Cessation of daily wheel running differentially alters fat oxidation capacity in liver, muscle, and adipose tissue

• Published in: Journal of applied physiology (1985) Vol. 106; no. 1; pp. 161 - 168
• Main Authors: Laye, Matthew J, Rector, R. Scott, Borengasser, Sarah J, Naples, Scott P, Uptergrove, Grace M, Ibdah, Jamal A, Booth, Frank W, Thyfault, John P
• Format: Journal Article
• Language: English
• Published: Bethesda, MD Am Physiological Soc 01.01.2009; American Physiological Society
• Subjects: Adaptation, Physiological; Adipose tissue; Adipose Tissue - enzymology; Adipose Tissue - metabolism; Animal models; Animals; Biological and medical sciences; Body Composition; Carnitine O-Palmitoyltransferase - metabolism; Eating; Energy Metabolism; Enzymatic activity; Fatty acids; Fundamental and applied biological sciences. Psychology; Liver; Liver - enzymology; Liver - metabolism; Male; Metabolic disorders; Metabolites; Mitochondria, Liver - enzymology; Mitochondria, Liver - metabolism; Mitochondria, Muscle - enzymology; Mitochondria, Muscle - metabolism; Muscle, Skeletal - enzymology; Muscle, Skeletal - metabolism; Muscular system; Oxidation; Oxidation-Reduction; Palmitic Acid - metabolism; Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha; Physical Exertion; Physiology; Rats; Rats, Inbred BN; Rats, Inbred F344; RNA, Messenger - metabolism; RNA-Binding Proteins - genetics; RNA-Binding Proteins - metabolism; Rodents; Time Factors; Tissues; Transcription Factors - genetics; Transcription Factors - metabolism; Vertebrata; Mitochondria; Mammalia; Adipose tissue; Digestive system; Running-wheel; Liver; Fat; Oxidation; Striated muscle; Metabolism
• ISSN: 8750-7587; 1522-1601
• DOI: 10.1152/japplphysiol.91186.2008

1 Research Service, Harry S. Truman Veterans Affairs Medical Center, and Departments of 2 Biomedical Sciences, 3 Medical Pharmacology and Physiology, 4 Nutritional Sciences, and 5 Internal Medicine-Division of Gastroenterology and Hepatology, University of Missouri, Columbia, Missouri Submitted 4 September 2008 ; accepted in final form 28 October 2008 Physical inactivity is associated with the increased risk of developing chronic metabolic diseases. To understand early alterations caused by physical inactivity, we utilize an animal model in which rats are transitioned from daily voluntary wheel running to a sedentary condition. In the hours and days following this transition, adipose tissue mass rapidly increases, due in part to increased lipogenesis. However, whether a concurrent decrease in fatty acid oxidative capacity (FAO) in skeletal muscle, liver, and adipose tissue occurs during this period is unknown. Following 6 wk of access to voluntary running wheels (average distance of 6 km a night), rats were rapidly transitioned to a sedentary state by locking the wheels for 5 h (WL5) or 173 h (WL173). Complete ([ 14 C]palmitate oxidation to 14 CO 2 ) and incomplete ([ 14 C]palmitate oxidation to 14 C-labeled acid soluble metabolites) was determined in isolated mitochondrial and whole homogenate preparations from skeletal muscle and liver and in isolated adipocytes. Strikingly, the elevated complete FAO in the red gastrocnemius at WL5 fell to that of rats that never ran (SED) by WL173. In contrast, hepatic FAO was elevated at WL173 above both WL5 and SED groups, while in isolated adipocytes, FAO remained higher in both running groups (WL5 and WL173) compared with the SED group. The alterations in muscle and liver fat oxidation were associated with changes in carnitine palmitoyl transferase-1 activity and inhibition, but not significant changes in other mitochondrial enzyme activities. In addition, peroxisome proliferator-activated receptor coactivator-1 mRNA levels that were higher in both skeletal muscle and liver at WL5 fell to SED levels at WL173. This study is the first to demonstrate that the transition from high to low daily physical activity causes rapid, tissue-specific changes in FAO. mitochondria; metabolism Address for reprint requests and other correspondence: J. P. Thyfault, Research Service, Harry S. Truman Memorial VA Hospital, Depts of Nutritional Sciences and Internal Medicine-Gastroenterology, Univ. of Missouri, Columbia, MO 65211 (e-mail: thyfaultj{at}missouri.edu )