Treating NAFLD in OLETF rats with vigorous-intensity interval exercise training

Medicine and Science in Sports and Exercise

Volumn 47, Issue 3, 2014, Pages 556-567

  Linden, Melissa A ^a,b   Fletcher, Justin A ^a,b   Morris, E Matthew ^a,b   Meers, Grace M ^a,b   Laughlin, M Harold ^c   Booth, Frank W ^b,c,d   Sowers, James R ^a,b   Ibdah, Jamal A ^a,b   Thyfault, John P ^a,b   Rector, R Scott ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

de novo lipogenesis; macrophage polarization; mitochondria; Nonalcoholic fatty liver disease; physical exercise

Indexed keywords

COLLAGEN TYPE 1; GLUCOSE BLOOD LEVEL; LIPID; MESSENGER RNA; TRIACYLGLYCEROL;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL EXPERIMENT; BLOOD; DISEASE MODEL; GLUCOSE BLOOD LEVEL; GLYCOLYSIS; HEART; KINESIOTHERAPY; LIPOGENESIS; LIVER; LIVER MITOCHONDRION; MALE; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGAN SIZE; OTSUKA LONG EVANS TOKUSHIMA FATTY RAT; PROCEDURES; WEIGHT REDUCTION;

ANIMALS; BLOOD GLUCOSE; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; EXERCISE THERAPY; GLYCOLYSIS; HEART; LIPIDS; LIPOGENESIS; LIVER; MALE; MITOCHONDRIA, LIVER; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGAN SIZE; PHYSICAL CONDITIONING, ANIMAL; RATS, INBRED OLETF; RNA, MESSENGER; TRIGLYCERIDES; WEIGHT LOSS;

EID: 84995322591     PISSN: 01959131     EISSN: 15300315     Source Type: Journal    
DOI: 10.1249/MSS.0000000000000430     Document Type: Article

References (49)

