The role of butyrate, a histone deacetylase inhibitor in diabetes mellitus: Experimental evidence for therapeutic intervention

Epigenomics

Volumn 7, Issue 4, 2015, Pages 669-680

  Khan, Sabbir ^a   Jena, Gopabandhu ^a  

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

Author keywords

butyrate; diabetes; epigenetics; HDAC inhibitors; histone deacetylase; insulin signaling; cell

Indexed keywords

BUTYRIC ACID; BUTYRIC ACID DERIVATIVE; HISTONE DEACETYLASE INHIBITOR;

APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN; DIABETES MELLITUS; DRUG MECHANISM; ENERGY METABOLISM; ENZYME INHIBITION; EPIGENETICS; GLUCOSE HOMEOSTASIS; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANIMAL; GENETIC EPIGENESIS; GENETICS;

ANIMALS; BUTYRATES; DIABETES MELLITUS; EPIGENESIS, GENETIC; HISTONE DEACETYLASE INHIBITORS; HUMANS;

EID: 84933566722     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.15.20     Document Type: Review

References (93)

1. Van Belle TL, Coppieters KT, Von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol. Rev. 91(1), 79-118 (2011).
2. Khan S, Jena G, Tikoo K, Kumar V. Valproate attenuates the proteinuria, podocyte and renal injury by facilitating autophagy and inactivation of NF-kappaB/iNOS signaling in diabetic rat. Biochimie. 110, 1-16 (2015).
3. Pirola L, Balcerczyk A, Okabe J, El-Osta A. Epigenetic phenomena linked to diabetic complications. Nat. Rev. Endocrinol. 6(12), 665-675 (2010).
4. Ilonen J, Vaarala O, Akerblom HK, Knip M. Environmental factors and primary prevention in Type 1 diabetes. Pediatr. Endocrinol. Diabetes Metab. 15(4), 227-232 (2009).
5. Miao F, Chen Z, Zhang L et al. Profiles of epigenetic histone post-translational modifications at Type 1 diabetes susceptible genes. J. Biol. Chem. 287(20), 16335-16345 (2012).
6. Volkmar M, Dedeurwaerder S, Cunha DA et al. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from Type 2 diabetic patients. EMBO J. 31(6), 1405-1426 (2012).
7. Bramswig NC, Kaestner KH. Epigenetics and diabetes treatment: an unrealized promise? Trends Endocrinol. Metab. 23(6), 286-291 (2012).
8. Gray SG, De Meyts P. Role of histone and transcription factor acetylation in diabetes pathogenesis. Diabetes Metab. Res. Rev. 21(5), 416-433 (2005).
9. Lawless MW, Norris S, O'byrne KJ, Gray SG. Targeting histone deacetylases for the treatment of disease. J. Cell. Mol. Med. 13(5), 826-852 (2009).
10. Keating ST, El-Osta A. Epigenetic changes in diabetes. Clin. Genet. 84(1), 1-10 (2013).
11. Karpac J, Jasper H. Metabolic homeostasis: HDACs take center stage. Cell 145(4), 497-499 (2011).
12. Pham TX, Lee J. Dietary regulation of histone acetylases and deacetylases for the prevention of metabolic diseases. Nutrients 4(12), 1868-1886 (2012).
13. Kariz S, Petrovic D. Minor association of kinase insert domain-containing receptor gene polymorphism (rs2071559) with myocardial infarction in Caucasians with Type 2 diabetes mellitus: case-control cross-sectional study. Clin. Biochem. 47(16-17), 192-196 (2014).
14. Petrovic D. Candidate genes for proliferative diabetic retinopathy. BioMed Res. Int. 2013, 540416 (2013).
15. Christensen DP, Dahllof M, Lundh M et al. Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol. Med. 17(5-6), 378-390 (2011).
16. Mihaylova MM, Vasquez DS, Ravnskjaer K et al. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145(4), 607-621 (2011).
17. Aher JS, Khan S, Jain S, Tikoo K, Jena G. Valproate ameliorates thioacetamide-induced fibrosis by hepatic stellate cell inactivation. Hum. Exp. Toxicol. 34(1), 44-55 (2015).
18. 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. 1-11 (2014).
19. Villeneuve LM, Natarajan R. The role of epigenetics in the pathology of diabetic complications. Am. J. Physiol. Renal Physiol. 299(1), F14-F25 (2010).
20. Lee HB, Noh H, Seo JY, Yu MR, Ha H. Histone deacetylase inhibitors: a novel class of therapeutic agents in diabetic nephropathy. Kidney Int. Suppl. (106), S61-S66 (2007).
21. Chou DH, Holson EB, Wagner FF et al. Inhibition of histone deacetylase 3 protects beta cells from cytokineinduced apoptosis. Chem. Biol. 19(6), 669-673 (2012).
