Histone deacetylases and mechanisms of regulation of gene expression

Critical Reviews in Oncogenesis

Volumn 20, Issue 1-2, 2015, Pages 35-47

  Chen, Hong Ping ^a,b   Zhao, Yu Tina ^a   Zhao, Ting C ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NANCHANG UNIVERSITY   (China)

Author keywords

Cancer; Drug target; Histone acetylation; Histone deacetylase

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR;

ARTICLE; BLADDER CANCER; CARCINOGENESIS; COLON CANCER; GENE EXPRESSION REGULATION; HEMATOLOGIC MALIGNANCY; INFLAMMATION; LIVER CELL CARCINOMA; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; ANIMAL; COLON TUMOR; DRUG EFFECTS; FEMALE; GENETICS; HEMATOLOGIC DISEASE; HUMAN; LIVER TUMOR; MALE; METABOLISM; PHYSIOLOGY; UROGENITAL TRACT TUMOR;

ANIMALS; CARCINOMA, HEPATOCELLULAR; COLONIC NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION; HEMATOLOGIC NEOPLASMS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; INFLAMMATION; LIVER NEOPLASMS; MALE; UROGENITAL NEOPLASMS;

EID: 84922794905     PISSN: 08939675     EISSN: 21626448     Source Type: Journal    
DOI: 10.1615/CritRevOncog.2015012997     Document Type: Article

References (75)

