Abstract
Endurance training results in adaptations that enhance regulation of energy storage and expenditure at rest and during exercise. While processes involved in skeletal muscle oxidative remodelling are well described, it is unknown whether oxidative capacity of human subcutaneous white adipose tissue (WAT) is modified by endurance training. Since human WAT retains rudimentary characteristics required for upregulation of oxidative function, we hypothesised that 10 days of intense endurance training would promote changes in WAT that favour an increase in oxidative capacity. Eleven untrained males (age 22 ± 1 years, body mass 81 ± 5 kg, peak oxygen uptake (VO2peak) 3.7 ± 0.2 l/min) undertook a 10-day endurance training protocol. Subcutaneous adipose tissue biopsies were taken from the abdomen prior to and 1 day after completion of training and analysed for fatty acid oxidative capacity, citrate synthase activity, and mitochondrial content via electron microscopy and gene expression analyses. There was a reduction in whole-body rates of carbohydrate oxidation, and concomitant increases in fat oxidation rate measured during 20-min of submaximal cycling (70% of pre-training VO2peak) and an increase in basal GLUT4 protein in skeletal muscle. Despite these training-induced adaptations, there were no changes in WAT of ex-vivo fat oxidation rate, maximal citrate synthase activity, mitochondrial volume or in selected genes involved in adipose tissue oxidative capacity. We conclude that 10 days training in previously untrained subjects results in adaptations in skeletal muscle but does not increase the oxidative capacity of WAT.
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References
Almind K, Manieri M, Sivitz WI, Cinti S, Kahn CR (2007) Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice. Proc Natl Acad Sci USA 104:2366–2371
Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, Hawley JA (2003) Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 88:5444–5451
Bulow J, Madsen J (1978) Human adipose tissue blood flow during prolonged exercise II. Pflugers Arch 376:41–45
Cinti S (2009) Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol Endocrinol Metab 297:E977–E986
Collins S, Surwit RS (2001) The beta-adrenergic receptors and the control of adipose tissue metabolism and thermogenesis. Recent Prog Horm Res 56:309–328
Crowe S, Turpin SM, Ke F, Kemp BE, Watt MJ (2008) Metabolic remodeling in adipocytes promotes ciliary neurotrophic factor-mediated fat loss in obesity. Endocrinology 149:2546–2556
Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509–1517
De Matteis R, Arch JR, Petroni ML, Ferrari D, Cinti S, Stock MJ (2002) Immunohistochemical identification of the beta(3)-adrenoceptor in intact human adipocytes and ventricular myocardium: effect of obesity and treatment with ephedrine and caffeine. Int J Obes Relat Metab Disord 26:1442–1450
Feldmann HM, Golozoubova V, Cannon B, Nedergaard J (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203–209
Frayn KN (1998) Regulation of fatty acid delivery in vivo. Adv Exp Med Biol 441:171–179
Frayn KN, Langin D, Karpe F (2008) Fatty acid-induced mitochondrial uncoupling in adipocytes is not a promising target for treatment of insulin resistance unless adipocyte oxidative capacity is increased. Diabetologia 51:394–397
Gesta S, Tseng Y, Kahn R (2007) Developmental origin of fat: tracking obesity to its source. Cell 131:242–256
Gibala MJ, Little JP, van Essen M, Wilkin GP, Burgomaster KA, Safdar A, Raha S, Tarnopolsky MA (2006) Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J Physiol 575:901–911
Green HJ, Jones S, Ball-Burnett ME, Smith D, Livesey J, Farrance BW (1991) Early muscular and metabolic adaptations to prolonged exercise training in humans. J Appl Physiol 70:2032–2038
Green HJ, Jones S, Ball-Burnett M, Farrance B, Ranney D (1995) Adaptations in muscle metabolism to prolonged voluntary exercise and training. J Appl Physiol 78:138–145
Hallgren P, Korsback S, Sjostrom L (1986) Measurements of adipose tissue respiration in a closed chamber using an oxygen sensor: methodological considerations. J Lipid Res 27:996–1005
Hamosh M, Hamosh P, Bar-Maor JA, Cohen H (1963) Fatty-acid metabolism by human adipose tissues. J Clin Invest 42:1648–1652
Hawley JA, Noakes TD (1992) Peak power output predicts maximal oxygen uptake and performance time in trained cyclists. Eur J Appl Physiol Occup Physiol 65:79–83
Horowitz JF, Klein S (2000) Whole body and abdominal lipolytic sensitivity to epinephrine is suppressed in upper body obese women. Am J Physiol Endocrinol Metab 278:E1144–E1152
Hotamisligil G (2006) Inflammation and metabolic disorders. Nature 444:860–867
Hull D, Segall MM (1965) Sympathetic nervous control of brown adipose tissue and heat production in the new-born rabbit. J Physiol 181:458–467
Huttunen P, Hirvonen J, Kinnula V (1981) The occurrence of brown adipose tissue in outdoor workers. Eur J Appl Physiol Occup Physiol 46:339–345
Jeukendrup A, Saris W, Schrauwen P, Brouns F, Wagenmakers A (1995) Metabolic availability of medium chain triglycerides co-ingested with carbohydrates during prolonged exercise. J Appl Physiol 79:756–762
Krief S, Lonnqvist F, Raimbault S, Baude B, Van Spronsen A, Arner P, Strosberg AD, Ricquier D, Emorine LJ (1993) Tissue distribution of beta 3-adrenergic receptor mRNA in man. J Clin Invest 91:344–349
Larue-Achagiotis C, Goubern M, Laury MC, Louis-Sylvestre J (1994) Energy balance in an inbred strain of rats: comparison with the Wistar strain. Physiol Behav 55:483–487
