HDAC inhibitors in experimental liver and kidney fibrosis

Fibrogenesis and Tissue Repair

Volumn 6, Issue 1, 2013, Pages

  Van Beneden, Katrien ^a   Mannaerts, Inge ^a   Pauwels, Marina ^a   Van den Branden, Christiane ^a   van Grunsven, Leo A ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

HDAC and liver; Histone deacetylase; Kidney or hepatic; Renal fibrosis

Indexed keywords

BELINOSTAT; CUDC 101; ENTINOSTAT; HISTONE DEACETYLASE INHIBITOR; LBN 589; MYC PROTEIN; PANOBINOSTAT; PLATELET DERIVED GROWTH FACTOR; PROTEIN P53; PX 105684; SIRTUIN 1; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; SIRTUIN 5; SIRTUIN 6; SIRTUIN 7; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CROSS LINKING; DEACETYLATION; DRUG MECHANISM; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GLOMERULOSCLEROSIS; INTERSTITIAL NEPHRITIS; KIDNEY FIBROSIS; LIVER FIBROSIS; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; REVIEW; WOUND HEALING;

EID: 84873431254     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-6-1     Document Type: Review

References (171)

1. Adam R, Karam V, Delvart V, O'Grady J, Mirza D, Klempnauer J, Castaing D, Neuhaus P, Jamieson N, Salizzoni M, Pollard S, Lerut J, Paul A, Garcia-Valdecasas JC, Rodríguez FS, Burroughs A, all contributing centers (www.eltr.org); European Liver and Intestine Transplant Association (ELITA) Evolution of indications and results of liver transplantation in Europe. A report from the European Liver Transplant Registry (ELTR). J Hepatol 2012, 57:675-688. 10.1016/j.jhep.2012.04.015, 22609307, all contributing centers (www.eltr.org); European Liver and Intestine Transplant Association (ELITA).
2. European Association for the Study of the Liver EASL Annual Report 2009 2010, European Association for the Study of the Liver, Geneva, Switzerland, European Association for the Study of the Liver.
3. Kamath PS, Wiesner RH, Malinchoc M, Kremers W, Therneau TM, Kosberg CL, D'Amico G, Dickson ER, Kim WR. A model to predict survival in patients with end-stage liver disease. Hepatology 2001, 33:464-470. 10.1053/jhep.2001.22172, 11172350.
4. Yu Y, Fisher JE, Lillegard JB, Rodysill B, Amiot B, Nyberg SL. Cell therapies for liver diseases. Liver Transpl 2012, 18:9-21. 10.1002/lt.22467, 3245367, 22140063.
5. Adam R, McMaster P, O'Grady JG, Castaing D, Klempnauer JL, Jamieson N, Neuhaus P, Lerut J, Salizzoni M, Pollard S, Muhlbacher F, Rogiers X, Garcia Valdecasas JC, Berenguer J, Jaeck D, Moreno Gonzalez E, European Liver Transplant Association Evolution of liver transplantation in Europe: report of the European Liver Transplant Registry. Liver Transpl 2003, 9:1231-1243. 10.1016/j.lts.2003.09.018, 14625822, European Liver Transplant Association.
6. Couser WG, Remuzzi G, Mendis S, Tonelli M. The contribution of chronic kidney disease to the global burden of major noncommunicable diseases. Kidney Int 2011, 80:1258-1270. 10.1038/ki.2011.368, 21993585.
7. James MT, Hemmelgarn BR, Tonelli M. Early recognition and prevention of chronic kidney disease. Lancet 2010, 375:1296-1309. 10.1016/S0140-6736(09)62004-3, 20382326.
8. Narayan KM, Ali MK, Koplan JP. Global noncommunicable diseases-where worlds meet. N Engl J Med 2010, 363:1196-1198. 10.1056/NEJMp1002024, 20860499.
9. Schieppati A, Remuzzi G. Chronic renal diseases as a public health problem: epidemiology, social, and economic implications. Kidney Int Suppl 2005, 98:S7-S10.
10. EKHA The European Kidney Health Alliance 2011, http://www.ekha.eu, EKHA.
11. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmoulière A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012, 180:1340-1355. 10.1016/j.ajpath.2012.02.004, 22387320.
12. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008, 214:199-210. 10.1002/path.2277, 2693329, 18161745.
13. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 2007, 127:526-537. 10.1038/sj.jid.5700613, 17299435.
14. Hinz B. The myofibroblast: paradigm for a mechanically active cell. J Biomech 2010, 43:146-155. 10.1016/j.jbiomech.2009.09.020, 19800625.
15. Hinz B, Gabbian G. Fibrosis: recent advances in myofibroblast biology and new therapeutic perspectives. F1000 Biol Rep 2010, 2:78. 2998803, 21170369.
16. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007, 170:1807-1816. 10.2353/ajpath.2007.070112, 1899462, 17525249.
17. Forbes SJ, Parola M. Liver fibrogenic cells. Best Pract Res Clin Gastroenterol 2011, 25:207-217. 10.1016/j.bpg.2011.02.006, 21497739.
18. Lin SL, Kisseleva T, Brenner DA, Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 2008, 173:1617-1627. 10.2353/ajpath.2008.080433, 2626374, 19008372.
19. Meran S, Steadman R. Fibroblasts and myofibroblasts in renal fibrosis. Int J Exp Pathol 2011, 92:158-167. 10.1111/j.1365-2613.2011.00764.x, 3101489, 21355940.
20. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 2010, 176:85-97. 10.2353/ajpath.2010.090517, 2797872, 20008127.
21. Herzog EL, Bucala R. Fibrocytes in health and disease. Exp Hematol 2010, 38:548-556. 10.1016/j.exphem.2010.03.004, 3136351, 20303382.
22. Quan TE, Cowper S, Wu SP, Bockenstedt LK, Bucala R. Circulating fibrocytes: collagen-secreting cells of the peripheral blood. Int J Biochem Cell Biol 2004, 36:598-606. 10.1016/j.biocel.2003.10.005, 15010326.
23. Higashiyama R, Moro T, Nakao S, Mikami K, Fukumitsu H, Ueda Y, Ikeda K, Adachi E, Bou-Gharios G, Okazaki I, Inagaki Y. Negligible contribution of bone marrow-derived cells to collagen production during hepatic fibrogenesis in mice. Gastroenterology 2009, 137:1459-1466.e1. 10.1053/j.gastro.2009.07.006, 19596008.
24. Zeisberg EM, Potenta SE, Sugimoto H, Zeisberg M, Kalluri R. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 2008, 19:2282-2287. 10.1681/ASN.2008050513, 2588112, 18987304.
25. Fragiadaki M, Mason RM. Epithelial-mesenchymal transition in renal fibrosis - evidence for and against. Int J Exp Pathol 2011, 92:143-150. 10.1111/j.1365-2613.2011.00775.x, 3101487, 21554437.
26. Liu Y. New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 2010, 21:212-222. 10.1681/ASN.2008121226, 20019167.
27. Quaggin SE, Kapus A. Scar wars: mapping the fate of epithelial-mesenchymal-myofibroblast transition. Kidney Int 2011, 80:41-50. 10.1038/ki.2011.77, 21430641.
28. Zeisberg M, Duffield JS. Resolved: EMT produces fibroblasts in the kidney. J Am Soc Nephrol 2010, 21:1247-1253. 10.1681/ASN.2010060616, 20651165.
29. Taura K, Miura K, Iwaisako K, Osterreicher CH, Kodama Y, Penz-Osterreicher M, Brenner DA. Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice. Hepatology 2010, 51:1027-1036. 10.1002/hep.23368, 2906231, 20052656.
30. Scholten D, Osterreicher CH, Scholten A, Iwaisako K, Gu G, Brenner DA, Kisseleva T. Genetic labeling does not detect epithelial-to-mesenchymal transition of cholangiocytes in liver fibrosis in mice. Gastroenterology 2010, 139:987-998. 10.1053/j.gastro.2010.05.005, 2930026, 20546735.
31. Chu AS, Diaz R, Hui JJ, Yanger K, Zong Y, Alpini G, Stanger BZ, Wells RG. Lineage tracing demonstrates no evidence of cholangiocyte epithelial-to-mesenchymal transition in murine models of hepatic fibrosis. Hepatology 2011, 53:1685-1695. 10.1002/hep.24206, 3082729, 21520179.
32. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 2002, 110:341-350. 151091, 12163453.
33. Pinzani M. Epithelial-mesenchymal transition in chronic liver disease: fibrogenesis or escape from death?. J Hepatol 2011, 55:459-465. 10.1016/j.jhep.2011.02.001, 21320559.
34. Cook HT. The origin of renal fibroblasts and progression of kidney disease. Am J Pathol 2010, 176:22-24. 10.2353/ajpath.2010.090898, 2797864, 20008128.
35. Geerts A. On the origin of stellate cells: mesodermal, endodermal or neuro-ectodermal?. J Hepatol 2004, 40:331-334. 10.1016/j.jhep.2003.12.006, 14739107.
36. Blomhoff R, Wake K. Perisinusoidal stellate cells of the liver: important roles in retinol metabolism and fibrosis. FASEB J 1991, 5:271-277.
37. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008, 88:125-172. 10.1152/physrev.00013.2007, 2888531, 18195085.
38. Geerts A. History, heterogeneity, developmental biology, and functions of quiescent hepatic stellate cells. Semin Liver Dis 2001, 21:311-335. 10.1055/s-2001-17550, 11586463.
39. Pinzani M, Marra F. Cytokine receptors and signaling in hepatic stellate cells. Semin Liver Dis 2001, 21:397-416. 10.1055/s-2001-17554, 11586468.
40. Dooley S, ten Dijke P. TGF-beta in progression of liver disease. Cell Tissue Res 2012, 347:245-256. 10.1007/s00441-011-1246-y, 3250614, 22006249.
41. Kent G, Gay S, Inouye T, Bahu R, Minick OT, Popper H. Vitamin A-containing lipocytes and formation of type III collagen in liver injury. Proc Natl Acad Sci U S A 1976, 73:3719-3722. 10.1073/pnas.73.10.3719, 431190, 1068482.
42. McLean AJ, Morgan DJ. Clinical pharmacokinetics in patients with liver disease. Clin Pharmacokinet 1991, 21:42-69. 10.2165/00003088-199121010-00004, 1914341.
43. Kisseleva T, Brenner DA. Anti-fibrogenic strategies and the regression of fibrosis. Best Pract Res Clin Gastroenterol 2011, 25:305-317. 10.1016/j.bpg.2011.02.011, 3086317, 21497747.
