Plant HDAC inhibitor chrysin arrest cell growth and induce p21 WAF1 by altering chromatin of STAT response element in A375 cells

详细信息    查看全文

• 作者：Manika Pal-Bhadra (1)
  M Janaki Ramaiah (1) (2)
  T Lakshminarayan Reddy (1)
  Anita Krishnan (1) (2)
  SNCVL Pushpavalli (1)
  K Suresh Babu (3)
  Ashok K Tiwari (4)
  J Madhusudana Rao (3)
  Jhillu S Yadav (1)
  Utpal Bhadra (2)
  
• 关键词：HDAC ; 8 ; Chrysin ; A375 cells ; HDAC inhibitor ; p21WAF1 ; Cell cycle arrest ; p21 promoter ; STAT ; Apoptosis
• 刊名：BMC Cancer
• 出版年：2012
• 出版时间：December 2012
• 年：2012
• 卷：12
• 期：1
• 全文大小：1897KB
• 参考文献：1. Peltonen K, Kiviharju TM, J?rvinen PM, Ra R, Laiho M: plus-plus">Melanoma cell lines are susceptible to histone deacetylase inhibitor TSA provoked cell cycle arrest and apoptosis. / Pigment Cell Res 2005, plus-plus">18:196-02. p://dx.doi.org/10.1111/j.1600-0749.2005.00225.x">CrossRef
  2. Boyle GM, Martyn AC, Parsons PG: plus-plus">Histone deacetylase inhibitors and malignant melanoma. / Pigment Cell Res 2005, plus-plus">18:160-66. p://dx.doi.org/10.1111/j.1600-0749.2005.00228.x">CrossRef
  3. Gray SG, Teh BT: plus-plus">Histone acetylation/deacetylation and cancer: an "open" and "shut" case? / Curr Mol Med 2001, plus-plus">1:401-29. p://dx.doi.org/10.2174/1566524013363537">CrossRef
  4. Gibbons RJ: plus-plus">Histone modifying and chromatin remodelling enzymes in cancer and dysplastic syndromes. / Hum Mol Genet 2005, plus-plus">14:85-2. p://dx.doi.org/10.1093/hmg/ddi106">CrossRef
  5. Espino PS, Drobic B, Dunn KL, Davie JR: plus-plus">Histone modifications as a platform for cancer therapy. / J Cell Biochem 2005, plus-plus">94:1088-102. p://dx.doi.org/10.1002/jcb.20387">CrossRef
  6. Yang XJ, Seto E: plus-plus">HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. / Oncogene 2007, plus-plus">26:5310-318. p://dx.doi.org/10.1038/sj.onc.1210599">CrossRef
  7. De ruijter A, Van Gennio A, Caron H, Kemp S, Van kuilenburg A: plus-plus">Histone deacetylases: Characterization of the classical HDAC family. / Biochem J 2002, plus-plus">370:737-49. p://dx.doi.org/10.1042/BJ20021321">CrossRef
  8. Khochbin S, Verdel A, Lemercier C, Seigneurin-Berny D: plus-plus">Functional significance of histone deacetylase diversity. / Curr Opin Genet Dev 2001, plus-plus">11:162-66. p://dx.doi.org/10.1016/S0959-437X(00)00174-X">CrossRef
  9. Marks PA, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK: plus-plus">Histone deacetylases and cancer: causes and therapies. / Nat Rev Cancer 2001, plus-plus">1:194-02. p://dx.doi.org/10.1038/35106079">CrossRef
  10. Roth SY, Denu JM, Allis CD: plus-plus">Histone acetyltransferases. / Annu Rev Biochem 2001, plus-plus">70:81-20. p://dx.doi.org/10.1146/annurev.biochem.70.1.81">CrossRef
  11. Marks PA, Richon VM, Miller T, Kelly WK: plus-plus">Histone deacetylase inhibitors. / Adv Cancer Res 2004, plus-plus">91:137-68. p://dx.doi.org/10.1016/S0065-230X(04)91004-4">CrossRef
  12. Turner BM: plus-plus">Histone acetylation and an epigenetic code. / BioEssays 2000, plus-plus">22:836-45. p://dx.doi.org/10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X">CrossRef
  13. Richon VM, Sandhoff TW, Rifkind RA, Marks PA: plus-plus">Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. / Proc Natl Acad Sci USA 2000, plus-plus">97:10014-0019. p://dx.doi.org/10.1073/pnas.180316197">CrossRef
  14. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA: plus-plus">Histone deacetylase (HDAC) inhibitor activation of p21 WAF1involves changes in promoter-associated proteins, including HDAC1. / Proc Natl Acad Sci USA 2004, plus-plus">101:1241-246. p://dx.doi.org/10.1073/pnas.0307708100">CrossRef
