Histone Deacetylases: A Saga of Perturbed Acetylation Homeostasis in Cancer

Journal of Histochemistry and Cytochemistry

Volumn 62, Issue 1, 2014, Pages 11-33

  Parbin, Sabnam ^a   Kar, Swayamsiddha ^a   Shilpi, Arunima ^a   Sengupta, Dipta ^a   Deb, Moonmoon ^a   Rath, Sandip Kumar ^a   Patra, Samir Kumar ^a  

^a NATIONAL INSTITUTE OF TECHNOLOGY   (India)

Author keywords

acetylation homeostasis; cancer; epigenetics; histone deacetylase inhibitors (HDACi); histone deacetylases (HDACs); tumor suppressor genes

Indexed keywords

CYTOPLASM PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; SIRTUIN; TRANSCRIPTION FACTOR;

ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL PROLIFERATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME CHEMISTRY; HISTONE ACETYLATION; HOMEOSTASIS; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL;

EID: 84891071460     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155413506582     Document Type: Article

References (159)

1. Aghdassi A,Sendler M,Guenther A,Mayerle J,Behn CO,Heidecke CD,Friess H,Büchler M,Evert M,Lerch MM,Weiss FU.Recruitment of histone deacetylases HDAC1 and HDAC2 by the transcriptional repressor ZEB1 downregulates E-cadherin expression in pancreatic cancer.Gut. 2012;61:439-448.
2. Aguilera DG,Das CM,Sinnappah-Kang ND,Joyce C,Taylor PH,Wen S,Hasselblatt M,Paulus W,Fuller G,Wolff JE,Gopalakrishnan V.Reactivation of death receptor 4 (DR4) expression sensitizes medulloblastoma cell lines to TRAIL.J Neurooncol. 2009;93:303-318.
3. Alhazzazi TY,Kamarajan P,Joo N,Huang JY,Verdin E,D'Silva NJ,Kapila YL.Sirtuin-3 (SIRT3), a novel potential therapeutic target for oral cancer.Cancer. 2011;117:1670-1678.
4. Amann JM,Nip J,Strom DK,Lutterbach B,Harada H,Lenny N,Downing JR,Meyers S,Hiebert SW.ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain.Mol Cell Biol. 2001;21:6470-6483.
5. Ammanamanchi S,Brattain MG.Restoration of transforming growth factor-beta signaling through receptor RI induction by histone deacetylase activity inhibition in breast cancer cells.J Biol Chem. 2004;279:32620-32625.
6. Annicotte JS,Iankova I,Miard S,Fritz V,Sarruf D,Abella A,Berthe ML,Noël D,Pillon A,Iborra F,Dubus P,Maudelonde T,Culine S,Fajas L.Peroxisome proliferator-activated receptor gamma regulates E-cadherin expression and inhibits growth and invasion of prostate cancer.Mol Cell Biol. 2006;26:7561-7574.
7. Backlund MG,Mann JR,Holla VR,Shi Q,Daikoku T,Dey SK,DuBois RN.Repression of 15-hydroxyprostaglandin dehydrogenase involves histone deacetylase 2 and snail in colorectal cancer.Cancer Res. 2008;68:9331-9337.
8. Bali P,Pranpat M,Bradner J,Balasis M,Fiskus W,Guo F,Rocha K,Kumaraswamy S,Boyapalle S,Atadja P,Seto E,Bhalla K.Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors.J Biol Chem. 2005;280:26729-26734.
9. Barber MF,Michishita-Kioi E,Xi Y,Tasselli L,Kioi M,Moqtaderi Z,Tennen RI,Paredes S,Young NL,Chen K,Struhl K,Garcia BA,Gozani O,Li W,Chua KF.SIRT7 links H3K18 deacetylation to maintenance of oncogenic transformation.Nature. 2012;487:114-118.
10. Bereshchenko OR,Gu W,Dalla-Favera R.Acetylation inactivates the transcriptional repressor BCL6.Nat Genet. 2002;32:606-613.
11. Brunet A,Sweeney LB,Sturgill JF,Chua KF,Greer PL,Lin Y,Tran H,Ross SE,Mostoslavsky R,Cohen HY,Hu LS,Cheng HL,Jedrychowski MP,Gygi SP,Sinclair DA,Alt FW,Greenberg ME.Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.Science. 2004;303:2011-2015.
12. Burger-van Paassen N,Vincent A,Puiman PJ,van der Sluis M,Bouma J,Boehm G,van Goudoever JB,van Seuningen I,Renes IB.The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection.Biochem J. 2009;420:211-219.
13. Butler LM,Liapis V,Bouralexis S,Welldon K,Hay S,Thai le M,Labrinidis A,Tilley WD,Findlay DM,Evdokiou A.The histone deacetylase inhibitor, suberoylanilide hydroxamic acid, overcomes resistance of human breast cancer cells to Apo2L/TRAIL.Int J Cancer. 2006;119:944-954.
14. Campbell KJ,Rocha S,Perkins ND.Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B.Mol Cell. 2004;13:853-865.
15. Chang TL,Ito K,Ko TK,Liu Q,Salto-Tellez M,Yeoh KG,Fukamachi H,Ito Y.Claudin-1 has tumor suppressive activity and is a direct target of RUNX3 in gastric epithelial cells.Gastroenterology. 2010;138:255-265.
