Adipose tissue NAD+-homeostasis, sirtuins and poly(ADP-ribose) polymerases - important players in mitochondrial metabolism and metabolic health

Redox Biology

Volumn 12, Issue , 2017, Pages 246-263

  Jokinen, Riikka ^a   Pirnes Karhu, Sini ^a   Pietiläinen, Kirsi H ^a,b   Pirinen, Eija ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Adipose tissue; Mitochondria; NAD+; Obesity; Poly(ADP ribose) polymerases; Sirtuins

Indexed keywords

ADIPOCYTOKINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN;

ADIPOGENESIS; ADIPOSE TISSUE; BROWN ADIPOSE TISSUE; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FATTY ACID OXIDATION; GLUCOSE METABOLISM; HEALTH; HOMEOSTASIS; HUMAN; INFLAMMATION; LIPID METABOLISM; METABOLIC DISORDER; METABOLIC HEALTH; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OBESITY; OXIDATION REDUCTION REACTION; PROTEIN FUNCTION; REVIEW; THERMOGENESIS; WHITE ADIPOSE TISSUE; ANIMAL; ENERGY METABOLISM; METABOLISM;

ADIPOSE TISSUE; ANIMALS; ENERGY METABOLISM; HOMEOSTASIS; HUMANS; MITOCHONDRIA; NAD; OBESITY; OXIDATION-REDUCTION; POLY(ADP-RIBOSE) POLYMERASES; SIRTUINS;

EID: 85014449357     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.02.011     Document Type: Review

References (159)

1. [1] Koh, E.H., Park, J.-Y., Park, H.-S., et al. Essential role of mitochondrial function in adiponectin synthesis in adipocytes. Diabetes 56 (2007), 2973–2981.
2. [2] Wang, C.-H., Wang, C.-C., Huang, H.-C., Wei, Y.-H., Mitochondrial dysfunction leads to impairment of insulin sensitivity and adiponectin secretion in adipocytes. FEBS J. 280 (2013), 1039–1050.
3. [3] Björntorp, P., Bengtsson, C., Blohmé, G., et al. Adipose tissue fat cell size and number in relation to metabolism in randomly selected middle-aged men and women. Metabolism 20 (1971), 927–935.
4. [4] Heinonen, S., Saarinen, L., Naukkarinen, J., et al. Adipocyte morphology and implications for metabolic derangements in acquired obesity. Int. J. Obes. 38 (2014), 1423–1431.
5. [5] Heilbronn, L., Smith, S.R., Ravussin, E., Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus. Int. J. Obes. Relat. Metab. Disord. 28 (2004), S12–S21.
6. [6] Virtue, S., Vidal-Puig, A., Adipose tissue expandability, lipotoxicity and the metabolic syndrome – an allostatic perspective. Biochim. Et. Biophys. Acta (BBA) - Mol. Cell Biol. Lipids 1801 (2010), 338–349.
7. [7] Pietiläinen, K.H., Naukkarinen, J., Rissanen, A., et al. Global transcript profiles of fat in monozygotic twins discordant for BMI: pathways behind acquired obesity. PLoS Med., 5, 2008, e51.
8. [8] Pérez, L.M., Bernal, A., de Lucas, B., et al. Altered metabolic and stemness capacity of adipose tissue-derived stem cells from obese mouse and human. PloS One, 10, 2015, e0123397.
9. [9] V. Tormos Kathryn, E. Anso, B.R.Hamanaka, et al. Mitochondrial complex III ROS regulate adipocyte Differentiation, Cell Metab. 14: pp. 537–544.
10. [10] Naukkarinen, J., Heinonen, S., Hakkarainen, A., et al. Characterising metabolically healthy obesity in weight-discordant monozygotic twins. Diabetologia 57 (2014), 167–176.
11. [11] Heinonen, S., Buzkova, J., Muniandy, M., et al. Impaired mitochondrial biogenesis in adipose tissue in acquired obesity. Diabetes, 64, 2015, 3135.
12. [12] Christodoulides, C., Lagathu, C., Sethi, J.K., Vidal-Puig, A., Adipogenesis and WNT signalling. Trends Endocrinol. Metab.: TEM 20 (2009), 16–24.
13. [13] Bai, P., Canto, C., Brunyanszki, A., et al. PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab. 13 (2011), 450–460.