44. Pinzani M, Rombouts K. Liver fibrosis: from the bench to clinical targets. Dig Liver Dis 2004, 36:231-242. 10.1016/j.dld.2004.01.003, 15115333.
45. Bechtel W, McGoohan S, Zeisberg EM, Müller GA, Kalbacher H, Salant DJ, Müller CA, Kalluri R, Zeisberg M. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med 2010, 16:544-550. 10.1038/nm.2135, 3106179, 20418885.
46. Kisseleva T, Cong M, Paik Y, Scholten D, Jiang C, Benner C, Iwaisako K, Moore-Morris T, Scott B, Tsukamoto H, Evans SM, Dillmann W, Glass CK, Brenner DA. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc Natl Acad Sci U S A 2012, 109:9448-9453. 10.1073/pnas.1201840109, 3386114, 22566629.
47. Troeger JS, Mederacke I, Gwak GY, Dapito DH, Mu X, Hsu CC, Pradere JP, Friedman RA, Schwabe RF. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice. Gastroenterology 2012, 143:1073-1083. 10.1053/j.gastro.2012.06.036, 22750464.
48. Dechêne A, Sowa JP, Gieseler RK, Jochum C, Bechmann LP, El Fouly A, Schlattjan M, Saner F, Baba HA, Paul A, Dries V, Odenthal M, Gerken G, Friedman SL, Canbay A. Acute liver failure is associated with elevated liver stiffness and hepatic stellate cell activation. Hepatology 2010, 52:1008-1016. 10.1002/hep.23754, 20684020.
49. Rastogi A, Bihari C, Maiwall R, Ahuja A, Sharma MK, Kumar A, Sarin SK. Hepatic stellate cells are involved in the pathogenesis of acute-on-chronic liver failure (ACLF). Virchows Arch 2012, 461:393-398. 10.1007/s00428-012-1291-2, 22886437.
50. Starkel P, Leclercq IA. Animal models for the study of hepatic fibrosis. Best Pract Res Clin Gastroenterol 2011, 25:319-333. 10.1016/j.bpg.2011.02.004, 21497748.
51. Jennette JC, Olson JL, Schwarz MM, Silva FG. Heptinstall's Pathology of the Kidney 2007, Lippincott Williams & Wilkins, Philadelphia, PA, 6.
52. Kriz W, Gretz N, Lemley KV. Progression of glomerular diseases: is the podocyte the culprit?. Kidney Int 1998, 54:687-697. 10.1046/j.1523-1755.1998.00044.x, 9734594.
53. Hennessy A, Makris A. Preeclamptic nephropathy. Nephrology (Carlton) 2011, 16:134-143.
54. Schlondorff D, Banas B. The mesangial cell revisited: no cell is an island. J Am Soc Nephrol 2009, 20:1179-1187. 10.1681/ASN.2008050549, 19470685.
55. Hanson H, Storey H, Pagan J, Flinter F. The value of clinical criteria in identifying patients with X-linked Alport syndrome. Clin J Am Soc Nephrol 2011, 6:198-203. 10.2215/CJN.00200110, 3022243, 20884774.
56. Li JG, Ding J, Wang F, Zhang HW, et al. Drugs controlling proteinuria of patients with Alport syndrome. World J Pediatr 2009, 5:308-311. 10.1007/s12519-009-0059-5, 19911149.
57. Kashtan CE. Alport syndrome and thin glomerular basement membrane disease. J Am Soc Nephrol 1998, 9:1736-1750.
58. Sato Y, Wharram BL, Lee SK, Wickman L, Goyal M, Venkatareddy M, Chang JW, Wiggins JE, Lienczewski C, Kretzler M, Wiggins RC. Urine podocyte mRNAs mark progression of renal disease. J Am Soc Nephrol 2009, 20:1041-1052. 10.1681/ASN.2007121328, 2678045, 19389856.
59. Kriz W, LeHir M. Pathways to nephron loss starting from glomerular diseases-insights from animal models. Kidney Int 2005, 67:404-419. 10.1111/j.1523-1755.2005.67097.x, 15673288.
60. Boor P, Ostendorf T, Floege J. Renal fibrosis: novel insights into mechanisms and therapeutic targets. Nat Rev Nephrol 2010, 6:643-656. 10.1038/nrneph.2010.120, 20838416.
61. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol 2010, 21:1819-1834. 10.1681/ASN.2010080793, 20864689.
62. Nangaku M. Mechanisms of tubulointerstitial injury in the kidney: final common pathways to end-stage renal failure. Intern Med 2004, 43:9-17. 10.2169/internalmedicine.43.9, 14964574.
63. Pippin JW, Brinkkoetter PT, Cormack-Aboud FC, Durvasula RV, Hauser PV, Kowalewska J, Krofft RD, Logar CM, Marshall CB, Ohse T, Shankland SJ. Inducible rodent models of acquired podocyte diseases. Am J Physiol Renal Physiol 2009, 296:F213-F229.
64. Kliem V, Johnson RJ, Alpers CE, Yoshimura A, Couser WG, Koch KM, Floege J. Mechanisms involved in the pathogenesis of tubulointerstitial fibrosis in 5/6-nephrectomized rats. Kidney Int 1996, 49:666-678. 10.1038/ki.1996.95, 8648907.