16. Chen C,Edelstein LC,Gelinas C.The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L).Mol Cell Biol. 2000;20:2687-2695.
17. Chen CS,Wang YC,Yang HC,Huang PH,Kulp SK,Yang CC,Lu YS,Matsuyama S,Chen CY,Chen CS.Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation.Cancer Res. 2007;67:5318-5327.
18. Chen L,Fischle W,Verdin E,Greene WC.Duration of nuclear NF-kappaB action regulated by reversible acetylation.Science. 2001;293:1653-1657.
19. Chen LF,Mu Y,Greene WC.Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB.EMBO J. 2002;21:6539-6548.
20. Chevallier N,Corcoran CM,Lennon C,Hyjek E,Chadburn A,Bardwell VJ,Licht JD,Melnick A.ETO protein of t(8;21) AML is a corepressor for Bcl-6 B-cell lymphoma oncoprotein.Blood. 2004;103:1454-1463.
21. Choudhary C,Kumar C,Gnad F,Nielsen ML,Rehman M,Walther TC,Olsen JV,Mann M.Lysine acetylation targets protein complexes and co-regulates major cellular functions.Science. 2009;325:834-840.
22. Cohen HY,Miller C,Bitterman KJ,Wall NR,Hekking B,Kessler B,Howitz KT,Gorospe M,de Cabo R,Sinclair DA.Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase.Science. 2004;305:390-392.
23. Compton LA,Hiebert SW.Anticancer therapy SMRT-ens up: targeting the BCL6-SMRT interaction in B cell lymphoma.Cancer Cell. 2010;17:315-316.
24. Dan L,Klimenkova O,Klimiankou M,Klusman JH,van den Heuvel-Eibrink MM,Reinhardt D,Welte K,Skokowa J.The role of sirtuin 2 activation by nicotinamide phosphoribosyltransferase in the aberrant proliferation and survival of myeloid leukemia cells.Haematologica. 2012;97:551-559.
25. Della Ragione F,Criniti V,Della Pietra V,Borriello A,Oliva A,Indaco S,Yamamoto T,Zappia V.Genes modulated by histone acetylation as new effectors of butyrate activity.FEBS Lett. 2001;499:199-204.
26. Deroanne CF,Bonjean K,Servotte S,Devy L,Colige A,Clausse N,Blacher S,Verdin E,Foidart JM,Nusgens BV,Castronovo V.Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling.Oncogene. 2002;21:427-436.
27. Ding G,Liu HD,Huang Q,Liang HX,Ding ZH,Liao ZJ,Huang G.HDAC6 promotes hepatocellular carcinoma progression by inhibiting P53 transcriptional activity.FEBS Lett. 2013;587:880-886.
28. Dokmanovic M,Clarke C,Marks PA.Histone deacetylase inhibitors: overview and perspectives.Mol Cancer Res. 2007;5:981-989.
29. Duan H,Heckman CA,Boxer LM.Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas.Mol Cell Biol. 2005;25:1608-1619.
30. Durst KL,Lutterbach B,Kummalue T,Friedman AD,Hiebert SW.The inv(16) fusion protein associates with corepressors via a smooth muscle myosin heavy-chain domain.Mol Cell Biol. 2003;23:607-619.
31. Finnin MS,Donigian JR,Cohen A,Richon VM,Rifkind RA,Marks PA,Breslow R,Pavletich NP.Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors.Nature. 1999;401:188-193.
32. Follows GA,Tagoh H,Lefevre P,Hodge D,Morgan GJ,Bonifer C.Epigenetic consequences of AML1-ETO action at the human c-FMS locus.EMBO J. 2003;22:2798-2809.
33. Fritsche P,Seidler B,Schüler S,Schnieke A,Göttlicher M,Schmid RM,Saur D,Schneider G.HDAC2 mediates therapeutic resistance of pancreatic cancer cells via the BH3-only protein NOXA.Gut. 2009;58:1399-1409.
34. Frye RA.Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity.Biochem Biophys Res Commun. 1999;260:273-279.
35. Geng H,Harvey CT,Pittsenbarger J,Liu Q,Beer TM,Xue C,Qian DZ.HDAC4 protein regulates HIF1alpha protein lysine acetylation and cancer cell response to hypoxia.J Biol Chem. 2011;286:38095-38102.
36. Grignani F,De Matteis S,Nervi C,Tomassoni L,Gelmetti V,Cioce M,Fanelli M,Ruthardt M,Ferrara FF,Zamir I,Seiser C,Grignani F,Lazar MA,Minucci S,Pelicci PG.Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia.Nature. 1998;391:815-818.
37. Grunstein M.Histone acetylation in chromatin structure and transcription.Nature. 1997;389:349-352.
38. Haberland M,Montgomery RL,Olson EN.The many roles of histone deacetylases in development and physiology: implications for disease and therapy.Nat Rev Genet. 2009;10:32-42.
