User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Training in the fasted state improves glucose tolerance during fat-rich diet

Primary tabs

download
  • Open access
  • PDF
  • 572.70 K
Van Proeyen, Karen [KUL] Szlufcik, Karolina [KUL] Nielens, Henri [UCL] Pelgrim, Koen [KUL] Deldicque, Louise [UCL] Hespel, Peter [KUL]

A fat-rich energy-dense diet is an important cause of insulin resistance. Stimulation of fat turnover in muscle cells during dietary fat challenge may contribute to maintenance of insulin sensitivity. Exercise in the fasted state markedly stimulates energy provision via fat oxidation. Therefore, we investigated whether exercise training in the fasted state is more potent than exercise in the fed state to rescue whole-body glucose tolerance and insulin sensitivity during a period of hyper-caloric fat-rich diet. Healthy male volunteers (18-25 y) received a hyper-caloric (∼+30% kcal day(-1)) fat-rich (50% of kcal) diet for 6 weeks. Some of the subjects performed endurance exercise training (4 days per week) in the fasted state (F; n = 10), whilst the others ingested carbohydrates before and during the training sessions (CHO; n = 10). The control group did not train (CON; n = 7). Body weight increased in CON (+3.0 ± 0.8 kg) and CHO (+1.4 ± 0.4 kg) (P < 0.01), but not in F (+0.7 ± 0.4 kg, P = 0.13). Compared with CON, F but not CHO enhanced whole-body glucose tolerance and the Matsuda insulin sensitivity index (P < 0.05). Muscle GLUT4 protein content was increased in F (+28%) compared with both CHO (P = 0.05) and CON (P < 0.05). Furthermore, only training in F elevated AMP-activated protein kinase α phosphorylation (+25%) as well as up-regulated fatty acid translocase/CD36 and carnitine palmitoyltransferase 1 mRNA levels compared with CON (∼+30%). High-fat diet increased intramyocellular lipid but not diacylglycerol and ceramide contents, either in the absence or presence of training. This study for the first time shows that fasted training is more potent than fed training to facilitate adaptations in muscle and to improve whole-body glucose tolerance and insulin sensitivity during hyper-caloric fat-rich diet.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2010
Language Anglais
Journal information "The Journal of Physiology" - Vol. 588, no. Pt 21, p. 4289-4302 (2010)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd. ((United Kingdom) Oxford)
issn 0022-3751
e-issn 1469-7793
Publication status Publié
Affiliations UCL - SSS/IONS - Institute of NeuroScience
UCL - (SLuc) Service de médecine physique et de réadaptation motrice
UCL - SSS/IONS/CEMO - Pôle Cellulaire et moléculaire
MESH Subject Body Composition - physiology ; Dietary Fats - metabolism ; Male ; Muscle, Skeletal - metabolism ; Physical Endurance - physiology ; Young Adult ; Exercise - physiology ; Fasting - physiology ; Fatty Acids, Nonesterified - blood ; Glucose - metabolism ; Glycogen - metabolism ; Humans ; Insulin Resistance - physiology ; Lipid Metabolism - physiology
Links
  1. ACHTEN JUUL, GLEESON MICHAEL, JEUKENDRUP ASKER E., Determination of the exercise intensity that elicits maximal fat oxidation : , 10.1097/00005768-200201000-00015
  2. Adochio Rebecca L, Leitner J Wayne, Gray Karen, Draznin Boris, Cornier Marc-Andre, Early responses of insulin signaling to high-carbohydrate and high-fat overfeeding, 10.1186/1743-7075-6-37
  3. Akerstrom Thorbjorn C.A., Birk Jesper B., Klein Ditte K., Erikstrup Christian, Plomgaard Peter, Pedersen Bente Klarlund, Wojtaszewski Jørgen F.P., Oral glucose ingestion attenuates exercise-induced activation of 5′-AMP-activated protein kinase in human skeletal muscle, 10.1016/j.bbrc.2006.02.057
