SIRT1 enhances glucose tolerance by potentiating brown adipose tissue function

Molecular Metabolism

Volumn 4, Issue 2, 2015, Pages 118-131

  Boutant, Marie ^a   Joffraud, Magali ^a   Kulkarni, Sameer S ^a   García Casarrubios, Ester ^b,c   García Roves, Pablo M ^c,d   Ratajczak, Joanna ^a,e   Fernández Marcos, Pablo J ^f   Valverde, Angela M ^b,c   Serrano, Manuel ^f   Cantó, Carles ^a  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^e EPFL   (Switzerland)

^f Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

Brown adipose tissue; Energy homeostasis; Insulin resistance; SIRT1

Indexed keywords

BETA 3 ADRENERGIC RECEPTOR; GLUCOSE; SIRTUIN 1;

ADIPOGENESIS; ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME ANALYSIS; GLUCOSE CLAMP TECHNIQUE; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; HISTOLOGY; HYPERINSULINEMIA; INSULIN SENSITIVITY; LOW FAT DIET; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

MUS;

EID: 84921829213     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.12.008     Document Type: Article

References (40)

1. Canto C., Auwerx J. Targeting sirtuin 1 to improve metabolism: all you need is NAD(+)?. Pharmacological Reviews 2012, 64(1):166-187.
2. Baur J.A., Ungvari Z., Minor R.K., Le Couteur D.G., de Cabo R. Are sirtuins viable targets for improving healthspan and lifespan?. Nature Review Drug Discovery 2012, 11(6):443-461.
3. Pacholec M., Bleasdale J.E., Chrunyk B., Cunningham D., Flynn D., Garofalo R.S., et al. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. Journal of Biological Chemistry 2010, 285(11):8340-8351.
4. Pfluger P.T., Herranz D., Velasco-Miguel S., Serrano M., Tschop M.H. Sirt1 protects against high-fat diet-induced metabolic damage. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(28):9793-9798.
5. Banks A.S., Kon N., Knight C., Matsumoto M., Gutierrez-Juarez R., Rossetti L., et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metabolism 2008, 8(4):333-341.
6. Champy M.F., Selloum M., Zeitler V., Caradec C., Jung B., Rousseau S., et al. Genetic background determines metabolic phenotypes in the mouse. Mammalian Genome 2008, 19(5):318-331.
7. Virtue S., Vidal-Puig A. Assessment of brown adipose tissue function. Frontiers in Physiology 2013, 4128.
8. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127(6):1109-1122.
9. Holmstrom M.H., Iglesias-Gutierrez E., Zierath J.R., Garcia-Roves P.M. Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes. American Journal of Physiology. Endocrinology and Metabolism 2012, 302(6):E731-E739.
10. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 2008, 3(6):1101-1108.
11. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genetics 2003, 34(3):267-273.
12. Ortega-Molina A., Efeyan A., Lopez-Guadamillas E., Munoz-Martin M., Gomez-Lopez G., Canamero M., et al. Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metabolism 2012, 15(3):382-394.
13. Feige J.N., Lagouge M., Canto C., Strehle A., Houten S.M., Milne J.C., et al. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metabolism 2008, 8(5):347-358.
14. White A.T., Philp A., Fridolfsson H.N., Schilling J.M., Murphy A.N., Hamilton D.L., et al. High-fat diet-induced impairment of skeletal muscle insulin sensitivity is not prevented by SIRT1 overexpression. American Journal of Physiology. Endocrinology and Metabolism 2014, 9(307):E764-E772.
15. 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(7):1629-1637.
16. Gerhart-Hines Z., Rodgers J.T., Bare O., Lerin C., Kim S.H., Mostoslavsky R., et al. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO Journal 2007, 26(7):1913-1923.
17. Gerhart-Hines Z., Dominy J.E., Blattler S.M., Jedrychowski M.P., Banks A.S., Lim J.H., et al. The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Molecular Cell 2011, 44(6):851-863.
18. Cannon B., Nedergaard J. Nonshivering thermogenesis and its adequate measurement in metabolic studies. Journal of Experimental Biology 2011, 214(Pt 2):242-253.