39. Halder SK,Cho YJ,Datta A,Anumanthan G,Ham AJ,Carbone DP,Datta PK.Elucidating the mechanism of regulation of transforming growth factor beta Type II receptor expression in human lung cancer cell lines.Neoplasia. 2011;13:912-922.
40. Halkidou K,Gaughan L,Cook S,Leung HY,Neal DE,Robson CN.Upregulation and nuclear recruitment of HDAC1 in hormone refractory prostate cancer.Prostate. 2004;59:177-189.
41. Harms KL,Chen X.Histone deacetylase 2 modulates p53 transcriptional activities through regulation of p53-DNA binding activity.Cancer Res. 2007;67:3145-3152.
42. Hatayama H,Iwashita J,Kuwajima A,Abe T.The short chain fatty acid, butyrate, stimulates MUC2 mucin production in the human colon cancer cell line, LS174T.Biochem Biophys Res Commun. 2007;356:599-603.
43. Hellebrekers DM,Castermans K,Viré E,Dings RP,Hoebers NT,Mayo KH,Oude Egbrink MG,Molema G,Fuks F,van Engeland M,Griffioen AW.Epigenetic regulation of tumor endothelial cell anergy: silencing of intercellular adhesion molecule-1 by histone modifications.Cancer Res. 2006;66:10770-10777.
44. Heltweg B,Jung M.A microplate reader-based nonisotopic histone deacetylase activity assay.Anal Biochem. 2002;302:175-183.
45. Heltweg B,Jung M.A homogeneous nonisotopic histone deacetylase activity assay.J Biomol Screen. 2003;8:89-95.
46. Heltweg B,Trapp J,Jung M.In vitro assays for the determination of histone deacetylase activity.Methods. 2005;36:332-337.
47. Hinshelwood RA,Huschtscha LI,Melki J,Stirzaker C,Abdipranoto A,Vissel B,Ravasi T,Wells CA,Hume DA,Reddel RR,Clark SJ.Concordant epigenetic silencing of transforming growth factor-beta signaling pathway genes occurs early in breast carcinogenesis.Cancer Res. 2007;67:11517-11527.
48. Hoffmann K,Brosch G,Loidl P,Jung M.A non-isotopic assay for histone deacetylase activity.Nucleic Acids Res. 1999;27:2057-2058.
49. Hoffmann K,Brosch G,Loidl P,Jung M.First non-radioactive assay for in vitro screening of histone deacetylase inhibitors.Pharmazie. 2000;55:601-606.
50. Hrzenjak A,Moinfar F,Kremser ML,Strohmeier B,Staber PB,Zatloukal K,Denk H.Valproate inhibition of histone deacetylase 2 affects differentiation and decreases proliferation of endometrial stromal sarcoma cells.Mol Cancer Ther. 2006;5:2203-2210.
51. Hu E,Dul E,Sung CM,Chen Z,Kirkpatrick R,Zhang GF,Johanson K,Liu R,Lago A,Hofmann G,Macarron R,de los Frailes M,Perez P,Krawiec J,Winkler J,Jaye M.Identification of novel isoform-selective inhibitors within class I histone deacetylases.J Pharmacol Exp Ther. 2003;307:720-728.
52. Huang BH,Laban M,Leung CH,Lee L,Lee CK,Salto-Tellez M,Raju GC,Hooi SC.Inhibition of histone deacetylase 2 increases apoptosis and p21Cip1/WAF1 expression, independent of histone deacetylase 1.Cell Death Differ. 2005a;12:395-404.
53. Huang W,Zhao S,Ammanamanchi S,Brattain M,Venkatasubbarao K,Freeman JW.Trichostatin A induces transforming growth factor beta type II receptor promoter activity and acetylation of Sp1 by recruitment of PCAF/p300 to a Sp1.NF-Y complex.J Biol Chem. 2005b;280:10047-10054.
54. Ito K,Lim AC,Salto-Tellez M,Motoda L,Osato M,Chuang LS,Lee CW,Voon DC,Koo JK,Wang H,Fukamachi H,Ito Y.RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis.Cancer Cell. 2008;14:226-237.
55. Jeon HS,Lee SY,Lee EJ,Yun SC,Cha EJ,Choi E,Na MJ,Park JY,Kang J,Son JW.Combining microRNA-449a/b with a HDAC inhibitor has a synergistic effect on growth arrest in lung cancer.Lung Cancer. 2012;76:171-176.
56. Jin YH,Jeon EJ,Li QL,Lee YH,Choi JK,Kim WJ,Lee KY,Bae SC.Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation.J Biol Chem. 2004;279:29409-29417.
57. Juan LJ,Shia WJ,Chen MH,Yang WM,Seto E,Lin YS,Wu CW.Histone deacetylases specifically down-regulate p53-dependent gene activation.J Biol Chem. 2000;275:20436-20443.
58. Jung KH,Noh JH,Kim JK,Eun JW,Bae HJ,Xie HJ,Chang YG,Kim MG,Park H,Lee JY,Nam SW.HDAC2 overexpression confers oncogenic potential to human lung cancer cells by deregulating expression of apoptosis and cell cycle proteins.J Cell Biochem. 2012;113:2167-2177.