  4. Akerstrom T. C. A., Fischer C. P., Plomgaard P., Thomsen C., van Hall G., Pedersen B. K., Glucose ingestion during endurance training does not alter adaptation, 10.1152/japplphysiol.91534.2008
  5. Bachmann O. P., Dahl D. B., Brechtel K., Machann J., Haap M., Maier T., Loviscach M., Stumvoll M., Claussen C. D., Schick F., Haring H. U., Jacob S., Effects of Intravenous and Dietary Lipid Challenge on Intramyocellular Lipid Content and the Relation With Insulin Sensitivity in Humans, 10.2337/diabetes.50.11.2579
  6. Bennard Patrick, Doucet Éric, Acute effects of exercise timing and breakfast meal glycemic index on exercise-induced fat oxidation, 10.1139/h06-027
  7. Bonen A., Holloway G. P., Tandon N. N., Han X.-X., McFarlan J., Glatz J. F. C., Luiken J. J. F. P., Cardiac and skeletal muscle fatty acid transport and transporters and triacylglycerol and fatty acid oxidation in lean and Zucker diabetic fatty rats, 10.1152/ajpregu.90820.2008
  8. Bruce C. R., Hoy A. J., Turner N., Watt M. J., Allen T. L., Carpenter K., Cooney G. J., Febbraio M. A., Kraegen E. W., Overexpression of Carnitine Palmitoyltransferase-1 in Skeletal Muscle Is Sufficient to Enhance Fatty Acid Oxidation and Improve High-Fat Diet-Induced Insulin Resistance, 10.2337/db08-1078
  9. Bruce C. R., Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content, 10.1152/ajpendo.00587.2005
  10. Bruce, Pediatrics, 32, 742 (1963)
  11. Cantó Carles, Jiang Lake Q., Deshmukh Atul S., Mataki Chikage, Coste Agnes, Lagouge Marie, Zierath Juleen R., Auwerx Johan, Interdependence of AMPK and SIRT1 for Metabolic Adaptation to Fasting and Exercise in Skeletal Muscle, 10.1016/j.cmet.2010.02.006
  12. Civitarese A. E., Glucose ingestion during exercise blunts exercise-induced gene expression of skeletal muscle fat oxidative genes, 10.1152/ajpendo.00193.2005
  13. Cluberton L. J., Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression, 10.1152/japplphysiol.00197.2005
  14. De Bock K., Richter E. A., Russell A. P., Eijnde B. O., Derave W., Ramaekers M., Koninckx E., Léger B., Verhaeghe J., Hespel P., Exercise in the fasted state facilitates fibre type-specific intramyocellular lipid breakdown and stimulates glycogen resynthesis in humans : Exercise and fasting, 10.1113/jphysiol.2005.083170
  15. De Bock K., Derave W., Eijnde B. O., Hesselink M. K., Koninckx E., Rose A. J., Schrauwen P., Bonen A., Richter E. A., Hespel P., Effect of training in the fasted state on metabolic responses during exercise with carbohydrate intake, 10.1152/japplphysiol.01195.2007
  16. DeFronzo R A, Ferrannini E, Sato Y, Felig P, Wahren J, Synergistic interaction between exercise and insulin on peripheral glucose uptake., 10.1172/jci110399
  17. den Hoed M., Hesselink M. K. C., van Kranenburg G. P. J., Westerterp K. R., Habitual physical activity in daily life correlates positively with markers for mitochondrial capacity, 10.1152/japplphysiol.00091.2008
  18. Dube J. J., Amati F., Stefanovic-Racic M., Toledo F. G. S., Sauers S. E., Goodpaster B. H., Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited, 10.1152/ajpendo.00769.2007
  19. Fluck M., Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli, 10.1242/jeb.02149
  20. Goodpaster Bret H., He Jing, Watkins Simon, Kelley David E., Skeletal Muscle Lipid Content and Insulin Resistance: Evidence for a Paradox in Endurance-Trained Athletes, 10.1210/jcem.86.12.8075
  21. Hancock C. R., Han D.-H., Chen M., Terada S., Yasuda T., Wright D. C., Holloszy J. O., High-fat diets cause insulin resistance despite an increase in muscle mitochondria, 10.1073/pnas.0802057105
  22. Hansen A. K., Skeletal muscle adaptation: training twice every second day vs. training once daily, 10.1152/japplphysiol.00163.2004