14. [14] Houtkooper, R.H., Pirinen, E., Auwerx, J., Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13 (2012), 225–238.
15. [15] Pagliarini, D.J., Calvo, S.E., Chang, B., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134 (2008), 112–123.
16. [16] Wai, T., Langer, T., Mitochondrial dynamics and metabolic regulation. Trends Endocrinol. Metab. 27 (2016), 105–117.
17. [17] Phillips, M.J., Voeltz, G.K., Structure and function of ER membrane contact sites with other organelles. Nat. Rev. Mol. Cell Biol. 17 (2016), 69–82.
18. [18] Cantó, C., Gerhart-Hines, Z., Feige, J.N., et al. AMPK regulates energy expenditure by modulating NAD(+) metabolism and SIRT1 activity. Nature 458 (2009), 1056–1060.
19. [19] Jäger, S., Handschin, C., St.-Pierre, J., Spiegelman, B.M., AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc. Natl. Acad. Sci. 104 (2007), 12017–12022.
20. [20] Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M., Spiegelman, B.M., A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (1998), 829–839.
21. [21] Yamamoto, H., Williams, E.G., Mouchiroud, L., et al. NCoR1 is a conserved physiological modulator of muscle mass and oxidative function. Cell 147 (2011), 827–839.
22. [22] Pérez-Schindler, J., Summermatter, S., Salatino, S., et al. The corepressor NCoR1 antagonizes PGC-1α and estrogen-related receptor α in the regulation of skeletal muscle function and oxidative metabolism. Mol. Cell. Biol. 32 (2012), 4913–4924.
23. [23] Li, P., Fan, W., Xu, J., et al. Adipocyte NCoR knockout decreases PPARγ phosphorylation and enhances PPARγ activity and insulin sensitivity. Cell 147 (2011), 815–826.
24. [24] Dominy, J.E., Puigserver, P., Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb. Perspect. Biol., 5, 2013, a015008.
25. [25] Quiros, P.M., Langer, T., Lopez-Otin, C., New roles for mitochondrial proteases in health, ageing and disease. Nat. Rev. Mol. Cell Biol. 16 (2015), 345–359.
26. [26] Karbowski, M., Youle, R.J., Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr. Opin. Cell Biol. 23 (2011), 476–482.
27. [27] Jovaisaite, V., Mouchiroud, L., Auwerx, J., The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J. Exp. Biol. 217 (2014), 137–143.
28. [28] Sugiura, A., McLelland, G.-L., Fon, E.A., McBride, H.M., A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. Embo J. 33 (2014), 2142–2156.
29. [29] Youle, R.J., Narendra, D.P., Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12 (2011), 9–14.
30. [30] Canto, C., Menzies, K.J., Auwerx, J., NAD(+) metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab. 22 (2015), 31–53.
31. [31] Dashty, M., A quick look at biochemistry: carbohydrate metabolism. Clin. Biochem. 46 (2013), 1339–1352.
32. [32] McKenna, M.C., Waagepetersen, H.S., Schousboe, A., Sonnewald, U., Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: current evidence and pharmacological tools. Biochem. Pharmacol. 71 (2006), 399–407.
33. [33] Eaton, S., Control of mitochondrial beta-oxidation flux. Prog. Lipid Res. 41 (2002), 197–239.
34. [34] Ussher, J.R., Jaswal, J.S., Lopaschuk, G.D., Pyridine nucleotide regulation of cardiac intermediary metabolism. Circ. Res. 111 (2012), 628–641.
35. [35] Lynch, C.J., Adams, S.H., Branched-chain amino acids in metabolic signalling and insulin resistance. Nat. Rev. Endocrinol. 10 (2014), 723–736.
36. [36] Heinonen, S., Muniandy, M., Buzkova, J., et al. Mitochondria-related transcriptional signature is downregulated in adipocytes in obesity: a study of young healthy MZ twins. Diabetologia, 2016, 1–13.
37. [37] Bogacka, I., Xie, H., Bray, G.A., Smith, S.R., Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 54 (2005), 1392–1399.
38. [38] Choo, H.-J., Kim, J.-H., Kwon, O.-B., et al. Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49 (2006), 784–791.
39. [39] Kaaman, M., Sparks, L.M., van Harmelen, V., et al. Strong association between mitochondrial DNA copy number and lipogenesis in human white adipose tissue. Diabetologia 50 (2007), 2526–2533.