59. Kaminskyy VO,Surova OV,Vaculova A,Zhivotovsky B.Combined inhibition of DNA methyltransferase and histone deacetylase restores caspase-8 expression and sensitizes SCLC cells to TRAIL.Carcinogenesis. 2011;32:1450-1458.
60. Kashiwagi Y,Horie K,Kanno C,Inomata M,Imamura T,Kato M,Yamamoto T,Yamashita H.Trichostatin A-induced TGF-beta type II receptor expression in retinoblastoma cell lines.Invest Ophthalmol Vis Sci. 2010;51:679-685.
61. Kawahara TL,Michishita E,Adler AS,Damian M,Berber E,Lin M,McCord RA,Ongaigui KC,Boxer LD,Chang HY,Chua KF.SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span.Cell. 2009;136:62-74.
62. Kerr E,Holohan C,McLaughlin KM,Majkut J,Dolan S,Redmond K,Riley J,McLaughlin K,Stasik I,Crudden M,Van Schaeybroeck S,Fenning C,O'Connor R,Kiely P,Sgobba M,Haigh D,Johnston PG,Longley DB.Identification of an acetylation-dependant Ku70/FLIP complex that regulates FLIP expression and HDAC inhibitor-induced apoptosis.Cell Death Differ. 2012;19:1317-1327.
63. Kim HS,Patel K,Muldoon-Jacobs K,Bisht KS,Aykin-Burns N,Pennington JD,van der Meer R,Nguyen P,Savage J,Owens KM,Vassilopoulos A,Ozden O,Park SH,Singh KK,Abdulkadir SA,Spitz DR,Deng CX,Gius D.SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress.Cancer Cell. 2010;17:41-52.
64. Kim HS,Vassilopoulos A,Wang RH,Lahusen T,Xiao Z,Xu X,Li C,Veenstra TD,Li B,Yu H,Ji J,Wang XW,Park SH,Cha YI,Gius D,Deng CX.SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity.Cancer Cell. 2011a;20:487-499.
65. Kim MS,Kwon HJ,Lee YM,Baek JH,Jang JE,Lee SW,Moon EJ,Kim HS,Lee SK,Chung HY,Kim CW,Kim KW.Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes.Nature Med. 2001;7:437-443.
66. Kim NH,Kim SN,Kim YK.Involvement of HDAC1 in E-cadherin expression in prostate cancer cells; its implication for cell motility and invasion.Biochem Biophys Res Commun. 2011b;404:915-921.
67. Kim SH,Kim KW,Jeong JW.Inhibition of hypoxia-induced angiogenesis by sodium butyrate, a histone deacetylase inhibitor, through hypoxia-inducible factor-1alpha suppression.Oncol Rep. 2007;17:793-797.
68. Kolle D,Brosch G,Lechner T,Lusser A,Loidl P.Biochemical methods for analysis of histone deacetylases.Methods. 1998;15:323-331.
69. Kovacs JJ,Murphy PJ,Gaillard S,Zhao X,Wu JT,Nicchitta CV,Yoshida M,Toft DO,Pratt WB,Yao TP.HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor.Mol Cell. 2005;18:601-607.
70. Kress S,Stein A,Maurer P,Weber B,Reichert J,Buchmann A,Huppert P,Schwarz M.Expression of hypoxia-inducible genes in tumor cells.J Cancer Res Clin Oncol. 1998;124:315-320.
71. Lagger G,Doetzlhofer A,Schuettengruber B,Haidweger E,Simboeck E,Tischler J,Chiocca S,Suske G,Rotheneder H,Wintersberger E,Seiser C.The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene.Mol Cell Biol. 2003;23:2669-2679.
72. Lagger G,O'Carroll D,Rembold M,Khier H,Tischler J,Weitzer G,Schuettengruber B,Hauser C,Brunmeir R,Jenuwein T,Seiser C.Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression.EMBO J. 2002;21:2672-2681.
73. Lamonica JM,Vakoc CR,Blobel GA.Acetylation of GATA-1 is required for chromatin occupancy.Blood. 2006;108:3736-3738.
74. Langley E,Pearson M,Faretta M,Bauer UM,Frye RA,Minucci S,Pelicci PG,Kouzarides T.Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence.EMBO J. 2002;21:2383-2396.
75. Lemercier C,Brocard MP,Puvion-Dutilleul F,Kao HY,Albagli O,Khochbin S.Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor.J Biol Chem. 2002;277:22045-22052.
76. Li Y,Li X,Fan G,Fukushi J,Matsumoto Y,Iwamoto Y,Zhu Y.Impairment of p53 acetylation by EWS-Fli1 chimeric protein in Ewing family tumors.Cancer Lett. 2012;320:14-22.
77. Lin FC,Liu YP,Lai CH,Shan YS,Cheng HC,Hsu PI,Lee CH,Lee YC,Wang HY,Wang CH,Cheng JQ,Hsiao M,Lu PJ.RUNX3-mediated transcriptional inhibition of Akt suppresses tumorigenesis of human gastric cancer cells.Oncogene. 2012;31:4302-4316.
