HDAC1 inhibition by maspin abrogates epigenetic silencing of glutathione S-transferase Pi in prostate carcinoma cells

Molecular Cancer Research

Volumn 9, Issue 6, 2011, Pages 733-745

  Li, Xiaohua ^a   Kaplun, Alexander ^a   Lonardo, Fulvio ^a   Heath, Elisabeth ^a   Sarkar, Fazlul H ^a   Irish, Jonathan ^a   Sakr, Wael ^a   Sheng, Shijie ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; GLUTATHIONE TRANSFERASE P1; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITOR; HISTONE H2A; HISTONE H3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; M 344; MASPIN; METHYL CPG BINDING PROTEIN; METHYLTRANSFERASE; PANOBINOSTAT; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; DNA METHYLATION; DRUG SENSITIVITY; ENZYME INHIBITION; EPIGENETICS; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CARCINOMA; PROTEIN EXPRESSION; WESTERN BLOTTING;

CARCINOMA; CELL LINE, TUMOR; CELL SURVIVAL; GENE SILENCING; GLUTATHIONE S-TRANSFERASE PI; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MALE; PROSTATIC NEOPLASMS; SERPINS;

EID: 79959257557     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0505     Document Type: Article

References (74)

1. Ou JN, Torrisani J, Unterberger A, Provençal N, Shikimi K, Karimi M, et al. Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem Pharmacol 2007;73:1297-307. (Pubitemid 46452588)
2. Singal R, van Wert J, Bashambu M. Cytosine methylation represses glutathione S-transferase P1 (GSTP1) gene expression in human prostate cancer cells. Cancer Res 2001;61:4820-6. (Pubitemid 32691897)
3. Halkidou K, Gaughan L, Cook S, Leung HY, Neal DE, Robson CN, et al. Upregulation and nuclear recruitment of HDAC1 in hormone refractory prostate cancer. Prostate 2004;59:177-89. (Pubitemid 38481229)
4. Choi JH, Kwon HJ, Yoon BI, Kim JH, Han SU, Joo HJ, et al. Expression profile of histone deacetylase 1 in gastric cancer tissues. Jpn J Cancer Res 2001;92:1300-4. (Pubitemid 34036893)
5. Fitzpatrick PA, Wong DT, Barr PJ, Pemberton PA. Functional implications of the modeled structure of maspin. Protein Eng 1996;9:585-9. (Pubitemid 26241635)
6. Pemberton PA, Wong DT, Gibson HL, Kiefer MC, Fitzpatrick PA, Sager R, et al. The tumor suppressor maspin does not undergo the stressed to relaxed transition or inhibit trypsin-like serine proteases. Evidence that maspin is not a protease inhibitory serpin. J Biol Chem 1995;270:15832-7.
7. Law RH, Irving JA, Buckle AM, Ruzyla K, Buzza M, Bashtannyk-Puhalovich TA, et al. The high resolution crystal structure of the human tumor suppressor maspin reveals a novel conformational switch in the G-helix. J Biol Chem 2005;280:22356-64. (Pubitemid 40827892)
8. Emiliani S, Fischle W, Van Lint C, Al-Abed Y, Verdin E. Characterization of a human RPD3 ortholog, HDAC3. Proc Natl Acad Sci U S A 1998;95:2795-800.
9. Mai A, Massa S, Ragno R, Esposito M, Sbardella G, Nocca G, et al. Binding mode analysis of 3-(4-benzoyl-1-methyl-1H-2-pyrrolyl)-N-hydroxy-2-propenamide: a new synthetic histone deacetylase inhibitor inducing histone hyperacetylation, growth inhibition, and terminal cell differentiation. J Med Chem 2002;45:1778-84. (Pubitemid 34415373)
10. Hassig CA, Tong JK, Fleischer TC, Owa T, Grable PG, Ayer DE, et al. A role for histone deacetylase activity in HDAC1-mediated transcriptional repression. Proc Natl Acad Sci U S A 1998;95:3519-24. (Pubitemid 28173160)
11. Archer SY, Meng S, Shei A, Hodin RA. p21(WAF1) is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc Natl Acad Sci U S A 1998;95:6791-6.
12. Juan LJ, Shia WJ, Chen MH, Yang WM, Seto E, Lin YS, et al. Histone deacetylases specifically down-regulate p53-dependent gene activation. J Biol Chem 2000;275:20436-43. (Pubitemid 30457621)
13. Cher ML, Biliran HR, Bhagat S, Meng Y, Che M, Lockett J, et al. Maspin expression inhibits osteolysis, tumor growth, and angiogenesis in a model of prostate cancer bone metastasis. Proc Natl Acad Sci U S A 2003;100:7847-52. (Pubitemid 36760058)