40. [40] Cummins, T.D., Holden, C.R., Sansbury, B.E., et al. Metabolic remodeling of white adipose tissue in obesity. Am. J. Physiol. - Endocrinol. Metab. 307 (2014), E262–E277.
41. [41] Rong, J.X., Qiu, Y., Hansen, M.K., et al. Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet–fed mice and improved by rosiglitazone. Diabetes 56 (2007), 1751–1760.
42. [42] Tol, M.J., Ottenhoff, R., van Eijk, M., et al. A PPARγ-Bnip3 axis couples adipose mitochondrial fusion-fission balance to systemic insulin sensitivity. Diabetes 65 (2016), 2591–2605.
43. [43] Jukarainen, S., Heinonen, S., Rämö, J.T., et al. Obesity is associated with low NAD+/SIRT pathway expression in adipose tissue of BMI-discordant monozygotic twins. J. Clin. Endocrinol. Metab. 101 (2016), 275–283.
44. [44] Moreno-Viedma, V., Amor, M., Sarabi, A., et al. Common dysregulated pathways in obese adipose tissue and atherosclerosis. Cardiovasc. Diabetol., 15, 2016, 120.
45. [45] She, P., Van Horn, C., Reid, T., Hutson, S.M., Cooney, R.N., Lynch, C.J., Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am. J. Physiol. Endocrinol. Metab. 293 (2007), E1552–E1563.
46. [46] Dahlman, I., Forsgren, M., Sjögren, A., et al. Downregulation of electron transport chain genes in visceral adipose tissue in type 2 diabetes independent of obesity and possibly involving tumor necrosis factor-α. Diabetes 55 (2006), 1792–1799.
47. [47] Lindinger, P.W., Christe, M., Eberle, A.N., et al. Important mitochondrial proteins in human omental adipose tissue show reduced expression in obesity. J. Proteom. 124 (2015), 79–87.
48. [48] Xie, X., Yi, Z., Bowen, B., et al. Characterization of the human adipocyte proteome and reproducibility of protein abundance by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. J. Proteome Res. 9 (2010), 4521–4534.
49. [49] Christe, M., Hirzel, E., Lindinger, A., et al. Obesity affects mitochondrial citrate synthase in human omental adipose tissue. ISRN Obes., 2013, 2013, 826027.
50. [50] Fischer, B., Schöttl, T., Schempp, C., et al. Inverse relationship between body mass index and mitochondrial oxidative phosphorylation capacity in human subcutaneous adipocytes. Am. J. Physiol. - Endocrinol. Metab. 309 (2015), E380–E387.
51. [51] Yin, X., Lanza, I.R., Swain, J.M., Sarr, M.G., Nair, K.S., Jensen, M.D., Adipocyte mitochondrial function is reduced in human obesity independent of fat cell size. J. Clin. Endocrinol. Metab. 99 (2014), E209–E216.
52. [52] Chattopadhyay, M., GuhaThakurta, I., Behera, P., et al. Mitochondrial bioenergetics is not impaired in nonobese subjects with type 2 diabetes mellitus. Metab. - Clin. Exp. 60 (2011), 1702–1710.
53. [53] Schöttl, T., Kappler, L., Fromme, T., Klingenspor, M., Limited OXPHOS capacity in white adipocytes is a hallmark of obesity in laboratory mice irrespective of the glucose tolerance status. Mol. Metab. 4 (2015), 631–642.
54. [54] Wilson-Fritch, L., Nicoloro, S., Chouinard, M., et al. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Investig. 114 (2004), 1281–1289.
55. [55] Calderon-Dominguez, M., Mir, J.F., Fucho, R., Weber, M., Serra, D., Herrero, L., Fatty acid metabolism and the basis of brown adipose tissue function. Adipocyte 5 (2016), 98–118.
56. [56] Virtanen, K.A., Lidell, M.E., Orava, J., et al. Functional brown adipose tissue in healthy adults. New Engl. J. Med. 360 (2009), 1518–1525.
57. [57] Hondares, E., Rosell, M., Diaz-Delfin, J., et al. Peroxisome proliferator-activated receptor alpha (PPARalpha) induces PPARgamma coactivator 1alpha (PGC-1alpha) gene expression and contributes to thermogenic activation of brown fat: involvement of PRDM16. J. Biol. Chem. 286 (2011), 43112–43122.