65. Shimamura T, Morrison AB. A progressive glomerulosclerosis occurring in partial five-sixths nephrectomized rats. Am J Pathol 1975, 79:95-106. 1913032, 164779.
66. Diamond JR, Karnovsky MJ. Focal and segmental glomerulosclerosis following a single intravenous dose of puromycin aminonucleoside. Am J Pathol 1986, 122:481-487. 1888219, 3953770.
67. Kim YH, Goyal M, Kurnit D, Wharram B, Wiggins J, Holzman L, Kershaw D, Wiggins R. Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int 2001, 60:957-968. 10.1046/j.1523-1755.2001.060003957.x, 11532090.
68. Bugeon L, Danou A, Carpentier D, Langridge P, Syed N, Dallman MJ. Inducible gene silencing in podocytes: a new tool for studying glomerular function. J Am Soc Nephrol 2003, 14:786-791. 10.1097/01.ASN.0000050222.86847.EA, 12595517.
69. Shigehara T, Zaragoza C, Kitiyakara C, Takahashi H, Lu H, Moeller M, Holzman LB, Kopp JB. Inducible podocyte-specific gene expression in transgenic mice. J Am Soc Nephrol 2003, 14:1998-2003.
70. Assmann KJ, van Son JP, Dïjkman HB, Mentzel S, Wetzels JF. Antibody-induced albuminuria and accelerated focal glomerulosclerosis in the Thy-1.1 transgenic mouse. Kidney Int 2002, 62:116-126. 10.1046/j.1523-1755.2002.00428.x, 12081570.
71. Smeets B, Dijkman HB, te Loeke NA, van Son JP, Steenbergen EJ, Assmann KJ, Wetzels JF, Groenen PJ. Podocyte changes upon induction of albuminuria in Thy-1.1 transgenic mice. Nephrol Dial Transplant 2003, 18:2524-2533. 10.1093/ndt/gfg438, 14605274.
72. Chen A, Sheu LF, Ho YS, Lin YF, Chou WY, Chou TC, Lee WH. Experimental focal segmental glomerulosclerosis in mice. Nephron 1998, 78:440-452. 10.1159/000044974, 9578071.
73. Lee VW, Harris DC. Adriamycin nephropathy: a model of focal segmental glomerulosclerosis. Nephrology (Carlton) 2011, 16:30-38.
74. Van Beneden K, van Grunsven LA, Geers C, Pauwels M, Desmoulière A, Verbeelen D, Geerts A, Van den Branden C. CRBP-I in the renal tubulointerstitial compartment of healthy rats and rats with renal fibrosis. Nephrol Dial Transplant 2008, 23:3464-3471. 10.1093/ndt/gfn290, 18503097.
75. Wang Y, Wang YP, Tay YC, Harris DC. Progressive adriamycin nephropathy in mice: sequence of histologic and immunohistochemical events. Kidney Int 2000, 58:1797-1804. 10.1046/j.1523-1755.2000.00342.x, 11012915.
76. Chevalier RL, Forbes MS, Thornhill BA. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 2009, 75:1145-1152. 10.1038/ki.2009.86, 19340094.
77. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011, 21:381-395. 10.1038/cr.2011.22, 3193420, 21321607.
78. Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation?. EMBO J 2000, 19:1176-1179. 10.1093/emboj/19.6.1176, 305658, 10716917.
79. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705. 10.1016/j.cell.2007.02.005, 17320507.
80. López-Rodas G, Brosch G, Georgieva EI, Sendra R, Franco L, Loidl P. Histone deacetylase: A key enzyme for the binding of regulatory proteins to chromatin. FEBS Lett 1993, 317:175-180. 10.1016/0014-5793(93)81271-Z, 8425601.
81. Spange S, Wagner T, Heinzel T, Krämer OH. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol 2009, 41:185-198. 10.1016/j.biocel.2008.08.027, 18804549.
82. Norris KL, Lee JY, Yao TP. Acetylation goes global: the emergence of acetylation biology. Sci Signal 2009, 2:pe76. 10.1126/scisignal.297pe76, 2812806, 19920250.
83. 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. 10.1126/science.1175371, 19608861.
84. Kim HJ, Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 2011, 3:166-179. 3056563, 21416059.
85. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003, 370:737-749. 10.1042/BJ20021321, 1223209, 12429021.
86. Johnstone RW. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 2002, 1:287-299. 10.1038/nrd772, 12120280.
87. Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, Khramtsov N, Qian X, Mills E, Berghs SC, Carey N, Finn PW, Collins LS, Tumber A, Ritchie JW, Jensen PB, Lichenstein HS, Sehested M. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008, 409:581-589. 10.1042/BJ20070779, 17868033.
88. Hallows WC, Lee S, Denu JM. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci U S A 2006, 103:10230-10235. 10.1073/pnas.0604392103, 1480596, 16790548.
89. Denu JM. The Sir 2 family of protein deacetylases. Curr Opin Chem Biol 2005, 9:431-440. 10.1016/j.cbpa.2005.08.010, 16122969.
90. Gray SG, Ekstrom TJ. The human histone deacetylase family. Exp Cell Res 2001, 262:75-83. 10.1006/excr.2000.5080, 11139331.
91. Marks PA, Xu WS. Histone deacetylase inhibitors: Potential in cancer therapy. J Cell Biochem 2009, 107:600-608. 10.1002/jcb.22185, 2766855, 19459166.
92. 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 Ther 2007, 6:795-801. 10.4161/cbt.6.5.4007, 17387270.
