The physiological regulation of glucose flux into muscle in vivo

Journal of Experimental Biology

Volumn 214, Issue 2, 2011, Pages 254-262

  Wasserman, David H ^a   Kang, Li ^a   Ayala, Julio E ^a,b   Fueger, Patrick T ^a,c   Lee Young, Robert S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Flux; Glucose; In vivo

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; NITRIC OXIDE SYNTHASE;

ANIMAL; ARTICLE; EXERCISE; HUMAN; INSULIN RESISTANCE; METABOLISM; PHOSPHORYLATION; SKELETAL MUSCLE; TRANSPORT AT THE CELLULAR LEVEL;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BIOLOGICAL TRANSPORT; EXERCISE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RESISTANCE; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE; PHOSPHORYLATION;

EID: 78651276331     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.048041     Document Type: Article

References (99)

1. Ayala, J. E., Bracy, D. P., McGuinness, O. P. and Wasserman, D. H. (2006). Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55, 390-397.
2. Ayala, J. E., Bracy, D. P., Julien, B. M., Rottman, J. N., Fueger, P. T. and Wasserman, D. H. (2007). Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice. Diabetes 56, 1025-1033.
3. Berglund, E. D., Li, C. Y., Poffenberger, G., Ayala, J. E., Fueger, P. T., Willis, S. E., Jewell, M. M., Powers, A. C. and Wasserman, D. H. (2008). Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 57, 1790-1799.
4. Berglund, E. D., Lee-Young, R. S., Lustig, D. G., Lynes, S. E., Donahue, E. P., Camacho, R. C., Meredith, M. E., Magnuson, M. A., Charron, M. J. and Wasserman, D. H. (2009). Hepatic energy state is regulated by glucagon receptor signaling in mice. J. Clin. Invest. 119, 2412-2422.
5. Berria, R., Wang, L., Richardson, D. K., Finlayson, J., Belfort, R., Pratipanawatr, T., De Filippis, E. A., Kashyap, S. and Mandarino, L. J. (2006). Increased collagen content in insulin-resistant skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 290, E560-E565.
6. Bonadonna, R., Prato, S. D., Bonora, E., Saccomani, M., Gulli, G., Natali, A., Frascerra, S., Pecori, N., Ferrannini, E., Bier, D. et al. (1996). Roles of glucose transport and glucose phosphorylation in muscle insulin resistance of NIDDM. Diabetes 45, 915-925.
7. Bradley, S. J., Kingwell, B. A. and McConell, G. K. (1999). Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes 48, 1815-1821.
8. Braithwaite, S. S., Palazuk, B., Colca, J. R., Edwards, C. W. and Hofmann, C. (1995). Reduced expression of hexokinase II in insulin-resistant diabetes. Diabetes 44, 43-48.
9. Canto, C., Jiang, L. Q., Deshmukh, A. S., Mataki, C., Coste, A., Lagouge, M., Zierath, J. R. and Auwerx, J. (2010). Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab. 11, 213-219.
10. Clerk, L. H., Vincent, M. A., Barrett, E. J., Lankford, M. F. and Lindner, J. R. (2007). Skeletal muscle capillary responses to insulin are abnormal in late-stage diabetes and are restored by angiotensin-converting enzyme inhibition. Am. J. Physiol. Endocrinol. Metab. 293, E1804-E1809.
11. Coker, R. H., Krishna, M. G., Lacy, D. B., Bracy, D. P. and Wasserman, D. H. (1997). Role of hepatic alpha-and beta-adrenergic receptor stimulation on hepatic glucose production during heavy exercise. Am. J. Physiol. 273, E831-E838.
12. Coker, R. H., Lacy, D. B., Krishna, M. G. and Wasserman, D. H. (1999). Splanchnic glucagon kinetics in exercising alloxan-diabetic dogs. J. Appl. Physiol. 86, 1626-1631.
13. Duplain, H., Burcelin, R., Sartori, C., Cook, S., Egli, M., Lepori, M., Vollenweider, P., Pedrazzini, T., Nicod, P., Thorens, B. et al. (2001). Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104, 342-345.
