HDAC4 mediates IFN-γ induced disruption of energy expenditure-related gene expression by repressing SIRT1 transcription in skeletal muscle cells

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1859, Issue 2, 2016, Pages 294-305

  Fang, Mingming ^a,b   Fan, Zhiwen ^a   Tian, Wenfang ^a   Zhao, Yuhao ^a   Li, Ping ^a   Xu, Huihui ^a   Zhou, Bisheng ^a   Zhang, Liping ^c   Wu, Xiaoyan ^a   Xu, Yong ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Jiangsu Jiankang Vocational Institute   (China)

^c XINJIANG MEDICAL UNIVERSITY   (China)

Author keywords

CIITA; Epigenetics; HDAC4; IFN ; Transcriptional regulation

Indexed keywords

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; GAMMA INTERFERON; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 7; HYPERMETHYLATED IN CANCER 1 PROTEIN; PROTEIN; SIRTUIN 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; HDAC4 PROTEIN, HUMAN; HIC1 PROTEIN, HUMAN; HISTONE DEACETYLASE; KRUPPEL LIKE FACTOR; MHC CLASS II TRANSACTIVATOR PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SIRT1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL METABOLISM; CHROMATIN IMMUNOPRECIPITATION; DEACETYLATION; DOWN REGULATION; ENERGY EXPENDITURE; GASTROCNEMIUS MUSCLE; GENE OVEREXPRESSION; GENE REPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; MOUSE; MUSCLE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SKELETAL MUSCLE; SKELETAL MUSCLE CELL; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ACETYLATION; ANIMAL; BIOSYNTHESIS; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; OBESITY; PATHOLOGY; TRANSCRIPTION INITIATION;

ACETYLATION; ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; INTERFERON-GAMMA; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MUSCLE FIBERS, SKELETAL; NUCLEAR PROTEINS; OBESITY; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SIRTUIN 1; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84949637539     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.11.010     Document Type: Article

References (54)