78. Lin HY,Chen CS,Lin SP,Weng JR,Chen CS.Targeting histone deacetylase in cancer therapy.Med Res Rev. 2006;26:397-413.
79. Linggi B,Müller-Tidow C,van de,Locht L,Hu M,Nip J,Serve H,Berdel WE,van der Reijden B,Quelle DE,Rowley JD,Cleveland J,Jansen JH,Pandolfi PP,Hiebert SW.The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia.Nature Med. 2002;8:743-750.
80. Liu S,Klisovic RB,Vukosavljevic T,Yu J,Paschka P,Huynh L,Pang J,Neviani P,Liu Z,Blum W,Chan KK,Perrotti D,Marcucci G.Targeting AML1/ETO-histone deacetylase repressor complex: a novel mechanism for valproic acid-mediated gene expression and cellular differentiation in AML1/ETO-positive acute myeloid leukemia cells.J Pharmacol Exp Ther. 2007;321:953-960.
81. Liu Y,Li YM,Tian RF,Liu WP,Fei Z,Long QF,Wang XA,Zhang X.The expression and significance of HIF-1alpha and GLUT-3 in glioma.Brain Res. 2009;1304:149-154.
82. 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;101:2259-2264.
83. Luo J,Nikolaev AY,Imai S,Chen D,Su F,Shiloh A,Guarente L,Gu W.Negative control of p53 by Sir2alpha promotes cell survival under stress.Cell. 2001;107:137-148.
84. Luo J,Su F,Chen D,Shiloh A,Gu W.Deacetylation of p53 modulates its effect on cell growth and apoptosis.Nature. 2000;408:377-381.
85. Ma L,Gao JS,Guan Y,Shi X,Zhang H,Ayrapetov MK,Zhang Z,Xu L,Hyun YM,Kim M,Zhuang S,Chin YE.Acetylation modulates prolactin receptor dimerization.Proc Natl Acad Sci U S A. 2010;107:19314-19319.
86. Marks PA.Discovery and development of SAHA as an anticancer agent.Oncogene. 2007;26:1351-1356.
87. Matsuyama A,Shimazu T,Sumida Y,Saito A,Yoshimatsu Y,Seigneurin-Berny D,Osada H,Komatsu Y,Nishino N,Khochbin S,Horinouchi S,Yoshida M.In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation.EMBO J. 2002;21:6820-6831.
88. Melnick AM,Westendorf JJ,Polinger A,Carlile GW,Arai S,Ball HJ,Lutterbach B,Hiebert SW,Licht JD.The ETO protein disrupted in t(8;21)-associated acute myeloid leukemia is a corepressor for the promyelocytic leukemia zinc finger protein.Mol Cell Biol. 2000;20:2075-2086.
89. Menssen A,Hydbring P,Kapelle K,Vervoorts J,Diebold J,Lüscher B,Larsson LG,Hermeking H.The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop.Proc Natl Acad Sci U S A. 2012;109:E187-196.
90. Minucci S,Pelicci PG.Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer.Nature Rev Cancer. 2006;6:38-51.
91. Mizuguchi Y,Specht S,Lunz JG,Isse K,Corbitt N,Takizawa T,Demetris AJ.SPRR2A enhances p53 deacetylation through HDAC1 and down regulates p21 promoter activity.BMC Mol Biol. 2012;13:20.
92. Mottet D,Pirotte S,Lamour V,Hagedorn M,Javerzat S,Bikfalvi A,Bellahcène A,Verdin E,Castronovo V.HDAC4 represses p21(WAF1/Cip1) expression in human cancer cells through a Sp1-dependent, p53-independent mechanism.Oncogene. 2009;28:243-256.
93. Nare B,Allocco JJ,Kuningas R,Galuska S,Myers RW,Bednarek MA,Schmatz DM.Development of a scintillation proximity assay for histone deacetylase using a biotinylated peptide derived from histone-H4.Anal Biochem. 1999;267:390-396.
94. Nohata N,Hanazawa T,Kinoshita T,Inamine A,Kikkawa N,Itesako T,Yoshino H,Enokida H,Nakagawa M,Okamoto Y,Seki N.Tumour-suppressive microRNA-874 contributes to cell proliferation through targeting of histone deacetylase 1 in head and neck squamous cell carcinoma.Br J Cancer. 2013;108:1648-1658.
95. Noonan EJ,Place RF,Pookot D,Basak S,Whitson JM,Hirata H,Giardina C,Dahiya R.miR-449a targets HDAC-1 and induces growth arrest in prostate cancer.Oncogene. 2009;28:1714-1724.
96. North BJ,Marshall BL,Borra MT,Denu JM,Verdin E.The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase.Mol Cell. 2003;11:437-444.
97. Obach M,Navarro-Sabaté A,Caro J,Kong X,Duran J,Gómez M,Perales JC,Ventura F,Rosa JL,Bartrons R.6-Phosphofructo-2-kinase (pfkfb3) gene promoter contains hypoxia-inducible factor-1 binding sites necessary for transactivation in response to hypoxia.J Biol Chem. 2004;279:53562-53570.
98. Oehme I,Deubzer HE,Wegener D,Pickert D,Linke JP,Hero B,Kopp-Schneider A,Westermann F,Ulrich SM,von Deimling A,Fischer M,Witt O.Histone deacetylase 8 in neuroblastoma tumorigenesis.Clin Cancer Res. 2009;15:91-99.