14. Etgen, G. J., Jr, Wilson, C. M., Jensen, J., Cushman, S. W. and Ivy, J. L. (1996). Glucose transport and cell surface GLUT-4 protein in skeletal muscle of the obese Zucker rat. Am. J. Physiol. 271, E294-E301.
15. Febbraio, M. A., Hiscock, N., Sacchetti, M., Fischer, C. P. and Pedersen, B. K. (2004). Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 53, 1643-1648.
16. Fueger, P. T., Heikkinen, S., Bracy, D. P., Malabanan, C. M., Laakso, M. and Wasserman, D. H. (2003). Hexokinase II partial knockout impairs exercisestimulated muscle glucose uptake in oxidative muscles of mice. Am. J. Physiol. 285, 958-963.
17. Fueger, P. T., Bracy, D. P., Malabanan, C. M., Pencek, R. R., Granner, D. K. and Wasserman, D. H. (2004a). Hexokinase II overexpression improves exercisestimulated but not insulin-stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53, 306-314.
18. Fueger, P. T., Hess, H. S., Bracy, D. P., Pencek, R. R., Posey, K. A., Charron, M. J. and Wasserman, D. H. (2004b). Regulation of insulin-stimulated muscle glucose uptake in the conscious mouse: role of glucose transport is dependent on glucose phosphorylation capacity. Endocrinology 145, 4912-4916.
19. Fueger, P. T., Hess, H. S., Posey, K. A., Bracy, D. P., Pencek, R. R., Charron, M. J. and Wasserman, D. H. (2004c). Control of exercise-stimulated muscle glucose uptake by GLUT4 is dependent on glucose phosphorylation capacity in the conscious mouse. J. Biol. Chem. 279, 50956-50961.
20. Fueger, P. T., Lee-Young, R. S., Shearer, J., Bracy, D. P., Heikkinen, S., Laakso, M., Rottman, J. N. and Wasserman, D. H. (2007a). Phosphorylation barriers to skeletal and cardiac muscle glucose uptakes in high-fat fed mice: studies in mice with a 50% reduction of hexokinase II. Diabetes 56, 2476-2484.
21. Fueger, P. T., Li, C. Y., Ayala, J. E., Shearer, J., Bracy, D. P., Charron, M. J., Rottman, J. N. and Wasserman, D. H. (2007b). Glucose kinetics and exercise tolerance in mice lacking the GLUT4 glucose transporter. J. Physiol. 582, 801-812.
22. Funai, K., Schweitzer, G. G., Sharma, N., Kanzaki, M. and Cartee, G. D. (2009). Increased AS160 phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 297, E242-E251.
23. Goodyear, L. J., Hirshman, M. F., King, P. A., Thompson, C. M., Horton, E. D. and Horton, E. S. (1990). Skeletal muscle plasma membrane glucose transport and glucose transporters after exercise. J. Appl. Physiol. 68, 193-198.
24. Halseth, A. E., Bracy, D. P. and Wasserman, D. H. (1998). Limitations to exerciseand maximal insulin-stimulated muscle glucose uptake. J. Appl. Physiol. 85, 2305-2313.
25. Halseth, A., Bracy, D. and Wasserman, D. (1999). Overexpression of hexokinase II increases insulin-and exercise-stimulated muscle glucose uptake in vivo. Am. J. Physiol. 276, E70-E77.
26. Halseth, A. E., Bracy, D. P. and Wasserman, D. H. (2000). Limitations to basal and insulin-stimulated skeletal muscle glucose uptake in the high-fat-fed rat. Am. J. Physiol. Endocrinol. Metab. 279, E1064-E1071.
27. Halseth, A. E., Bracy, D. P. and Wasserman, D. H. (2001). Functional limitations to glucose uptake in muscles comprised of different fiber types. Am. J. Physiol. Endocrinol. Metab. 280, E994-E999.
28. Han, X. X., Handberg, A., Petersen, L. N., Ploug, T. and Galbo, H. (1995). Stability of GLUT-1 and GLUT-4 expression in perfused rat muscle stimulated by insulin and exercise. J. Appl. Physiol. 78, 46-52.
