HDAC7 is overexpressed in human diabetic islets and impairs insulin secretion in rat islets and clonal beta cells

Diabetologia

Volumn 60, Issue 1, 2017, Pages 116-125

  Daneshpajooh, Mahboubeh ^a   Bacos, Karl ^a   Bysani, Madhusudhan ^a   Bagge, Annika ^a   Ottosson Laakso, Emilia ^a   Vikman, Petter ^a   Eliasson, Lena ^b   Mulder, Hindrik ^a   Ling, Charlotte ^a  

^a LUND UNIVERSITY DIABETES CENTRE   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Apoptosis; Beta cells; Epigenetic modification; HDAC7; Human pancreatic islets; Insulin secretion; MC1568; Trichostatin A; Type 2 diabetes

Indexed keywords

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; GLUCOSE; HISTONE DEACETYLASE 7; INSULIN; SMALL INTERFERING RNA; TRICHOSTATIN A; GLYCOSYLATED HEMOGLOBIN; HDAC7 PROTEIN, HUMAN; HISTONE DEACETYLASE;

ADULT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; FEMALE; GENE OVEREXPRESSION; HUMAN; INS-1 CELL LINE; INSULIN RELEASE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MITOCHONDRIAL RESPIRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE METABOLISM; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; RNA SEQUENCE; AGED; GENE EXPRESSION REGULATION; GENETICS; IN VITRO STUDY; METABOLISM; PANCREAS ISLET; SECRETION (PROCESS);

AGED; DIABETES MELLITUS, TYPE 2; FEMALE; GENE EXPRESSION REGULATION; HEMOGLOBIN A, GLYCOSYLATED; HISTONE DEACETYLASES; HUMANS; IN VITRO TECHNIQUES; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MIDDLE AGED;

EID: 84992709105     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-4113-2     Document Type: Article

References (38)

