Effects of endurance exercise training, metformin, and their combination on Adipose tissue leptin and IL-10 secretion in OLETF rats

Journal of Applied Physiology

Volumn 113, Issue 12, 2012, Pages 1873-1883

  Jenkins, Nathan T ^a   Padilla, Jaume ^a   Arce Esquivel, Arturo A ^a   Bayless, David S ^a   Martin, Jeffrey S ^a   Leidy, Heather J ^b   Booth, Frank W ^a,b,c   Scott Rector, R ^b,d   Harold Laughlin, M ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cardiovascular disease; Inflammation; Insulin resistance; Obesity

Indexed keywords

INTERLEUKIN 10; LEPTIN; METFORMIN;

ADIPOSE TISSUE; ANIMAL; ANIMAL EXPERIMENT; ARTICLE; DRUG EFFECT; ENDURANCE; MALE; METABOLISM; METHODOLOGY; MULTIMODALITY CANCER THERAPY; NON INSULIN DEPENDENT DIABETES MELLITUS; OTSUKA LONG EVANS TOKUSHIMA FATTY RAT; PATHOPHYSIOLOGY; RAT; TREATMENT OUTCOME;

ADIPOSE TISSUE; ANIMALS; COMBINED MODALITY THERAPY; DIABETES MELLITUS, TYPE 2; INTERLEUKIN-10; LEPTIN; MALE; METFORMIN; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; RATS; RATS, INBRED OLETF; TREATMENT OUTCOME;

EID: 84871602981     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00936.2012     Document Type: Article

References (49)

