradiated prostate epithelial cells: role of apoptotic and clonogenic cell kill. Prostate Cancer Prostatic Dis 2003;6:73-85. (Pubitemid 36432625)
23. Noh EJ, Lee JS. Functional interplay between modulation of histone deacetylase activity and its regulatory role in G2-M transition. Biochem Biophys Res Commun 2003;310:267-73. (Pubitemid 37163659)
24. Rosato RR, Almenara JA, Yu C, Grant S. Evidence of a functional role for p21WAF1/CIP1 down-regulation in synergistic antileukemic interactions between the histone deacetylase inhibitor sodium butyrate and flavopiridol. Mol Pharmacol 2004;65:571-81. (Pubitemid 38264024)
25. Rashid SF, Moore JS, Walker E, Driver PM, Engel J, Edwards CE, et al. Synergistic growth inhibition of prostate cancer cells by 1 alpha,25- Dihydroxyvitamin D(3) and its 19-nor-hexafluoride analogs in combination with either sodium butyrate or trichostatin A. Oncogene 2001;20:1860-72. (Pubitemid 32458696)
26. Orrenius S. Mitochondrial regulation of apoptotic cell death. Toxicol Lett 2004;149:19-23. (Pubitemid 38469816)
27. Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem 2004;73:87-106. (Pubitemid 39050364)
28. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 2005;62:223-9. (Pubitemid 40591946)
29. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004;303: 1010-4. (Pubitemid 38209704)
30. Mihara M, Moll UM. Detection of mitochondrial localization of p53. Methods Mol Biol 2003;234:203-9.
31. Wendt J, von Haefen C, Hemmati P, Belka C, Dorken B, Daniel PT. TRAIL sensitizes for ionizing irradiation-induced apoptosis through an entirely Bax-dependent mitochondrial cell death pathway. Oncogene 2005;24:4052-64. (Pubitemid 40897052)
32. Isaacs WB, Carter BS, Ewing CM. Wild-type p53 suppresses growth of human prostate cancer cells containing mutant p53 alleles. Cancer Res 1991;51:4716-20.
33. Roy S, Tenniswood M. Site-specific acetylation of p53 directs selective transcription complex assembly. J Biol Chem 2007;282: 4765-71. (Pubitemid 47100922)
34. Tang Y, Luo J, Zhang W, Gu W. Tip60-dependent acetylation of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol Cell 2006;24:827-39. (Pubitemid 44960094)
35. Sykes SM, Stanek TJ, Frank A, Murphy ME, McMahon SB. Acetylation of the DNA binding domain regulates transcription-independent apoptosis by p53. J Biol Chem 2009;284:20197-205.
36. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS, et al. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol Cell 2006;24:841-51. (Pubitemid 44960096)
37. Chen X, Wong P, Radany E, Wong JY. HDAC inhibitor, valproic acid, induces p53-dependent radiosensitization of colon cancer cells. Cancer Biother Radiopharm 2009;24:689-99.
38. Kim IA, Shin JH, Kim IH, Kim JH, Kim JS, Wu HG, et al. Histone deacetylase inhibitor-mediated radiosensitization of human cancer cells: class differences and the potential influence of p53. Clin Cancer Res 2006;12:940-9. (Pubitemid 43259877)
39. Haupt S, Berger M, Goldberg Z, Haupt Y. Apoptosis-the p53 network. J Cell Sci 2003;116:4077-85.
40. Norbury CJ, Zhivotovsky B. DNA damage-induced apoptosis. Oncogene 2004;23:2797-808. (Pubitemid 38638843)
41. Sarkaria JN, Eshleman JS. ATM as a target for novel radiosensitizers. Semin Radiat Oncol 2001;11:316-27. (Pubitemid 32959666)
42. Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys 2004;59:928-42. (Pubitemid 38834285)
43. Hostanska K, Vuong V, Rocha S, Soengas MS, Glanzmann C, Saller R, et al. Recombinant mistletoe lectin induces p53-independent apoptosis in tumour cells and cooperates with ionising radiation. Br J Cancer 2003;88:1785-92. (Pubitemid 36760425)
44. Manfredi JJ. p53 and apoptosis: it's not just in the nucleus anymore. Mol Cell 2003;11:552-4. (Pubitemid 36385111)
45. Chipuk JE, Green DR. Cytoplasmic p53: Bax and forward. Cell Cycle 2004;3:429-31. (Pubitemid 40278229)
46. Bykov VJ, Issaeva N, Shilov A, Hultcrantz M, Pugacheva E, Chumakov P, et al. Restoration of the tumor suppressor function to mutant p53 by a low-molecular-weight compound. Nat Med 2002;8:282-8. (Pubitemid 34250107)
47. Yamaguchi H, Woods NT, Piluso LG, Lee HH, Chen J, Bhalla KN, et al. p53 acetylation is crucial for its transcription-independent proapoptotic functions. J Biol Chem 2009;284:11171-83.