1. Arnsdorf EJ, Tummala P, Castillo AB, Zhang F, Jacobs CR. The epigenetic mechanism of mechanically induced osteogenic differentiation. J Biomech. 2010;43:2881-6.
2. Pons D, de Vries FR, van den Elsen PJ, Heijmans BT, Quax PH, Jukema JW. Epigenetic histone acetylation modifiers in vascular remodelling: new targets for therapy in cardiovascular disease. Eur Heart J. 2009;30:266-77.
3. Nagase H, Ghosh S. Epigenetics: differential DNA methylation in mammalian somatic tissues. FEBS J. 2008;275:1617-23.
4. Vaissiere T, Sawan C, Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res. 2008;659:40-8.
5. 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.
6. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science. 2001;293:1653-7.
7. Dai JM, Wang ZY, Sun DC, Lin RX, Wang SQ, SIRTl interacts with P73 and suppresses P73-dependent transcriptional activity. J Cell Physiol. 2007;210:161-6.
8. Sundaresan NR, Samant SA, Pillai VB, Rajamohan SB, Gupta MP. SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol Cell Biol. 2008;28:6384-40L
9. Verdin E, Dequiedt F, Kasler HG. Class II Histone deacetylases: versatile regulators. Trends Genet. 2003;19:286-93.
10. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov. 2006;5:769-84.
11. Yang XJ, Seto E. The Rpd3/Hdal family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol. 2008;9:206-18.
12. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell. 2005;16:4623-35.
13. 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; 25:151-9.
14. Hayashi A, Horiuchi A, Kikuchi N, Hayashi T, Fuseya C, Suzuki A, Konishi I, Shiozawa T. Type-specific roles of histone deacetylase (HDAC) overexpression in ovarian carcinoma: HDAC1 enhances cell proliferation and HDAC3 stimulates cell migration with downregulation of E-cadherin. Int J Cancer. 2010;127:1332-46.
15. Muller BM, Jana L, Kasajima A, Lehmann A, Prinzler J, Budczies J, Winzer KJ, Dietel M, Weichert W, Denkert C. Differential expression of histone deacetylases HDAC1, 2 and 3 in human breast cancer-overexpression of HDAC2 and HDAC3 is associated with clinicopathological indicators of disease progression. BMC Cancer. 2013;13:215.
16. Poyet C, Jentsch B, Hermanns T, Schweckendiek D, Seifert HH, Schmidtpeter M, Sulser T, Moch H, Wild PJ, Kristiansen G. Expression of histone deacetylases 1, 2 and 3 in urothelial bladder cancer. BMC Clin Pathol. 2014;14:10.
17. Adams H, Fritzsche FR, Dirnhofer S, Kristiansen G, Tzankov A. Class I histone deacetylases 1,2 and 3 are highly expressed in classical Hodgkin’s lymphoma. Expert Opin Ther Targets.2010;14:577-84.
18. Gruhn B, Naumann T, Gruner D, Walther M, Wittig S, Becker S, Beck JF, Sonnemann J. The expression of histone deacetylase 4 is associated with prednisone poor-response in childhood acute lymphoblastic leukemia. Leuk Res. 2013;37: 1200-7.
19. Marquard L, Poulsen CB, Gjerdrum LM, de Nully Brown P, Christensen IJ, Jensen PB, Sehested M, Johansen P, Ralfkiaer E. Histone deacetylase 1, 2, 6 and acetylated histone H4 in B- and T-cell lymphomas. Histopathology. 2009;54:688-98.
20. Lepore I, Dell’Aversana C, Pilyugin M, Conte M, Nebbioso A, De Bellis F, Tambaro FP, Izzo T, Garcia-Manero G, Ferrara F, Irminger-Finger I, Altucci L. HDAC inhibitors repress BARD1 isoform expression in acute myeloid leukemia cells via activation of MiR-19a and/or b. PloS One. 2013;8:e83018.
21. Yoshida M, Kijima M, Akita M, Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem. 1990;265:17174-9.
22. Duvic M, Vu J. Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs. 2007;16:1111-20.
23. Tan J, Cang S, Ma Y, Petrillo RL, Liu D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol. 2010;3:5.
24. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci U S A. 2003;100:4389-94.
25. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related Inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis. 2009;30:1073-81.
26. Grausenburger R, Bilic I, Boucheron N, Zupkovitz G, El-Housseiny L, Tschismarov R, Zhang Y, Rembold M, Gaisberger M, Hard A, Epstein MM, Matthias P, Seiser C, Ellmeier W. Conditional deletion of histone deacetylase 1 in T cells leads to enhanced airway inflammation and increased Th2 cytokine production. J Immunol. 2010; 185:3489-97.
27. Elsharkawy AM, Oakley F, Lin F, Packham G, Mann DA, Mann J. The NF-kappaB p50:p50:HDAC-l repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes. J Hepatol. 2010;53:519-27.
28. Pakala SB, Bui-Nguyen TM, Reddy SD, Li DQ, Peng S, Rayala SK, Behringer RR, Kumar R. Regulation of NF-kappaB circuitry by a component of the nucleosome remodeling and deacetylase complex controls inflammatory response homeostasis. J Biol Chem. 2010;285:23590-7.
29. Bauer I, Grozio A, Lasiglie D, Basile G, Sturla L, Magnone M, Sociali G, Soncini D, Caffa I, Poggi A, Zoppoli G, Cea M, Feldmann G, Mostoslavsky R, Ballestrero A, Patrone F, Bruzzone S, Nencioni A. The NAD+-dependent histone deacetylase SIRT6 promotes cytokine production and migration in pancreatic cancer cells by regulating Ca2+ responses. J Biol Chem. 2012;287:40924-37.
30. Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, Mietton F, Matteoli G, Hiebert S, Natoli G. Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci U S A. 2012;109:E2865-74.
31. Kaliman P, Alvarez-Lopez MJ, Cosin-Tomas M, Rosenkranz MA, Lutz A, Davidson RJ. Rapid changes in histone deacetylases and inflammatory gene expression in expert meditators. Psychoneuroendocrinology. 2014;40:96-107.
32. Glauben R, Batra A, Stroh T, Erben U, Fedke I, Lehr HA, Leoni F, Mascagni P, Dinarello CA, Zeitz M, Siegmund B. Histone deacetylases: novel targets for prevention of colitis-associated cancer in mice. Gut. 2008;57:613-22.
33. Santoro F, Botrugno OA, Dal Zuffo R, Pallavicini I, Matthews GM, Cluse L, Barozzi I, Senese S, Fornasari L, Moretti S, Altucci L, Pelicci PG, Chiocca S, Johnstone RW, Minucci S. A dual role for Hdacl: oncosuppressor in tumorigenesis, oncogene in tumor maintenance. Blood. 2013;121:3459-68.
34. Dong LH, Cheng S, Zheng Z, Wang L, Shen Y, Shen ZX, Chen SJ, Zhao WL. Histone deacetylase inhibitor potentiated the ability of MTOR inhibitor to induce autophagic cell death in Burkitt leukemia/ lymphoma. J Hematol Oncol. 2013;6:53.
35. Jordaan G, Liao W, Sharma S. E-cadherin gene re-expression in chronic lymphocytic leukemia cells by HDAC inhibitors. BMC Cancer. 2013;13:88.
36. Weichert W, Roske 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;98:604-10.
37. Wang L, Zou X, Berger AD, Twiss C, Peng Y, Li Y, Chiu J, Guo H, Satagopan J, Wilton A, Gerald W, Basch R, Wang Z, Osman I, Lee P. Increased expression of histone deacetylaces (HDACs) and inhibition of prostate cancer growth and invasion by HDAC inhibitor SAHA. Am J Transi Res. 2009;1:62-71.
38. 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;28:1714-24.
39. Deubzer HE, Schier MC, Oehme I, Lodrini M, Haendler B, Sommer A, Sommer A, Witt O. HDAC11 is a novel drug target in carcinomas. Int J Cancer. 2013;132:2200-8.
40. Fortson WS, Kayarthodi S, Fujimura Y, Xu H, Matthews R, Grizzle WE, Rao VN, Bhat GK, Reddy ES. Histone deacetylase inhibitors, valproic acid and trichostatin-A induce apoptosis and affect acetylation status of P53 in ERG-positive Prostate cancer cells. Int J Oncol. 2011;39:111-9.
41. Patra N, De U, Kim TH, Lee YJ, Ahn MY, Kim ND, Yoon JH, Choi WS, Moon HR, Lee BM, Kim HS. A novel histone deacetylase (HDAC) inhibitor MHY219 induces apoptosis via up-regulation of androgen receptor expression in human prostate cancer cells. Biomed Pharmacother. 2013;67:407-15.
42. Choi ES, Han G, Park SK, Lee K, Kim HJ, Cho SD, Kim HM. A248, a novel synthetic HDAC inhibitor, induces apoptosis through the inhibition of specificity protein 1 and its downstream proteins in human prostate cancer cells. Mol Med Rep. 2013;8:195-200.
43. Khabele D, Son DS, Parl AK, Goldberg GL, Augenlicht LH, Mariadason JM, Rice VM. Drug-induced inactivation or gene silencing of class I histone deacetylases suppresses ovarian cancer cell growth: implications for therapy. Cancer Biol Trier. 2007;6:795-801.
44. Jin KL, Pak JH, Park JY, Choi WH, Lee JY, Kim JH, Nam JH. Expression profile of histone deacetylases 1, 2 and 3 in ovarian cancer tissues. J Gynecol Oncol. 2008; 19: 185-90.
45. Weichert W, Denkert C, Noske A, Darb-Esfahani S, Dietel M, Kalloger SE, Huntsman DG, Kobel M. Expression of class I histone deacetylases indicates poor prognosis in endometrioid subtypes of ovarian and endometrial carcinomas. Neoplasia. 2008;10:1021-7.
46. Stronach EA, Alfraidi A, Rama N, Datler C, Studd JB, Agarwal R, Guney TG, Gourley C, Hennessy BT, Mills GB, Mai A, Brown R, Dina R, Gabra H. HDAC4-regulated STATl activation mediates platinum resistance in ovarian cancer. Cancer Res. 2011;7:4412-22.
47. Wilson AJ, Cheng YQ, Khabele D. Thailandepsins are new small molecule class I HDAC inhibitors with potent cytotoxic activity in ovarian cancer cells: a preclinical study of epigenetic ovarian cancer therapy. J Ovarian Res. 2012;5:12.
48. Kwiecinska P, Wrobel A, Tauboll E, Gregoraszczuk EL. Valproic acid, but not levetiracetam, selectively decreases HDAC7 and HDAC2 expression in human ovarian cancer cells. Toxicol Lett. 2014;224:225-32.
49. Xu XS, Wang L, Abrams J, Wang G. Histone deacetylases (HDACs) in XPC gene silencing and bladder cancer. J Hematol Oncol. 2011;4:17.
50. Buckley MT, Yoon J, Yee H, Chiriboga L, Liebes L, Ara G, Qian X, Bajorin DF, Sun TT, Wu XR, Osman I. The histone deacetylase inhibitor belinostat (PXD101) suppresses bladder cancer cell growth in vitro and in vivo. J Transi Med. 2007;5:49.
51. Qu W, Kang YD, Zhou MS, Fu LL, Hua ZH, Wang LM. Experimental study on inhibitory effects of histone deacetylase inhibitor MS-275 and TSA on bladder cancer cells. Urol Oncol. 2010;28: 648-54.
