European Journal of Applied Physiology

, Volume 109, Issue 2, pp 307–316

Short-term endurance training does not alter the oxidative capacity of human subcutaneous adipose tissue

  • Donny M. Camera
  • Mitchell J. Anderson
  • John A. Hawley
  • Andrew L. Carey
Original Article

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.

Keywords

White adipose Brown adipose WAT BAT Mitochondrial Obesity Adrenergic UCP1 

References

  1. 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 104:2366–2371CrossRefPubMedGoogle Scholar
  2. 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 88:5444–5451CrossRefPubMedGoogle Scholar
  3. Bulow J, Madsen J (1978) Human adipose tissue blood flow during prolonged exercise II. Pflugers Arch 376:41–45CrossRefPubMedGoogle Scholar
  4. Cinti S (2009) Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol Endocrinol Metab 297:E977–E986CrossRefGoogle Scholar
  5. Collins S, Surwit RS (2001) The beta-adrenergic receptors and the control of adipose tissue metabolism and thermogenesis. Recent Prog Horm Res 56:309–328CrossRefPubMedGoogle Scholar
  6. 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 149:2546–2556CrossRefPubMedGoogle Scholar
  7. 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 360:1509–1517CrossRefPubMedGoogle Scholar
  8. 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 26:1442–1450CrossRefPubMedGoogle Scholar
  9. 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 9:203–209CrossRefPubMedGoogle Scholar
  10. Frayn KN (1998) Regulation of fatty acid delivery in vivo. Adv Exp Med Biol 441:171–179PubMedGoogle Scholar
  11. 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 51:394–397CrossRefPubMedGoogle Scholar
  12. Gesta S, Tseng Y, Kahn R (2007) Developmental origin of fat: tracking obesity to its source. Cell 131:242–256CrossRefPubMedGoogle Scholar
  13. 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 575:901–911CrossRefPubMedGoogle Scholar
  14. 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 70:2032–2038PubMedGoogle Scholar
  15. 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 78:138–145PubMedGoogle Scholar
  16. 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 27:996–1005PubMedGoogle Scholar
  17. Hamosh M, Hamosh P, Bar-Maor JA, Cohen H (1963) Fatty-acid metabolism by human adipose tissues. J Clin Invest 42:1648–1652CrossRefPubMedGoogle Scholar
  18. Hawley JA, Noakes TD (1992) Peak power output predicts maximal oxygen uptake and performance time in trained cyclists. Eur J Appl Physiol Occup Physiol 65:79–83CrossRefPubMedGoogle Scholar
  19. 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–E1152PubMedGoogle Scholar
  20. Hotamisligil G (2006) Inflammation and metabolic disorders. Nature 444:860–867CrossRefPubMedGoogle Scholar
  21. Hull D, Segall MM (1965) Sympathetic nervous control of brown adipose tissue and heat production in the new-born rabbit. J Physiol 181:458–467PubMedGoogle Scholar
  22. Huttunen P, Hirvonen J, Kinnula V (1981) The occurrence of brown adipose tissue in outdoor workers. Eur J Appl Physiol Occup Physiol 46:339–345CrossRefPubMedGoogle Scholar
  23. 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 79:756–762PubMedGoogle Scholar
  24. 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 91:344–349CrossRefPubMedGoogle Scholar
  25. 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 55:483–487CrossRefPubMedGoogle Scholar
  26. 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 587:3729–3739CrossRefPubMedGoogle Scholar
  27. 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 47:98–103CrossRefPubMedGoogle Scholar
  28. 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 270:12953–12956CrossRefPubMedGoogle Scholar
  29. 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 50:2036–2041CrossRefPubMedGoogle Scholar
  30. 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 568:665–676CrossRefPubMedGoogle Scholar
  31. Nedergaard J, Bengtsson T, Cannon B (2007) Active brown adipose tissue and adult humans. Am J Physiol Endocrinol Metab 293:444–452CrossRefGoogle Scholar
  32. 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 38:2125–2133PubMedGoogle Scholar
  33. Ostman J, Arner P, Engfeldt P, Kager L (1979) Regional differences in the control of lipolysis in human adipose tissue. Metabolism 28:1198–1205CrossRefPubMedGoogle Scholar
  34. Peronnet F, Massicotte D (1991) Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16:23–29PubMedGoogle Scholar
  35. 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 51:812–815PubMedGoogle Scholar
  36. 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–E296CrossRefPubMedGoogle Scholar
  37. 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–E272PubMedGoogle Scholar
  38. Puigserver P (2005) Tissue-specific regulation of metabolic pathways through the transcriptional coactivator PGC1-alpha. Int J Obes (Lond) 29:S5–S9CrossRefGoogle Scholar
  39. Ricquier D, Nechad M, Mory G (1982) Ultrastructural and biochemical characterization of human brown adipose tissue in pheochromocytoma. Clin Endocrinol Metab 54:803–807CrossRefGoogle Scholar
  40. 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 58:1526–1531CrossRefPubMedGoogle Scholar
  41. 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 6:38–54CrossRefPubMedGoogle Scholar
  42. 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 454:21CrossRefGoogle Scholar
  43. Smith DJ, Deuster PA, Ryan CJ, Doubt TJ (1990) Prolonged whole body immersion in cold water: hormonal and metabolic changes. Undersea Biomed Res 17:139–147PubMedGoogle Scholar
  44. 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 453:783–787CrossRefPubMedGoogle Scholar
  45. 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–E414PubMedGoogle Scholar
  46. 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 587:1607–1617CrossRefPubMedGoogle Scholar
  47. 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 104:4401–4406CrossRefPubMedGoogle Scholar
  48. 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 278:33370–33376CrossRefPubMedGoogle Scholar
  49. 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 454:1000–1004CrossRefPubMedGoogle Scholar
  50. 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 116:2791–2798PubMedGoogle Scholar
  51. 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 360:1500–1508CrossRefPubMedGoogle Scholar
  52. 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 360:1518–1525CrossRefPubMedGoogle Scholar
  53. 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 23:1085–1094CrossRefPubMedGoogle Scholar
  54. Yang X, Enerback S, Smith U (2003) Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 11:1182–1191CrossRefPubMedGoogle Scholar
  55. 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–E533PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Donny M. Camera
    • 1
  • Mitchell J. Anderson
    • 1
  • John A. Hawley
    • 1
  • Andrew L. Carey
    • 1
    • 2
  1. 1.Exercise Metabolism Group, School of Medical SciencesRMIT UniversityBundooraAustralia
  2. 2.Metabolic and Vascular Physiology LaboratoryBaker IDI Heart and Diabetes InstituteMelbourneAustralia

Personalised recommendations