  15. Gavin DP, Kartan S, Chase K, Jayaraman S, Sharma RP: plus-plus">Histone deacetylase inhibitors and candidate gene expression: An invivo and invitro approach to studying chromatin remodeling in a clinical population. / J Psychiatr Res 2009, plus-plus">43:870-76. p://dx.doi.org/10.1016/j.jpsychires.2008.12.006">CrossRef
  16. Jenuwein T, Allis CD: plus-plus">Translating the histone code. / Science 2001, plus-plus">293:1074-080. p://dx.doi.org/10.1126/science.1063127">CrossRef
  17. Agalioti T, Chen G, Thanos D: plus-plus">Deciphering the transcriptional histone acetylation code for a human gene. / Cell 2002, plus-plus">111:381-92. p://dx.doi.org/10.1016/S0092-8674(02)01077-2">CrossRef
  18. Lin YC, Lin JH, Chou CW, Chang YF, Yeh SH, Chen CC: plus-plus">Statins increase p21 through inhibition of histone deacetylase activity and release of promoter-associated HDAC-1/2. / Cancer Res 2008, plus-plus">68:2375-383. p://dx.doi.org/10.1158/0008-5472.CAN-07-5807">CrossRef
  19. Battle TE, Frank DA: plus-plus">The role of STATs in apoptosis. / Curr Mol Med 2002,plus-plus">2(4)plus-plus">:381-92. p://dx.doi.org/10.2174/1566524023362456">CrossRef
  20. Stephanou A, Latchman DS: plus-plus">Opposing actions of STAT-1 and STAT-3. / Growth Factors 2005,plus-plus">23(3)plus-plus">:177-82. p://dx.doi.org/10.1080/08977190500178745">CrossRef
  21. Kim HS, Lee MS: plus-plus">STAT1 as a key modulator of cell death. / Cell Signal 2007,plus-plus">19(3)plus-plus">:454-65. p://dx.doi.org/10.1016/j.cellsig.2006.09.003">CrossRef
  22. Middleton E, Kandaswami C, Theoharides TC: plus-plus">The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. / Pharmacol Rev 2000,plus-plus">52(4)plus-plus">:673-51.
  23. Chang H, Mi M, Ling W, Zhu J, Zhang Q, Wei N, Zhou Y, Tang Y, Yuan J: plus-plus">Structurally related cytotoxic effects of flavonoids on human cancer cells in vitro. / Arch Pharm Res 2008,plus-plus">31(9)plus-plus">:1137-144. p://dx.doi.org/10.1007/s12272-001-1280-8">CrossRef
  24. Androutsopoulos VP, Papakyriakou A, Vourloumis D, Spandidos DA: plus-plus">Comparative CYP1A1 and CYP1B1 substrate and inhibitor profile of dietary flavonoids. / Bioorg Med Chem 2011,plus-plus">19(9)plus-plus">:2842-849. p://dx.doi.org/10.1016/j.bmc.2011.03.042">CrossRef
  25. Gan YH, Zhang S: plus-plus">PTEN/AKT pathway involved in histone deacetylases inhibitor induced cell growth inhibition and apoptosis of oral squamous cell carcinoma cells. / Oral Oncol 2009,plus-plus">45(10)plus-plus">:e150-e154. p://dx.doi.org/10.1016/j.oraloncology.2009.05.563">CrossRef
  26. Huang WJ, Liang YC, Chuang SE, Chi LL, Lee CY, Lin CW, Chen AL, Huang JS, Chiu CJ, Lee CF, Huang CY, Chen CN: plus-plus">NBM-HD-1: A Novel histone deacetylase inhibitor with anti-cancer activity. / Evid Based Complement Alternat Med 2011, plus-plus">2012:781417. 2012
  27. Hantz H, Lee K, Bjeldanes L: plus-plus">3, 3-Diindolylmethane inhibits activation of Akt through inhibition of hepatocyte growth factor receptor c-Met signaling. / Cancer Res 2009,plus-plus">69(24)plus-plus">:6117. p://dx.doi.org/10.1158/0008-5472.SABCS-09-6117">CrossRef
  28. Li Y, Li X, Guo B: plus-plus">Chemopreventive agent 3, 3-diindolyl methane selectively induces proteasomal degradation of class I histone deacetylases. / Cancer Res 2010,plus-plus">70(2)plus-plus">:646-4. p://dx.doi.org/10.1158/0008-5472.CAN-09-1924">CrossRef
  29. Woo KJ, Jeong YJ, Park JW, Kwan TK: plus-plus">Chrysin-induced apoptosis is mediated through caspase activation and Akt-inactivation in U937 leukemia cells. / Biochem Biophys Res Commun 2004, plus-plus">325:1215-222. p://dx.doi.org/10.1016/j.bbrc.2004.09.225">CrossRef
  30. Khoo BY, Chua SL, Balaram P: plus-plus">Apoptotic effects of chrysin in human cancer cell lines. / Int J Mol Sci 2010, plus-plus">11:2188-199. p://dx.doi.org/10.3390/ijms11052188">CrossRef
