NAG-1/GDF-15 prevents obesity by increasing thermogenesis, lipolysis and oxidative metabolism

International Journal of Obesity

Volumn 38, Issue 12, 2014, Pages 1555-1564

  Chrysovergis, K ^a   Wang, X ^b   Kosak, J ^a   Lee, S H ^c   Kim, J S ^a   Foley, J F ^b   Travlos, G ^b   Singh, S ^a   Baek, S J ^a   Eling, T E ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c Andong National University   (South Korea)

Author keywords

BAT; insulin resistance; lipolysis; NAG 1 GDF 15; thermogenesis

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 15; INSULIN; MITOCHONDRIAL DNA; GDF15 PROTEIN, HUMAN;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; ENERGY EXPENDITURE; ENERGY METABOLISM; FEMALE; FOOD INTAKE; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID ABSORPTION; LIPID DIET; LIPID STORAGE; LIPOLYSIS; LOW FAT DIET; MALE; MELANOMA CELL; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROPERITONEAL FAT; THERMOGENESIS; WHITE ADIPOSE TISSUE; XENOGRAFT; ADIPOSE TISSUE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; EATING; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; METABOLISM; MOUSE MUTANT; OXIDATIVE STRESS; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; DIET, HIGH-FAT; EATING; ENERGY METABOLISM; ENZYME-LINKED IMMUNOSORBENT ASSAY; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; INSULIN RESISTANCE; LIPOLYSIS; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; THERMOGENESIS;

EID: 84927177513     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2014.27     Document Type: Article

References (52)