29. Higaki, Y., Hirshman, M. F., Fujii, N. and Goodyear, L. J. (2001). Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 50, 241-247.
30. Hirsch, I. B., Marker, J. C., Smith, L. J., Spina, R. J., Parvin, C. A., Holloszy, J. O. and Cryer, P. E. (1991). Insulin and glucagon in prevention of hypoglycemia during exercise in humans. Am. J. Physiol. 260, E695-E704.
31. Holmang, A., Muller, M., Andersson, O. K. and Lonnroth, P. (1998). Minimal influence of blood flow on interstitial glucose and lactate-normal and insulin-resistant muscle. Am. J. Physiol. 274, E446-E452.
32. Hoppeler, H. and Weibel, E. R. (1998). Limits for oxygen and substrate transport in mammals. J. Exp. Biol. 201, 1051-1064.
33. Inyard, A. C., Chong, D. G., Klibanov, A. L. and Barrett, E. J. (2009). Muscle contraction, but not insulin, increases microvascular blood volume in the presence of free fatty acid-induced insulin resistance. Diabetes 58, 2457-2463.
34. Jensen, T. E., Schjerling, P., Viollet, B., Wojtaszewski, J. F. and Richter, E. A. (2008). AMPK alpha1 activation is required for stimulation of glucose uptake by twitch contraction, but not by H2O2, in mouse skeletal muscle. PLoS ONE 3, e2102.
35. Jensen, T. E., Wojtaszewski, J. F. and Richter, E. A. (2009). AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient? Acta Physiol. (Oxf.) 196, 155-174.
36. Kacser, H. and Burns, J. A. (1995). The control of flux: 21 years on. Biochem. Soc. Trans. 23, 341-366.
37. Katz, A., Broberg, S., Sahlin, K. and Wahren, J. (1986). Leg glucose uptake during maximal dynamic exercise in humans. Am. J. Physiol. 251, E65-E70.
38. Katz, A., Sahlin, K. and Broberg, S. (1991). Regulation of glucose utilization in human skeletal muscle during moderate dynamic exercise. Am. J. Physiol. 260, E411-E415.
39. Kramer, H. F., Witczak, C. A., Taylor, E. B., Fujii, N., Hirshman, M. F. and Goodyear, L. J. (2006). AS160 regulates insulin-and contraction-stimulated glucose uptake in mouse skeletal muscle. J. Biol. Chem. 281, 31478-31485.
40. Kramer, H. F., Taylor, E. B., Witczak, C. A., Fujii, N., Hirshman, M. F. and Goodyear, L. J. (2007). Calmodulin-binding domain of AS160 regulates contractionbut not insulin-stimulated glucose uptake in skeletal muscle. Diabetes 56, 2854-2862.
41. Kraniou, G. N., Cameron-Smith, D. and Hargreaves, M. (2006). Acute exercise and GLUT4 expression in human skeletal muscle: influence of exercise intensity. J. Appl. Physiol. 101, 934-937.
42. Laakso, M., Edelman, S. V., Brechtel, G. and Baron, A. D. (1992). Impaired insulinmediated skeletal muscle blood flow in patients with NIDDM. Diabetes 41, 1076-1083.
43. Lavoie, C., Ducros, F., Bourque, J., Langelier, H. and Chiasson, J. L. (1997). Glucose metabolism during exercise in man: the role of insulin and glucagon in the regulation of hepatic glucose production and gluconeogenesis. Can. J. Physiol. Pharmacol. 75, 26-35.
44. Lee-Young, R. S., Griffee, S. R., Lynes, S. E., Bracy, D. P., Ayala, J. E., McGuinness, O. P. and Wasserman, D. H. (2009). Skeletal muscle AMP-activated protein kinase is essential for the metabolic response to exercise in vivo. J. Biol. Chem. 284, 23925-23934.
45. Lee-Young, R. S., Ayala, J. E., Hunley, C. F., James, F. D., Bracy, D. P., Kang, L. and Wasserman, D. H. (2010). Endothelial nitric oxide synthase is central to skeletal muscle metabolic regulation and enzymatic signaling during exercise in vivo. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1399-R1408.