1. Rosengren AH, Braun M, Mahdi T et al (2012) Reduced insulin exocytosis in human pancreatic β-cells with gene variants linked to type 2 diabetes. Diabetes 61:1726–1733
2. Groop L, Pociot F (2014) Genetics of diabetes-are we missing the genes or the disease? Mol Cell Endocrinol 382:726–739
3. Dayeh T, Volkov P, Salo S et al (2014) 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:e1004160
4. Ling C, Del Guerra S, Lupi R et al (2008) Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 51:615–622
5. Nilsson E, Jansson PA, Perfilyev A et al (2014) Altered DNA methylation and differential expression of genes influencing metabolism and inflammation in adipose tissue from subjects with type 2 diabetes. Diabetes 63:2962–2976
6. Nilsson E, Matte A, Perfilyev A et al (2015) Epigenetic alterations in human liver from subjects with type 2 diabetes in parallel with reduced folate levels. J Clin Endocrinol Metab 100:E1491–E1501
7. Yang BT, Dayeh TA, Kirkpatrick CL et al (2011) Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA(1c) levels in human pancreatic islets. Diabetologia 54:360–367
8. Yang BT, Dayeh TA, Volkov PA et al (2012) Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol Endocrinol 26:1203–1212
9. Lenoir O, Flosseau K, Ma FX et al (2011) Specific control of pancreatic endocrine β- and δ-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9. Diabetes 60:2861–2871
10. Lundh M, Galbo T, Poulsen SS, Mandrup-Poulsen T (2015) Histone deacetylase 3 inhibition improves glycaemia and insulin secretion in obese diabetic rats. Diabetes Obes Metab 17:703–707
11. Mihaylova MM, Vasquez DS, Ravnskjaer K et al (2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145:607–621
12. Fadista J, Vikman P, Laakso EO et al (2014) Global genomic and transcriptomic analysis of human pancreatic islets reveals novel genes influencing glucose metabolism. Proc Natl Acad Sci U S A A111:13924–13929
13. Eliasson L, Ma X, Renstrom E et al (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121:181–197
14. National Research Council of the National Academies (2011) Guide for the Care and Use of Laboratory Animals. The National Academies Presss, Washington, DC
15. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49:424–430
16. Wang J, Gong B, Zhao W et al (2014) Epigenetic mechanisms linking diabetes and synaptic impairments. Diabetes 63:645–654
17. Tiernan AR, Champion JA, Sambanis A (2015) Trichostatin A affects the secretion pathways of beta and intestinal endocrine cells. Exp Cell Res 330:212–221
18. Malmgren S, Spegel P, Danielsson AP et al (2013) Coordinate changes in histone modifications, mRNA levels, and metabolite profiles in clonal INS-1 832/13 β-cells accompany functional adaptations to lipotoxicity. J Biol Chem 288:11973–11987
19. Mootha VK, Lindgren CM, Eriksson KF et al (2003) PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273
20. Subramanian A, Tamayo P, Mootha VK et al (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545–15550
21. Lyssenko V, Lupi R, Marchetti P et al (2007) Mechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes. J Clin Investig 117:2155–2163
22. Hoffmann K, Czapp M, Loscher W (2008) Increase in antiepileptic efficacy during prolonged treatment with valproic acid: role of inhibition of histone deacetylases? Epilepsy Res 81:107–113
23. Waibel M, Christiansen AJ, Hibbs ML et al (2015) Manipulation of B-cell responses with histone deacetylase inhibitors. Nat Commun 6:6838
24. Christensen DP, Gysemans C, Lundh M et al (2014) Lysine deacetylase inhibition prevents diabetes by chromatin-independent immunoregulation and β-cell protection. Proc Natl Acad Sci U S A 111:1055–1059
25. Lundh M, Christensen DP, Damgaard Nielsen M et al (2012) Histone deacetylases 1 and 3 but not 2 mediate cytokine-induced 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 55:2421–2431
26. Lundh M, Christensen DP, Rasmussen DN et al (2010) Lysine deacetylases are produced in pancreatic beta cells and are differentially regulated by proinflammatory cytokines. Diabetologia 53:2569–2578
27. Koeck T, Olsson AH, Nitert MD et al (2011) A common variant in TFB1M is associated with reduced insulin secretion and increased future risk of type 2 diabetes. Cell Metab 13:80–91
28. Malmgren S, Nicholls DG, Taneera J et al (2009) Tight coupling between glucose and mitochondrial metabolism in clonal β-cells is required for robust insulin secretion. J Biol Chem 284:32395–32404
29. Olsson AH, Yang BT, Hall E et al (2011) Decreased expression of genes involved in oxidative phosphorylation in human pancreatic islets from patients with type 2 diabetes. Eur J Endocrinol 165:589–595
30. Kato H, Tamamizu-Kato S, Shibasaki F (2004) Histone deacetylase 7 associates with hypoxia-inducible factor 1α and increases transcriptional activity. J Biol Chem 279:41966–41974
31. Semenza GL (2011) Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta 1813:1263–1268
32. Galmozzi A, Mitro N, Ferrari A et al (2013) Inhibition of class I histone deacetylases unveils a mitochondrial signature and enhances oxidative metabolism in skeletal muscle and adipose tissue. Diabetes 62:732–742
33. Barneda-Zahonero B, Collazo O, Azagra A et al (2015) The transcriptional repressor HDAC7 promotes apoptosis and c-Myc downregulation in particular types of leukemia and lymphoma. Cell Death Dis 6:e1635
34. Treppendahl MB, Kristensen LS, Gronbaek K (2014) Predicting response to epigenetic therapy. J Clin Investig 124:47–55
35. Hall E, Volkov P, Dayeh T et al (2014) Effects of palmitate on genome-wide mRNA expression and DNA methylation patterns in human pancreatic islets. BMC Med 12:103
36. Olsson AH, Volkov P, Bacos K et al (2014) Genome-wide associations between genetic and epigenetic variation influence mRNA expression and insulin secretion in human pancreatic islets. PLoS Genet 10:e1004735
37. Haumaitre C, Lenoir O, Scharfmann R (2009) Directing cell differentiation with small-molecule histone deacetylase inhibitors: the example of promoting pancreatic endocrine cells. Cell Cycle 8:536–544
38. Dorrell C, Schug J, Lin CF et al (2011) Transcriptomes of the major human pancreatic cell types. Diabetologia 54:2832–2844