Intrinsic aerobic capacity impacts susceptibility to acute high-fat diet-induced hepatic steatosis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 4, 2014, Pages

  Morris, E Matthew ^a   Jackman, Matthew R ^f   Johnson, Ginger C ^f   Liu, Tzu Wen ^b   Lopez, Jordan L ^f   Kearney, Monica L ^b   Fletcher, Justin A ^b   Meers, Grace M E ^a   Koch, Lauren G ^d   Britton, Stephen L ^d   Rector, R Scott ^a,b,c   Ibdah, Jamal A ^a,b,c   MacLean, Paul S ^e,f   Thyfault, John P ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e Anschutz Health and Wellness Center ^*  (United States)

^f UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Energy expenditure; Energy intake; Fatty liver; Fitness; Obesity

Indexed keywords

AEROBIC CAPACITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY FAT; BODY WEIGHT; CALORIC INTAKE; CALORIMETRY; CELL ISOLATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENERGY BALANCE; ENERGY METABOLISM; EX VIVO STUDY; FAT INTAKE; FATTY ACID OXIDATION; FATTY LIVER; FOOD; ISOTOPE LABELING; LIPID DIET; LIPID LIVER LEVEL; LIPID STORAGE; LIVER HOMOGENATE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT; RESTING ENERGY EXPENDITURE; WEIGHT GAIN;

ENERGY EXPENDITURE; ENERGY INTAKE; FATTY LIVER; FITNESS; OBESITY;

ANIMALS; CELLS, CULTURED; DIET, HIGH-FAT; DIETARY FATS; DISEASE SUSCEPTIBILITY; ENERGY METABOLISM; EXERCISE TOLERANCE; FATTY LIVER; MALE; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL FITNESS; RATS; RATS, INBRED STRAINS;

EID: 84908051532     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00093.2014     Document Type: Article

References (43)

1. Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 10: 330-344, 2013.
2. Church TS, Kuk JL, Ross R, Priest EL, Biltoft E, Blair SN. Association of cardiorespiratory fitness, body mass index, and waist circumference to nonalcoholic fatty liver disease. Gastroenterology 130: 2023-2030, 2006.
3. Croci I, Byrne NM, Choquette S, Hills AP, Chachay VS, Clouston AD, O'Moore-Sullivan TM, Macdonald GA, Prins JB, Hickman IJ. Whole-body substrate metabolism is associated with disease severity in patients with non-alcoholic fatty liver disease. Gut 2012.
4. Dole VP. A relation between non-esterified fatty acids in plasma and the metabolism of glucose. J Clin Invest 35: 150-154, 1956.
5. Eaton S. Control of mitochondrial beta-oxidation flux. Prog Lipid Res 41: 197-239, 2002.
6. Friedman MI. Fuel partitioning and food intake. Am J Clin Nutr 67: 513S-518S, 1998.
7. Friedman MI, Harris RB, Ji H, Ramirez I, Tordoff MG. Fatty acid oxidation affects food intake by altering hepatic energy status. Am J Physiol Regul Integr Comp Physiol 276: R1046-R1053, 1999.
8. Galgani J, Ravussin E. Energy metabolism, fuel selection and body weight regulation. Int J Obes 32, Suppl 7: S109-S119, 2008.
9. Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 295: E1009-E1017, 2008.
10. Gavini CK, Mukherjee S, Shukla C, Britton SL, Koch LG, Shi H, Novak CM. Leanness and heightened nonresting energy expenditure: role of skeletal muscle activity thermogenesis. Am J Physiol Endocrinol Metab 306: E635-E647, 2014.
11. Gugen-Guillouzo C. Isolation and culture of animal and human hepatocytes. In: Culture of Epithelial Cells, edited by Freshney RI and Freshney MG. Wilmington, DE: Wiley-Liss, 2002, p. 337-379.
12. Haufe S, Engeli S, Budziarek P, Utz W, Schulz-Menger J, Hermsdorf M, Wiesner S, Otto C, Haas V, de Greiff A, Luft FC, Boschmann M, Jordan J. Cardiorespiratory fitness and insulin sensitivity in overweight or obese subjects may be linked through intrahepatic lipid content. Diabetes 59: 1640-1647, 2010.
13. Jackman MR, Kramer RE, MacLean PS, Bessesen DH. Trafficking of dietary fat in obesity-prone and obesity-resistant rats. Am J Physiol Endocrinol Metab 291: E1083-E1091, 2006.
14. Jackman MR, MacLean PS, Bessesen DH. Energy expenditure in obesity-prone and obesity-resistant rats before and after the introduction of a high-fat diet. Am J Physiol Regul Integr Comp Physiol 299: R1097-R1105, 2010.
15. Jackman MR, Steig A, Higgins JA, Johnson GC, Fleming-Elder BK, Bessesen DH, MacLean PS. Weight regain after sustained weight reduction is accompanied by suppressed oxidation of dietary fat and adipocyte hyperplasia. Am J Physiol Regul Integr Comp Physiol 294: R1117-R1129, 2008.
16. Kantartzis K, Thamer C, Peter A, Machann J, Schick F, Schraml C, Konigsrainer A, Konigsrainer I, Krober S, Niess A, Fritsche A, Haring HU, Stefan N. High cardiorespiratory fitness is an independent predictor of the reduction in liver fat during a lifestyle intervention in non-alcoholic fatty liver disease. Gut 58: 1281-1288, 2009.
17. Koch LG, Britton SL. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 5: 45-52, 2001.
18. Kodama S, Saito K, Tanaka S, Maki M, Yachi Y, Asumi M, Sugawara A, Totsuka K, Shimano H, Ohashi Y, Yamada N, Sone H. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA 301: 2024-2035, 2009.
19. Kokkinos P, Myers J, Faselis C, Panagiotakos DB, Doumas M, Pittaras A, Manolis A, Kokkinos JP, Karasik P, Greenberg M, Papademetriou V, Fletcher R. Exercise capacity and mortality in older men: a 20-year follow-up study. Circulation 122: 790-797, 2010.
20. Kraegen EW, Clark PW, Jenkins AB, Daley EA, Chisholm DJ, Storlien LH. Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 40: 1397-1403, 1991.
21. la Fleur SE, Ji H, Manalo SL, Friedman MI, Dallman MF. The hepatic vagus mediates fat-induced inhibition of diabetic hyperphagia. Diabetes 52: 2321-2330, 2003.
22. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Donahoo WT, Melanson EL, Hill JO. Enhanced metabolic efficiency contributes to weight regain after weight loss in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 287: R1306-R1315, 2004.
23. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Peters JC, Hill JO. Metabolic adjustments with the development, treatment, and recurrence of obesity in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 287: R288-R297, 2004.
24. Morris EM, Jackman MR, Meers GM, Johnson GC, Lopez JL, MacLean PS, Thyfault JP. Reduced hepatic mitochondrial respiration following acute high-fat diet is prevented by PGC-1α overexpression. Am J Physiol Gastrointest Liver Physiol 305: G868-G880, 2013.