  23. Helge J. W, Watt P. W, Richter E. A, Rennie M. J, Kiens B., Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans, 10.1113/jphysiol.2001.012933
  24. Holloway G. P., Benton C. R., Mullen K. L., Yoshida Y., Snook L. A., Han X.-X., Glatz J. F. C., Luiken J. J. F. P., Lally J., Dyck D. J., Bonen A., In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation, 10.1152/ajpendo.90896.2008
  25. Jager S., Handschin C., St.-Pierre J., Spiegelman B. M., AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1 , 10.1073/pnas.0705070104
  26. Jensen T. E., Wojtaszewski J. F. P., Richter E. A., AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient?, 10.1111/j.1748-1716.2009.01979.x
  27. Jorgensen S. B., Treebak J. T., Viollet B., Schjerling P., Vaulont S., Wojtaszewski J. F. P., Richter E. A., Role of AMPK 2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle, 10.1152/ajpendo.00243.2006
  28. Koves Timothy R., Ussher John R., Noland Robert C., Slentz Dorothy, Mosedale Merrie, Ilkayeva Olga, Bain James, Stevens Robert, Dyck Jason R.B., Newgard Christopher B., Lopaschuk Gary D., Muoio Deborah M., Mitochondrial Overload and Incomplete Fatty Acid Oxidation Contribute to Skeletal Muscle Insulin Resistance, 10.1016/j.cmet.2007.10.013
  29. Koves Timothy R., Li Ping, An Jie, Akimoto Takayuki, Slentz Dorothy, Ilkayeva Olga, Dohm G. Lynis, Yan Zhen, Newgard Christopher B., Muoio Deborah M., Peroxisome Proliferator-activated Receptor-γ Co-activator 1α-mediated Metabolic Remodeling of Skeletal Myocytes Mimics Exercise Training and Reverses Lipid-induced Mitochondrial Inefficiency, 10.1074/jbc.m507621200
  30. Kraegen E. W., Cooney G. J., Turner N., Muscle insulin resistance: A case of fat overconsumption, not mitochondrial dysfunction, 10.1073/pnas.0803901105
  31. Lee-Young R. S., Carbohydrate ingestion does not alter skeletal muscle AMPK signaling during exercise in humans, 10.1152/ajpendo.00023.2006
  32. Liu Li, Zhang Yiying, Chen Nancy, Shi Xiaojing, Tsang Bonny, Yu Yi-Hao, Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance, 10.1172/jci30565
  33. Lowry, A Flexible System of Enzymatic Analysis (1972)
  34. Maarbjerg S. J., Jorgensen S. B., Rose A. J., Jeppesen J., Jensen T. E., Treebak J. T., Birk J. B., Schjerling P., Wojtaszewski J. F. P., Richter E. A., Genetic impairment of AMPK 2 signaling does not reduce muscle glucose uptake during treadmill exercise in mice, 10.1152/ajpendo.90653.2008
  35. Matsuda M., DeFronzo R. A., Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp, 10.2337/diacare.22.9.1462
  36. McConell, J Appl Physiol, 87, 1083 (1999)
  37. Misra Anoop, Khurana Lokesh, Obesity and the Metabolic Syndrome in Developing Countries, 10.1210/jc.2008-1595
  38. Moro C., Bajpeyi S., Smith S. R., Determinants of intramyocellular triglyceride turnover: implications for insulin sensitivity, 10.1152/ajpendo.00624.2007
  39. Morton J. P., Croft L., Bartlett J. D., MacLaren D. P. M., Reilly T., Evans L., McArdle A., Drust B., Reduced carbohydrate availability does not modulate training-induced heat shock protein adaptations but does upregulate oxidative enzyme activity in human skeletal muscle, 10.1152/japplphysiol.00003.2009
  40. Murgia Marta, Jensen Thomas E., Cusinato Marzia, Garcia Marta, Richter Erik A., Schiaffino Stefano, Multiple signalling pathways redundantly control glucose transporterGLUT4gene transcription in skeletal muscle : GLUT4 gene transcriptional control, 10.1113/jphysiol.2009.174888
  41. Nybo L., Pedersen K., Christensen B., Aagaard P., Brandt N., Kiens B., Impact of carbohydrate supplementation during endurance training on glycogen storage and performance, 10.1111/j.1748-1716.2009.01996.x