99. Osada H,Tatematsu Y,Masuda A,Saito T,Sugiyama M,Yanagisawa K,Takahashi T.Heterogeneous transforming growth factor (TGF)-beta unresponsiveness and loss of TGF-beta receptor type II expression caused by histone deacetylation in lung cancer cell lines.Cancer Res. 2001;61:8331-8339.
100. Osada H,Tatematsu Y,Saito H,Yatabe Y,Mitsudomi T,Takahashi T.Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients.Int J Cancer. 2004;112:26-32.
101. Patra SK,Deb M,Patra A.Molecular marks for epigenetic identification of developmental and cancer stem cells.Clin Epigenetics. 2011;2:27-53.
102. Patra SK,Patra A,Dahiya R.Histone deacetylase and DNA methyltransferase in human prostate cancer.Biochem Biophys Res Commun. 2001;287:705-713.
103. Peart MJ,Tainton KM,Ruefli AA,Dear AE,Sedelies KA,O'Reilly LA,Waterhouse NJ,Trapani JA,Johnstone RW.Novel mechanisms of apoptosis induced by histone deacetylase inhibitors.Cancer Res. 2003;63:4460-4471.
104. Peinado H,Ballestar E,Esteller M,Cano A.Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex.Mol Cell Biol. 2004;24:306-319.
105. Peixoto P,Castronovo V,Matheus N,Polese C,Peulen O,Gonzalez A,Boxus M,Verdin E,Thiry M,Dequiedt F,Mottet D.HDAC5 is required for maintenance of pericentric heterochromatin, and controls cell-cycle progression and survival of human cancer cells.Cell Death Differ. 2012;19:1239-1252.
106. Prives C,Manley JL.Why is p53 acetylated?.Cell. 2001;107:815-818.
107. Qian DZ,Kachhap SK,Collis SJ,Verheul HM,Carducci MA,Atadja P,Pili R.Class II histone deacetylases are associated with VHL-independent regulation of hypoxia-inducible factor 1 alpha.Cancer Res. 2006;66:8814-8821.
108. Rajendran P,Ho E,Williams DE,Dashwood RH.Dietary phytochemicals, HDAC inhibition, and DNA damage/repair defects in cancer cells.Clin Epigenetics. 2011;3:4.
109. Rao R,Fiskus W,Yang Y,Lee P,Joshi R,Fernandez P,Mandawat A,Atadja P,Bradner JE,Bhalla K.HDAC6 inhibition enhances 17-AAG-mediated abrogation of hsp90 chaperone function in human leukemia cells.Blood. 2008;112:1886-1893.
110. Richon VM,Sandhoff TW,Rifkind RA,Marks PA.Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation.Proc Natl Acad Sci U S A. 2000;97:10014-10019.
111. Saha RN,Pahan K.HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis.Cell Death Differ. 2006;13:539-550.
112. Saji S,Kawakami M,Hayashi S,Yoshida N,Hirose M,Horiguchi S,Itoh A,Funata N,Schreiber SL,Yoshida M,Toi M.Significance of HDAC6 regulation via estrogen signaling for cell motility and prognosis in estrogen receptor-positive breast cancer.Oncogene. 2005;24:4531-4539.
113. Sasakawa Y,Naoe Y,Noto T,Inoue T,Sasakawa T,Matsuo M,Manda T,Mutoh S.Antitumor efficacy of FK228, a novel histone deacetylase inhibitor, depends on the effect on expression of angiogenesis factors.Biochem Pharmacol. 2003;66:897-906.
114. Schüler S,Fritsche P,Diersch S,Arlt A,Schmid RM,Saur D,Schneider G.HDAC2 attenuates TRAIL-induced apoptosis of pancreatic cancer cells.Mol Cancer. 2010;9:80.
115. Scroggins BT,Robzyk K,Wang D,Marcu MG,Tsutsumi S,Beebe K,Cotter RJ,Felts S,Toft D,Karnitz L,Rosen N,Neckers L.An acetylation site in the middle domain of Hsp90 regulates chaperone function.Mol Cell. 2007;25:151-159.
116. Senese S,Zaragoza K,Minardi S,Muradore I,Ronzoni S,Passafaro A,Bernard L,Draetta GF,Alcalay M,Seiser C,Chiocca S.Role for histone deacetylase 1 in human tumor cell proliferation.Mol Cell Biol. 2007;27:4784-4795.
117. Shankar S,Davis R,Singh KP,Kurzrock R,Ross DD,Srivastava RK.Suberoylanilide hydroxamic acid (Zolinza/vorinostat) sensitizes TRAIL-resistant breast cancer cells orthotopically implanted in BALB/c nude mice.Mol Cancer Ther. 2009;8:1596-1605.
118. Shogren-Knaak M,Ishii H,Sun JM,Pazin MJ,Davie JR,Peterson CL.Histone H4-K16 acetylation controls chromatin structure and protein interactions.Science. 2006;311:844-847.
119. Smith BC,Denu JM.Chemical mechanisms of histone lysine and arginine modifications.Biochim Biophys Acta. 2009;1789:45-57.
