Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-β1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats

Food and Chemical Toxicology

Volumn 73, Issue , 2014, Pages 127-139

  Khan, Sabbir ^a   Jena, Gopabandhu ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

Apoptosis; DNA damage; Fibrosis; HDAC inhibitor; Juvenile diabetes; Sodium butyrate

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BUTYRIC ACID; COLLAGEN; COLLAGEN TYPE 1; CREATININE; DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBRONECTIN; GLUCOSE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; STREPTOZOCIN; TRANSFORMING GROWTH FACTOR BETA1; UREA; FIBRIN; HISTONE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIABETIC NEPHROPATHY; DNA DAMAGE; FIBROGENESIS; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY FUNCTION; MALE; MOLECULAR MECHANICS; NICK END LABELING; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UREA BLOOD LEVEL; WESTERN BLOTTING; ACETYLATION; ANIMAL; BIOSYNTHESIS; COMET ASSAY; DRUG EFFECTS; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ACETYLATION; ANIMALS; APOPTOSIS; BUTYRIC ACID; COMET ASSAY; DIABETES MELLITUS, EXPERIMENTAL; DNA DAMAGE; FIBRIN; HISTONE DEACETYLASE INHIBITORS; HISTONES; KIDNEY; MALE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; STREPTOZOCIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84908051558     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2014.08.010     Document Type: Article

References (45)

