Tubastatin A suppresses renal fibrosis via regulation of epigenetic histone modification and Smad3-dependent fibrotic genes

Vascular Pharmacology

Volumn 72, Issue , 2015, Pages 130-140

  Choi, Sin Young ^a   Ryu, Yuhee ^a   Kee, Hae Jin ^a   Cho, Soo Na ^a   Kim, Gwi Ran ^a   Cho, Jae Yeong ^a   Kim, Hyung Seok ^b   Kim, In Kyeom ^c   Jeong, Myung Ho ^a  

^a Chonnam National University Medical School   (South Korea)

^b Chonnam National University Medical School   (South Korea)

^c Kyungpook National University School of Medicine   (South Korea)

Author keywords

Collagen type I; Fibrosis; Histone deacetylase 6; Inflammation; Tubastatin A

Indexed keywords

ANGIOTENSIN II; COLLAGEN TYPE 1; DEOXYCORTICOSTERONE ACETATE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; HISTONE H4; SMAD3 PROTEIN; SMALL INTERFERING RNA; TUBASTATIN A; UNCLASSIFIED DRUG; HDAC6 PROTEIN, MOUSE; HISTONE; HYDROXAMIC ACID; INDOLE DERIVATIVE; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ACETYLATION; ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BLOOD PRESSURE; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; GENE REPRESSION; HISTONE MODIFICATION; HYPERTENSION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; KIDNEY FIBROSIS; KIDNEY INJURY; MALE; MARKER GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; FIBROSIS; GENETIC EPIGENESIS; INFLAMMATION; INSTITUTE FOR CANCER RESEARCH MOUSE; KIDNEY; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANGIOTENSIN II; ANIMALS; CELLS, CULTURED; COLLAGEN TYPE I; EPIGENESIS, GENETIC; FIBROSIS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HYDROXAMIC ACIDS; INDOLES; INFLAMMATION; KIDNEY; MALE; MICE; MICE, INBRED ICR; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84940759369     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2015.04.006     Document Type: Article

References (43)