120. Song J,Noh JH,Lee JH,Eun JW,Ahn YM,Kim SY,Lee SH,Park WS,Yoo NJ,Lee JY,Nam SW.Increased expression of histone deacetylase 2 is found in human gastric cancer.APMIS. 2005;113:264-268.
121. Spurling CC,Godman CA,Noonan EJ,Rasmussen TP,Rosenberg DW,Giardina C.HDAC3 overexpression and colon cancer cell proliferation and differentiation.Mol Carcinog. 2008;47:137-147.
122. Srivastava RK,Kurzrock R,Shankar S.MS-275 sensitizes TRAIL-resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses epithelial-mesenchymal transition in vivo.Mol Cancer Ther. 2010;9:3254-3266.
123. Su H,Altucci L,You Q.Competitive or noncompetitive, that's the question: research toward histone deacetylase inhibitors.Mol Cancer Ther. 2008;7:1007-1012.
124. Subramanian C,Jarzembowski JA,Opipari AW,Castle VP,Kwok RP.HDAC6 deacetylates Ku70 and regulates Ku70-Bax binding in neuroblastoma.Neoplasia. 2011;13:726-734.
125. Subramanian C,Opipari AW,Bian X,Castle VP,Kwok RP.Ku70 acetylation mediates neuroblastoma cell death induced by histone deacetylase inhibitors.Proc Natl Acad Sci U S A. 2005;102:4842-4847.
126. Taunton J,Hassig CA,Schreiber SL.A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.Science. 1996;272:408-411.
127. Taylor MD,Liu Y,Nagji AS,Theodosakis N,Jones DR.Combined proteasome and histone deacetylase inhibition attenuates epithelial-mesenchymal transition through E-cadherin in esophageal cancer cells.J Thorac Cardiovasc Surg. 2010;139:1224-1232.
128. Tong ZT,Cai MY,Wang XG,Kong LL,Mai SJ,Liu YH,Zhang HB,Liao YJ,Zheng F,Zhu W,Liu TH,Bian XW,Guan XY,Lin MC,Zeng MS,Zeng YX,Kung HF,Xie D.EZH2 supports nasopharyngeal carcinoma cell aggressiveness by forming a co-repressor complex with HDAC1/HDAC2 and Snail to inhibit E-cadherin.Oncogene. 2012;31:583-594.
129. Truyers C,Kellen E,Arbyn M,Trommelmans L,Nys H,Hensen K,Aertgeerts B,Bartholomeeusen S,Hansson M,Buntinx F.The use of human tissue in epidemiological research; ethical and legal considerations in two biobanks in Belgium.Med Health Care Philos. 2010;13:169-175.
130. Vaissiere T,Sawan C,Herceg Z.Epigenetic interplay between histone modifications and DNA methylation in gene silencing.Mutat Res. 2008;659:40-48.
131. Vallot C,Stransky N,Bernard-Pierrot I,Hérault A,Zucman-Rossi J,Chapeaublanc E,Vordos D,Laplanche A,Benhamou S,Lebret T,Southgate J,Allory Y,Radvanyi F.A novel epigenetic phenotype associated with the most aggressive pathway of bladder tumor progression.J Natl Cancer Inst. 2011;103:47-60.
132. Van Gool F,Gallí M,Gueydan C,Kruys V,Prevot PP,Bedalov A,Mostoslavsky R,Alt FW,De Smedt T,Leo O.Intracellular NAD levels regulate tumor necrosis factor protein synthesis in a sirtuin-dependent manner.Nat Med. 2009;15:206-210.
133. Vanhaecke T,Papeleu P,Elaut G,Rogiers V.Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: toxicological point of view.Curr Med Chem. 2004;11:1629-1643.
134. Vaziri H,Dessain SK,Ng Eaton E,Imai SI,Frye RA,Pandita TK,Guarente L,Weinberg RA.hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase.Cell. 2001;107:149-159.
135. Velcich A,Yang W,Heyer J,Fragale A,Nicholas C,Viani S,Kucherlapati R,Lipkin M,Yang K,Augenlicht L.Colorectal cancer in mice genetically deficient in the mucin Muc2.Science. 2002;295:1726-1729.
136. Vigushin DM,Ali S,Pace PE,Mirsaidi N,Ito K,Adcock I,Coombes RC.Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo.Clin Cancer Res. 2001;7:971-976.
137. Vincent A,Perrais M,Desseyn JL,Aubert JP,Pigny P,Van Seuningen I.Epigenetic regulation (DNA methylation, histone modifications) of the 11p15 mucin genes (MUC2, MUC5AC, MUC5B, MUC6) in epithelial cancer cells.Oncogene. 2007;26:6566-6576.
138. von Burstin J,Eser S,Paul MC,Seidler B,Brandl M,Messer M,von Werder A,Schmidt A,Mages J,Pagel P,Schnieke A,Schmid RM,Schneider G,Saur D.E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex.Gastroenterology. 2009;137:361-371.
139. Wang R,Cherukuri P,Luo J.Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation.J Biol Chem. 2005;280:11528-11534.