1. Aron-Wisnewsky J, Tordjman J, Poitou C, et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab. 2009; 94(11):4619-23.
2. Bass A, Brdiczka D, Eyer P, Hofer S, Pette D. Metabolic differentiation of distinct muscle types at the level of enzymatic organization. Eur J Biochem. 1969; 10(2):198-206.
3. Bellentani S, Saccoccio G, Masutti F, et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med. 2000; 132(2):112-7.
4. Borengasser SJ, Rector RS, Uptergrove GM, et al. Exercise and omega-3 polyunsaturated fatty acid supplementation for the treatment of hepatic steatosis in hyperphagic OLETF rats. J Nutr Metab. 2012; 2012:268680.
5. Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004; 40(6):1387-95.
6. Burgomaster KA, Heigenhauser GJ, Gibala MJ. Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J Appl Physiol (1985). 2006; 100(6):2041-7.
7. Burgomaster KA, Howarth KR, Phillips SM, et al. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol. 2008; 586(1): 151-60.
8. Caldwell S, Lazo M. Is exercise an effective treatment for NASH. Knowns and unknowns. Ann Hepatol. 2009; 8(1 Suppl):S60-6.
9. Chilibeck PD, Bell GJ, Farrar RP, Martin TP. Higher mitochondrial fatty acid oxidation following intermittent versus continuous endurance exercise training. Can J Physiol Pharmacol. 1998; 76(9): 891-4.
10. Claria J, Gonzalez-Periz A, Lopez-Vicario C, Rius B, Titos E. New insights into the role of macrophages in adipose tissue inflammation and fatty liver disease: modulation by endogenous omega-3 fatty acid-derived lipid mediators. Front Immunol. 2011; 2:49.
11. Cortez MY, Torgan CE, Brozinick JT Jr, Ivy JL. Insulin resistance of obese zucker rats exercise trained at two different intensities. Am J Physiol. 1991; 261(5 Pt 1):E613-9.
12. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest. 2005; 115(5):1343-51.
13. Dudley GA, Abraham WM, Terjung RL. Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. J Appl Physiol Respir Environ Exerc Physiol. 1982; 53(4):844-50.
14. Genc H, Dogru T, Kara M, et al. Association of plasma visfatin with hepatic and systemic inflammation in nonalcoholic fatty liver disease. Ann Hepatol. 2013; 12(4):548-55.
15. Haram PM, Kemi OJ, Lee SJ, et al. Aerobic interval training vs continuous moderate exercise in the metabolic syndrome of rats artificially selected for low aerobic capacity. Cardiovasc Res. 2009; 81(4):723-32.
16. Haskell WL, Lee IM, Pate RR, et al. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc. 2007; 39(8):1423-34.
17. Johnson NA, Sachinwalla T, Walton DW, et al. Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss. Hepatology. 2009; 50(4):1105-12.
18. Kawanishi N, Yano H, Mizokami T, Takahashi M, Oyanagi E, Suzuki K. Exercise training attenuates hepatic inflammation, fibrosis and macrophage infiltration during diet induced-obesity in mice. Brain Behav Immun. 2012; 26(6):931-41.
19. Kistler KD, Brunt EM, Clark JM, Diehl AM, Sallis JF, Schwimmer JB. Physical activity recommendations, exercise intensity, and histological severity of nonalcoholic fatty liver disease. Am J Gastroenterol. 2011; 106(3):460-8; quiz
20. Laughlin MH, Korthuis RJ, Sexton WL, Armstrong RB. Regional muscle blood flow capacity and exercise hyperemia in highintensity trained rats. J Appl Physiol (1985). 1988; 64(6):2420-7.
21. Laughlin MH, Woodman CR, Schrage WG, Gute D, Price EM. Interval sprint training enhances endothelial function and enos content in some arteries that perfuse white gastrocnemius muscle. J Appl Physiol (1985). 2004; 96(1):233-44.
22. Li Z, Diehl AM. Innate immunity in the liver. Curr Opin Gastroenterol. 2003; 19(6):565-71.
23. Linden MA, Fletcher JA, Morris EM, et al. Combining metformin and aerobic exercise training in the treatment of type 2 diabetes and NAFLD in OLETF rats. Am J Physiol Endocrinol Metab. 2014; 306(3):E300-10.
24. Linden MA, Meers GM, Ruebel ML, et al. Hepatic steatosis development with four weeks of physical inactivity in previously active, hyperphagic OLETF rats. Am J Physiol Regul Integr Comp Physiol. 2013; 304(9):R763-71.
25. Lucero D, Zago V, Lopez GI, et al. Pro-inflammatory and atherogenic circulating factors in non-Alcoholic fatty liver disease associated to metabolic syndrome. Clin Chim Acta. 2011; 412(1-2):143-7.
26. MacDougall JD, Hicks AL, MacDonald JR, McKelvie RS, Green HJ, Smith KM. Muscle performance and enzymatic adaptations to sprint interval training. J Appl Physiol (1985). 1998; 84(6):2138-42.