  42. Oakes N. D., Cooney G. J., Camilleri S., Chisholm D. J., Kraegen E. W., Mechanisms of Liver and Muscle Insulin Resistance Induced by Chronic High-Fat Feeding, 10.2337/diab.46.11.1768
  43. Ojuka Edward O., Jones Terry E., Nolte Lorraine A., Chen May, Wamhoff Brian R., Sturek Michael, Holloszy John O., Regulation of GLUT4 biogenesis in muscle: evidence for involvement of AMPK and Ca2+, 10.1152/ajpendo.00512.2001
  44. Pan D. A., Lillioja S., Kriketos A. D., Milner M. R., Baur L. A., Bogardus C., Jenkins A. B., Storlien L. H., Skeletal Muscle Triglyceride Levels Are Inversely Related to Insulin Action, 10.2337/diab.46.6.983
  45. Schenk Simon, Horowitz Jeffrey F., Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid–induced insulin resistance, 10.1172/jci30566
  46. Schrauwen-Hinderling Vera B., Kooi Marianne Eline, Hesselink Matthijs K.C., Moonen-Kornips Esther, Schaart Gert, Mustard Kirsty J., Hardie D. Grahame, Saris Wim H.M., Nicolay Klaas, Schrauwen Patrick, Intramyocellular Lipid Content and Molecular Adaptations in Response to a 1-Week High-Fat Diet, 10.1038/oby.2005.259
  47. Spencer, Am J Physiol Cell Physiol, 261, C71 (1991)
  48. Stannard Stephen R., Buckley Alex J., Edge Johann A., Thompson Martin W., Adaptations to skeletal muscle with endurance exercise training in the acutely fed versus overnight-fasted state, 10.1016/j.jsams.2010.03.002
  49. Storlien, Am J Physiol Endocrinol Metab, 251, E576 (1986)
  50. SUMMERS S, Ceramides in insulin resistance and lipotoxicity, 10.1016/j.plipres.2005.11.002
  51. Timmers Silvie, Schrauwen Patrick, de Vogel Johan, Muscular diacylglycerol metabolism and insulin resistance, 10.1016/j.physbeh.2007.12.002
  52. Tsao T.-S., Burcelin R., Katz E. B., Huang L., Charron M. J., Enhanced Insulin Action Due to Targeted GLUT4 Overexpression Exclusively in Muscle, 10.2337/diab.45.1.28
  53. Turcotte, Am J Physiol Endocrinol Metab, 262, E791 (1992)
  54. Turner Nigel, Bruce Clinton R., Beale Susan M., Hoehn Kyle L., So Trina, Rolph Michael S., Cooney Gregory J., Excess Lipid Availability Increases Mitochondrial Fatty Acid Oxidative Capacity in Muscle : Evidence Against a Role for Reduced Fatty Acid Oxidation in Lipid-Induced Insulin Resistance in Rodents, 10.2337/db07-0093
  55. Van Veldhoven Paul P., Bell Robert M., Effect of harvesting methods, growth conditions and growth phase on diacylglycerol levels in cultured human adherent cells, 10.1016/0005-2760(88)90030-6
  56. Van Veldhoven, Biochem Molec Biol Intern, 36, 21 (1995)
  57. Van Veldhoven Paul P., Matthews Tom J., Bolognesi Dani P., Bell Robert M., Changes in bioactive lipids, alkylacylglycerol and ceramide, occur in HIV-infected cells, 10.1016/s0006-291x(05)81480-9
  58. Vandesompele Jo, De Preter Katleen, Pattyn Filip, Poppe Bruce, Van Roy Nadine, De Paepe Anne, Speleman Frank, 10.1186/gb-2002-3-7-research0034
  59. Winder, J Appl Physiol, 91, 1017 (2001)
  60. Winder, J Appl Physiol, 88, 2219 (2000)
  61. Yeo W. K., Paton C. D., Garnham A. P., Burke L. M., Carey A. L., Hawley J. A., Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens, 10.1152/japplphysiol.90882.2008
  62. Zimmet Paul, Alberti K. G. M. M., Shaw Jonathan, Global and societal implications of the diabetes epidemic, 10.1038/414782a
  63. Kahn Barbara B., Zisman Ariel, Peroni Odile D., Abel E. Dale, Michael M. Dodson, Mauvais-Jarvis Franck, Lowell Bradford B., Wojtaszewski Jørgen F.P., Hirshman Michael F., Virkamaki Antti, Goodyear Laurie J., Kahn C. Ronald, 10.1038/78693
Bibliographic reference Van Proeyen, Karen ; Szlufcik, Karolina ; Nielens, Henri ; Pelgrim, Koen ; Deldicque, Louise ; et. al. Training in the fasted state improves glucose tolerance during fat-rich diet. In: The Journal of Physiology, Vol. 588, no. Pt 21, p. 4289-4302 (2010)
Permanent URL http://hdl.handle.net/2078.1/110104