58. [58] Seale, P., Kajimura, S., Yang, W., et al. Transcriptional control of brown fat determination by PRDM16. Cell Metab. 6 (2007), 38–54.
59. [59] Uldry, M., Yang, W., St-Pierre, J., Lin, J., Seale, P., Spiegelman, B.M., Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 3 (2006), 333–341.
60. [60] Goodbody, A.E., Trayhurn, P., GDP binding to brown-adipose-tissue mitochondria of diabetic-obese (db/db) mice. Decreased binding in both the obese and pre-obese states. Biochem. J. 194 (1981), 1019–1022.
61. [61] Himms-Hagen, J., Desautels, M., A mitochondrial defect in brown adipose tissue of the obese (ob/ob) mouse: reduced binding of purine nucleotides and a failure to respond to cold by an increase in binding. Biochem. Biophys. Res. Commun. 83 (1978), 628–634.
62. [62] Shimizu, I., Aprahamian, T., Kikuchi, R., et al. Vascular rarefaction mediates whitening of brown fat in obesity. J. Clin. Invest. 124 (2014), 2099–2112.
63. [63] Vijgen, G.H., Bouvy, N.D., Teule, G.J., Brans, B., Schrauwen, P., van Marken Lichtenbelt, W.D., Brown adipose tissue in morbidly obese subjects. PloS One, 6, 2011, e17247.
64. [64] Vernochet, C., Damilano, F., Mourier, A., et al. Adipose tissue mitochondrial dysfunction triggers a lipodystrophic syndrome with insulin resistance, hepatosteatosis, and cardiovascular complications. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 28 (2014), 4408–4419.
65. [65] Caton, P.W., Kieswich, J., Yaqoob, M.M., Holness, M.J., Sugden, M.C., Nicotinamide mononucleotide protects against pro-inflammatory cytokine-mediated impairment of mouse islet function. Diabetologia 54 (2011), 3083–3092.
66. [66] Mercader, J., Granados, N., Caimari, A., Oliver, P., Bonet, M.L., Palou, A., Retinol-binding protein 4 and nicotinamide phosphoribosyltransferase/visfatin in rat obesity models. Horm. Metab. Res. 40 (2008), 467–472.
67. [67] Yoshino, J., Mills, K.F., Yoon, M.J., Imai, S., Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 14 (2011), 528–536.
68. [68] Pagano, C., Pilon, C., Olivieri, M., et al. Reduced plasma visfatin/pre-B cell colony-enhancing factor in obesity is not related to insulin resistance in humans. J. Clin. Endocrinol. Metab. 91 (2006), 3165–3170.
69. [69] Rappou, E., Jukarainen, S., Rinnankoski-Tuikka, R., et al. Weight loss is associated with increased NAD+/SIRT1 expression but reduced PARP activity in white adipose tissue. J. Clin. Endocrinol. Metab. 101 (2016), 1263–1273.
70. [70] Yoon, M.J., Yoshida, M., Johnson, S., et al. SIRT1-mediated eNAMPT secretion from adipose tissue regulates hypothalamic NAD+ and function in mice. Cell Metab. 21 (2015), 706–717.
71. [71] Canto, C., Houtkooper, R.H., Pirinen, E., et al. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab. 15 (2012), 838–847.
72. [72] Nikiforov, A., Kulikova, V., Ziegler, M., The human NAD metabolome: functions, metabolism and compartmentalization. Crit. Rev. Biochem. Mol. Biol. 50 (2015), 284–297.
73. [73] Stein, L.R., Imai, S., The dynamic regulation of NAD metabolism in mitochondria. Trends Endocrinol. Metab. 23 (2012), 420–428.
74. [74] Houtkooper, R.H., Canto, C., Wanders, R.J., Auwerx, J., The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr. Rev. 31 (2010), 194–223.
75. [75] Ratajczak, J., Joffraud, M., Trammell, S.A., et al. NRK1 controls nicotinamide mononucleotide and nicotinamide riboside metabolism in mammalian cells. Nat. Commun., 7, 2016, 13103.
76. [76] Revollo, J.R., Korner, A., Mills, K.F., et al. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab. 6 (2007), 363–375.