Laye MJ, Rector RS, Warner SO, Naples SP, Perretta AL, Uptergrove GM, Laughlin MH, Thyfault JP, Booth FW, Ibdah JA (2009) Changes in visceral adipose tissue mitochondrial content with type 2 diabetes and daily voluntary wheel running in OLETF rats. J Physiol 587:3729–3739
Lefebvre AM, Laville M, Vega N, Riou JP, van Gaal L, Auwerx J, Vidal H (1998) Depot-specific differences in adipose tissue gene expression in lean and obese subjects. Diabetes 47:98–103
Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270:12953–12956
Maassen JA, Romijn JA, Heine RJ (2007) Fatty acid-induced mitochondrial uncoupling in adipocytes as a key protective factor against insulin resistance and beta cell dysfunction: a new concept in the pathogenesis of obesity-associated type 2 diabetes mellitus. Diabetologia 50:2036–2041
McConell GK, Lee-Young RS, Chen ZP, Stepto NK, Huynh NN, Stephens TJ, Canny BJ, Kemp BE (2005) Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen. J Physiol 568:665–676
Nedergaard J, Bengtsson T, Cannon B (2007) Active brown adipose tissue and adult humans. Am J Physiol Endocrinol Metab 293:444–452
Oberkofler H, Dallinger G, Liu YM, Hell E, Krempler F, Patsch W (1997) Uncoupling protein gene: quantification of expression levels in adipose tissues of obese and non-obese humans. J Lipid Res 38:2125–2133
Ostman J, Arner P, Engfeldt P, Kager L (1979) Regional differences in the control of lipolysis in human adipose tissue. Metabolism 28:1198–1205
Peronnet F, Massicotte D (1991) Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16:23–29
Peronnet F, Cleroux J, Perrault H, Cousineau D, De Champlain J, Nadeau R (1981) Plasma norepinephrine response to exercise before and after training in humans. J Appl Physiol 51:812–815
Petrovic N, Shabalina IG, Timmons JA, Cannon B, Nedergaard J (2008) Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPARgamma agonist. Am J Physiol Endocrinol Metab 295:E287–E296
Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GJ, Grant SM (1996) Progressive effect of endurance training on metabolic adaptations in working skeletal muscle. Am J Physiol 270:E265–E272
Puigserver P (2005) Tissue-specific regulation of metabolic pathways through the transcriptional coactivator PGC1-alpha. Int J Obes (Lond) 29:S5–S9
Ricquier D, Nechad M, Mory G (1982) Ultrastructural and biochemical characterization of human brown adipose tissue in pheochromocytoma. Clin Endocrinol Metab 54:803–807
Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531
Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M, Tavernier G, Langin D, Spiegelman BM (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab 6:38–54
Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe H, Erdjument-Bromage H, Tempst P, Rudnick M, Beier D, Spigelman B (2008) PRMD16 controls a brown fat/skeletal muscle switch. Nature 454:21
Smith DJ, Deuster PA, Ryan CJ, Doubt TJ (1990) Prolonged whole body immersion in cold water: hormonal and metabolic changes. Undersea Biomed Res 17:139–147
Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Ryden M, Frisen J, Arner P (2008) Dynamics of fat cell turnover in humans. Nature 453:783–787
Stallknecht B, Vinten J, Ploug T, Galbo H (1991) Increased activities of mitochondrial enzymes in white adipose tissue in trained rats. Am J Physiol 261:E410–E414
Sutherland LN, Bomhof MR, Capozzi LC, Basaraba SA, Wright DC (2009) Exercise and adrenaline increase PGC-1{alpha} mRNA expression in rat adipose tissue. J Physiol 587:1607–1617
Timmons J, Wennmalm K, Larsson O, Walden T, Lassman T, Petrovic N, Hamilton D, Gimeno R, Wahlestedt C, Baar K, Nedergaard J, Cannon B (2007) Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc Natl Acad Sci USA 104:4401–4406
Tiraby C, Tavernier G, Lefort C, Larrouy D, Bouillaud F, Ricquier D, Langin D (2003) Acquirement of brown fat cell features by human white adipocytes. J Biol Chem 278:33370–33376
Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN, Kahn CR (2008b) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454:1000–1004
Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116:2791–2798
van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508
Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525
Wilson-Fritch L, Burkart A, Bell G, Mendelson K, Leszyk J, Nicoloro S, Czech M, Corvera S (2003) Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol Cell Biol 23:1085–1094
Yang X, Enerback S, Smith U (2003) Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 11:1182–1191
Youngren JF, Keen S, Kulp JL, Tanner CJ, Houmard JA, Goldfine ID (2001) Enhanced muscle insulin receptor autophosphorylation with short-term aerobic exercise training. Am J Physiol Endocrinol Metab 280:E528–E533
Acknowledgments
This study was supported by an Early Career Researcher grant from RMIT University. ALC was supported by a Peter Doherty Fellowship from the National Health and Medical Research Council of Australia. The authors would like to thank the research participants for volunteering their time end effort, and Dr Matthew Watt, Monica Amezquita and Kate Pattison for technical assistance. No conflict of interest exists.
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Communicated by Jacques Poortmans.
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Camera, D.M., Anderson, M.J., Hawley, J.A. et al. Short-term endurance training does not alter the oxidative capacity of human subcutaneous adipose tissue. Eur J Appl Physiol 109, 307–316 (2010). https://doi.org/10.1007/s00421-010-1356-3
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DOI: https://doi.org/10.1007/s00421-010-1356-3