93. 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. 10.1038/sj.onc.1208646, 15806142.
94. Taddei A, Roche D, Bickmore WA, Almouzni G. The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy?. EMBO Rep 2005, 6:520-524. 10.1038/sj.embor.7400441, 1369099, 15940285.
95. Takai N, Desmond JC, Kumagai T, Gui D, Said JW, Whittaker S, Miyakawa I, Koeffler HP. Histone deacetylase inhibitors have a profound antigrowth activity in endometrial cancer cells. Clin Cancer Res 2004, 10:1141-1149. 10.1158/1078-0432.CCR-03-0100, 14871994.
96. Williams SA, Chen LF, Kwon H, Ruiz-Jarabo CM, Verdin E, Greene WC. NF-kappaB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. EMBO J 2006, 25:139-149. 10.1038/sj.emboj.7600900, 1356344, 16319923.
97. 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, 265:17174-17179.
98. Sanderson L, Taylor GW, Aboagye EO, Alao JP, Latigo JR, Coombes RC, Vigushin DM. Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metab Dispos 2004, 32:1132-1138. 10.1124/dmd.104.000638, 15269190.
99. Elaut G, Laus G, Alexandre E, Richert L, Bachellier P, Tourwé D, Rogiers V, Vanhaecke T. A metabolic screening study of trichostatin A (TSA) and TSA-like histone deacetylase inhibitors in rat and human primary hepatocyte cultures. J Pharmacol Exp Ther 2007, 321:400-408. 10.1124/jpet.106.116202, 17218485.
100. Fraczek J, Deleu S, Lukaszuk A, Doktorova T, Tourwé D, Geerts A, Vanhaecke T, Vanderkerken K, Rogiers V. Screening of amide analogues of Trichostatin A in cultures of primary rat hepatocytes: search for potent and safe HDAC inhibitors. Invest New Drugs 2009, 27:338-346. 10.1007/s10637-008-9180-x, 18825314.
101. Richon VM, Emiliani S, Verdin E, Webb Y, Breslow R, Rifkind RA, Marks PA. A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci U S A 1998, 95:3003-3007. 10.1073/pnas.95.6.3003, 19684, 9501205.
102. 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. 10.2174/0929867043365099, 15180568.
103. Bieliauskas AV, Pflum MK. Isoform-selective histone deacetylase inhibitors. Chem Soc Rev 2008, 37:1402-1413. 10.1039/b703830p, 2593472, 18568166.
104. Davis R, Peters DH, McTavish D. Valproic acid. A reappraisal of its pharmacological properties and clinical efficacy in epilepsy. Drugs 1994, 47:332-372. 10.2165/00003495-199447020-00008, 7512905.
105. Mannaerts I, Nuytten NR, Rogiers V, Vanderkerken K, van Grunsven LA, Geerts A. Chronic administration of valproic acid inhibits activation of mouse hepatic stellate cells in vitro and in vivo. Hepatology 2010, 51:603-614. 10.1002/hep.23334, 19957378.
106. Van Beneden K, Geers C, Pauwels M, Mannaerts I, Verbeelen D, van Grunsven LA, Van den Branden C. Valproic acid attenuates proteinuria and kidney injury. J Am Soc Nephrol 2011, 22:1863-1875. 10.1681/ASN.2010111196, 3279948, 21868496.
107. Blaheta RA, Michaelis M, Driever PH, Cinatl J. Evolving anticancer drug valproic acid: insights into the mechanism and clinical studies. Med Res Rev 2005, 25:383-397. 10.1002/med.20027, 15637697.
108. Chateauvieux S, Morceau F, Dicato M, Diederich M. Molecular and therapeutic potential and toxicity of valproic acid. J Biomed Biotechnol 2010, .
109. Göttlicher M, Minucci S, Zhu P, Krämer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001, 20:6969-6978. 10.1093/emboj/20.24.6969, 125788, 11742974.
110. Gurvich N, Tsygankova OM, Meinkoth JL, Klein PS. Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res 2004, 64:1079-1086. 10.1158/0008-5472.CAN-03-0799, 14871841.
111. Johannessen CU. Mechanisms of action of valproate: a commentatory. Neurochem Int 2000, 37:103-110. 10.1016/S0197-0186(00)00013-9, 10812195.
112. Krämer OH, Zhu P, Ostendorff HP, Golebiewski M, Tiefenbach J, Peters MA, Brill B, Groner B, Bach I, Heinzel T, Göttlicher M. The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J 2003, 22:3411-3420. 10.1093/emboj/cdg315, 165640, 12840003.
113. Lagace DC, O'Brien WT, Gurvich N, Nachtigal MW, Klein PS. Valproic acid: how it works. Or not. Clin Neurosci Res 2004, 4:215-225.
114. ClinicalTrials.gov A service of the U. S. National Institutes of Health 2012, http://www.clinicaltrials.gov, ClinicalTrials.gov.
115. Federico M, Bagella L. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J Biomed Biotechnol 2011, 2011:475-641.
116. 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. 10.1186/1756-8722-3-5, 2827364, 20132536.
117. Niki T, Rombouts K, De Bleser P, De Smet K, Rogiers V, Schuppan D, Yoshida M, Gabbiani G, Geerts A. A histone deacetylase inhibitor, trichostatin A, suppresses myofibroblastic differentiation of rat hepatic stellate cells in primary culture. Hepatology 1999, 29:858-867. 10.1002/hep.510290328, 10051490.