22. Lenoir O, Flosseau K, Ma FX et al. Specific control of pancreatic endocrine beta-and delta-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9. Diabetes 60(11), 2861-2871 (2011).
23. Lewis EC, Blaabjerg L, Storling J et al. The oral histone deacetylase inhibitor ITF2357 reduces cytokines and protects islet beta cells in vivo and in vitro. Mol. Med. 17(5-6), 369-377 (2011).
24. Lundh M, Christensen DP, Damgaard Nielsen M et al. Histone deacetylases 1 and 3 but not 2 mediate cytokineinduced beta cell apoptosis in INS-1 cells and dispersed primary islets from rats and are differentially regulated in the islets of Type 1 diabetic children. Diabetologia 55(9), 2421-2431 (2012).
25. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23 (2005).
26. Mutskov V, Raaka BM, Felsenfeld G, Gershengorn MC. The human insulin gene displays transcriptionally active epigenetic marks in islet-derived mesenchymal precursor cells in the absence of insulin expression. Stem Cells 25(12), 3223-3233 (2007).
27. Kaiser C, James SR. Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Biol. 2, 23 (2004).
28. Offield MF, Jetton TL, Labosky PA et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122(3), 983-995 (1996).
29. Meier BC, Wagner BK. Inhibition of HDAC3 as a strategy for developing novel diabetes therapeutics. Epigenomics 6(2), 209-214 (2014).
30. Weems J, Olson AL. Class II histone deacetylases limit GLUT4 gene expression during adipocyte differentiation. J. Biol. Chem. 286(1), 460-468 (2011).
31. Weems JC, Griesel BA, Olson AL. ccccc II histone deacetylasesdownregulate GLUT4 transcription in response to increased cAMP signaling in cultured adipocytes and fasting mice. Diabetes 61(6), 1404-1414 (2012).
32. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 17(12), 1519-1528 (2011).
33. Gao Z, Yin J, Zhang J et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58(7), 1509-1517 (2009).
34. Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol. Cell 48(4), 612-626 (2012).
35. Li N, Hatch M, Wasserfall CH et al. Butyrate and Type 1 diabetes mellitus: can we fix the intestinal leak? J. Pediatr. Gastroenterol. Nutr. 51(4), 414-417 (2010).
36. BerniCanani R, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin. Epigenet. 4(1), 4 (2012).
37. Goicoa S, Alvarez S, Ricordi C, Inverardi L, Dominguez-Bendala J. Sodium butyrate activates genes of early pancreatic development in embryonic stem cells. Cloning Stem Cells 8(3), 140-149 (2006).
38. Khan S, Jena GB. 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. 213C, 1-12 (2014).
39. Anderson JW, Baird P, Davis RH Jr et al. Health benefits of dietary fiber. Nutr. Rev. 67(4), 188-205 (2009).
40. Anderson JW, Zeigler JA, Deakins DA et al. Metabolic effects of high-carbohydrate, high-fiber diets for insulindependent diabetic individuals. Am. J. Clin. Nutr. 54(5), 936-943 (1991).
41. Jakobsdottir G, Xu J, Molin G, Ahrne S, Nyman M. Highfat diet reduces the formation of butyrate, but increases succinate, inflammation, liver fat and cholesterol in rats, while dietary fibre counteracts these effects. PLoS ONE 8(11), e80476 (2013).
42. Yadav H, Lee JH, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J. Biol. Chem. 288(35), 25088-25097 (2013).
43. De Goffau MC, Fuentes S, Van Den Bogert B et al. Aberrant gut microbiota composition at the onset of Type 1 diabetes in young children. Diabetologia 57(8), 1569-1577 (2014).
44. Vaarala O. Human intestinal microbiota and Type 1 diabetes. Curr. Diab. Rep. 13(5), 601-607 (2013).
45. De Goffau MC, Luopajarvi K, Knip M et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62(4), 1238-1244 (2013).
46. Furusawa Y, Obata Y, Fukuda S et al. Commensal microbederived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480), 446-450 (2013).
47. Khan S, Jena G. Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-beta1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats. Food Chem. Toxicol. 73c, 127-139 (2014).
48. Mosley AL, Ozcan S. The pancreatic duodenal homeobox-1 protein (Pdx-1) interacts with histone deacetylases Hdac-1 and Hdac-2 on low levels of glucose. J. Biol. Chem. 279(52), 54241-54247 (2004).
49. Haumaitre C, Lenoir O, Scharfmann R. Histone deacetylase inhibitors modify pancreatic cell fate determination and amplify endocrine progenitors. Mol. Cell. Biol. 28(20), 6373-6383 (2008).