1. Androulakis E., Tousoulis D., Papageorgiou N., Latsios G., Siasos G., Tsioufis C., Giolis A., Stefanadis C. Inflammation in hypertension: current therapeutic approaches. Curr Pharm Des 2011, 17:4121-4131.
2. Asano Y., Trojanowska M. Fli1 represses transcription of the human alpha2(I) collagen gene by recruitment of the HDAC1/p300 complex. PLoS One 2013, 8. e74930.
3. Blom I.E., Goldschmeding R., Leask A. Gene regulation of connective tissue growth factor: new targets for antifibrotic therapy?. Matrix Biol J Int Soc Matrix Biol 2002, 21:473-482.
4. Cardinale J.P., Sriramula S., Pariaut R., Guggilam A., Mariappan N., Elks C.M., Francis J. HDAC inhibition attenuates inflammatory, hypertrophic, and hypertensive responses in spontaneously hypertensive rats. Hypertension 2010, 56:437-444.
5. Christov M. Fibroblast growth factor 23 in acute kidney injury. Curr Opin Nephrol Hypertens 2014, 23:340-345.
6. Chuang P.Y., Menon M.C., He J.C. Molecular targets for treatment of kidney fibrosis. J Mol Med 2013, 91:549-559.
7. Ciarlo E., Savva A., Roger T. Epigenetics in sepsis: targeting histone deacetylases. Int J Antimicrob Agents 2013, 42(Suppl.):S8-S12.
8. Duan W.J., Yu X., Huang X.R., Yu J.W., Lan H.Y. Opposing roles for Smad2 and Smad3 in peritoneal fibrosis in vivo and in vitro. Am J Pathol 2014, 184:2275-2284.
9. Gao X., Li J., Huang H., Li X. Connective tissue growth factor stimulates renal cortical myofibroblast-like cell proliferation and matrix protein production. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society 2008, 16:408-415.
10. Ghosh A.K., Bhattacharyya S., Wei J., Kim S., Barak Y., Mori Y., Varga J. Peroxisome proliferator-activated receptor-gamma abrogates Smad-dependent collagen stimulation by targeting the p300 transcriptional coactivator. FASEB J 2009, 23:2968-2977.
11. Gradilone S.A., Habringer S., Masyuk T.V., Howard B.N., Masyuk A.I., Larusso N.F. HDAC6 is overexpressed in cystic cholangiocytes and its inhibition reduces cystogenesis. Am J Pathol 2014, 184:600-608.
12. Haakenson J., Zhang X. HDAC6 and ovarian cancer. Int J Mol Sci 2013, 14:9514-9535.
13. Iyer A., Fenning A., Lim J., Le G.T., Reid R.C., Halili M.A., Fairlie D.P., Brown L. Antifibrotic activity of an inhibitor of histone deacetylases in DOCA-salt hypertensive rats. Br J Pharmacol 2010, 159:1408-1417.
14. Kagami S. Involvement of glomerular renin-angiotensin system (RAS) activation in the development and progression of glomerular injury. Clin Exp Nephrol 2012, 16:214-220.
15. Kee H.J., Bae E.H., Park S., Lee K.E., Suh S.H., Kim S.W., Jeong M.H. HDAC inhibition suppresses cardiac hypertrophy and fibrosis in DOCA-salt hypertensive rats via regulation of HDAC6/HDAC8 enzyme activity. Kidney Blood Press Res 2013, 37:229-239.
16. Kee H.J., Kim J.R., Nam K.I., Park H.Y., Shin S., Kim J.C., Shimono Y., Takahashi M., Jeong M.H., Kim N., Kim K.K., Kook H. Enhancer of polycomb1, a novel homeodomain only protein-binding partner, induces skeletal muscle differentiation. J Biol Chem 2007, 282:7700-7709.
17. Kee H.J., Sohn I.S., Nam K.I., Park J.E., Qian Y.R., Yin Z., Ahn Y., Jeong M.H., Bang Y.J., Kim N., Kim J.K., Kim K.K., Epstein J.A., Kook H. Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 2006, 113:51-59.
18. Kim J.R., Kee H.J., Kim J.Y., Joung H., Nam K.I., Eom G.H., Choe N., Kim H.S., Kim J.C., Kook H., Seo S.B. Enhancer of polycomb1 acts on serum response factor to regulate skeletal muscle differentiation. J Biol Chem 2009, 284:16308-16316.
19. Lan H.Y. Diverse roles of TGF-beta/Smads in renal fibrosis and inflammation. Int J Biol Sci 2011, 7:1056-1067.
20. Lee H.A., Lee D.Y., Cho H.M., Kim S.Y., Iwasaki Y., Kim I.K. Histone deacetylase inhibition attenuates transcriptional activity of mineralocorticoid receptor through its acetylation and prevents development of hypertension. Circ Res 2013, 112:1004-1012.
21. Lemon D.D., Horn T.R., Cavasin M.A., Jeong M.Y., Haubold K.W., Long C.S., Irwin D.C., McCune S.A., Chung E., Leinwand L.A., McKinsey T.A. Cardiac HDAC6 catalytic activity is induced in response to chronic hypertension. J Mol Cell Cardiol 2011, 51:41-50.
22. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev 2005, 19:2783-2810.
23. Meng X.M., Huang X.R., Chung A.C., Qin W., Shao X., Igarashi P., Ju W., Bottinger E.P., Lan H.Y. Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis. J Am Soc Nephrol 2010, 21:1477-1487.