25. Morris EM, Meers GM, Booth FW, Fritsche KL, Hardin CD, Thyfault JP, Ibdah JA. PGC-1α overexpression results in increased hepatic fatty acid oxidation with reduced triacylglycerol accumulation and secretion. Am J Physiol Gastrointest Liver Physiol 303: G979-G992, 2012.
26. Muoio DM. Intramuscular triacylglycerol and insulin resistance: guilty as charged or wrongly accused? Biochim Biophys Acta 1801: 281-288, 2010.
27. Noland RC, Thyfault JP, Henes ST, Whitfield BR, Woodlief TL, Evans JR, Lust JA, Britton SL, Koch LG, Dudek RW, Dohm GL, Cortright RN, Lust RM. Artificial selection for high-capacity endurance running is protective against high-fat diet-induced insulin resistance. Am J Physiol Endocrinol Metab 293: E31-E41, 2007.
28. Ramsey JJ, Harper ME, Weindruch R. Restriction of energy intake, energy expenditure, and aging. Free Radic Biol Med 29: 946-968, 2000.
29. Rector RS, Thyfault JP. Does physical inactivity cause nonalcoholic fatty liver disease? J Appl Physiol 111: 1828-1835, 2011.
30. Rector RS, Thyfault JP, Morris RT, Laye MJ, Borengasser SJ, Booth FW, Ibdah JA. Daily exercise increases hepatic fatty acid oxidation and prevents steatosis in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Am J Physiol Gastrointest Liver Physiol 294: G619-G626, 2008.
31. 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 non-alcoholic fatty liver disease in an obese rodent model. J Hepatol 52: 727-736, 2010.
32. Reilly SM, Chiang SH, Decker SJ, Chang L, Uhm M, Larsen MJ, Rubin JR, Mowers J, White NM, Hochberg I, Downes M, Yu RT, Liddle C, Evans RM, Oh D, Li P, Olefsky JM, Saltiel AR. An inhibitor of the protein kinases TBK1 and IKK-varepsilon improves obesity-related metabolic dysfunctions in mice. Nat Med 19: 313-321, 2013.
33. Rodriguez B, Torres DM, Harrison SA. Physical activity: an essential component of lifestyle modification in NAFLD. Nat Rev Gastroenterol Hepatol 9: 726-731, 2012.
34. Sawada SS, Lee IM, Naito H, Noguchi J, Tsukamoto K, Muto T, Higaki Y, Tanaka H, Blair SN. Long-term trends in cardiorespiratory fitness and the incidence of type 2 diabetes. Diabetes Care 33: 1353-1357, 2010.
35. Shi SY, Martin RG, Duncan RE, Choi D, Lu SY, Schroer SA, Cai EP, Luk CT, Hopperton KE, Domenichiello AF, Tang C, Naples M, Dekker MJ, Giacca A, Adeli K, Wagner KU, Bazinet RP, Woo M. Hepatocyte-specific deletion of Janus kinase 2 (JAK2) protects against diet-induced steatohepatitis and glucose intolerance. J Biol Chem 287: 10277-10288, 2012.
36. Sobrecases H, Le KA, Bortolotti M, Schneiter P, Ith M, Kreis R, Boesch C, Tappy L. Effects of short-term overfeeding with fructose, fat and fructose plus fat on plasma and hepatic lipids in healthy men. Diabetes Metab 36: 244-246, 2010.
37. Soderberg C, Stal P, Askling J, Glaumann H, Lindberg G, Marmur J, Hultcrantz R. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology 51: 595-602, 2010.
38. Steig AJ, Jackman MR, Giles ED, Higgins JA, Johnson GC, Mahan C, Melanson EL, Wyatt HR, Eckel RH, Hill JO, MacLean PS. Exercise reduces appetite and traffics excess nutrients away from energetically efficient pathways of lipid deposition during the early stages of weight regain. Am J Physiol Regul Integr Comp Physiol 301: R656-R667, 2011.
39. Thyfault JP, Rector RS, Uptergrove GM, Borengasser SJ, Morris EM, Wei Y, Laye MJ, Burant CF, Qi NR, Ridenhour SE, Koch LG, Britton SL, Ibdah JA. Rats selectively bred for low aerobic capacity have reduced hepatic mitochondrial oxidative capacity and susceptibility to hepatic steatosis and injury. J Physiol 587: 1805-1816, 2009.
40. Vial G, Dubouchaud H, Couturier K, Cottet-Rousselle C, Taleux N, Athias A, Galinier A, Casteilla L, Leverve XM. Effects of a high-fat diet on energy metabolism and ROS production in rat liver. J Hepatol 54: 348-356, 2011.
41. Watt MJ, Hoy AJ. Lipid metabolism in skeletal muscle: generation of adaptive and maladaptive intracellular signals for cellular function. Am J Physiol Endocrinol Metab 302: E1315-E1328, 2012.
42. Wisloff U, Najjar SM, Ellingsen O, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei K, Lee SJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307: 418-420, 2005.
43. Zhang X, Xu A, Chung SK, Cresser JH, Sweeney G, Wong RL, Lin A, Lam KS. Selective inactivation of c-Jun NH2-terminal kinase in adipose tissue protects against diet-induced obesity and improves insulin sensitivity in both liver and skeletal muscle in mice. Diabetes 60: 486-495, 2011.