  31. Shen CC, Chang YS, Ho LK: plus-plus">Nuclear magnetic resonance studies of 5,7-Dihydroxyflavonoids. / Phytochemistry 1993, plus-plus">34:843-45. p://dx.doi.org/10.1016/0031-9422(93)85370-7">CrossRef
  32. Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG, Davidsen SK: plus-plus">Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. / Mol Cancer Ther 2003, plus-plus">2:151-63. p://dx.doi.org/10.4161/cbt.2.2.349">CrossRef
  33. Pandey M, Kaur P, Shukla S, Abbas A, Fu P, Gupta S: plus-plus">Plant flavone Apigenin inhibits HDAC and remodels chromatin to induce growth arrest and apoptosis in human prostate cancer cells: Invitro and Invivo study. / Mol Carcinog 2011.
  34. Kalita A, Maroun C, Bonfils C, Glemon K, Siu LL, Tolcher A, Carducci M, Besterman JM, Reid GK, Li Z: plus-plus">Pharmacodynamic effect of MGCD0103, an oral isotype selective histone deacetylase ( HDAC) inhibitor, on HDAC enzyme inhibition and histone acetylation induction in phase I clinical trials in patients (pts) with advanced solid tumors or non-Hodgkin’s lymphoma ( NHL). / J Clin Oncol 2005, plus-plus">23:9631.
  35. Cai K, Dynlacht BD: plus-plus">Activity and nature of p21 WAF1 complexes during the cell cycle. / Proc Natl Acad Sci USA 1998, plus-plus">95:12254-. p://dx.doi.org/10.1073/pnas.95.21.12254">CrossRef
  36. Chopin V, Toillon RA, Jouy N, LeBourhis X: plus-plus">P21 WAF1/CIP1 is dispensable for G1 arrest, but indispensable for apoptosis induced by sodium butyrate in MCF-7 breast cancer cells. / Oncogene 2004, plus-plus">23:21-9. p://dx.doi.org/10.1038/sj.onc.1207020">CrossRef
  37. Jin M, Zhao W, Zhang Y, Kobayashi M, Duan H, Kong D: plus-plus">Anti-proliferative effect of Aaptamine on human chronic myeloid leukemia K562 cells. / Int J Mol Sci 2011, plus-plus">12:7352-359. p://dx.doi.org/10.3390/ijms12117352">CrossRef
  38. Agarwal S, Agarwal ML, Chatterjee-kishore M, Stark GR, Chisolm GM: plus-plus">Stat-1 dependent p53-independent expression of p21 (waf1) modulates oxysterol- induced apoptosis. / Mol Cell Biol 2002,plus-plus">22(7)plus-plus">:1981-2. p://dx.doi.org/10.1128/MCB.22.7.1981-1992.2002">CrossRef
  39. Gong Y, Yue J, Wu X, Wang X, Wen J, Lu L, Peng X, Qiang B, Yuan J: plus-plus">NSPc1 is a cell growth regulator that acts as a transcriptional repressor of p21Waf1/Cip1 via the RARE element. / Nucleic Acids Res 2006, plus-plus">34:6158-169. p://dx.doi.org/10.1093/nar/gkl834">CrossRef
  40. Kr?mer OH, Baus D, Knauer SK, Stein S, J?ger E, Stauber RH, Grez M, Pfitzner E, Heinzel T: plus-plus">Acetylation of Stat1 modulates NF-kappaB activity. / Genes Dev 2006, plus-plus">20:473-85. p://dx.doi.org/10.1101/gad.364306">CrossRef
  41. Pines J: plus-plus">Cyclins and cyclin-dependent kinases: take your partners. / Trends Biochem Sci 1993, plus-plus">18:195-97. p://dx.doi.org/10.1016/0968-0004(93)90185-P">CrossRef
  42. Sherr CJ, Roberts JM: plus-plus">Inhibitors of mammalian G1 cyclin-dependent kinases. / Genes Dev 1995, plus-plus">9:1149-163. p://dx.doi.org/10.1101/gad.9.10.1149">CrossRef
  43. Zhou Q, Dalgard CL, Wynder C, Doughty ML: plus-plus">Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult subventricular cells. / BMC Neurosci 2011, plus-plus">12:50. p://dx.doi.org/10.1186/1471-2202-12-50">CrossRef
  44. McLaughlin F, La Thangue NB: plus-plus">Histone deacetylase inhibitors open new doors in cancer therapy. / Biochem Pharmacol 2004, plus-plus">68:1139-144. p://dx.doi.org/10.1016/j.bcp.2004.05.034">CrossRef