19. Herranz D., Munoz-Martin M., Canamero M., Mulero F., Martinez-Pastor B., Fernandez-Capetillo O., et al. Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nature Communications 2010, (1). (Article number 3). http://www.nature.com/ncomms/journal/v1/n1/full/ncomms1001.html.
20. Qiang L., Wang L., Kon N., Zhao W., Lee S., Zhang Y., et al. Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Ppargamma. Cell 2012, 150(3):620-632.
21. Moynihan K.A., Grimm A.A., Plueger M.M., Bernal-Mizrachi E., Ford E., Cras-Meneur C., et al. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metabolism 2005, 2(2):105-117.
22. Bordone L., Motta M.C., Picard F., Robinson A., Jhala U.S., Apfeld J., et al. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biology 2006, 4(2):e31.
23. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005, 434(7029):113-118.
24. Nemoto S., Fergusson M.M., Finkel T. SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. Journal of Biological Chemistry 2005, 280(16):16456-16460.
25. Cantó C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., et al. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458(7241):1056-1060.
26. Bordone L., Cohen D., Robinson A., Motta M.C., van Veen E., Czopik A., et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 2007, 6(6):759-767.
27. Chalkiadaki A., Guarente L. High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metabolism 2012, 16(2):180-188.
28. Xu C., Bai B., Fan P., Cai Y., Huang B., Law I.K., et al. Selective overexpression of human SIRT1 in adipose tissue enhances energy homeostasis and prevents the deterioration of insulin sensitivity with ageing in mice. American Journal of Translational Research 2013, 5(4):412-426.
29. Price N.L., Gomes A.P., Ling A.J.Y., Duarte F.V., Martin-Montalvo A., North B.J., et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metabolism 2012, 15(5):675-690.
30. 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 Metabolism 2009, 9(4):327-338.
31. Planavila A., Iglesias R., Giralt M., Villarroya F. Sirt1 acts in association with PPARalpha to protect the heart from hypertrophy, metabolic dysregulation, and inflammation. Cardiovascular Research 2011, 90(2):276-284.
32. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004, 303(5666):2011-2015.
33. Banks A.S., Kim-Muller J.Y., Mastracci T.L., Kofler N.M., Qiang L., Haeusler R.A., et al. Dissociation of the glucose and lipid regulatory functions of FoxO1 by targeted knockin of acetylation-defective alleles in mice. Cell Metabolism 2011, 14(5):587-597.
34. Barbera M.J., Schluter A., Pedraza N., Iglesias R., Villarroya F., Giralt M. Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene. A link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. Journal of Biological Chemistry 2001, 276(2):1486-1493.
35. Petersen K.F., Shulman G.I. Etiology of insulin resistance. American Journal of Medicine 2006, 119(5 Suppl.1):S10-S16.
36. Girousse A., Tavernier G., Valle C., Moro C., Mejhert N., Dinel A.L., et al. Partial inhibition of adipose tissue lipolysis improves glucose metabolism and insulin sensitivity without alteration of fat mass. PLoS Biology 2013, 11(2):e1001485.
37. Badin P.M., Louche K., Mairal A., Liebisch G., Schmitz G., Rustan A.C., et al. Altered skeletal muscle lipase expression and activity contribute to insulin resistance in humans. Diabetes 2011, 60(6):1734-1742.
38. Stanford K.I., Middelbeek R.J., Townsend K.L., An D., Nygaard E.B., Hitchcox K.M., et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. Journal of Clinical Investigation 2013, 123(1):215-223.
39. Canto C., Houtkooper R.H., Pirinen E., Youn D.Y., Oosterveer M.H., Cen Y., et al. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metabolism 2012, 15(6):838-847.
40. Brown K.D., Maqsood S., Huang J.Y., Pan Y., Harkcom W., Li W., et al. Activation of SIRT3 by the NAD(+) precursor nicotinamide riboside protects from noise-induced hearing loss. Cell Metabolism 2014, 20(6):1059-1068.