14. Bailey CM, Khalkhali-Ellis Z, Seftor EA, Hendrix MJ. Biological functions of maspin. J Cell Physiol 2006;209:617-24. (Pubitemid 44665678)
15. Li X, Yin S, Meng Y, Sakr W, Sheng S. Endogenous inhibition of histone deacetylase 1 by tumor-suppressive maspin. Cancer Res 2006;66:9323-9. (Pubitemid 44521155)
16. Yin S, Li X, Meng Y, Finley RL Jr, Sakr W, Yang H, et al. Tumor-suppressive maspin regulates cell response to oxidative stress by direct interaction with glutathione S-transferase. J Biol Chem 2005;280:34985-96. (Pubitemid 41504634)
17. Frey A, Soubani AO, Adam AK, Sheng S, Pass HI, Lonardo F, et al. Nuclear, compared with combined nuclear and cytoplasmic expression of maspin, is linked in lung adenocarcinoma to reduced VEGF-A levels and in Stage I, improved survival. Histopathology 2009;54:590-7.
18. Lonardo F, Li X, Siddiq F, Singh R, Al-Abbadi M, Pass HI, et al. Maspin nuclear localization is linked to favorable morphological features in pulmonary adenocarcinoma. Lung Cancer 2006;51:31-9. (Pubitemid 43088622)
19. Pandey M, Shukla S, Gupta S. Promoter demethylation and chromatin remodeling by green tea polyphenols leads to re-expression of GSTP1 in human prostate cancer cells. Int J Cancer 2010;126:2520-33.
20. Samuni Y, Flores-Santana W, Krishna MC, Mitchell JB, Wink DA. The inhibitors of histone deacetylase suberoylanilide hydroxamate and trichostatin A release nitric oxide upon oxidation. Free Radic Biol Med 2009;47:419-23.
21. Lee WH, Morton RA, Epstein JI, Brooks JD, Campbell PA, Bova GS, et al. Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis. Proc Natl Acad Sci U S A 1994;91:11733-7. (Pubitemid 24356419)
22. Pierson CR, McGowen R, Grignon D, Sakr W, Dey J, Sheng S, et al. Maspin is up-regulated in premalignant prostate epithelia. Prostate 2002;53:255-62. (Pubitemid 35398496)
23. Nakayama M, Bennett CJ, Hicks JL, Epstein JI, Platz EA, Nelson WG, et al. Hypermethylation of the human glutathione S-transferase-pi gene (GSTP1) CpG island is present in a subset of proliferative inflammatory atrophy lesions but not in normal or hyperplastic epithelium of the prostate: a detailed study using laser-capture microdissection. Am J Pathol 2003;163:923-33. (Pubitemid 37040128)
24. Parsons JK, Nelson CP, Gage WR, Nelson WG, Kensler TW, De Marzo AM, et al. GSTA1 expression in normal, preneoplastic, and neoplastic human prostate tissue. Prostate 2001;49:30-7.
25. Jung M, Brosch G, Kölle D, Scherf H, Gerhäuser C, Loidl P, et al. Amide analogues of trichostatin A as inhibitors of histone deacetylase and inducers of terminal cell differentiation. J Med Chem 1999;42:4669-79. (Pubitemid 29530020)
26. Li X, Chen BD. Histone deacetylase inhibitor M344 inhibits cell proliferation and induces apoptosis in human THP-1 leukemia cells. Am J Biomed Sci 2009;1:352-63.
27. Biliran H Jr, Sheng S. Pleiotrophic inhibition of pericellular urokinase-type plasminogen activator system by endogenous tumor suppressive maspin. Cancer Res 2001;61:8676-82. (Pubitemid 34013876)
28. Jung KK, Liu XW, Chirco R, Fridman R, Kim HR. Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J 2006;25:3934-42. (Pubitemid 44338736)
29. Okino ST, Pookot D, Majid S, Zhao H, Li LC, Place RF, et al. Chromatin changes on the GSTP1 promoter associated with its inactivation in prostate cancer. Mol Carcinog 2007;46:839-46. (Pubitemid 47549769)
30. Haskill S, Peace A, Morris J, Sporn SA, Anisowicz A, Lee SW, et al. Identification of three related human GRO genes encoding cytokine functions. Proc Natl Acad Sci U S A 1990;87:7732-6. (Pubitemid 20341791)
31. Zou Z, Anisowicz A, Hendrix MJ, Thor A, Neveu M, Sheng S, et al. Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 1994;263:526-9. (Pubitemid 24082753)
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8. (Pubitemid 34164012)
33. Bryzgunova OE, Morozkin ES, Yarmoschuk SV, Vlassov VV, Laktionov PP. Methylation-specific sequencing of GSTP1 gene promoter in circulating/ extracellular DNA from blood and urine of healthy donors and prostate cancer patients. Ann N Y Acad Sci 2008;1137:222-5.