46. Liljenquist, J. E., Mueller, G. L., Cherrington, A. D., Keller, U., Chiasson, J. L., Perry, J. M., Lacy, W. W. and Rabinowitz, D. (1977). Evidence for an important role of glucagon in the regulation of hepatic glucose production in normal man. J. Clin. Invest. 59, 369-374.
47. Lins, P. E., Wajngot, A., Adamson, U., Vranic, M. and Efendic, S. (1983). Minimal increases in glucagon levels enhance glucose production in man with partial hypoinsulinemia. Diabetes 32, 633-636.
48. Liu, S., Baracos, V. E., Quinney, H. and Clandinin, M. T. (1996). Dietary fat modifies exercise-dependent glucose transport in skeletal muscle. J. Appl. Physiol. 80, 1219-1224.
49. Maarbjerg, S. J., Jørgensen, S. B., Rose, A. J., Jeppesen, J., Jensen, T. E., Treebak, J. T., Birk, J. B., Schjerling, P., Wojtaszewski, J. F., Richter, E. A. (2009). Genetic impairment of AMPKalpha2 signaling does not reduce muscle glucose uptake during treadmill exercise in mice. Am. J. Physiol. Endocrinol. Metab. 297, E924-E934.
50. MacLean, D. A., Bangsbo, J. and Saltin, B. (1999). Muscle interstitial glucose and lactate levels during dynamic exercise in humans determined by microdialysis. J. Appl. Physiol. 87, 1483-1490.
51. McConell, G. K. and Wadley, G. D. (2008). Potential role of nitric oxide in contractionstimulated glucose uptake and mitochondrial biogenesis in skeletal muscle. Clin. Exp. Pharmacol. Physiol. 35, 1488-1492.
52. McConell, G. K., Huynh, N. N., Lee-Young, R. S., Canny, B. J. and Wadley, G. D. (2006). L-Arginine infusion increases glucose clearance during prolonged exercise in humans. Am. J. Physiol. Endocrinol. Metab. 290, E60-E66.
53. Moates, J. M., Lacy, D. B., Goldstein, R. E., Cherrington, A. D. and Wasserman, D. H. (1988). Metabolic role of the exercise-induced increment in epinephrine in the dog. Am. J. Physiol. 255, E428-E436.
54. Morgan, H. E., Regen, D. M. and Park, C. R. (1964). Identification of a mobile carriermediated sugar transport system in muscle. J. Biol. Chem. 239, 369-374.
55. Mu, J., Brozinick, J. T., Valladares, O., Bucan, M. and Birnbaum, M. J. (2001). A role of AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell 7, 1085-1094.
56. O'Doherty, R. M., Bracy, D. P., Osawa, H., Wasserman, D. H. and Granner, D. K. (1994). Rat skeletal muscle hexokinase II mRNA and activity are increased by a single bout of acute exercise. Am. J. Physiol. 266, E171-E178.
57. O'Doherty, R. M., Bracy, D. P., Granner, D. K. and Wasserman, D. H. (1996). Transcription of the rat skeletal muscle hexokinase II gene is increased by acute exercise. J. Appl. Physiol. 81, 789-793.
58. O'Doherty, R. M., Halseth, A. E., Granner, D. K., Bracy, D. P. and Wasserman, D. H. (1998). Analysis of insulin-stimulated skeletal muscle glucose uptake in conscious rat using isotopic glucose analogs. Am. J. Physiol. 274, E287-E296.
59. Pendergrass, M., Koval, J., Vogt, C., Yki-Jarvinen, H., Iozzo, P., Pipek, R., Ardehali, H., Printz, R., Granner, D. K., DeFronzo, R. A. et al. (1998). Insulininduced hexokinase II expression is reduced in obesity and NIDDM. Diabetes 47, 387-394.
60. Petersen, H. A., Fueger, P. T., Bracy, D. P., Wasserman, D. H. and Halseth, A. E. (2003). Fiber type-specific determinants of Vmax for insulin-stimulated muscle glucose uptake in vivo. Am. J. Physiol. Endocrinol. Metab. 284, E541-E548.