1. American Diabetes Association. Standards of medical care in diabetes-2012. Diabetes Care 35 Suppl 1:S11-S63, 2012.
2. Bays HE. Adiposopathy is "sick fat" a cardiovascular disease? J Am Coll Cardiol 57:2461-2473, 2011.
3. Bunker AK, Arce-Esquivel AA, Rector RS, Booth FW, Ibdah JA, Laughlin MH. Physical activity maintains aortic endothelium-dependent relaxation in the obese type 2 diabetic OLETF rat. Am J Physiol Heart Circ Physiol 298:H1889-H1901, 2010.
4. Diabetes Prevention Program Research Group. Reduction in the incidence of Type 2 diabetes with lifestyle intervention or metformin. N Eng J Med 346:393-403, 2002.
5. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98-107, 2011.
6. Ellingsgaard H, Hauselmann I, Schuler B, Habib AM, Baggio LL, Meier DT, Eppler E, Bouzakri K, Wueest S, Muller YD, Hansen AM, Reinecke M, Konrad D, Gassmann M, Reimann F, Halban PA, Gromada J, Drucker DJ, Gribble FM, Ehses JA, Donath MY. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and alpha cells. Nat Med 17:1481-1489, 2011.
7. Fain JN. Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediators Inflamm 2010:513948, 2010.
8. Gomez-Diaz RA, Talavera JO, Pool EC, Ortiz-Navarrete FV, Solorzano-Santos F, Mondragon-Gonzalez R, Valladares-Salgado A, Cruz M, Aguilar-Salinas CA, Wacher NH. Metformin decreases plasma resistin concentrations in pediatric patients with impaired glucose tolerance: a placebo-controlled randomized clinical trial. Metabolism 61:1247-1255, 2012.
9. Hajer GR, van Haeften TW, Visseren FL. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 29:2959-2971, 2008.
10. Hall JE, da Silva AA, do Carmo JM, Dubinion J, Hamza S, Munusamy S, Smith G, Stec DE. Obesity-induced hypertension: role of sympathetic nervous system, leptin, and melanocortins. J Biol Chem 285:17271-17276, 2010.
11. Ishizuka T, Ernsberger P, Liu S, Bedol D, Lehman TM, Koletsky RJ, Friedman JE. Phenotypic consequences of a nonsense mutation in the leptin receptor gene (fak) in obese spontaneously hypertensive Koletsky rats (SHROB). J Nutr 128:2299-2306, 1998. (Pubitemid 29012975)
12. Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T. Spontaneous long-term hyperglycemic rat with diabetic complications. Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 41:1422-1428, 1992.
13. Klimcakova E, Kovacikova M, Stich V, Langin D. Adipokines and dietary interventions in human obesity. Obes Rev 11:446-456, 2010.
14. Knudson JD, Payne GA, Borbouse L, Tune JD. Leptin and mechanisms of endothelial dysfunction and cardiovascular disease. Curr Hypertens Rep 10:434-439, 2008.
15. Kohrt WM, Landt M, Birge SJ Jr. Serum leptin levels are reduced in response to exercise training, but not hormone replacement therapy, in older women. J Clin Endocrinol Metab 81:3980-3985, 1996. (Pubitemid 26380405)
16. Kraemer RR, Kraemer GR, Acevedo EO, Hebert EP, Temple E, Bates M, Etie A, Haltom R, Quinn S, Castracane VD. Effects of aerobic exercise on serum leptin levels in obese women. Eur J Appl Physiol Occup Physiol 80:154-158, 1999. (Pubitemid 29296549)
17. Laye MJ, Rector RS, Warner SO, Naples SP, Perretta AL, Uptergrove GM, Laughlin MH, Thyfault JP, Booth FW, Ibdah JA. Changes in visceral adipose tissue mitochondrial content with type 2 diabetes and daily voluntary wheel running in OLETF rats. J Physiol 587:3729-3739, 2009.
18. Laye MJ, Thyfault JP, Stump CS, Booth FW. Inactivity induces increases in abdominal fat. J Appl Physiol 102:1341-1347, 2007. (Pubitemid 46571026)
19. Lira FS, Rosa JC, Yamashita AS, Koyama CH, Batista ML Jr, Seelaender M. Endurance training induces depot-specific changes in IL-10/TNF-Alpha ratio in rat adipose tissue. Cytokine 45:80-85, 2009.
20. Lira FS, Yamashita AS, Rosa JC, Koyama CH, Caperuto EC, Batista ML Jr, Seelaender MC. Exercise training decreases adipose tissue inflammation in cachectic rats. Horm Metab Res 44:91-98, 2012.
21. Lowndes J, Zoeller RF, Caplan JD, Kyriazis GA, Moyna NM, Seip RL, Thompson PD, Angelopoulos TJ. Leptin responses to long-term cardiorespiratory exercise training without concomitant weight loss: a prospective study. J Sports Med Phys Fitness 48:391-397, 2008.
22. Malin SK, Gerber R, Chipkin SR, Braun B. Independent and combined effects of exercise training and metformin on insulin sensitivity in individuals with prediabetes. Diabetes Care 35:131-136, 2012.
23. Malin SK, Nightingale J, Choi SE, Chipkin SR, Braun B. Metformin modifies the exercise training effects on risk factors for cardiovascular disease in impaired glucose tolerant adults. Obesity (Silver Spring). First published May 25, 2012; doi:10.1038/oby.2012.133.
24. Malin SK, Stephens BR, Sharoff CG, Hagobian TA, Chipkin SR, Braun B. Metformin's effect on exercise and postexercise substrate oxidation. Int J Sport Nutr Exerc Metab 20:63-71, 2010.
25. Matsumoto T, Noguchi E, Ishida K, Kobayashi T, Yamada N, Kamata K. Metformin normalizes endothelial function by suppressing vasoconstrictor prostanoids in mesenteric arteries from OLETF rats, a model of type 2 diabetes. Am J Physiol Heart Circ Physiol 295:H1165-H1176, 2008.