1. OgDen CL, Carroll MD, Kit BK, FLegal KM. PrevaLence of obesity in the United States, 2009-2010. NCHS Data Brief 2012; 82: 1-8
2. Apovian CM, Bigornia S, Mott M, Meyers MR, Ulloor J, Gagua M et al. Adipose macrophage infiltration is associated with insulin resistance and vascular endothelial dysfunction in obese subjects. ArterioscLer Thromb Vasc Biol 2008; 28: 1654-1659
3. CalLe EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003; 348: 1625-1638
4. Hotamisligil GS. Inflammation and metabolic disorDers. Nature 2006; 444: 860-867
5. Harwood HJ Jr. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012; 63: 57-75
6. Heeren J, Mnzberg H. Novel aspects of brown adipose tissue biology. Endocrinol Metab Clin 2013; 42: 89-107
7. Marcelin G, Chua S Jr. Contributions of adipocyte lipid metabolism to body fat content and implications for the treatment of obesity. Curr Opin Pharmacol 2010; 10: 588-593
8. Ruan H, Lodish HF. Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α. Cytokine Growth Factor Rev 2003; 14: 447-455
9. Ruan H, Lodish HF. Regulation of insulin sensitivity by adipose tissue-Derived hormones and inflammatory cytokines. Curr Opin Lipidol 2004; 15: 297-302
10. Cannon B, NeDergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277-359
11. Zamani N, Brown CW. Emerging roLes for the transforming growth factor-β superfamily in regulating adiposity and energy expenditure. Endocr Rev 2011; 32: 387-403
12. Wang W, Yang Y, Meng Y, Shi Y. GDF-3 is an adipogenic cytokine unDer high fat dietary condition. Biochem Biophys Res Commun 2004; 321: 1024-1031
13. Shen JJ, Huang L, Li L, Jorgez C, Matzuk MM, Brown CW. Deficiency of growth differentiation factor 3 protects against diet-induced obesity by seLectively acting on white adipose. Mol Endocrinol 2009; 23: 113-123
14. AnDersson O, Korach-Andre M, Reissmann E, Ibez CF, Bertolino P. Growth differentiation factor 3 signals through ALK7 and regulates accumulation of adipose tissue and diet-induced obesity. Proc Natl Acad Sci USA 2008; 105: 7252-7256
15. Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN et al. Induction of cachexia in mice by systemically administered myostatin. Science 2002; 296: 1486-1488
16. Feldman BJ, Streeper RS, Farese JrRV, Yamamoto K. Myostatin modulates adiogenesis to generate adipocytes with favorabLe metabolic effects. Proc Natl Acad Sci USA 2006; 103: 15675-15680
17. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM et al. New roLe of bone morphogenic protein 7 in brown adipogenesis and energy expenditure. Nature 2008; 454: 1000-1004
18. WhittLe AJ, Carobbio S, Martins L, Slawik M, Hondares E, Vzquez MJ et al. BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 2012; 149: 871-885
19. Bttner M, Suter-Crazzolara C, Schober A, Unsicker K. Expression of a novel member of the TGF-beta superfamily, growth/differentiation factor-15/macrophage inhibitory cytokine-1 (GDF-15/MIC-1) in adult rat tissues. Cell Tissue Res 1999; 297: 103-110
20. Bootcov MR, Bauskin AR, VaLenzuela SM, Moore AG, Bansal M, He XY et al. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc Natl Acad Sci USA 1997; 94: 11514-11519
21. Baek SJ, Kim KS, Nixon JB, Wilson LC, Eling TE. Cyclooxygenase inhibitors regulate the expression of a TGF-beta superfamily member that has proapoptotic and antitumorigenic activities. Mol Pharmacol 2001; 59: 901-908
22. Baek SJ, Okazaki R, Lee SH, Martinez J, Kim JS, Yamaguchi K et al. Nonsteroidal anti-inflammatory drug-Activated gene-1 over expression in transgenic mice suppresses intestinal neoplasia. Gastroenterology 2006; 131: 1553-1560
23. Kim JM, Kosak JP, Kim JK, Kissling G, GermoLec DR, Zeldin DR et al. NAG-1/GDF15 transgenic mouse has Less white adipose tissue and a reduced inflammatory response. Mediators Inflamm 2013; 2013: 641851
24. Johnen H, Lin S, Kuffner T, Brown DA, Tsai VW, Bauskin AR et al. Tumor-induced anorexia and weight loss are mediated by the TGF-β superfamily cytokine MIC-1. Nat Med 2007; 13: 1333-1340
25. Wang X, Chrysovergis K, Bienstock RJ, Shim M, Eling TE. The H6D variant of NAG-1/GDF15 inhibits prostate xenograft growth in vivo. Prostate 2012; 72: 677-689
26. HumbLe MM, Young MJ, FoLey JF, Pandiri AR, Travlos GS, Copeland WC. Polg2 is essential for mammalian embryogenesis and is required for mtDNA maintenance. Hum Mol Genet 2012; 22: 1017-1025
27. Carpenter KJ, Mayer J. Physiologic observations on yellow obesity in the mouse. Am J Physiol 1958; 193: 499-504