50. Chen T-H, Chen W-M, Hsu K-H, Kuo C-D, Hung S-C. Sodium butyrate activates ERK to regulate differentiation of mesenchymal stem cells. Biochem. Biophys. Res. Commun. 355(4), 913-918 (2007).
51. Aramata S, Han SI, Yasuda K, Kataoka K. Synergistic activation of the insulin gene promoter by the beta-cell enriched transcription factors MafA, Beta2, and Pdx1. Biochim. Biophys. Acta 1730(1), 41-46 (2005).
52. Oetjen E, Blume R, Cierny I et al. Inhibition of MafA transcriptional activity and human insulin gene transcription by interleukin-1beta and mitogen-activated protein kinase kinasekinase in pancreatic islet beta cells. Diabetologia 50(8), 1678-1687 (2007).
53. Lundh M, Christensen DP, Rasmussen DN et al. Lysine deacetylases are produced in pancreatic beta cells and are differentially regulated by proinflammatory cytokines. Diabetologia 53(12), 2569-2578 (2010).
54. Mosley AL, Ozcan S. Glucose regulates insulin gene transcription by hyperacetylation of histone h4. J. Biol. Chem. 278(22), 19660-19666 (2003).
55. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10(1), 32-42 (2009).
56. Hara N, Alkanani AK, Dinarello CA, Zipris D. Histone deacetylase inhibitor suppresses virus-induced proinflammatory responses and Type 1 diabetes. J. Mol. Med. (Berl.) 92(1), 93-102 (2014).
57. Christensen DP, Gysemans C, Lundh M et al. Lysine deacetylase inhibition prevents diabetes by chromatinindependent immunoregulation and beta-cell protection. Proc. Natl Acad. Sci. USA 111(3), 1055-1059 (2014).
58. He YW, Wang HS, Zeng J et al. Sodium butyrate inhibits interferon-gamma induced indoleamine 2, 3-dioxygenase expression via STAT1 in nasopharyngeal carcinoma cells. Life Sci. 93(15), 509-515 (2013).
59. Ohira H, Fujioka Y, Katagiri C et al. Butyrate attenuates inflammation and lipolysis generated by the interaction of adipocytes and macrophages. J. Atheroscler. Thrombos. 20(5), 425-442 (2013).
60. Place RF, Noonan EJ, Giardina C M. HDAC inhibition prevents NF-kappa B activation by suppressing proteasome activity: down-regulation of proteasome subunit expression stabilizes I kappa B alpha. Biochem. Pharmacol. 70(3), 394-406 (2005).
61. Song M, Xia B, Li J. Effects of topical treatment of sodium butyrate and 5-aminosalicylic acid on expression of trefoil factor 3, interleukin 1beta, and nuclear factor kappaB in trinitrobenzenesulphonic acid induced colitis in rats. Postgrad. Med. J. 82(964), 130-135 (2006).
62. Kanika G, Khan S, Jena G. Sodium butyrate ameliorates L-arginine-induced pancreatitis and associated fibrosis in wistar rat: Role of inflammation and nitrosative stress. J. Biochem. Mol. Toxicol. (2015) (In press).
63. Dayeh T, Volkov P, Salo S et al. Genome-wide DNA methylation analysis of human pancreatic islets from Type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet. 10(3), e1004160 (2014).
64. Sandovici I, Hammerle CM, Ozanne SE, Constancias M. Developmental and environmental epigenetic programming of the endocrine pancreas: consequences for Type 2 diabetes. Cell. Mol. Life Sci. 70(9), 1575-1595 (2013).
65. Sparling DP, Griesel BA, Weems J, Olson AL. GLUT4 enhancer factor (GEF) interacts with MEF2A and HDAC5 to regulate the GLUT4 promoter in adipocytes. J. Biol. Chem. 283(12), 7429-7437 (2008).
66. Mcgee SL, Van Denderen BJ, Howlett KF et al. AMPactivated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57(4), 860-867 (2008).
67. Raichur S, Teh SH, Ohwaki K et al. Histone deacetylase 5 regulates glucose uptake and insulin action in muscle cells. J. Mol. Endocrinol. 49(3), 203-211 (2012).
68. Oiso H, Furukawa N, Suefuji M et al. The role of class I histone deacetylase (HDAC) on gluconeogenesis in liver. Biochem. Biophys. Res. Commun. 404(1), 166-172 (2011).
69. Sun C, Zhou J. Trichostatin A improves insulin stimulated glucose utilization and insulin signaling transduction through the repression of HDAC2. Biochem. Pharmacol. 76(1), 120-127 (2008).
70. Rumberger JM, Arch JR, Green A. Butyrate and other short-chain fatty acids increase the rate of lipolysis in 3T3-L1 adipocytes. PeerJ. 2, e611 (2014).