34. Rand K, Qu W, Ho T, Clark SJ, Molloy P. Conversion-specific detection of DNA methylation using real-time polymerase chain reaction (ConLight-MSP) to avoid false positives. Methods 2002;27:114-20. (Pubitemid 34757121)
35. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, et al. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res 2000;28:E32.
36. Lin X, Nelson WG. Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 breast cancer cells. Cancer Res 2003;63:498-504. (Pubitemid 36152513)
37. Kobayashi H, Tan EM, Fleming SE. Acetylation of histones associated with the p21WAF1/CIP1 gene by butyrate is not sufficient for p21WAF1/CIP1 gene transcription in human colorectal adenocarcinoma cells. Int J Cancer 2004;109:207-13. (Pubitemid 38240922)
38. Domann FE, Rice JC, Hendrix MJ, Futscher BW. Epigenetic silencing of maspin gene expression in human breast cancers. Int J Cancer 2000;85:805-10. (Pubitemid 30131470)
39. Millar DS, Ow KK, Paul CL, Russell PJ, Molloy PL, Clark SJ, et al. Detailed methylation analysis of the glutathione S-transferase pi (GSTP1) gene in prostate cancer. Oncogene 1999;18:1313-24. (Pubitemid 29094883)
40. Hurtubise A, Momparler RL. Evaluation of antineoplastic action of 5-aza-2′-deoxycytidine (Dacogen) and docetaxel (Taxotere) on human breast, lung and prostate carcinoma cell lines. Anticancer Drugs 2004;15:161-7. (Pubitemid 38316750)
41. Lee WH, Isaacs WB, Bova GS, Nelson WG. CG island methylation changes near the GSTP1 gene in prostatic carcinoma cells detected using the polymerase chain reaction: a new prostate cancer biomarker. Cancer Epidemiol Biomarkers Prev 1997;6:443-50. (Pubitemid 27270550)
42. Ghoshal K, Datta J, Majumder S, Bai S, Dong X, Parthun M, et al. Inhibitors of histone deacetylase and DNA methyltransferase synergistically activate the methylated metallothionein I promoter by activating the transcription factor MTF-1 and forming an open chromatin structure. Mol Cell Biol 2002;22:8302-19. (Pubitemid 35304062)
43. Tan CP, Nakielny S. Control of the DNA methylation system component MBD2 by protein arginine methylation. Mol Cell Biol 2006;26:7224-35. (Pubitemid 44477698)
44. Jiang N, Meng Y, Zhang S, Mensah-Osman E, Sheng S. Maspin sensitizes breast carcinoma cells to induced apoptosis. Oncogene 2002;21:4089-98. (Pubitemid 34712876)
45. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, et al. Regulation of JNK signaling by GSTp. EMBO J 1999;18:1321-34. (Pubitemid 29110316)
46. Li X, Chen D, Yin S, Meng Y, Yang H, Landis-Piwowar KR, et al. Maspin augments proteasome inhibitor-induced apoptosis in prostate cancer cells. J Cell Physiol 2007;212:298-306. (Pubitemid 47025618)
47. Murakami J, Asaumi J, Maki Y, Tsujigiwa H, Kuroda M, Nagai N, et al. Effects of demethylating agent 5-aza-2(′)-deoxycytidine and histone deacetylase inhibitor FR901228 on maspin gene expression in oral cancer cell lines. Oral Oncol 2004;40:597-603. (Pubitemid 38452679)
48. Yamaguchi H, Ding Y, Lee JF, Zhang M, Pal A, Bornmann W, et al. Interferon-inducible protein IFIXalpha inhibits cell invasion by upregulating the metastasis suppressor maspin. Mol Carcinog 2008;47:739-43.
49. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306-9. (Pubitemid 20066716)
50. Liu J, Yin S, Reddy N, Spencer C, Sheng S. Bax mediates the apoptosis-sensitizing effect of maspin. Cancer Res 2004;64:1703-11. (Pubitemid 38428692)
51. Di Padova M, Bruno T, De Nicola F, Iezzi S, D'Angelo C, Gallo R, et al. Che-1 arrests human colon carcinoma cell proliferation by displacing HDAC1 from the p21WAF1/CIP1 promoter. J Biol Chem 2003;278:36496-504. (Pubitemid 37139979)
52. Kim YB, Lee KH, Sugita K, Yoshida M, Horinouchi S. Oxamflatin is a novel antitumor compound that inhibits mammalian histone deacetylase. Oncogene 1999;18:2461-70. (Pubitemid 29206159)
53. Pettazzoni P, Pizzimenti S, Toaldo C, Sotomayor P, Tagliavacca L, Liu S, et al. Induction of cell cycle arrest and DNA damage by the HDAC inhibitor panobinostat (LBH589) and the lipid peroxidation end product 4-hydroxynonenal in prostate cancer cells. Free Radic Biol Med 2011;50:313-22.