27. Matsuzaka T, Atsumi A, Matsumori R, et al. Elovl6 promotes nonalcoholic steatohepatitis. Hepatology. 2012; 56(6):2199-208.
28. Miquilena-Colina ME, Lima-Cabello E, Sanchez-Campos S, et al. Hepatic fatty acid translocase Cd36 upregulation is associated with insulin resistance, hyperinsulinaemia and increased steatosis in nNon-Alcoholic steatohepatitis and chronic hepatitis C. Gut. 2011; 60(10):1394-402.
29. Miura K, Kodama Y, Inokuchi S, et al. Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1beta in mice. Gastroenterology. 2010; 139(1):323-34.e7.
30. Morris EM, Meers GM, Booth FW, et al. Pgc-1alpha overexpression results in increased hepatic fatty acid oxidation with reduced triacylglycerol accumulation and secretion. Am J Physiol Gastrointest Liver Physiol. 2012; 303(8):G979-92.
31. Patch LD,Brooks GA. Effects of training on VO2 max and VO2 during two running intensities in rats. Pflugers Arch. 1980; 386(3):215-9.
32. Perseghin G, Lattuada G, De Cobelli F, et al. Habitual physical activity is associated with intrahepatic fat content in humans. Diabetes Care. 2007; 30(3):683-8.
33. Racil G, Ben Ounis O, Hammouda O, et al. Effects of high vs moderate exercise intensity during interval training on lipids and adiponectin levels in obese young females. Eur J Appl Physiol. 2013; 113(10):2531-40.
34. Rector RS, Thyfault JP. Does physical inactivity cause nonalcoholic fatty liver disease. J Appl Physiol (1985). 2011; 111(6):1828-35.
35. Rector RS, Thyfault JP, Laye MJ, et al. Cessation of daily exercise dramatically alters precursors of hepatic steatosis in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. J Physiol. 2008; 586(Pt 17): 4241-9.
36. Rector RS, Thyfault JP, Morris RT, et al. Daily exercise increases hepatic fatty acid oxidation and prevents steatosis in Otsuka Long-Evans Tokushima Fatty rats. Am J Physiol Gastrointest Liver Physiol. 2008; 294(3):G619-26.
37. Rector RS, Thyfault JP, Uptergrove GM, et al. Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-Alcoholic fatty liver disease in an obese rodent model. J Hepatol. 2010; 52(5):727-36.
38. Rector RS, Thyfault JP, Wei Y, Ibdah JA. Non-Alcoholic fatty liver disease and the metabolic syndrome: an update. World J Gastroenterol. 2008; 14(2):185-92.
39. Rector RS, Uptergrove GM, Borengasser SJ, et al. 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. 2010; 298(6):E1179-87.
40. Rector RS, Uptergrove GM, Morris EM, et al. Daily exercise vs caloric restriction for prevention of nonalcoholic fatty liver disease in the OELTF rat model. Am J Physiol Gastrointest Liver Physiol. 2011; 300(5):G874-83.
41. Richards JC, Johnson TK, Kuzma JN, et al. Short-term sprint interval training increases insulin sensitivity in healthy adults but does not affect the thermogenic response to beta-Adrenergic stimulation. J Physiol. 2010; 588(Pt 15):2961-72.
42. Salter AM, Wiggins D, Sessions VA, Gibbons GF. The intracellular triacylglycerol/fatty acid cycle: a comparison of its activity in hepatocytes which secrete exclusively apolipoprotein (Apo) B100 very-low-density lipoprotein (VLDL) and in those which secrete predominantly Apob48 VLDL. Biochem J. 1998; 332(Pt 3):667-72.
43. Shepherd RE, Gollnick PD. Oxygen uptake of rats at different work intensities. Pflugers Arch. 1976; 362(3):219-22.
44. Srere PA. Citrate synthase. Meth Enzymol. 1969; 13:3-5.
45. Sullivan S, Kirk EP, Mittendorfer B, Patterson BW, Klein S. Randomized trial of exercise effect on intrahepatic triglyceride content and lipid kinetics in nonalcoholic fatty liver disease. Hepatology. 2012; 55(6):1738-45.
46. Tai MM. A mathematical model for the determination of total area under glucose tolerance and other metabolic curves. Diabetes Care. 1994; 17(2):152-4.
47. Tjonna AE, Lee SJ, Rognmo O, et al. Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: a pilot study. Circulation. 2008; 118(4): 346-54.
48. van der Heijden GJ, Wang ZJ, Chu ZD, et al. A 12-week aerobic exercise program reduces hepatic fat accumulation and insulin resistance in obese, Hispanic adolescents. Obesity (Silver Spring). 2010; 18(2):384-90.
49. Wan J, Benkdane M, Teixeira-Clerc F, et al. M2 Kupffer cells promote M1 Kupffer cell apoptosis: a protective mechanism against alcoholic and nonalcoholic fatty liver disease. Hepatology. 2014; 59(1):130-42