118. Rombouts K, Niki T, Wielant A, Hellemans K, Geerts A. Trichostatin A, lead compound for development of antifibrogenic drugs. Acta Gastroenterol Belg 2001, 64:239-246.
119. Rombouts K, Knittel T, Machesky L, Braet F, Wielant A, Hellemans K, De Bleser P, Gelman I, Ramadori G, Geerts A. Actin filament formation, reorganization and migration are impaired in hepatic stellate cells under influence of trichostatin A, a histone deacetylase inhibitor. J Hepatol 2002, 37:788-796. 10.1016/S0168-8278(02)00275-1, 12445420.
120. Zhang L, Wan J, Jiang R, Wang W, Deng H, Shen Y, Zheng W, Wang Y. Protective effects of trichostatin A on liver injury in septic mice. Hepatol Res 2009, 39:931-938. 10.1111/j.1872-034X.2009.00521.x, 19456897.
121. Finkelstein RA, Li Y, Liu B, Shuja F, Fukudome E, Velmahos GC, de Moya M, Alam HB. Treatment with histone deacetylase inhibitor attenuates MAP kinase mediated liver injury in a lethal model of septic shock. J Surg Res 2010, 163:146-154. 10.1016/j.jss.2010.04.024, 20599223.
122. Elsharkawy AM, Oakley F, Lin F, Packham G, Mann DA, Mann J. The NF-kappaB p50:p50:HDAC-1 repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes. J Hepatol 2010, 53:519-527. 10.1016/j.jhep.2010.03.025, 3098379, 20579762.
123. Oakley F, Mann J, Nailard S, Smart DE, Mungalsingh N, Constandinou C, Ali S, Wilson SJ, Millward-Sadler H, Iredale JP, Mann DA. Nuclear factor-kappaB1 (p50) limits the inflammatory and fibrogenic responses to chronic injury. Am J Pathol 2005, 166:695-708. 10.1016/S0002-9440(10)62291-2, 1602348, 15743782.
124. Lee SH, Zhao YZ, Park EJ, Che XH, Seo GS, Sohn DH. 2',4',6'-Tris(methoxymethoxy) chalcone induces apoptosis by enhancing Fas-ligand in activated hepatic stellate cells. Eur J Pharmacol 2011, 658:9-15. 10.1016/j.ejphar.2011.01.067, 21349266.
125. Qin L, Han YP. Epigenetic repression of matrix metalloproteinases in myofibroblastic hepatic stellate cells through histone deacetylases 4. implication in tissue fibrosis. Am J Pathol 2010, 177:1915-1928. 10.2353/ajpath.2010.100011, 2947286, 20847282.
126. Shepard BD, Joseph RA, Kannarkat GT, Rutledge TM, Tuma DJ, Tuma PL. Alcohol-induced alterations in hepatic microtubule dynamics can be explained by impaired histone deacetylase 6 function. Hepatology 2008, 48:1671-1679. 10.1002/hep.22481, 2965519, 18697214.
127. Watanabe T, Tajima H, Hironori H, Nakagawara H, Ohnishi I, Takamura H, Ninomiya I, Kitagawa H, Fushida S, Tani T, Fujimura T, Ota T, Wakayama T, Iseki S, Harada S. Sodium valproate blocks the transforming growth factor (TGF)-beta1 autocrine loop and attenuates the TGF-beta1-induced collagen synthesis in a human hepatic stellate cell line. Int J Mol Med 2011, 28:919-925.
128. Bai X, Wu L, Liang T, Liu Z, Li J, Li D, Xie H, Yin S, Yu J, Lin Q, Zheng S. Overexpression of myocyte enhancer factor 2 and histone hyperacetylation in hepatocellular carcinoma. J Cancer Res Clin Oncol 2008, 134:83-91.
129. Santamato A, Fransvea E, Dituri F, Caligiuri A, Quaranta M, Niimi T, Pinzani M, Antonaci S, Giannelli G. Hepatic stellate cells stimulate HCC cell migration via laminin-5 production. Clin Sci (Lond) 2011, 121:159-168.
130. Yang JD, Nakamura I, Roberts LR. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin Cancer Biol 2011, 21:35-43. 10.1016/j.semcancer.2010.10.007, 3050428, 20946957.
131. Amann T, Bataille F, Spruss T, Mühlbauer M, Gäbele E, Schölmerich J, Kiefer P, Bosserhoff AK, Hellerbrand C. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Cancer Sci 2009, 100:646-653. 10.1111/j.1349-7006.2009.01087.x, 19175606.
132. van Zijl F, Mair M, Csiszar A, Schneller D, Zulehner G, Huber H, Eferl R, Beug H, Dolznig H, Mikulits W. Hepatic tumor-stroma crosstalk guides epithelial to mesenchymal transition at the tumor edge. Oncogene 2009, 28:4022-4033. 10.1038/onc.2009.253, 2900602, 19718050.
133. Sancho-Bru P, Juez E, Moreno M, Khurdayan V, Morales-Ruiz M, Colmenero J, Arroyo V, Brenner DA, Ginès P, Bataller R. Hepatocarcinoma cells stimulate the growth, migration and expression of pro-angiogenic genes in human hepatic stellate cells. Liver Int 2010, 30:31-41. 10.1111/j.1478-3231.2009.02161.x, 19929904.
