One week of bed rest leads to substantial muscle atrophy and induces whole-body insulin resistance in the absence of skeletal muscle lipid accumulation

Diabetes

Volumn 65, Issue 10, 2016, Pages 2862-2875

  Dirks, Marlou L ^a   Wall, Benjamin T ^a   Van De Valk, Bas ^a   Holloway, Tanya M ^b   Holloway, Graham P ^b   Chabowski, Adrian ^c   Goossens, Gijs H ^a   Van Loon, Luc J ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF GUELPH   (Canada)

^c MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; LIPID; OXYGEN;

ADULT; ARTICLE; BED REST; CAPILLARY DENSITY; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED TOMOGRAPHY; DUAL ENERGY X RAY ABSORPTIOMETRY; ENERGY EXPENDITURE; GLYCEMIC CONTROL; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; HYPERINSULINEMIC-EUGLYCEMIC CLAMP TECHNIQUE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LEAN TISSUE; LIPID DIET; LIPID METABOLISM; LIPID STORAGE; MALE; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE MASS; MUSCLE STRENGTH; NORMAL HUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; SKELETAL MUSCLE; YOUNG ADULT; ADVERSE EFFECTS; GLUCOSE CLAMP TECHNIQUE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOTON ABSORPTIOMETRY; PHYSIOLOGY;

ABSORPTIOMETRY, PHOTON; ADULT; BED REST; DIET, HIGH-FAT; GLUCOSE CLAMP TECHNIQUE; HUMANS; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; QUADRICEPS MUSCLE; YOUNG ADULT;

EID: 84988718704     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1661     Document Type: Article

References (62)