77. [77] Mouchiroud, L., Houtkooper, R.H., Auwerx, J., NAD(+) metabolism: a therapeutic target for age-related metabolic disease. Crit. Rev. Biochem. Mol. Biol. 48 (2013), 397–408.
78. [78] Bai, P., Cantó, C., The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab. 16 (2012), 290–295.
79. [79] Bai, P., Nagy, L., Fodor, T., Liaudet, L., Pacher, P., Poly(ADP-ribose) polymerases as modulators of mitochondrial activity. Trends Endocrinol. Metab. 26 (2015), 75–83.
80. [80] Bai, P., Canto, C., Oudart, H., et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 13 (2011), 461–468.
81. [81] Pirinen, E., Canto, C., Jo, Y.S., et al. Pharmacological inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab. 19 (2014), 1034–1041.
82. [82] Rajamohan, S.B., Pillai, V.B., Gupta, M., et al. SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1. Mol. Cell. Biol. 29 (2009), 4116–4129.
83. [83] Ramsey, K.M., Yoshino, J., Brace, C.S., et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324 (2009), 651–654.
84. [84] Frydelund-Larsen, L., Akerstrom, T., Nielsen, S., Keller, P., Keller, C., Pedersen, B.K., Visfatin mRNA expression in human subcutaneous adipose tissue is regulated by exercise. Am. J. Physiol. Endocrinol. Metab. 292 (2007), E24–E31.
85. [85] Chen, D., Bruno, J., Easlon, E., et al. Tissue-specific regulation of SIRT1 by calorie restriction. Genes Dev. 22 (2008), 1753–1757.
86. [86] Song, J., Ke, S.F., Zhou, C.C., et al. Nicotinamide phosphoribosyltransferase is required for the calorie restriction-mediated improvements in oxidative stress, mitochondrial biogenesis, and metabolic adaptation. J. Gerontol. A Biol. Sci. Med. Sci. 69 (2014), 44–57.
87. [87] Caton, P.W., Kieswich, J., Yaqoob, M.M., Holness, M.J., Sugden, M.C., Metformin opposes impaired AMPK and SIRT1 function and deleterious changes in core clock protein expression in white adipose tissue of genetically-obese db/db mice. Diabetes Obes. Metab. 13 (2011), 1097–1104.
88. [88] Curtin, N.J., Szabo, C., Therapeutic applications of PARP inhibitors: anticancer therapy and beyond. Mol. Asp. Med. 34 (2013), 1217–1256.
89. [89] Feige, J.N., Lagouge, M., Canto, C., et al. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab. 8 (2008), 347–358.
90. [90] Lagouge, M., Argmann, C., Gerhart-Hines, Z., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127 (2006), 1109–1122.
91. [91] Choi, K.C., Ryu, O.H., Lee, K.W., et al. Effect of PPAR-alpha and -gamma agonist on the expression of visfatin, adiponectin, and TNF-alpha in visceral fat of OLETF rats. Biochem. Biophys. Res. Commun. 336 (2005), 747–753.
92. [92] Choi, K.C., Lee, S.Y., Yoo, H.J., et al. Effect of PPAR-delta agonist on the expression of visfatin, adiponectin, and resistin in rat adipose tissue and 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 357 (2007), 62–67.
93. [93] Stromsdorfer, K.L., Yamaguchi, S., Yoon, M.J., et al. NAMPT-mediated NAD(+) biosynthesis in adipocytes regulates adipose tissue function and multi-organ insulin sensitivity in mice. Cell Rep. 16 (2016), 1851–1860.
94. [94] Birjmohun, R.S., Hutten, B.A., Kastelein, J.J., Stroes, E.S., Efficacy and safety of high-density lipoprotein cholesterol-increasing compounds: a meta-analysis of randomized controlled trials. J. Am. Coll. Cardiol. 45 (2005), 185–197.
95. [95] Barbosa, M.T., Soares, S.M., Novak, C.M., et al. The enzyme CD38 (a NAD glycohydrolase, EC 3.2.2.5) is necessary for the development of diet-induced obesity. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 21 (2007), 3629–3639.
96. [96] Gariani, K., Ryu, D., Menzies, K.J., et al. Inhibiting poly ADP-ribosylation increases fatty acid oxidation and protects against fatty liver disease. J. Hepatol. 66 (2016), 132–141.