1. Advani A., Huang Q., Thai K., Advani S.L., White K.E., Kelly D.J., Yuen D.A., Connelly K.A., Marsden P.A., Gilbert R.E. 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.
2. Aguilar E.C., Leonel A.J., Teixeira L.G., Silva A.R., Silva J.F., Pelaez J.M., Capettini L.S., Lemos V.S., Santos R.A., Alvarez-Leite J.I. Butyrate impairs atherogenesis by reducing plaque inflammation and vulnerability and decreasing NFkappaB activation. Nutr. Metab. Cardiovasc. Dis. 2014, 24:606-613. 10.1016/j.numecd.2014.01.002.
3. Aher, J., Khan, S., Jain, S., Tikoo, K., Jena, G., 2014. Valproate ameliorates thioacetamide-induced fibrosis by hepatic stellate cell inactivation. Hum. Exp. Toxicol. First published on May 8, 2014 as (in press). doi:10.1177/0960327114531992.
4. Arany I., Herbert J., Herbert Z., Safirstein R.L. Restoration of CREB function ameliorates cisplatin cytotoxicity in renal tubular cells. Am. J. Physiol. Renal Physiol. 2008, 294:F577-F581.
5. Arora M.K., Singh U.K. Molecular mechanisms in the pathogenesis of diabetic nephropathy: an update. Vascul. Pharmacol. 2013, 58:259-271.
6. Ban C.R., Twigg S.M. Fibrosis in diabetes complications: pathogenic mechanisms and circulating and urinary markers. Vasc. Health Risk Manag. 2008, 4:575-596.
7. Boffa L.C., Vidali G., Mann R.S., Allfrey V.G. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J. Biol. Chem. 1978, 253:3364-3366.
8. Carew J.S., Giles F.J., Nawrocki S.T. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 2008, 269:7-17.
9. Christensen D.P., Dahllof M., Lundh M., Rasmussen D.N., Nielsen M.D., Billestrup N., Grunnet L.G., Mandrup-Poulsen T. Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol. Med. 2011, 17:378-390.
10. Chung Y.L., Wang A.J., Yao L.F. Antitumor histone deacetylase inhibitors suppress cutaneous radiation syndrome: implications for increasing therapeutic gain in cancer radiotherapy. Mol. Cancer Ther. 2004, 3:317-325.
11. 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. 2009, 298:F293-F300.
12. Gilbert R.E., Huang Q., Thai K., Advani S.L., Lee K., Yuen D.A., Connelly K.A., 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.
13. Gomez-Garre D., Largo R., Tejera N., Fortes J., Manzarbeitia F., Egido J. Activation of NF-kappaB in tubular epithelial cells of rats with intense proteinuria: role of angiotensin II and endothelin-1. Hypertension 2001, 37:1171-1178.
14. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 1995, 21:1465-1468.
15. Hemmatazad H., Rodrigues H.M., Maurer B., Brentano F., Pileckyte M., Distler J.H., Gay R.E., Michel B.A., Gay S., Huber L.C., Distler O., Jungel A. Histone deacetylase 7, a potential target for the antifibrotic treatment of systemic sclerosis. Arthritis Rheum. 2009, 60:1519-1529.
16. Hirose K., Osterby R., Nozawa M., Gundersen H.J. Development of glomerular lesions in experimental long-term diabetes in the rat. Kidney Int. 1982, 21:689-695.
17. Ilonen J., Vaarala O., Akerblom H.K., Knip M. Environmental factors and primary prevention in type 1 diabetes. Pediatr. Endocrinol. Diabetes Metab. 2009, 15:227-232.
18. Khan S., Jena G. Effect of sodium valproate on the toxicity of cyclophosphamide in the testes of mice: influence of pre-and post-treatment schedule. Toxicol. Int. 2013, 20:68.
19. Khan S., Jena G. Sodium valproate, a histone deacetylase inhibitor ameliorates cyclophosphamide-induced genotoxicity and cytotoxicity in the colon of mice. J. Basic Clin. Physiol. Pharmacol. 2014, 1-11.
20. Khan S., Jena G.B. Protective role of sodium butyrate, a HDAC inhibitor on beta-cell proliferation, function and glucose homeostasis through modulation of p38/ERK MAPK and apoptotic pathways: study in juvenile diabetic rat. Chem. Biol. Interact. 2014, 213C:1-12.
21. Khan S., Ahmad T., Parekh C.V., Trivedi P.P., Kushwaha S., Jena G. Investigation on sodium valproate induced germ cell damage, oxidative stress and genotoxicity in male Swiss mice. Reprod. Toxicol. 2011, 32:385-394.
22. 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.
23. Lawless M.W., Norris S., O'Byrne K.J., Gray S.G. Targeting histone deacetylases for the treatment of disease. J. Cell Mol. Med. 2009, 13:826-852.
24. Layden B.T., Angueira A.R., Brodsky M., Durai V., Lowe W.L. Short chain fatty acids and their receptors: new metabolic targets. Transl. Res. 2012, 12:S1931-S5244.
25. Lee H.B., Noh H., Seo J.Y., Yu M.R., Ha H. Histone deacetylase inhibitors: a novel class of therapeutic agents in diabetic nephropathy. Kidney Int. Suppl. 2007, S61-S66.
26. Li N., Hatch M., Wasserfall C.H., Douglas-Escobar M., Atkinson M.A., Schatz D.A., Neu J. Butyrate and type 1 diabetes mellitus: can we fix the intestinal leak?. J. Pediatr. Gastroenterol. Nutr. 2010, 51:414-417.
27. Liu N., He S., Ma L., Ponnusamy M., Tang J., Tolbert E., Bayliss G., Zhao T.C., Yan H., Zhuang S. Blocking the Class I histone deacetylase ameliorates renal fibrosis and inhibits renal fibroblast activation via modulating TGF-beta and EGFR signaling. PLoS ONE 2013, 8:e54001.
28. Machado R.A., Constantino Lde S., Tomasi C.D., Rojas H.A., Vuolo F.S., Vitto M.F., Cesconetto P.A., de Souza C.T., Ritter C., Dal-Pizzol F. Sodium butyrate decreases the activation of NF-kappaB reducing inflammation and oxidative damage in the kidney of rats subjected to contrast-induced nephropathy. Nephrol. Dial. Transplant. 2012, 27:3136-3140.
29. Marchion D.C., Bicaku E., Daud A.I., Sullivan D.M., Munster P.N. In vivo synergy between topoisomerase II and histone deacetylase inhibitors: predictive correlates. Mol. Cancer Ther. 2005, 4:1993-2000.
30. Maremanda K.P., Khan S., Jena G. Zinc protects cyclophosphamide-induced testicular damage in rat: involvement of metallothionein, tesmin and Nrf2. Biochem. Biophys. Res. Commun. 2014, 445:591-596.
31. 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.
32. Mezzano S., Aros C., Droguett A., Burgos M.E., Ardiles L., Flores C., Schneider H., Ruiz-Ortega M., Egido J. NF-kappaB activation and overexpression of regulated genes in human diabetic nephropathy. Nephrol. Dial. Transplant. 2004, 19:2505-2512.
33. Miller A.C., Cohen S., Stewart M., Rivas R., Lison P. Radioprotection by the histone deacetylase inhibitor phenylbutyrate. Radiat. Environ. Biophys. 2011, 50:585-596.
34. Noh H., Oh E.Y., Seo J.Y., Yu M.R., Kim Y.O., Ha H., Lee H.B. 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.
35. Nor C., Sassi F.A., de Farias C.B., Schwartsmann G., Abujamra A.L., Lenz G., Brunetto A.L., Roesler R. The histone deacetylase inhibitor sodium butyrate promotes cell death and differentiation and reduces neurosphere formation in human medulloblastoma cells. Mol. Neurobiol. 2013, 48:533-543.
36. Pang M., Ma L., Liu N., Ponnusamy M., Zhao T.C., 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.
37. Riser B.L., Najmabadi F., Perbal B., Rambow J.A., Riser M.L., Sukowski E., Yeger H., Riser S.C., Peterson D.R. CCN3/CCN2 regulation and the fibrosis of diabetic renal disease. J. Cell Commun. Signal. 2010, 4:39-50.
38. Samuelsson U., Ludvigsson J. The concentrations of short-chain fatty acids and other microflora-associated characteristics in faeces from children with newly diagnosed Type 1 diabetes and control children and their family members. Diabet. Med. 2004, 21:64-67.
39. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25years of image analysis. Nat. Methods 2012, 9:671-675.
40. Sharma B., Singh N. Attenuation of vascular dementia by sodium butyrate in streptozotocin diabetic rats. Psychopharmacology 2011, 215:677-687.
41. Villeneuve L.M., Natarajan R. The role of epigenetics in the pathology of diabetic complications. Am. J. Physiol. Renal Physiol. 2010, 299:F14-F25.
42. Wang X., Wei X., Pang Q., Yi F. Histone deacetylases and their inhibitors: molecular mechanisms and therapeutic implications in diabetes mellitus. Acta Pharmaceut. Sin. 2012, 2:387-395.
43. Yokoi H., Mukoyama M., Mori K., Kasahara M., Suganami T., Sawai K., Yoshioka T., Saito Y., Ogawa Y., Kuwabara T., Sugawara A., Nakao K. Overexpression of connective tissue growth factor in podocytes worsens diabetic nephropathy in mice. Kidney Int. 2008, 73:446-455.
44. Yu Z., Kone B.C. 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.
45. Yu Z., Zhang W., Kone B.C. Histone deacetylases augment cytokine induction of the iNOS gene. J. Am. Soc. Nephrol. 2002, 13:2009-2017.