1. Hu F.B., Satija A., Manson J.E. Curbing the diabetes pandemic: the need for global policy solutions. JAMA 2015, 313:2319-2320.
2. Boucher J., Kleinridders A., Kahn C.R. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb. Perspect. Biol. 2014, 6.
3. Colca J.R., Tanis S.P., McDonald W.G., Kletzien R.F. Insulin sensitizers in 2013: new insights for the development of novel therapeutic agents to treat metabolic diseases. Expert Opin. Investig. Drugs 2014, 23:1-7.
4. Feige J.N., Lagouge M., Canto C., Strehle A., Houten S.M., Milne J.C., Lambert P.D., Mataki C., Elliott P.J., Auwerx J. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab. 2008, 8:347-358.
5. Pirinen E., Canto C., Jo Y.S., Morato L., Zhang H., Menzies K.J., Williams E.G., Mouchiroud L., Moullan N., Hagberg C., Li W., Timmers S., Imhof R., Verbeek J., Pujol A., van Loon B., Viscomi C., Zeviani M., Schrauwen P., Sauve A.A., Schoonjans K., Auwerx J. Pharmacological inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab. 2014, 19:1034-1041.
6. Bai P., Canto C., Brunyanszki A., Huber A., Szanto M., Cen Y., Yamamoto H., Houten S.M., Kiss B., Oudart H., Gergely P., Menissier-de Murcia J., Schreiber V., Sauve A.A., Auwerx J. PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab. 2011, 13:450-460.
7. Finkel T., Deng C.X., Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009, 460:587-591.
8. Lin S.J., Defossez P.A., Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 2000, 289:2126-2128.
9. Guarente L., Kenyon C. Genetic pathways that regulate ageing in model organisms. Nature 2000, 408:255-262.
10. Banks A.S., Kon N., Knight C., Matsumoto M., Gutierrez-Juarez R., Rossetti L., Gu W., Accili D. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008, 8:333-341.
11. Moynihan K.A., Grimm A.A., Plueger M.M., Bernal-Mizrachi E., Ford E., Cras-Meneur C., Permutt M.A., Imai S. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab. 2005, 2:105-117.
12. Luu L., Dai F.F., Prentice K.J., Huang X., Hardy A.B., Hansen J.B., Liu Y., Joseph J.W., Wheeler M.B. The loss of Sirt1 in mouse pancreatic beta cells impairs insulin secretion by disrupting glucose sensing. Diabetologia 2013, 56:2010-2020.
13. Purushotham A., Xu Q., Li X. Systemic SIRT1 insufficiency results in disruption of energy homeostasis and steroid hormone metabolism upon high-fat-diet feeding. FASEB J. 2012, 26:656-667.
14. Li Y., Xu S., Giles A., Nakamura K., Lee J.W., Hou X., Donmez G., Li J., Luo Z., Walsh K., Guarente L., Zang M. Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 2011, 25:1664-1679.
15. Purushotham A., Schug T.T., Xu Q., Surapureddi S., Guo X., Li X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 2009, 9:327-338.
16. Canto C., Jiang L.Q., Deshmukh A.S., Mataki C., Coste A., Lagouge M., Zierath J.R., Auwerx J. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab. 2010, 11:213-219.
17. Bordone L., Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat. Rev. Mol. Cell Biol. 2005, 6:298-305.
18. Rutanen J., Yaluri N., Modi S., Pihlajamaki J., Vanttinen M., Itkonen P., Kainulainen S., Yamamoto H., Lagouge M., Sinclair D.A., Elliott P., Westphal C., Auwerx J., Laakso M. SIRT1 mRNA expression may be associated with energy expenditure and insulin sensitivity. Diabetes 2010, 59:829-835.
19. Sun L., Li H., Chen J., Dehennaut V., Zhao Y., Yang Y., Iwasaki Y., Kahn-Perles B., Leprince D., Chen Q., Shen A., Xu Y. A SUMOylation-dependent pathway regulates SIRT1 transcription and lung cancer metastasis. J. Natl. Cancer Inst. 2013, 105:887-898.
20. Sun L., Li H., Chen J., Iwasaki Y., Kubota T., Matsuoka M., Shen A., Chen Q., Xu Y. PIASy mediates hypoxia-induced SIRT1 transcriptional repression and epithelial-to-mesenchymal transition in ovarian cancer cells. J. Cell Sci. 2013, 126:3939-3947.
21. Chalkiadaki A., Guarente L. High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab. 2012, 16:180-188.
22. Serrano-Marco L., Chacon M.R., Maymo-Masip E., Barroso E., Salvado L., Wabitsch M., Garrido-Sanchez L., Tinahones F.J., Palomer X., Vendrell J., Vazquez-Carrera M. TNF-alpha inhibits PPARbeta/delta activity and SIRT1 expression through NF-kappaB in human adipocytes. Biochim. Biophys. Acta 2012, 1821:1177-1185.
23. Schmidt F.M., Weschenfelder J., Sander C., Minkwitz J., Thormann J., Chittka T., Mergl R., Kirkby K.C., Fasshauer M., Stumvoll M., Holdt L.M., Teupser D., Hegerl U., Himmerich H. Inflammatory cytokines in general and central obesity and modulating effects of physical activity. PLoS One 2015, 10.
24. Jagannathan-Bogdan M., McDonnell M.E., Shin H., Rehman Q., Hasturk H., Apovian C.M., Nikolajczyk B.S. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J. Immunol. 2011, 186:1162-1172.
25. Li P., Zhao Y., Wu X., Xia M., Fang M., Iwasaki Y., Sha J., Chen Q., Xu Y., Shen A. Interferon gamma (IFN-gamma) disrupts energy expenditure and metabolic homeostasis by suppressing SIRT1 transcription. Nucleic Acids Res. 2012, 40:1609-1620.
26. Miska E.A., Karlsson C., Langley E., Nielsen S.J., Pines J., Kouzarides T. HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J. 1999, 18:5099-5107.
27. Fang M., Li P., Wu X., Xu Y. Class II transactivator (CIITA) mediates transcriptional repression of pdk4 gene by interacting with hypermethylated in cancer 1 (HIC1). J. Biomed. Res. 2015, 29:308-315.
28. Fang M., Kong X., Li P., Fang F., Wu X., Bai H., Qi X., Chen Q., Xu Y. RFXB and its splice variant RFXBSV mediate the antagonism between IFNgamma and TGFbeta on COL1A2 transcription in vascular smooth muscle cells. Nucleic Acids Res. 2009, 37:4393-4406.
29. Yang X.J., Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 2008, 9:206-218.