28. Dickerson GE, Gowan JW. Hereditary obesity and efficient food utilization in mice. Science 1947; 105: 496-498
29. Friedman JM, Leibel RL. Tackling a weighty probLem. Cell 1992; 69: 217-220
30. Reddy JK, Rao MS. Lipid metabolism and lipid inflammation. II. Fatty liver disease and fatty acid oxidation. Am J Physiol Gastrointest Liver Physiol 2006; 290: G852-G858
31. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. Adipocyte Death Defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005; 46: 2347-2355
32. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808
33. Stienstra R, Joosten LAB, Koenen T, Van Tits B, Van Diepen JA, Van Den Berg SAA et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metabol 2010; 12: 593-605
34. Liew CW, Boucher J, Cheong JK, Vernochet C, Koh HJ, Mallol C et al. Ablation of TRIP-Br2, a regulator of fat lipolysis, thermogenesis and oxidative metabolism, prevents diet-induced obesity and insulin resistance. Nat Med 2013; 19: 217-226
35. Guerra C, Koza RA, Yamashita H, Walsh K, Kozak LP. Emergence of brown adipocytes in white fat in mice is unDer genetic control. J Clin Invest 1998; 102: 412-420
36. Cheng Y, Meng Q, Wang C, Li H, Huang Z, Chen S et al. Leucine Deprivation Decreases fat mass by stimulation of lipolysis in white adipose tissue and upregulation of uncoupling protein 1 (UCP1) in brown adipose tissue. Diabetes 2010; 59: 17-25
37. Liu L, Wang X, Hu Y, Kang J, Wang L, Li S. Effects of a fatty acid synthase inhibitor on adipocyte differentiation of mouse 3T3-L1 cells. Acta Pharmacol Sin 2004; 25: 1052-1057
38. Ahima RS. Adipose tissue as an endocrine organ. Obesity 2006; 14: 242S-249S.
39. Hajer GR, Van Haeften TW, Visseren FLJ. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 2008; 29: 2959-2971
40. Ahmadian M, Duncan RE, Varady KA, Frasson D, HelLerstein MK, Birkenfeld AL et al. Adipose overexpression of Desnutrin promotes faty acid use and attenuates dietinduced obesity. Diabetes 2009; 58: 855-866
41. Stanford KI, MidDelbeek RJW, Townsend KL, An D, Nygaard EB, Hitchcox KM et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest 2013; 123: 215-223
42. ALexandraki K, Piperi C, Kalofoutis C, Singh J, Alaveras A, Kalofoutis A. Inflammatory process in type II diabetes: the roLe of cytokines. Ann NY Acad Sci 2006; 1084: 89-117
43. Lundgren M, Svensson M, Lindmark S, Renstrm F, Ruge T, Eriksson JW. Fat cell enlargement is an inDepenDent marker of insulin resistance and hyperLeptinaemia. Diabetologia 2007; 50: 625-633
44. Roberts R, Hodson L, Dennis A.L, NevilLe M.J, Humphreys SM, HarnDen KE et al. Markers of De novo lipogenesis in adipose tissue: associations with small adipocytes and insulin sensitivity in humans. Diabetologia 2009; 52: 882-890
45. Ding Q, Mracek T, GonzaLez-Muniesa P, Kos K, Wilding J, Trayhurn P et al. IDentification of macrophage inhibitory cytokine-1 in adipose tissue and its secretion as an adipokine by human adipocytes. Endocrinology 2009; 150: 1688-1696
46. Dostlov I, Roubcek T, Brtlov M, Mrz M, Lacinov Z, Haluzkov D et al. Increased serum concentrations of macrophage inhibitory cytokine-1 in patients with obesity and type 2 diabetes mellitus: the influence of very low calorie diet. Eur J Endocrinol 2009; 161: 397-404
47. Karczewska-Kupczewska M, Kowalska I, Nikolajuk A, Adamska A, Otziomek E, Gorska M et al. Hyperinsulinemia acutely increases serum macrophage inhibitory cytokine-1 concentration in anorexia nervosa and obesity. Clin Endocrin 2012; 76: 46-50
48. Vila G, Riedl M, AnDerwald C, Resl M, Handisurya A, Clodi M et al. The relationship between insulin resistance and the cardiovascular biomarker growth differentiation factor-15 in obese patients. Clin Chem 2011; 57: 309-316
49. Macia L, Tsai VW, Nguyen AD, Johnen H, Kuffner T, Shi YC et al. Macrophage inhibitory cytokine 1 (MIC-1/GDF15) Decreases food intake, body weight and improves glucose toLerance in mice on normal &obesogenic diets. PLoS One 2012; 7: e34868
50. OuelLet V, Labb SM, Blondin DP, Phoenix S, Gurin B, Haman F et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 2012; 122: 545-552
51. Virtanen KA, LiDell ME, Orava J, Heglind M, Westergren R, Niemi T et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518-1525
52. Cypess AM, Chen YC, Sze C, Wang K, English J, Chan O et al. Cold but not sympathomimetics activates human brown adipose tissue in vivo. Proc Natl Acad Sci USA 2012; 109: 10001-10005.