134. Rangwala F, Williams KP, Smith GR, Thomas Z, Allensworth JL, Lyerly HK, Diehl AM, Morse MA, Devi GR. Differential effects of arsenic trioxide on chemosensitization in human hepatic tumor and stellate cell lines. BMC Cancer 2012, 12:402. 10.1186/1471-2407-12-402, 3517386, 22963400.
135. Coulouarn C, Corlu A, Glaise D, Guénon I, Thorgeirsson SS, Clément B. Hepatocyte-stellate cell cross-talk in the liver engenders a permissive inflammatory microenvironment that drives progression in hepatocellular carcinoma. Cancer Res 2012, 72:2533-2542. 10.1158/0008-5472.CAN-11-3317, 22419664.
136. Zhang W, Kone BC. NF-kappaB inhibits transcription of the H(+)-K(+)-ATPase alpha(2)-subunit gene: role of histone deacetylases. Am J Physiol Renal Physiol 2002, 283:F904-F911.
137. Yu Z, Zhang W, Kone BC. Histone deacetylases augment cytokine induction of the iNOS gene. J Am Soc Nephrol 2002, 13:2009-2017. 10.1097/01.ASN.0000024253.59665.F1, 12138131.
138. Yu Z, Kone BC. Targeted histone H4 acetylation via phosphoinositide 3-kinase- and p70s6-kinase-dependent pathways inhibits iNOS induction in mesangial cells. Am J Physiol Renal Physiol 2006, 290:F496-F502. 10.1152/ajprenal.00316.2005, 16174862.
139. Freidkin I, Herman M, Tobar A, Chagnac A, Ori Y, Korzets A, Gafter U. Effects of histone deacetylase inhibitors on rat mesangial cells. Am J Physiol Renal Physiol 2010, 298:F426-F434. 10.1152/ajprenal.00107.2009, 19923417.
140. Wang Q, Usinger W, Nichols B, Gray J, Xu L, Seeley TW, Brenner M, Guo G, Zhang W, Oliver N, Lin A, Yeowell D. Cooperative interaction of CTGF and TGF-beta in animal models of fibrotic disease. Fibrogenesis Tissue Repair 2011, 4:4. 10.1186/1755-1536-4-4, 3042008, 21284856.
141. Komorowsky C, Ocker M, Goppelt-Struebe M. Differential regulation of connective tissue growth factor in renal cells by histone deacetylase inhibitors. J Cell Mol Med 2009, 13:2353-2364. 10.1111/j.1582-4934.2008.00674.x, 20141616.
142. Kroening S, Neubauer E, Wullich B, Aten J, Goppelt-Struebe M. Characterization of connective tissue growth factor expression in primary cultures of human tubular epithelial cells: modulation by hypoxia. Am J Physiol Renal Physiol 2010, 298:F796-F806. 10.1152/ajprenal.00528.2009, 20032117.
143. Yoshikawa M, Hishikawa K, Marumo T, Fujita T. Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells. J Am Soc Nephrol 2007, 18:58-65. 10.1681/ASN.2005111187, 17135397.
144. 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. 10.1128/MCB.24.1.306-319.2004, 303344, 14673164.
145. Pang M, Zhuang S. Histone deacetylase: a potential therapeutic target for fibrotic disorders. J Pharmacol Exp Ther 2010, 335:266-272. 10.1124/jpet.110.168385, 2967408, 20719940.
146. Arany I, Herbert J, Herbert Z, Safirstein RL. Restoration of CREB function ameliorates cisplatin cytotoxicity in renal tubular cells. Am J Physiol Renal Physiol 2008, 294:F577-F581. 10.1152/ajprenal.00487.2007, 18094030.
147. Dong G, Luo J, Kumar V, Dong Z. Inhibitors of histone deacetylases suppress cisplatin-induced p53 activation and apoptosis in renal tubular cells. Am J Physiol Renal Physiol 2010, 298:F293-F300. 10.1152/ajprenal.00410.2009, 2822515, 19889954.
148. Dong G, Wang L, Wang CY, Yang T, Kumar MV, Dong Z. Induction of apoptosis in renal tubular cells by histone deacetylase inhibitors, a family of anticancer agents. J Pharmacol Exp Ther 2008, 325:978-984. 10.1124/jpet.108.137398, 18310471.
149. Yoshikawa M, Hishikawa K, Idei M, Fujita T. Trichostatin a prevents TGF-beta1-induced apoptosis by inhibiting ERK activation in human renal tubular epithelial cells. Eur J Pharmacol 2010, 642:28-36. 10.1016/j.ejphar.2010.05.055, 20553909.
150. Pang M, Ma L, Liu N, Ponnusamy M, Zhao TC, Yan H, Zhuang S. Histone deacetylase 1/2 mediates proliferation of renal interstitial fibroblasts and expression of cell cycle proteins. J Cell Biochem 2011, 112:2138-2148. 10.1002/jcb.23135, 21465537.
151. Marumo T, Hishikawa K, Yoshikawa M, Hirahashi J, Kawachi S, Fujita T. Histone deacetylase modulates the proinflammatory and -fibrotic changes in tubulointerstitial injury. Am J Physiol Renal Physiol 2010, 298:F133-F141. 10.1152/ajprenal.00400.2009, 19906951.