52. Juengel E, Meyer dos Santos S, Schneider T, Makarevic J, Hudak L, Bartsch G, Haferkamp A, Wiesner C, Blaheta RA. HDAC inhibition suppresses bladder cancer cell adhesion to collagen under flow conditions. Exp Biol Med (Maywood). 2013;238:1297-304.
53. Quint K, Agaimy A, Di Fazio P, Montalbano R, Steindorf C, Jung R, Hellerbrand C, Hartmann A, Sitter H, Neureiter D, Ocker M. Clinical significance of histone deacetylases 1,2, 3, and 7: HDAC2 is an independent predictor of survival in HCC. Virchows Arch. 2011;459:129-39.
54. Liu C, Liu L, Shan J, Shen J, Xu Y, Zhang Q, Yang Z, Wu L, Xia F, Bie P, Cui Y, Zhang X, Bian X, Qian C. Histone deacetylase 3 participates in self-renewal of liver cancer stem cells through histone modification. Cancer Lett. 2013;339: 60-9.
55. Buurman R, Gurlevik E, Schaffer V, Eilers M, Sandbothe M, Kreipe H, Wilkens L, Schlegelberger B, Kuhnel F, Skawran B. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology. 2012;143:811-20.
56. Kim SO, Choi BT, Choi IW, Cheong J, Kim GY, Kwon TK, Kim ND, Choi YH. Anti-invasive activity of histone deacetylase inhibitors via the induction of Egr-1 and the modulation of tight junction-related proteins in human hepatocarcinoma cells. BMB Rep. 2009;42:655-60.
57. Wang HG, Huang XD, Shen P, Li LR, Xue HT, Ji GZ. Anticancer effects of sodium butyrate on hepatocellular carcinoma cells in vitro. Int J Mol Med. 2013;31:967-74.
58. Liu YL, Yang PM, Shun CT, Wu MS, Weng JR, Chen CC. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy. 2010;6:1057-65.
59. 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 caturation and P21 expression and are deregulated in human colon cancer. J Biol Chem. 2006;281:13548-58.
60. Spurling CC, Godman CA, Noonan EJ, Rasmussen TP, Rosenberg DW, Giardina C. HDAC3 over-expression and colon cancer cell proliferation and differentiation. Mol Carcinog. 2008;47:137-47.
61. Chen HP, Denicola M, Qin X, Zhao Y, Zhang L, Long XL, Zhuang S, Liu PY, Zhao TC. HDAC inhibition promotes cardiogenesis and the survival of embryonic stem cells through proteasome-dependent pathway. J Cell Biochem. 2011;112:3246-55.
62. 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;19:4062-75.
63. Jin JS, Tsao TY, Sun PC, Yu CP, Tzao C. SAHA inhibits the growth of colon tumors by decreasing histone deacetylase and the expression of cyclin Dl and survivin. Pathol Oncol Res. 2012;18:713-20.
64. Ravillah D, Mohammed A, Qian L, Brewer M, Zhang Y, Biddick L, Steele VE, Rao CV. Chemopreventive effects of an HDAC2-selective inhibitor on rat colon carcinogenesis and APCmin/+ mouse intestinal tumorigenesis. J Pharmacol Exp Tner. 2014;348:59-68.
65. Barrasa JI, Olmo N, Santiago-Gomez A, Lecona E, Anglard P, Turnay J, Lizarbe MA. Histone deacetylase inhibitors upregulate MMP11 gene expression through Spl/Smad complexes in human colon adenocarcinoma cells. Biochim Biophys Acta 2012;1823:570-81.
66. Moseley VR, Morris J, Knackstedt RW, Wargovich MJ. Green tea polyphenol epigallocatechin 3-gallate, contributes to the degradation of DNMT3A and HDAC3 in HCT 116 human colon cancer cells. Anticancer Res. 2013;33:5325-33.
67. Berger A, Venturelli S, Kallnischkies M, Bocker A, Busch C, Weiland T, Noor S, Leischner C, Weiss TS, Lauer UM, Bischoff SC, Bitzer M. Kaempferol, a new nutrition-derived pan-inhibitor of human histone deacetylases. TJ Nutr Biochem. 2013;24:977-85.
68. Marks PA, Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol. 2007;25:84-90.
69. Rasheed WK, Johnstone RW, Prince HM. Histone deacetylase inhibitors in cancer therapy. Exp Opin Investigat Drugs. 2007;16:659-78.
70. Kelly WK, O’Connor OA, Krug LM, Chiao JH, Heaney M, Curley T, MacGregore-Cortelli B, Tong W, Secrist JP, Schwartz L, Richardson S, Chu E, Olgac S, Marks PA, Scher H, Richon VM. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol. 2005;23:3923-31.
71. Ryan QC, Headlee D, Acharya M, Sparreboom A, Trepel JB, Ye J, Figg WD, Hwang K, Chung EJ, Murgo A, Melillo G, Elsayed Y, Monga M, Kalnitskiy M, Zwiebel J, Sausville EA. Phase I and pharmacokinetic study of MS-275, a histone deacetylase inhibitor, in patients with advanced and refractory solid tumors or lymphoma. J Clin Oncol. 2005;23:3912-22.
72. Montgomery RL, Hsieh J, Barbosa AC, Richardson JA, Olson EN. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci U S A. 2009;106:7876-81.
73. Chen Y, Wang H, Yoon SO, Xu X, Hottiger MO, Svaren J, Nave KA, Kim HA, Olson EN, Lu QR. HDAC-mediated deacetylation of NF-kappaB is critical for Schwann cell myelination. Nat Neurosci. 2011;14:437-41.
74. Montgomery RL, Potthoff MJ, Haberland M, Qi X, Matsuzaki S, Humphries KM, Richardson JA, Bassel-Duby R, Olson EN. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest. 2008;118:3588-97.
75. Knutson SK, Chyla BJ, Amann JM, Bhaskara S, Huppert SS, Hiebert SW. Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J. 2008;27:1017-28.