30. Illi B., Dello Russo C., Colussi C., Rosati J., Pallaoro M., Spallotta F., Rotili D., Valente S., Ragone G., Martelli F., Biglioli P., Steinkuhler C., Gallinari P., Mai A., Capogrossi M.C., Gaetano C. Nitric oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ. Res. 2008, 102:51-58.
31. Nemoto S., Fergusson M.M., Finkel T. SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α. J. Biol. Chem. 2005, 280:16456-16460.
32. Canto C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
33. Balestrieri M.L., Rienzo M., Felice F., Rossiello R., Grimaldi V., Milone L., Casamassimi A., Servillo L., Farzati B., Giovane A., Napoli C. High glucose downregulates endothelial progenitor cell number via SIRT1. Biochim. Biophys. Acta 2008, 1784:936-945.
34. Shao D., Fry J.L., Han J., Hou X., Pimentel D.R., Matsui R., Cohen R.A., Bachschmid M.M. A redox-resistant sirtuin-1 mutant protects against hepatic metabolic and oxidant stress. J. Biol. Chem. 2014, 289:7293-7306.
35. Wu L., Zhou L., Lu Y., Zhang J., Jian F., Liu Y., Li F., Li W., Wang X., Li G. Activation of SIRT1 protects pancreatic beta-cells against palmitate-induced dysfunction. Biochim. Biophys. Acta 2012, 1822:1815-1825.
36. Taheripak G., Bakhtiyari S., Rajabibazl M., Pasalar P., Meshkani R. Protein tyrosine phosphatase 1B inhibition ameliorates palmitate-induced mitochondrial dysfunction and apoptosis in skeletal muscle cells. Free Radic. Biol. Med. 2013, 65:1435-1446.
37. Oppenheimer H., Gabay O., Meir H., Haze A., Kandel L., Liebergall M., Gagarina V., Lee E.J., Dvir-Ginzberg M. 75-kd sirtuin 1 blocks tumor necrosis factor alpha-mediated apoptosis in human osteoarthritic chondrocytes. Arthritis Rheum. 2012, 64:718-728.
38. Lin Z., Yang H., Kong Q., Li J., Lee S.M., Gao B., Dong H., Wei J., Song J., Zhang D.D., Fang D. USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol. Cell 2012, 46:484-494.
39. Ford J., Ahmed S., Allison S., Jiang M., Milner J. JNK2-dependent regulation of SIRT1 protein stability. Cell Cycle 2008, 7:3091-3097.
40. Kyrylenko S., Kyrylenko O., Suuronen T., Salminen A. Differential regulation of the Sir2 histone deacetylase gene family by inhibitors of class I and II histone deacetylases. Cell. Mol. Life Sci. 2003, 60:1990-1997.
41. Li J., Chen J., Ricupero C.L., Hart R.P., Schwartz M.S., Kusnecov A., Herrup K. Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia. Nat. Med. 2012, 18:783-790.
42. Mihaylova M.M., Vasquez D.S., Ravnskjaer K., Denechaud P.D., Yu R.T., Alvarez J.G., Downes M., Evans R.M., Montminy M., Shaw R.J. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011, 145:607-621.
43. Henriksson E., Sall J., Gormand A., Wasserstrom S., Morrice N.A., Fritzen A.M., Foretz M., Campbell D.G., Sakamoto K., Ekelund M., Degerman E., Stenkula K.G., Goransson O. SIK2 regulates CRTCs, HDAC4 and glucose uptake in adipocytes. J. Cell Sci. 2015, 128:472-486.
44. Luan B., Goodarzi M.O., Phillips N.G., Guo X., Chen Y.D., Yao J., Allison M., Rotter J.I., Shaw R., Montminy M. Leptin-mediated increases in catecholamine signaling reduce adipose tissue inflammation via activation of macrophage HDAC4. Cell Metab. 2014, 19:1058-1065.
45. Abu-Farha M., Tiss A., Abubaker J., Khadir A., Al-Ghimlas F., Al-Khairi I., Baturcam E., Cherian P., Elkum N., Hammad M., John J., Kavalakatt S., Warsame S., Behbehani K., Dermime S., Dehbi M. Proteomics analysis of human obesity reveals the epigenetic factor HDAC4 as a potential target for obesity. PLoS One 2013, 8.
46. Lenoir O., Flosseau K., Ma F.X., Blondeau B., Mai A., Bassel-Duby R., Ravassard P., Olson E.N., Haumaitre C., Scharfmann R. Specific control of pancreatic endocrine beta- and delta-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9. Diabetes 2011, 60:2861-2871.
47. Somm E., Henrichot E., Pernin A., Juge-Aubry C.E., Muzzin P., Dayer J.M., Nicklin M.J., Meier C.A. Decreased fat mass in interleukin-1 receptor antagonist-deficient mice: impact on adipogenesis, food intake, and energy expenditure. Diabetes 2005, 54:3503-3509.
48. Pierre N., Deldicque L., Barbe C., Naslain D., Cani P.D., Francaux M. Toll-like receptor 4 knockout mice are protected against endoplasmic reticulum stress induced by a high-fat diet. PLoS One 2013, 8.
49. Everard A., Geurts L., Caesar R., Van Hul M., Matamoros S., Duparc T., Denis R.G., Cochez P., Pierard F., Castel J., Bindels L.B., Plovier H., Robine S., Muccioli G.G., Renauld J.C., Dumoutier L., Delzenne N.M., Luquet S., Backhed F., Cani P.D. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nat. Commun. 2014, 5:5648.
50. Ghosh S., George S., Roy U., Ramachandran D., Kolthur-Seetharam U. NAD: a master regulator of transcription. Biochim. Biophys. Acta 2010, 1799:681-693.
51. Hawley J.A., Hargreaves M., Joyner M.J., Zierath J.R. Integrative biology of exercise. Cell 2014, 159:738-749.
52. Brandon A.E., Tid-Ang J., Wright L.E., Stuart E., Suryana E., Bentley N., Turner N., Cooney G.J., Ruderman N.B., Kraegen E.W. Overexpression of SIRT1 in rat skeletal muscle does not alter glucose induced insulin resistance. PLoS One 2015, 10.
53. White A.T., McCurdy C.E., Philp A., Hamilton D.L., Johnson C.D., Schenk S. Skeletal muscle-specific overexpression of SIRT1 does not enhance whole-body energy expenditure or insulin sensitivity in young mice. Diabetologia 2013, 56:1629-1637.
54. White A.T., Philp A., Fridolfsson H.N., Schilling J.M., Murphy A.N., Hamilton D.L., McCurdy C.E., Patel H.H., Schenk S. High-fat diet-induced impairment of skeletal muscle insulin sensitivity is not prevented by SIRT1 overexpression. Am. J. Physiol. Endocrinol. Metab. 2014, 307:E764-E772.