  45. Nian H, Delage B, Pinto JT, Dashwood RH: plus-plus">Allyl mercaptan, a garlic-derived organosulfur compound, inhibits histone deacetylase and enhances Sp3 binding on the P21 WAF1 promoter. / Carcinogenesis 2008,plus-plus">29(9)plus-plus">:1816-824. p://dx.doi.org/10.1093/carcin/bgn165">CrossRef
  46. Kitazono M, Bates S, Fok P, Fojo T, Blagosklonny MV: plus-plus">The histone deacetylase inhibitor FR901228 (desipeptide) restores expression and function of pseudo-null p53. / Canc Biol Ther 2002, plus-plus">1:665-68.
  47. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY: plus-plus">Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21WAF1/CIP1 mediated by STAT1. / Science 1996, plus-plus">272:719-22. p://dx.doi.org/10.1126/science.272.5262.719">CrossRef
  48. Sambucetti LC, Fischer DD, Zabludoff S, Kwon PO, Chamberlin H, Trogani N, Xu H, Cohen D: plus-plus">Histone deacetylase inhibition selectively alters the activity and expression of cell cycle proteins leading to specific chromatin acetylation and antiproliferative effects. / J Biol Chem 1999, plus-plus">274:34940-4947. p://dx.doi.org/10.1074/jbc.274.49.34940">CrossRef
  49. Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T: plus-plus">Retinoblastoma protein recruits histone deacetylase to repress transcription. / Nature 1998, plus-plus">391:597-01. p://dx.doi.org/10.1038/35404">CrossRef
  50. Spotswood HT, Turner BM: plus-plus">An increasingly complex code. / J Clin Invest 2002, plus-plus">110:577-82.
  51. Carruthers LM, Hansen JC: plus-plus">The core histone N-termini function independently of linker histones during chromatin condensation. / J Biol Chem 2000, plus-plus">275:37285-7290. p://dx.doi.org/10.1074/jbc.M006801200">CrossRef
  52. Martin C, Zhang Y: plus-plus">The diverse functions of histone lysine methylation. / Nat Rev Mol Cell Biol 2005, plus-plus">6:838-49. p://dx.doi.org/10.1038/nrm1761">CrossRef
  53. Hansen JC: plus-plus">Conformational Dynamics of the Chromatin Fiber in solution: Determinants, Mechanisms and Functions. / Annu Rev Biophys Biomol Struct 2002, plus-plus">31:361-92. p://dx.doi.org/10.1146/annurev.biophys.31.101101.140858">CrossRef
  54. Ruthenburg AJ, Allis CD, Wysocka J: plus-plus">Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. / Mol cell 2007, plus-plus">25:15-0. p://dx.doi.org/10.1016/j.molcel.2006.12.014">CrossRef
  55. Grewal SI, Jia S: plus-plus">Heterochromatin revisited. / Nat Rev Genet 2007, plus-plus">8:35-6. p://dx.doi.org/10.1038/nrg2008">CrossRef
  56. Wissmann M, Yin N, Müller JM, Greschik H, Fodor BD, Jenuwein T, Vogler C, Schneider R, Günther T, Buettner R, Metzger E, Schüle R: plus-plus">Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. / Nat Cell Biol 2007, plus-plus">9:347-53. p://dx.doi.org/10.1038/ncb1546">CrossRef
  57. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T: plus-plus">Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. / Nature 2001, plus-plus">410:120-24. p://dx.doi.org/10.1038/35065138">CrossRef
  58. Fischle W, Wang Y, Allis CD: plus-plus">Binary switches and modification cassettes in histone biology and beyond. / Nature 2003, plus-plus">425:475-79. p://dx.doi.org/10.1038/nature02017">CrossRef
  59. Pray-Grant MG, Daniel JA, Schieltz D, Yates JR, Grant PA: plus-plus">Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. / Nature 2005, plus-plus">433:434-38. p://dx.doi.org/10.1038/nature03242">CrossRef
  60. Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD: plus-plus">WDR5 associates with histone H3 methylated at K4 and is essential for H3?K4 methylation and vertebrate development. / Cell 2005, plus-plus">121:859-72. p://dx.doi.org/10.1016/j.cell.2005.03.036">CrossRef
  61. Cameron EE, Bachman KE, My?h?nen S, Herman JG, Baylin SB: plus-plus">Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. / Nat Genet 1999, plus-plus">21:103-07. p://dx.doi.org/10.1038/5047">CrossRef