71. Hu GX, Chen GR, Xu H, Ge RS, Lin J. Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med. Hypotheses 74(1), 123-126 (2010).
72. Henagan TM, Stefanska B, Fang Z et al. Sodium butyrate epigenetically modulates high fat diet-induced skeletal muscle mitochondrial adaptation, obesity and insulin resistance through nucleosome positioning. Br. J. Pharmacol. doi: 10.1111/bph. 13058 (2015) (Epub ahead of print).
73. Endo H, Niioka M, Kobayashi N, Tanaka M, Watanabe T. Butyrate-producing probiotics reduce nonalcoholic fatty liver disease progression in rats: new insight into the probiotics for the gut-liver axis. PLoS ONE 8(5), e63388 (2013).
74. Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 150(6), 1223-1234 (2012).
75. Guo S, Dai C, Guo M et al. Inactivation of specific beta cell transcription factors in Type 2 diabetes. J. Clin. Invest. 123(8), 3305-3316 (2013).
76. Li HP, Chen X, Li MQ. Butyrate alleviates metabolic impairments and protects pancreatic beta cell function in pregnant mice with obesity. Int. J. Clin. Exp. Pathol. 6(8), 1574-1584 (2013).
77. Chakrabarti SK, Francis J, Ziesmann SM, Garmey JC, Mirmira RG. Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic beta cells. J. Biol. Chem. 278(26), 23617-23623 (2003).
78. Bramswig NC, Kaestner KH. Transcriptional and epigenetic regulation in human islets. Diabetologia 57(3), 451-454 (2014).
79. Lindholm CR, Ertel RL, Bauwens JD, Schmuck EG, Mulligan JD, Saupe KW. A high-fat diet decreases AMPK activity in multiple tissues in the absence of hyperglycemia or systemic inflammation in rats. J. Physiol. Biochem. 69(2), 165-175 (2013).
80. Vinolo MA, Rodrigues HG, Festuccia WT et al. Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. Am. J. Physiol. Endocrinol. Metab. 303(2), E272-E282 (2012).
81. Gao Z, He Q, Peng B, Chiao PJ, Ye J. Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferatoractivated receptor gamma function. J. Biol. Chem. 281(7), 4540-4547 (2006).
82. Li D, Wang X, Ren W et al. High expression of liver histone deacetylase 3 contributes to high-fat-diet-induced metabolic syndrome by suppressing the PPAR-gamma and LXR-alphapathways in E3 rats. Mol. Cell. Endocrinol. 344(1-2), 69-80 (2011).
83. Masui R, Sasaki M, Funaki Y et al. G protein-coupled receptor 43 moderates gut inflammation through cytokine regulation from mononuclear cells. Inflamm. Bowel Dis. 19(13), 2848-2856 (2013).
84. Remely M, Aumueller E, Merold C et al. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in Type 2 diabetes and obesity. Gene 537(1), 85-92 (2014).
85. Kaji I, Karaki S, Kuwahara A. Short-chain fatty acid receptor and its contribution to glucagon-like peptide-1 release. Digestion 89(1), 31-36 (2014).
86. Lin HV, Frassetto A, Kowalik EJ Jr et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 7(4), e35240 (2012).
87. Brownawell AM, Caers W, Gibson GR et al. Prebiotics and the health benefits of fiber: current regulatory status, future research, and goals. J. Nutr. 142(5), 962-974 (2012).
88. Kim SW, Hooker JM, Otto N et al. Whole-body pharmacokinetics of HDAC inhibitor drugs, butyric acid, valproic acid and 4-phenylbutyric acid measured with carbon-11 labeled analogs by PET. Nucl. Med. Biol. 40(7), 912-918 (2013).
89. MattaceRaso G, Simeoli R, Russo R et al. Effects of sodium butyrate and its synthetic amide derivative on liver inflammation and glucose tolerance in an animal model of steatosis induced by high fat diet. PLoS ONE 8(7), e68626 (2013).
90. Roda A, Simoni P, Magliulo M et al. A new oral formulation for the release of sodium butyrate in the ileo-cecal region and colon. World J. Gastroenterol. 13(7), 1079-1084 (2007).
91. Krokowicz L, Stojcev Z, Kaczmarek BF et al. Microencapsulated sodium butyrate administered to patients with diverticulosis decreases incidence of diverticulitis-a prospective randomized study. Int. J. Colorectal Dis. 29(3), 387-393 (2014).
92. Sekhavat A, Sun JM, Davie JR. Competitive inhibition of histone deacetylase activity by trichostatin A and butyrate. Biochem. Cell Biol. 85(6), 751-758 (2007).
93. Khan S, Jena G, Tikoo K. Sodium valproate ameliorates diabetes-induced fibrosis and renal damage by the inhibition of histone deacetylases in diabetic rat. Exp. Mol. Pathol. 98(2), 230-239 (2015).