48. Rakozy C, Grignon DJ, Li Y, Gheiler E, Gururajanna B, Pontes JE, et al. p53 gene alterations in prostate cancer after radiation failure and their association with clinical outcome: a molecular and immunohistochemical analysis. Pathol Res Pract 1999;195:129-35. (Pubitemid 29142209)
49. MacGrogan D, Bookstein R. Tumour suppressor genes in prostate cancer. Semin Cancer Biol 1997;8:11-9. (Pubitemid 27417425)
50. Prendergast NJ, Atkins MR, Schatte EC, Paulson DF, Walther PJ. p53 immunohistochemical and genetic alterations are associated at high incidence with post-irradiated locally persistent prostate carcinoma. J Urol 1996;155:1685-92. (Pubitemid 26126976)
51. Luo J, Li M, Tang Y, Laszkowska M, Roeder RG, Gu W. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc Natl Acad Sci U S A 2004;101:2259-64. (Pubitemid 38269299)
52. Liu L, Scolnick DM, Trievel RC, Zhang HB, Marmorstein R, Halazonetis TD, et al. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol 1999;19:1202-9. (Pubitemid 29046862)
53. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, Vassilev A, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev 1998;12:2831-41. (Pubitemid 28440142)
54. Jin Y, Zeng SX, Lee H, Lu H. MDM2 mediates p300/CREB-binding protein-associated factor ubiquitination and degradation. J Biol Chem 2004;279:20035-43. (Pubitemid 38623447)
55. Zhang S, Cao HJ, Davis FB, Tang HY, Davis PJ, Lin HY. Oestrogen inhibits resveratrol-induced post-translational modification of p53 and apoptosis in breast cancer cells. Br J Cancer 2004;91: 178-85. (Pubitemid 39013062)
56. Fu M, Wang C, Zhang X, Pestell RG. Acetylation of nuclear receptors in cellular growth and apoptosis. Biochem Pharmacol 2004;68:1199-208. (Pubitemid 39094285)
57. Vaghefi H, Neet KE. Deacetylation of p53 after nerve growth factor treatment in PC12 cells as a post-translational modification mechanism of neurotrophin-induced tumor suppressor activation. Oncogene 2004;23:8078-87. (Pubitemid 39531848)
58. Luo J, Su F, Chen D, Shiloh A, Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 2000; 408:377-81.
59. Li M, Luo J, Brooks CL, Gu W. Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 2002;277:50607-11. (Pubitemid 36042220)
60. Nakamura S, Roth JA, Mukhopadhyay T. Multiple lysine mutations in the C-terminal domain of p53 interfere with MDM2-dependent protein degradation and ubiquitination. Mol Cell Biol 2000;20:9391-8. (Pubitemid 32246123)
61. Zhao Y, Lu S, Wu L, Chai G, Wang H, Chen Y, et al. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 2006;26:2782-90.
62. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 2003;300:342-4.
63. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008;133:612-26. (Pubitemid 351636297)
64. Mellert HS, Stanek TJ, Sykes SM, Rauscher FJ III, Schultz DC, McMahon SB. Deacetylation of the DNA-binding domain regulates p53-mediated apoptosis. J Biol Chem 2011;286:4264-70.
65. Devi GR. XIAP as target for therapeutic apoptosis in prostate cancer. Drug News Perspect 2004;17:127-34. (Pubitemid 38568410)
66. Kaufmann SH, Vaux DL. Alterations in the apoptotic machinery and their potential role in anticancer drug resistance. Oncogene 2003; 22:7414-30. (Pubitemid 37487167)