97. [97] Haffner, C.D., Becherer, J.D., Boros, E.E., et al. Discovery, synthesis, and biological evaluation of thiazoloquin(az)olin(on)es as potent CD38 inhibitors. J. Med. Chem. 58 (2015), 3548–3571.
98. [98] Drew, J.E., Farquharson, A.J., Horgan, G.W., Williams, L.M., Tissue-specific regulation of sirtuin and nicotinamide adenine dinucleotide biosynthetic pathways identified in C57Bl/6 mice in response to high-fat feeding. J. Nutr. Biochem. 37 (2016), 20–29.
99. [99] Liu, Z., Gan, L., Liu, G., et al. Sirt1 decreased adipose inflammation by interacting with Akt2 and inhibiting mTOR/S6K1 pathway in mice. J. Lipid Res. 57 (2016), 1373–1381.
100. [100] Nisoli, E., Tonello, C., Cardile, A., et al. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310 (2005), 314–317.
101. [101] Chalkiadaki, A., Guarente, L., High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab. 16 (2012), 180–188.
102. [102] Krishnan, J., Danzer, C., Simka, T., et al. Dietary obesity-associated Hif1α activation in adipocytes restricts fatty acid oxidation and energy expenditure via suppression of the Sirt2-NAD(+) system. Genes Dev. 26 (2012), 259–270.
103. [103] Cohen, H.Y., Miller, C., Bitterman, K.J., et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305 (2004), 390–392.
104. [104] Laurent, G., German, N.J., Saha, A.K., et al. SIRT4 coordinates the balance between lipid synthesis and catabolism by repressing malonyl CoA decarboxylase. Mol. Cell 50 (2013), 686–698.
105. [105] Wang, F., Tong, Q., SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1's repressive interaction with PPARγ. Mol. Biol. Cell 20 (2009), 801–808.
106. [106] Clark, S.J., Falchi, M., Olsson, B., et al. Association of sirtuin 1 (SIRT1) gene SNPs and transcript expression levels with severe obesity. Obesity 20 (2012), 178–185.
107. [107] Gillum, M.P., Kotas, M.E., Erion, D.M., et al. SirT1 regulates adipose tissue inflammation. Diabetes 60 (2011), 3235–3245.
108. [108] Kurylowicz, A., Owczarz, M., Polosak, J., et al. SIRT1 and SIRT7 expression in adipose tissues of obese and normal-weight individuals is regulated by microRNAs but not by methylation status. Int. J. Obes. 40 (2016), 1635–1642.
109. [109] Pedersen, S.B., Olholm, J., Paulsen, S.K., Bennetzen, M.F., Richelsen, B., Low Sirt1 expression, which is upregulated by fasting, in human adipose tissue from obese women. Int. J. Obes. 32 (2008), 1250–1255.
110. [110] Song, Y.S., Lee, S.K., Jang, Y.J., et al. Association between low SIRT1 expression in visceral and subcutaneous adipose tissues and metabolic abnormalities in women with obesity and type 2 diabetes. Diabetes Res. Clin. Pract. 101 (2013), 341–348.
111. [111] Moschen, A.R., Wieser, V., Gerner, R.R., et al. Adipose tissue and liver expression of SIRT1, 3, and 6 increase after extensive weight loss in morbid obesity. J. Hepatol. 59 (2013), 1315–1322.
112. [112] Rosen, E.D., Walkey, C.J., Puigserver, P., Spiegelman, B.M., Transcriptional regulation of adipogenesis. Genes Dev. 14 (2000), 1293–1307.
113. [113] Wilson-Fritch, L., Burkart, A., Bell, G., et al. Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol. Cell. Biol. 23 (2003), 1085–1094.
114. [114] Picard, F., Kurtev, M., Chung, N., et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-[gamma]. Nature 429 (2004), 771–776.
115. [115] Mayoral, R., Osborn, O., McNelis, J., et al. Adipocyte SIRT1 knockout promotes PPARγ activity, adipogenesis and insulin sensitivity in chronic-HFD and obesity. Mol. Metab. 4 (2015), 378–391.
116. [116] Xu, F., Burk, D., Gao, Z., et al. Angiogenic deficiency and adipose tissue dysfunction are associated with macrophage malfunction in SIRT1(−/−) mice. Endocrinology 153 (2012), 1706–1716.