26. Mick GJ, Wang X, Ling Fu C, McCormick KL. Inhibition of leptin secretion by insulin and metformin in cultured rat adipose tissue. Biochim Biophys Acta 1502:426-432, 2000.
27. Miyazaki S, Izawa T, Ogasawara JE, Sakurai T, Nomura S, Kizaki T, Ohno H, Komabayashi T. Effect of exercise training on adipocyte-sizedependent expression of leptin and adiponectin. Life Sci 86:691-698, 2010.
28. Parola M, Marra F. Adipokines and redox signaling: impact on fatty liver disease. Antioxid Redox Signal 15:461-483, 2011.
29. Payne GA, Borbouse L, Bratz IN, Roell WC, Bohlen HG, Dick GM, Tune JD. Endogenous adipose-derived factors diminish coronary endothelial function via inhibition of nitric oxide synthase. Microcirculation 15:417-426, 2008. (Pubitemid 351927730)
30. Pedersen BK. The diseasome of physical inactivity-And the role of myokines in muscle-fat cross talk. J Physiol 587:5559-5568, 2009.
31. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8:457-465, 2012.
32. Perusse L, Collier G, Gagnon J, Leon AS, Rao DC, Skinner JS, Wilmore JH, Nadeau A, Zimmet PZ, Bouchard C. Acute and chronic effects of exercise on leptin levels in humans. J Appl Physiol 83:5-10, 1997. (Pubitemid 27304723)
33. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol 98:1154-1162, 2005. (Pubitemid 40396484)
34. Polak J, Klimcakova E, Moro C, Viguerie N, Berlan M, Hejnova J, Richterova B, Kraus I, Langin D, Stich V. Effect of aerobic training on plasma levels and subcutaneous abdominal adipose tissue gene expression of adiponectin, leptin, interleukin 6, and tumor necrosis factor alpha in obese women. Metabolism 55:1375-1381, 2006. (Pubitemid 44353556)
35. Rector RS, Thyfault JP, Uptergrove GM, Morris EM, Naples SP, Borengasser SJ, Mikus CR, Laye MJ, Laughlin MH, Booth FW, Ibdah JA. Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of nonalcoholic fatty liver disease in an obese rodent model. J Hepatol 52:727-736, 2010.
36. Rector RS, Uptergrove GM, Borengasser SJ, Mikus CR, Morris EM, Naples SP, Laye MJ, Laughlin MH, Booth FW, Ibdah JA, Thyfault JP. Changes in skeletal muscle mitochondria in response to the development of type 2 diabetes or prevention by daily wheel running in hyperphagic OLETF rats. Am J Physiol Endocrinol Metab 298:E1179-E1187, 2010.
37. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116:1793-1801, 2006. (Pubitemid 44033299)
38. Smith AC, Mullen KL, Junkin KA, Nickerson J, Chabowski A, Bonen A, Dyck DJ. Metformin and exercise reduce muscle FAT/CD36 and lipid accumulation and blunt the progression of high-fat diet-induced hyperglycemia. Am J Physiol Endocrinol Metab 293:E172-E181, 2007. (Pubitemid 47105931)
39. Smith JK, Dykes R, Douglas JE, Krishnaswamy G, Berk S. Long-term exercise and atherogenic activity of blood mononuclear cells in persons at risk of developing ischemic heart disease. JAMA 281:1722-1727, 1999. (Pubitemid 29226483)
40. Sweeney G, Keen J, Somwar R, Konrad D, Garg R, Klip A. High leptin levels acutely inhibit insulin-stimulated glucose uptake without affecting glucose transporter 4 translocation in l6 rat skeletal muscle cells. Endocrinology 142:4806-4812, 2001. (Pubitemid 33022356)
41. Tan BK, Heutling D, Chen J, Farhatullah S, Adya R, Keay SD, Kennedy CR, Lehnert H, Randeva HS. Metformin decreases the adipokine vaspin in overweight women with polycystic ovary syndrome concomitant with improvement in insulin sensitivity and a decrease in insulin resistance. Diabetes 57:1501-1507, 2008.
42. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86:515-581, 2006.
43. Thong FS, Hudson R, Ross R, Janssen I, Graham TE. Plasma leptin in moderately obese men: independent effects of weight loss and aerobic exercise. Am J Physiol Endocrinol Metab 279:E307-E313, 2000.
44. Thyfault JP, Rector RS. Exercise: not just a medicine for muscle? J Physiol 588:2687-2688, 2010.
45. van Hall G, Steensberg A, Sacchetti M, Fischer C, Keller C, Schjerling P, Hiscock N, Moller K, Saltin B, Febbraio MA, Pedersen BK. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J Clin Endocrinol Metab 88:3005-3010, 2003. (Pubitemid 36877463)
46. Vieira VJ, Valentine RJ, Wilund KR, Antao N, Baynard T, Woods JA. Effects of exercise and low-fat diet on adipose tissue inflammation and metabolic complications in obese mice. Am J Physiol Endocrinol Metab 296:E1164-E1171, 2009.
47. Vieira VJ, Valentine RJ, Wilund KR, Woods JA. Effects of diet and exercise on metabolic disturbances in high-fat diet-fed mice. Cytokine 46:339-345, 2009.
48. Wang JL, Chinookoswong N, Scully S, Qi M, Shi ZQ. Differential effects of leptin in regulation of tissue glucose utilization in vivo. Endocrinology 140:2117-2124, 1999. (Pubitemid 30636450)
49. Zachwieja JJ, Hendry SL, Smith SR, Harris RB. Voluntary wheel running decreases adipose tissue mass and expression of leptin mRNA in Osborne-Mendel rats. Diabetes 46:1159-1166, 1997. (Pubitemid 27271077)