24. Meng X.M., Nikolic-Paterson D.J., Lan H.Y. Inflammatory processes in renal fibrosis. Nat Rev Nephrol 2014, 10:493-503.
25. Noble N.A., Border W.A. Angiotensin II in renal fibrosis: should TGF-beta rather than blood pressure be the therapeutic target?. Semin Nephrol 1997, 17:455-466.
26. Okada H., Kikuta T., Kobayashi T., Inoue T., Kanno Y., Takigawa M., Sugaya T., Kopp J.B., Suzuki H. Connective tissue growth factor expressed in tubular epithelium plays a pivotal role in renal fibrogenesis. J Am Soc Nephrol 2005, 16:133-143.
27. Petersen M., Pardali E., van der Horst G., Cheung H., van den Hoogen C., van der Pluijm G., Ten Dijke P. Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis. Oncogene 2010, 29:1351-1361.
28. Royce S.G., Karagiannis T.C. Histone deacetylases and their inhibitors: new implications for asthma and chronic respiratory conditions. Curr Opin Allergy Clin Immunol 2014, 14:44-48.
29. Ruilope L.M., Bakris G.L. Renal function and target organ damage in hypertension. Eur Heart J 2011, 32:1599-1604.
30. Ruiz-Ortega M., Rodriguez-Vita J., Sanchez-Lopez E., Carvajal G., Egido J. TGF-beta signaling in vascular fibrosis. Cardiovasc Res 2007, 74:196-206.
31. Sanchez-Lopez E., Rayego S., Rodrigues-Diez R., Rodriguez J.S., Rodriguez-Vita J., Carvajal G., Aroeira L.S., Selgas R., Mezzano S.A., Ortiz A., Egido J., Ruiz-Ortega M. CTGF promotes inflammatory cell infiltration of the renal interstitium by activating NF-kappaB. J Am Soc Nephrol 2009, 20:1513-1526.
32. Selvi R.B., Kundu T.K. Reversible acetylation of chromatin: implication in regulation of gene expression, disease and therapeutics. Biotechnol J 2009, 4:375-390.
33. Tampe D., Zeisberg M. Potential approaches to reverse or repair renal fibrosis. Nat Rev Nephrol 2014, 10:226-237.
34. To W.S., Midwood K.S. Plasma and cellular fibronectin: distinct and independent functions during tissue repair. Fibrogenesis Tissue Repair 2011, 4:21.
35. Usui T., Okada M., Mizuno W., Oda M., Ide N., Morita T., Hara Y., Yamawaki H. HDAC4 mediates development of hypertension via vascular inflammation in spontaneous hypertensive rats. Am J Physiol Heart Circ Physiol 2012, 302:H1894-H1904.
36. Vishwakarma S., Iyer L.R., Muley M., Singh P.K., Shastry A., Saxena A., Kulathingal J., Vijaykanth G., Raghul J., Rajesh N., Rathinasamy S., Kachhadia V., Kilambi N., Rajgopal S., Balasubramanian G., Narayanan S. Tubastatin, a selective histone deacetylase 6 inhibitor shows anti-inflammatory and anti-rheumatic effects. Int Immunopharmacol 2013, 16:72-78.
37. Wang B., Jha J.C., Hagiwara S., McClelland A.D., Jandeleit-Dahm K., Thomas M.C., Cooper M.E., Kantharidis P. Transforming growth factor-beta1-mediated renal fibrosis is dependent on the regulation of transforming growth factor receptor 1 expression by let-7b. Kidney Int 2014, 85:352-361.
38. Weinrauch L.A., Desai A.S., Skali H., D'Elia J.A. Risk stratification of resistant hypertension in chronic kidney disease. J Am Coll Cardiol 2013, 61:2468-2470.
39. Yamashita S., Maeshima A., Kojima I., Nojima Y. Activin A is a potent activator of renal interstitial fibroblasts. J Am Soc Nephrol 2004, 15:91-101.
40. Yang F., Chung A.C., Huang X.R., Lan H.Y. Angiotensin II induces connective tissue growth factor and collagen I expression via transforming growth factor-beta-dependent and -independent Smad pathways: the role of Smad3. Hypertension 2009, 54:877-884.
41. Yu C.C., Tsai C.H., Hsu H.I., Chang Y.C. Elevation of S100A4 expression in buccal mucosal fibroblasts by arecoline: involvement in the pathogenesis of oral submucous fibrosis. PLoS One 2013, 8. e55122.
42. Zhang D., Wu C.T., Qi X., Meijering R.A., Hoogstra-Berends F., Tadevosyan A., Cubukcuoglu Deniz G., Durdu S., Akar A.R., Sibon O.C., Nattel S., Henning R.H., Brundel B.J. Activation of histone deacetylase-6 induces contractile dysfunction through derailment of alpha-tubulin proteostasis in experimental and human atrial fibrillation. Circulation 2014, 129:346-358.
43. Zhao L., Chen C.N., Hajji N., Oliver E., Cotroneo E., Wharton J., Wang D., Li M., McKinsey T.A., Stenmark K.R., Wilkins M.R. Histone deacetylation inhibition in pulmonary hypertension: therapeutic potential of valproic acid and suberoylanilide hydroxamic acid. Circulation 2012, 126:455-467.