140. Wang RH,Sengupta K,Li C,Kim HS,Cao L,Xiao C,Kim S,Xu X,Zheng Y,Chilton B,Jia R,Zheng ZM,Appella E,Wang XW,Ried T,Deng CX.Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice.Cancer Cell. 2008;14:312-323.
141. Watamoto K,Towatari M,Ozawa Y,Miyata Y,Okamoto M,Abe A,Naoe T,Saito H.Altered interaction of HDAC5 with GATA-1 during MEL cell differentiation.Oncogene. 2003;22:9176-9184.
142. Wegener D,Wirsching F,Riester D,Schwienhorst A.A fluorogenic histone deacetylase assay well suited for high-throughput activity screening.Chem Biol. 2003;10:61-68.
143. Weichert W,Röske A,Gekeler V,Beckers T,Stephan C,Jung K,Fritzsche FR,Niesporek S,Denkert C,Dietel M,Kristiansen G.Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy.Br J Cancer. 2008;98:604-610.
144. Whetstine JR,Ceron J,Ladd B,Dufourcq P,Reinke V,Shi Y.Regulation of tissue-specific and extracellular matrix-related genes by a class I histone deacetylase.Mol Cell. 2005;18:483-490.
145. Wieczorek M,Ginter T,Brand P,Heinzel T,Krämer OH.Acetylation modulates the STAT signaling code.Cytokine Growth Factor Rev. 2012;23:293-305.
146. Wilson AJ,Byun DS,Nasser S,Murray LB,Ayyanar K,Arango D,Figueroa M,Melnick A,Kao GD,Augenlicht LH,Mariadason JM.HDAC4 promotes growth of colon cancer cells via repression of p21.Mol Biol Cell. 2008;19:4062-4075.
147. Wilson AJ,Byun DS,Popova N,Murray LB,L'Italien K,Sowa Y,Arango D,Velcich A,Augenlicht LH,Mariadason JM.Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer.J Biol Chem. 2006;281:13548-13558.
148. Witt O,Deubzer HE,Milde T,Oehme I.HDAC family: What are the cancer relevant targets?.Cancer Lett. 2009;277:8-21.
149. Xie HJ,Noh JH,Kim JK,Jung KH,Eun JW,Bae HJ,Kim MG,Chang YG,Lee JY,Park H,Nam SW.HDAC1 inactivation induces mitotic defect and caspase-independent autophagic cell death in liver cancer.PLoS One 7, e34265. 2012;:.
150. Yamada N,Hamada T,Goto M,Tsutsumida H,Higashi M,Nomoto M,Yonezawa S.MUC2 expression is regulated by histone H3 modification and DNA methylation in pancreatic cancer.Int J Cancer. 2006;119:1850-1857.
151. Yang QC,Zeng BF,Shi ZM,Dong Y,Jiang ZM,Huang J,Lv YM,Yang CX,Liu YW.Inhibition of hypoxia-induced angiogenesis by trichostatin A via suppression of HIF-1a activity in human osteosarcoma.J Exp Clin Cancer Res. 2006;25:593-599.
152. Yang XJ,Gregoire S.Metabolism, cytoskeleton and cellular signalling in the grip of protein Nepsilon - and O-acetylation.EMBO Rep. 2007;8:556-562.
153. Yasui W,Oue N,Ono S,Mitani Y,Ito R,Nakayama H.Histone acetylation and gastrointestinal carcinogenesis.Ann N Y Acad Sci. 2003;983:220-231.
154. Yuan ZL,Guan YJ,Chatterjee D,Chin YE.Stat3 dimerization regulated by reversible acetylation of a single lysine residue.Science. 2005;307:269-273.
155. Zapotocky M,Mejstrikova E,Smetana K,Stary J,Trka J,Starkova J.Valproic acid triggers differentiation and apoptosis in AML1/ETO-positive leukemic cells specifically.Cancer Lett. 2012;319:144-153.
156. Zhong L,D'Urso A,Toiber D,Sebastian C,Henry RE,Vadysirisack DD,Guimaraes A,Marinelli B,Wikstrom JD,Nir T,Clish CB,Vaitheesvaran B,Iliopoulos O,Kurland I,Dor Y,Weissleder R,Shirihai OS,Ellisen LW,Espinosa JM,Mostoslavsky R.The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha.Cell. 2010;140:280-293.
157. Zhu P,Martin E,Mengwasser J,Schlag P,Janssen KP,Göttlicher M.Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis.Cancer Cell. 2004;5:455-463.
158. Zhuang WY,Cen JN,Zhao Y,Chen ZX.Epigenetic silencing of Bcl-2, CEBPA and p14(ARF) by the AML1-ETO oncoprotein contributing to growth arrest and differentiation block in the U937 cell line.Oncology Rep. 2013;30:185-192.
159. Zupkovitz G,Grausenburger R,Brunmeir R,Senese S,Tischler J,Jurkin J,Rembold M,Meunier D,Egger G,Lagger S,Chiocca S,Propst F,Weitzer G,Seiser C.The cyclin-dependent kinase inhibitor p21 is a crucial target for histone deacetylase 1 as a regulator of cellular proliferation.Mol Cell Biol. 2010;30:1171-1181.