117. [117] Zhou, Y., et al., Song, T., Peng, J., SIRT1 Suppresses Adipogenesis by Activating Wnt/β-Catenin Signaling In Vivo and In Vitro 7 (2016), 77707–77720.
118. [118] Simic, P., Zainabadi, K., Bell, E., et al. SIRT1 regulates differentiation of mesenchymal stem cells by deacetylating β-catenin. EMBO Mol. Med. 5 (2013), 430–440.
119. [119] Jing, E., Gesta, S., Kahn, C.R., SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab. 6 (2007), 105–114.
120. [120] Cioffi, M., Vallespinos-Serrano, M., Trabulo Sara, M., et al. MiR-93 controls adiposity via inhibition of Sirt7 and Tbx3. Cell Rep. 12 (2015), 1594–1605.
121. [121] Bober, E., Fang, J., Smolka, C., et al. Sirt7 promotes adipogenesis by binding to and inhibiting Sirt1. BMC Proc., 6, 2012, P57.
122. [122] Erener, S., Hesse, M., Kostadinova, R., Hottiger, M.O., Poly(ADP-Ribose)polymerase-1 (PARP1) controls adipogenic gene expression and adipocyte function. Mol. Endocrinol. 26 (2012), 79–86.
123. [123] Erener, S., Mirsaidi, A., Hesse, M., et al. ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. FASEB J. 26 (2012), 2631–2638.
124. [124] Lehmann, M., Pirinen, E., Mirsaidi, A., et al. ARTD1-induced poly-ADP-ribose formation enhances PPARγ ligand binding and co-factor exchange. Nucleic Acids Res. 43 (2015), 129–142.
125. [125] Bai, P., Houten, S.M., Huber, A., et al. Peroxisome proliferator-activated receptor (PPAR)-2 controls adipocyte differentiation and adipose tissue function through the regulation of the activity of the retinoid X receptor/PPARγ heterodimer. J. Biol. Chem. 282 (2007), 37738–37746.
126. [126] Xu, C., Bai, B., Fan, P., et al. Selective overexpression of human SIRT1 in adipose tissue enhances energy homeostasis and prevents the deterioration of insulin sensitivity with ageing in mice. Am. J. Transl. Res. 5 (2013), 412–426.
127. [127] Boutant, M., Joffraud, M., Kulkarni, S.S., et al. SIRT1 enhances glucose tolerance by potentiating brown adipose tissue function. Mol. Metab. 4 (2015), 118–131.
128. [128] Chakrabarti, P., English, T., Karki, S., et al. SIRT1 controls lipolysis in adipocytes via FOXO1-mediated expression of ATGL. J. Lipid Res. 52 (2011), 1693–1701.
129. [129] Fischer-Posovszky, P., Kukulus, V., Tews, D., et al. Resveratrol regulates human adipocyte number and function in a Sirt1-dependent manner. Am. J. Clin. Nutr. 92 (2010), 5–15.
130. [130] Foster, D.W., Malonyl-CoA: the regulator of fatty acid synthesis and oxidation. J. Clin. Invest. 122 (2012), 1958–1959.
131. [131] Kanfi, Y., Peshti, V., Gil, R., et al. SIRT6 protects against pathological damage caused by diet-induced obesity. Aging Cell 9 (2010), 162–173.
132. [132] Boutant, M., Kulkarni Sameer, S., Joffraud, M., et al. SIRT1 gain of function does not mimic or enhance the adaptations to intermittent fasting. Cell Rep. 14 (2016), 2068–2075.
133. [133] Lin, Q.-Q., Yan, C.-F., Lin, R., et al. SIRT1 regulates TNF-α-induced expression of CD40 in 3T3-L1 adipocytes via NF-κB pathway. Cytokine 60 (2012), 447–455.
134. [134] Xu, F., Gao, Z., Zhang, J., et al. Lack of SIRT1 (mammalian sirtuin 1) activity leads to liver steatosis in the SIRT1+/− mice: a role of lipid mobilization and inflammation. Endocrinology 151 (2010), 2504–2514.
135. [135] Yoshizawa, T., Karim, M.F., Sato, Y., et al. SIRT7 controls hepatic lipid metabolism by regulating the ubiquitin-proteasome pathway. Cell Metab. 19 (2014), 712–721.