152. Li HF, Cheng CF, Liao WJ, Lin H, Yang RB. ATF3-mediated epigenetic regulation protects against acute kidney injury. J Am Soc Nephrol 2010, 21:1003-1013. 10.1681/ASN.2009070690, 2900964, 20360311.
153. Kinugasa F, Noto T, Matsuoka H, Urano Y, Sudo Y, Takakura S, Mutoh S. Prevention of renal interstitial fibrosis via histone deacetylase inhibition in rats with unilateral ureteral obstruction. Transpl Immunol 2010, 23:18-23. 10.1016/j.trim.2010.02.003, 20206695.
154. Pang M, Kothapally J, Mao H, Tolbert E, Ponnusamy M, Chin YE, Zhuang S. Inhibition of histone deacetylase activity attenuates renal fibroblast activation and interstitial fibrosis in obstructive nephropathy. Am J Physiol Renal Physiol 2009, 297:F996-F1005. 10.1152/ajprenal.00282.2009, 2775583, 19640900.
155. Advani A, Huang Q, Thai K, Advani SL, White KE, Kelly DJ, Yuen DA, Connelly KA, Marsden PA, Gilbert RE. Long-term administration of the histone deacetylase inhibitor vorinostat attenuates renal injury in experimental diabetes through an endothelial nitric oxide synthase-dependent mechanism. Am J Pathol 2011, 178:2205-2214. 10.1016/j.ajpath.2011.01.044, 3081208, 21514434.
156. Gilbert RE, Huang Q, Thai K, Advani SL, Lee K, Yuen DA, Connelly KA, Advani A. Histone deacetylase inhibition attenuates diabetes-associated kidney growth: potential role for epigenetic modification of the epidermal growth factor receptor. Kidney Int 2011, 79:1312-1321. 10.1038/ki.2011.39, 21389970.
157. Noh H, Oh EY, Seo JY, Yu MR, Kim YO, Ha H, Lee HB. Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-beta1-induced renal injury. Am J Physiol Renal Physiol 2009, 297:F729-F739. 10.1152/ajprenal.00086.2009, 19553350.
158. Marumo T, Hishikawa K, Yoshikawa M, Fujita T. Epigenetic regulation of BMP7 in the regenerative response to ischemia. J Am Soc Nephrol 2008, 19:1311-1320. 10.1681/ASN.2007091040, 2440290, 18322163.
159. Zacharias N, Sailhamer EA, Li Y, Liu B, Butt MU, Shuja F, Velmahos GC, de Moya M, Alam HB. Histone deacetylase inhibitors prevent apoptosis following lethal hemorrhagic shock in rodent kidney cells. Resuscitation 2011, 82:105-109. 10.1016/j.resuscitation.2010.09.469, 21036453.
160. Brilli LL, Swanhart LM, de Caestecker MP, Hukriede NA, et al. HDAC inhibitors in kidney development and disease. Pediatr Nephrol 2012,
161. Shakespear MR, Halili MA, Irvine KM, Fairlie DP, Sweet MJ. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 2011, 32:335-343. 10.1016/j.it.2011.04.001, 21570914.
162. Sweet MJ, Shakespear MR, Kamal NA, Fairlie DP. HDAC inhibitors: modulating leukocyte differentiation, survival, proliferation and inflammation. Immunol Cell Biol 2012, 90:14-22. 10.1038/icb.2011.88, 22024621.
163. Wang D. Computational studies on the histone deacetylases and the design of selective histone deacetylase inhibitors. Curr Top Med Chem 2009, 9:241-256. 10.2174/156802609788085287, 2766262, 19355989.
164. Hellebrekers DM, Griffioen AW, van Engeland M. Dual targeting of epigenetic therapy in cancer. Biochim Biophys Acta 2006, 1775:7-91.
165. Yi TZ, Li J, Han X, Guo J, Qu Q, Guo L, Sun HD, Tan WH. DNMT inhibitors and HDAC Inhibitors regulate E-Cadherin and Bcl-2 expression in endometrial carcinoma in vitro and in vivo. Chemotherapy 2012, 58:19-29. 10.1159/000333077, 22343305.
166. Mann DA, Mann J. Epigenetic regulation of hepatic stellate cell activation. J Gastroenterol Hepatol 2008, 23(Suppl 1):S108-S111.
167. Mann J, Chu DC, Maxwell A, Oakley F, Zhu NL, Tsukamoto H, Mann DA. MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterology 2009, 138:705-714. 2819585, 19843474.
168. Mann J, Oakley F, Akiboye F, Elsharkawy A, Thorne AW, Mann DA. Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: implications for wound healing and fibrogenesis. Cell Death Differ 2007, 14:275-285. 10.1038/sj.cdd.4401979, 16763620.
169. Kee HJ, Kook H. Roles and targets of class I and IIa histone deacetylases in cardiac hypertrophy. J Biomed Biotechnol 2011, 2011:928326. 2997602, 21151616.
170. Wiech NL, Fisher JF, Helquist P, Wiest O. Inhibition of histone deacetylases: a pharmacological approach to the treatment of non-cancer disorders. Curr Top Med Chem 2009, 9(3):257-271. 10.2174/156802609788085241, 19355990.
171. Rishikof DC, Ricupero DA, Liu H, Goldstein RH. Phenylbutyrate decreases type I collagen production in human lung fibroblasts. J Cell Biochem 2004, 91:740-748. 10.1002/jcb.10742, 14991765.