  62. Huang Y, Shaw PG, Davidson NE: plus-plus">Inhibition of histone deacetylases. / Meth Mol Biol 2011, plus-plus">791:297-11. p://dx.doi.org/10.1007/978-1-61779-316-5_22">CrossRef
  63. Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB: plus-plus">Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. / Science 1995, plus-plus">267:1018-021. p://dx.doi.org/10.1126/science.7863327">CrossRef
  64. Coqueret O, Gascan H: plus-plus">Functional interaction of STAT3 transcription factor with the cell cycle inhibitor p21WAF1/CIPI/SDI1. / J Biol Chem 2000, plus-plus">275:18794-00. p://dx.doi.org/10.1074/jbc.M001601200">CrossRef
  65. Bromberg J: plus-plus">Stat proteins and oncogenesis. / J Clin Invest 2002, plus-plus">109:1139-142.
  66. The pre-publication history for this paper can be accessed here:p://www.biomedcentral.com/1471-2407/12/180/prepub" class="a-plus-plus">http://www.biomedcentral.com/1471-2407/12/180/prepub
  
• 作者单位：Manika Pal-Bhadra (1)
  M Janaki Ramaiah (1) (2)
  T Lakshminarayan Reddy (1)
  Anita Krishnan (1) (2)
  SNCVL Pushpavalli (1)
  K Suresh Babu (3)
  Ashok K Tiwari (4)
  J Madhusudana Rao (3)
  Jhillu S Yadav (1)
  Utpal Bhadra (2)
  
  1. Department of Chemical Biology, Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India
  2. Functional Genomics and Gene silencing Group, Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad, 500007, India
  3. Department of Natural Product, Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India
  4. Department of Pharmacology, Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India
  
• ISSN：1471-2407

文摘

Background Chrysin and its analogues, belongs to flavonoid family and possess potential anti-tumour activity. The aim of this study is to determine the molecular mechanism by which chrysin controls cell growth and induce apoptosis in A375 cells. Methods Effect of chrysin and its analogues on cell viability and cell cycle analysis was determined by MTT assay and flowcytometry. A series of Western blots was performed to determine the effect of chrysin on important cell cycle regulatory proteins (Cdk2, cyclin D1, p53, p21, p27). The fluorimetry and calorimetry based assays was conducted for characterization of chrysin as HDAC inhibitor. The changes in histone tail modification such as acetylation and methylation was studied after chrysin treatment was estimated by immuno-fluorescence and western blot analysis. The expression of Bcl-xL, survivin and caspase-3 was estimated in chrysin treated cells. The effect of chrysin on p21 promoter activity was studied by luciferase and ChIP assays. Results Chrysin cause G1 cell cycle arrest and found to inhibit HDAC-2 and HDAC-8. Chrysin treated cells have shown increase in the levels of H3acK14, H4acK12, H4acK16 and decrease in H3me2K9 methylation. The p21 induction by chrysin treatment was found to be independent of p53 status. The chromatin remodelling at p21WAF1 promoter induces p21 activity, increased STAT-1 expression and epigenetic modifications that are responsible for ultimate cell cycle arrest and apoptosis. Conclusion Chrysin shows in vitro anti-cancer activity that is correlated with induction of histone hyperacetylation and possible recruitment of STAT-1, 3, 5 proteins at STAT (?92 to ?84) region of p21 promoter. Our results also support an unexpected action of chrysin on the chromatin organization of p21 WAF1 promoter through histone methylation and hyper-acetylation. It proposes previously unknown sequence specific chromatin modulations in the STAT responsive elements for regulating cell cycle progression negatively via the induction of the CDK inhibitor p21 WAF1 .