136. [136] Qiao, L., Shao, J., SIRT1 regulates adiponectin gene expression through Foxo1-C/enhancer-binding protein α transcriptional complex. J. Biol. Chem. 281 (2006), 39915–39924.
137. [137] Qiang, L., Wang, H., Farmer, S.R., Adiponectin secretion is regulated by SIRT1 and the endoplasmic reticulum oxidoreductase Ero1-Lα. Mol. Cell. Biol. 27 (2007), 4698–4707.
138. [138] Xu, F., Zheng, X., Lin, B., et al. Diet-induced obesity and insulin resistance are associated with brown fat degeneration in SIRT1-deficient mice. Obesity 24 (2016), 634–642.
139. [139] Banks, A.S., Kon, N., Knight, C., et al. SirT1 gain-of-function increases energy efficiency and prevents diabetes in mice. Cell Metab. 8 (2008), 333–341.
140. [140] Bordone, L., Cohen, D., Robinson, A., et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6 (2007), 759–767.
141. [141] Shi, T., Wang, F., Stieren, E., Tong, Q., SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J. Biol. Chem. 280 (2005), 13560–13567.
142. [142] Hirschey, M.D., Shimazu, T., Goetzman, E., et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464 (2010), 121–125.
143. [143] Noriega, L.G., Feige, J.N., Canto, C., et al. CREB and ChREBP oppositely regulate SIRT1 expression in response to energy availability. EMBO Rep. 12 (2011), 1069–1076.
144. [144] Gerhart-Hines, Z., Dominy, J.E. Jr., Blattler, S.M., et al. The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Mol. Cell 44 (2011), 851–863.
145. [145] Giralt, A., Hondares, E., Villena, J.A., et al. Peroxisome proliferator-activated receptor-gamma coactivator-1alpha controls transcription of the Sirt3 gene, an essential component of the thermogenic brown adipocyte phenotype. J. Biol. Chem. 286 (2011), 16958–16966.
146. [146] Giralt, A., Hondares, E., Villena, J.A., et al. Peroxisome proliferator-activated receptor-γ coactivator-1α controls transcription of the Sirt3 gene, an essential component of the thermogenic brown adipocyte phenotype. J. Biol. Chem. 286 (2011), 16958–16966.
147. [147] Tiraby, C., Tavernier, G., Lefort, C., et al. Acquirement of brown fat cell features by human white adipocytes. J. Biol. Chem. 278 (2003), 33370–33376.
148. [148] Qiang, L., Wang, L., Kon, N., et al. Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Pparγ. Cell 150 (2012), 620–632.
149. [149] Potente, M., Ghaeni, L., Baldessari, D., et al. SIRT1 controls endothelial angiogenic functions during vascular growth. Genes Dev. 21 (2007), 2644–2658.
150. [150] Finley, L.W., Haas, W., Desquiret-Dumas, V., et al. Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PloS One, 6, 2011, e23295.
151. [151] Giralt, A., Villarroya, F., SIRT3, a pivotal actor in mitochondrial functions: metabolism, cell death and aging. Biochem. J. 444 (2012), 1–10.
152. [152] Bartelt, A., Bruns, O.T., Reimer, R., et al. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 17 (2011), 200–205.
153. [153] Cannon, B., Nedergaard, J., Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004), 277–359.
154. [154] Pfluger, P.T., Herranz, D., Velasco-Miguel, S., Serrano, M., Tschop, M.H., Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. USA 105 (2008), 9793–9798.
155. [155] Zhong, L., D'Urso, A., Toiber, D., et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1α. Cell 140 (2010), 280–293.
156. [156] Erion, D.M., Yonemitsu, S., Nie, Y., et al. SirT1 knockdown in liver decreases basal hepatic glucose production and increases hepatic insulin responsiveness in diabetic rats. Proc. Natl. Acad. Sci. USA 27 (2009), 11288–11293.
157. [157] Lombard, D.B., Alt, F.W., Cheng, H.L., et al. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 24 (2007), 8807–8814.
158. [158] Mostoslavsky, R., Chua, K.F., Lombard, D.B., et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124 (2006), 315–329.
159. [159] Devalaraja-Narashimha, K., Padanilam, B.J., PARP1 deficiency exacerbates diet-induced obesity in mice. J. Endocrinol. 205 (2010), 243–252.