54. Gahr S, Peter G, Wissniowski TT, Hahn EG, Herold C, Ocker M, et al. The histone-deacetylase inhibitor MS-275 and the CDK-inhibitor CYC-202 promote anti-tumor effects in hepatoma cell lines. Oncol Rep 2008;20:1249-56.
55. Futscher BW, Oshiro MM, Wozniak RJ, Holtan N, Hanigan CL, Duan H, et al. Role for DNA methylation in the control of cell type specific maspin expression. Nat Genet 2002;31:175-9.
56. Marioni G, Blandamura S, Giacomelli L, Calgaro N, Segato P, Leo G, et al. Nuclear expression of maspin is associated with a lower recurrence rate and a longer disease-free interval after surgery for squamous cell carcinoma of the larynx. Histopathology 2005;46:576-82. (Pubitemid 40632315)
57. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, et al. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002;31:141-9.
58. Cameron EE, Bachman KE, Myöhänen S, Herman JG, Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999;21:103-7. (Pubitemid 29036293)
59. Jenuwein T, Allis CD. Translating the histone code. Science 2001;293:1074-80. (Pubitemid 32758077)
60. Rice JC, Allis CD. Code of silence. Nature 2001;414:258-61. (Pubitemid 33097787)
61. Sims RJ III, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet 2003;19:629-39. (Pubitemid 37338383)
62. Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T, et al. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 2004;6:73-7. (Pubitemid 38425733)
63. Kim A, Dean A. Developmental stage differences in chromatin subdomains of the beta-globin locus. Proc Natl Acad Sci U S A 2004;101:7028-33. (Pubitemid 38596437)
64. Metzger E, Wissmann M, Yin N, Müller JM, Schneider R, Peters AH, et al. LSD1 demethylates repressive histone marks to promote androgen-receptor- dependent transcription. Nature 2005;437:436-9. (Pubitemid 41613508)
65. Forneris F, Binda C, Dall'Aglio A, Fraaije MW, Battaglioli E, Mattevi A, et al. A highly specific mechanism of histone H3-K4 recognition by histone demethylase LSD1. J Biol Chem 2006;281:35289-95. (Pubitemid 46036567)
66. Omisanjo OA, Biermann K, Hartmann S, Heukamp LC, Sonnack V, Hild A, et al. DNMT1 and HDAC1 gene expression in impaired spermatogenesis and testicular cancer. Histochem Cell Biol 2007;127:175-81. (Pubitemid 46147271)
67. Lockett J, Yin S, Li X, Meng Y, Sheng S. Tumor suppressive maspin and epithelial homeostasis. J Cell Biochem 2006;97:651-60.
68. Zheng HC, Saito H, Masuda S, Wang ZG, Takano Y. Cytoplasmic and nuclear maspin expression in lung carcinomas: an immunohistochemical study using tissue microarrays. Appl Immunohistochem Mol Morphol 2008;16:459-65.
69. Perquin M, Oster T, Maul A, Froment N, Untereiner M, Bagrel D, et al. The glutathione-related detoxification pathway in the human breast: a highly coordinated system disrupted in the tumour tissues. Cancer Lett 2000;158:7-16. (Pubitemid 30625225)
70. Townsend DM, Manevich Y, He L, Hutchens S, Pazoles CJ, Tew KD. Novel role for glutathione S-transferase pi. Regulator of protein S-Glutathionylation following oxidative and nitrosative stress. J Biol Chem 2009;284:436-45.
71. Cui H, Shen J, Lu D, Zhang T, Zhang W, Sun D, et al. 4-Aryl-1,3,2- oxathiazolylium-5-olate: a novel GST inhibitor to release JNK and activate c-Jun for cancer therapy. Cancer Chemother Pharmacol 2008;62:509-15.
72. Lu GD, Shen HM, Chung MC, Ong CN. Critical role of oxidative stress and sustained JNK activation in aloe-emodin-mediated apoptotic cell death in human hepatoma cells. Carcinogenesis. 2007;28:1937-45. (Pubitemid 47500606)
73. Brotherick I, Shenton BK, Egan M, Cunliffe WE, Browell DA, Lunt LG, et al. Examination of multidrug resistance in cell lines and primary breast tumours by flow cytometry. Eur J Cancer 1996;32A:2334-41.
74. van Brussel JP, van Steenbrugge GJ, Romijn JC, Schröder FH, Mickisch GH. Chemosensitivity of prostate cancer cell lines and expression of multidrug resistance-related proteins. Eur J Cancer 1999;35:664-71. (Pubitemid 29192979)