1. Bergouignan A, Rudwill F, Simon C, Blanc S. Physical inactivity as the culprit of metabolic inflexibility: Evidence from bed-rest studies. J Appl Physiol (1985) 2011;111:1201-1210
2. Wall BT, van Loon LJ. Nutritional strategies to attenuate muscle disuse atrophy. Nutr Rev 2013;71:195-208
3. Statistics Explained. Hospital discharges and length of stay statistics [article online], 2015. Available from http://ec.europa.eu/eurostat/statistics-explained/index .php/Hospital-discharges-and-length-of-stay-statistics. Accessed 17 February 2016
4. Dirks ML, Wall BT, Nilwik R, Weerts DH, Verdijk LB, van Loon LJ. Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men. J Nutr 2014;144:1196-1203
5. Dirks ML, Wall BT, Snijders T, Ottenbros CL, Verdijk LB, van Loon LJ. Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol (Oxf) 2014;210:628-641
6. Suetta C, Frandsen U, Mackey AL, et al. Ageing is associated with diminished muscle re-growth and myogenic precursor cell expansion early after immobilityinduced atrophy in human skeletal muscle. J Physiol 2013;591:3789-3804
7. English KL, Paddon-Jones D. Protecting muscle mass and function in older adults during bed rest. Curr Opin Clin Nutr Metab Care 2010;13:34-39
8. Wall BT, Dirks ML, van Loon LJ. Skeletal muscle atrophy during shortterm disuse: Implications for age-related sarcopenia. Ageing Res Rev 2013;12: 898-906
9. Yanagibori R, Suzuki Y, Kawakubo K, Makita Y, Gunji A. Carbohydrate and lipid metabolism after 20 days of bed rest. Acta Physiol Scand Suppl 1994;616:51-57
10. Bergouignan A, Schoeller DA, Normand S, et al. Effect of physical inactivity on the oxidation of saturated and monounsaturated dietary Fatty acids: Results of a randomized trial. PLoS Clin Trials 2006;1:e27
11. Gram M, Vigelsø A, Yokota T, Helge JW, Dela F, Hey-Mogensen M. Skeletal muscle mitochondrial H2 O2 emission increases with immobilization and decreases after aerobic training in young and older men. J Physiol 2015;593:4011-4027
12. Haruna Y, Suzuki Y, Kawakubo K, Yanagibori R, Gunji A. Decremental reset in basal metabolism during 20-days bed rest. Acta Physiol Scand Suppl 1994; 616:43-49
13. Weijs PJ, Looijaard WG, Dekker IM, et al. Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients. Crit Care 2014; 18:R12
14. Alibegovic AC, Højbjerre L, Sonne MP, et al. Impact of 9 days of bed rest on hepatic and peripheral insulin action, insulin secretion, and whole-body lipolysis in healthy young male offspring of patients with type 2 diabetes. Diabetes 2009; 58:2749-2756
15. Stuart CA, Shangraw RE, Prince MJ, Peters EJ, Wolfe RR. Bed-rest-induced insulin resistance occurs primarily in muscle. Metabolism 1988;37:802-806
16. Mikines KJ, Richter EA, Dela F, Galbo H. Seven days of bed rest decrease insulin action on glucose uptake in leg and whole body. J Appl Physiol (1985) 1991;70:1245-1254
17. Sonne MP, Alibegovic AC, Højbjerre L, Vaag A, Stallknecht B, Dela F. Effect of 10 days of bedrest on metabolic and vascular insulin action: A study in individuals at risk for type 2 diabetes. J Appl Physiol (1985) 2010;108:830-837
18. Biensø RS, Ringholm S, Kiilerich K, et al. GLUT4 and glycogen synthase are key players in bed rest-induced insulin resistance. Diabetes 2012;61:1090-1099
19. Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: A 1H NMR spectroscopy study. Diabetologia 1999;42:113-116
20. Bosma M, Kersten S, Hesselink MK, Schrauwen P. Re-evaluating lipotoxic triggers in skeletal muscle: Relating intramyocellular lipid metabolism to insulin sensitivity. Prog Lipid Res 2012;51:36-49
21. Max SR. Disuse atrophy of skeletal muscle: Loss of functional activity of mitochondria. Biochem Biophys Res Commun 1972;46:1394-1398
22. Abadi A, Glover EI, Isfort RJ, et al. Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS One 2009;4:e6518
23. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: Possible role in insulin resistance. Science 2003;300:1140-1142
24. Muris DM, Houben AJ, Schram MT, Stehouwer CD. Microvascular dysfunction is associated with a higher incidence of type 2 diabetes mellitus: A systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 2012;32: 3082-3094
25. Schoffelen PF, Westerterp KR, Saris WH, Ten Hoor F. A dual-respiration chamber system with automated calibration. J Appl Physiol (1985) 1997;83: 2064-2072
26. Strandberg S, Wretling ML, Wredmark T, Shalabi A. Reliability of computed tomography measurements in assessment of thigh muscle cross-sectional area and attenuation. BMC Med Imaging 2010;10:18
27. Veasey Rodrigues H, Baracos VE, Wheler JJ, et al. Body composition and survival in the early clinical trials setting. Eur J Cancer 2013;49:3068-3075
28. Conte C, Fabbrini E, Kars M, Mittendorfer B, Patterson BW, Klein S. Multiorgan insulin sensitivity in lean and obese subjects. Diabetes Care 2012;35:1316-1321
29. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 1981;30:1000-1007
30. Most J, Goossens GH, Jocken JW, Blaak EE. Short-term supplementation with a specific combination of dietary polyphenols increases energy expenditure and alters substrate metabolism in overweight subjects. Int J Obes 2014;38: 698-706
31. Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR, Bemben MG. Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitness 1995;35:108-113
32. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 2007;292:E151-E157
33. Guralnik JM, Ferrucci L, Penninx BW, et al. New and worsening conditions and change in physical and cognitive performance during weekly evaluations over 6 months: The Women's Health and Aging Study. J Gerontol A Biol Sci Med Sci 1999;54:M410-M422
34. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 1975;35:609-616
35. Leenders M, Verdijk LB, van der Hoeven L, van Kranenburg J, Nilwik R, van Loon LJ. Elderly men and women benefit equally from prolonged resistance-type exercise training. J Gerontol A Biol Sci Med Sci 2013;68:769-779
36. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. Computer control of microscopes using microManager. Curr Protoc Mol Biol 2010;Chapter 14:Unit14.20
37. Groen BB, Hamer HM, Snijders T, et al. Skeletal muscle capillary density and microvascular function are compromised with aging and type 2 diabetes. J Appl Physiol (1985) 2014;116:998-1005
38. Koopman R, Schaart G, Hesselink MK. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 2001;116:63-68
39. Moors CC, Blaak EE, van der Zijl NJ, Diamant M, Goossens GH. The effects of long-term valsartan treatment on skeletal muscle fatty acid handling in humans with impaired glucose metabolism. J Clin Endocrinol Metab 2013;98:E891-E896
40. Beaudoin MS, Perry CG, Arkell AM, et al. Impairments in mitochondrial palmitoyl-CoA respiratory kinetics that precede development of diabetic cardiomyopathy are prevented by resveratrol in ZDF rats. J Physiol 2014;592:2519-2533
41. Bergmeyer HU. Methods of Enzymatic Analysis. New York, Academic Press, 1974
42. Danson MJ, Hough DW. Citrate synthase from hyperthermophilic Archaea. Methods Enzymol 2001;331:3-12
43. Herbst EA, Paglialunga S, Gerling C, et al. Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle. J Physiol 2014;592:1341-1352
44. Snijders T, Res PT, Smeets JS, et al. Protein ingestion before sleep increases muscle mass and strength gains during prolonged resistance-type exercise training in healthy young men. J Nutr 2015;145:1178-1184
45. Mortensen B, Friedrichsen M, Andersen NR, et al. Physical inactivity affects skeletal muscle insulin signaling in a birth weight-dependent manner. J Diabetes Complications 2014;28:71-78
46. Wall BT, Dirks ML, Snijders T, et al. Short-term muscle disuse atrophy is not associated with increased intramuscular lipid deposition or a decline in the maximal activity of key mitochondrial enzymes in young and older males. Exp Gerontol 2015;61:76-83
47. Nielsen J, Mogensen M, Vind BF, et al. Increased subsarcolemmal lipids in type 2 diabetes: Effect of training on localization of lipids, mitochondria, and glycogen in sedentary human skeletal muscle. Am J Physiol Endocrinol Metab 2010;298:E706-E713
48. Nowotny B, Zahiragic L, Krog D, et al. Mechanisms underlying the onset of oral lipid-induced skeletal muscle insulin resistance in humans. Diabetes 2013; 62:2240-2248
49. Adams JM 2nd, Pratipanawatr T, Berria R, et al. Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 2004; 53:25-31
50. Bonen A, Jain SS, Snook LA, et al. Extremely rapid increase in fatty acid transport and intramyocellular lipid accumulation but markedly delayed insulin resistance after high fat feeding in rats. Diabetologia 2015;58:2381-2391
51. Sitnick MT, Basantani MK, Cai L, et al. Skeletal muscle triacylglycerol hydrolysis does not influence metabolic complications of obesity. Diabetes 2013;62: 3350-3361
52. Jocken JW, Goossens GH, Boon H, et al. Insulin-mediated suppression of lipolysis in adipose tissue and skeletal muscle of obese type 2 diabetic men and men with normal glucose tolerance. Diabetologia 2013;56:2255-2265
53. Anderson EJ, Lustig ME, Boyle KE, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009;119:573-581
54. Lee HY, Choi CS, Birkenfeld AL, et al. Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metab 2010;12:668-674
55. Ringholm S, Biensø RS, Kiilerich K, et al. Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am J Physiol Endocrinol Metab 2011;301:E649-E658
56. Levine S, Nguyen T, Taylor N, et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 2008;358:1327-1335
57. Larsen S, Nielsen J, Hansen CN, et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 2012; 590:3349-3360
58. Powers SK, Kavazis AN, DeRuisseau KC. Mechanisms of disuse muscle atrophy: Role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 2005; 288:R337-R344
59. Agostini F, Dalla Libera L, Rittweger J, et al. Effects of inactivity on human muscle glutathione synthesis by a double-tracer and single-biopsy approach. J Physiol 2010;588:5089-5104
60. Lillioja S, Young AA, Culter CL, et al. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 1987;80:415-424
61. Defronzo RA. Glucose intolerance and aging: Evidence for tissue insensitivity to insulin. Diabetes 1979;28:1095-1101
62. van den Berghe G, Wouters P, Weekers F, et al. Intensive insulin therapy in critically ill patients. N Engl J Med 2001;345:1359-1367