61. Pilegaard, H., Osada, T., Andersen, L. T., Helge, J. W., Saltin, B. and Neufer, P. D. (2005). Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism 54, 1048-1055.
62. Ploug, T., Galbo, H. and Richter, E. A. (1984). Increased muscle glucose uptake during contractions: no need for insulin. Am. J. Physiol. 247, E726-E731.
63. Ploug, T., Galbo, H., Ohkuwa, T., Tranum-Jensen, J. and Vinten, J. (1992). Kinetics of glucose transport in rat skeletal muscle membrane vesicles: effects of insulin and contractions. Am. J. Physiol. 262, E700-E711.
64. Ren, J. M., Semenkovich, C. F., Gulve, E. A., Gao, J. and Holloszy, J. O. (1994). Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle. J. Biol. Chem. 269, 14396-14401.
65. Richardson, D. K., Kashyap, S., Bajaj, M., Cusi, K., Mandarino, S. J., Finlayson, J., DeFronzo, R. A., Jenkinson, C. P. and Mandarino, L. J. (2005). Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J. Biol. Chem. 280, 10290-10297.
66. Richter, E. A., Ploug, T. and Galbo, H. (1985). Increased muscle glucose uptake after exercise. No need for insulin during exercise. Diabetes 34, 1041-1048.
67. Richter, E. A., Jensen, P., Kiens, B. and Kristiansen, S. (1998). Sarcolemmal glucose transport and GLUT-4 translocation during exercise are diminished by endurance training. Am. J. Physiol. 274, E89-E95.
68. Roberts, T. J., Weber, J. M., Hoppeler, H., Weibel, E. R. and Taylor, C. R. (1996). Design of the oxygen and substrate pathways. II. Defining the upper limits of carbohydrate and fat oxidation. J. Exp. Biol. 199, 1651-1658.
69. Rosdahl, H., Lind, L., Millgard, J., Lithell, H., Ungerstedt, U. and Henriksson, J. (1998). Effect of physiological hyperinsulinemia on blood flow and interstitial glucose concentration in human skeletal muscle and adipose tissue studied by microdialysis. Diabetes 47, 1296-1301.
70. Sakamoto, K. and Goodyear, L. J. (2002). Intracellular signaling in contracting skeletal muscle. J. Appl. Physiol. 93, 369-383.
71. Shearer, J., Fueger, P. T., Bracy, D. P., Rottman, J. N., Clanton, J. A. and Wasserman, D. H. (2004). AMP Kinase-induced skeletal muscle glucose but not LCFA uptake is dependent on nitric oxide. Diabetes 53, 1429-1435.
72. Surwit, R. S., Kuhn, C. M., Cochrane, C., McCubbin, J. A. and Feinglos, M. N. (1988). Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37, 1163-1167.
73. Taylor, C. R., Weibel, E. R., Weber, J. M., Vock, R., Hoppeler, H., Roberts, T. J. and Brichon, G. (1996). Design of the oxygen and substrate pathways. I. Model and strategy to test symmorphosis in a network structure. J. Exp. Biol. 199, 1643-1649.
74. Vock, R., Hoppeler, H., Claassen, H., Wu, D. X., Billeter, R., Weber, J. M., Taylor, C. R. and Weibel, E. R. (1996a). Design of the oxygen and substrate pathways. VI. structural basis of intracellular substrate supply to mitochondria in muscle cells. J. Exp. Biol. 199, 1689-1697.
75. Vock, R., Weibel, E. R., Hoppeler, H., Ordway, G., Weber, J. M. and Taylor, C. R. (1996b). Design of the oxygen and substrate pathways. V. Structural basis of vascular substrate supply to muscle cells. J. Exp. Biol. 199, 1675-1688.
76. Wallberg-Henriksson, H. and Holloszy, J. O. (1985). Activation of glucose transport in diabetic muscle: responses to contraction and insulin. Am. J. Physiol. 249, C233-C237.
77. Wasserman, D. H. (1995). Regulation of glucose fluxes during exercise in the postabsorptive state. Annu. Rev. Physiol. 57, 191-218.
78. Wasserman, D. H. (2009). Four grams of glucose. Am J. Physiol. Endocrinol. Metab. 296, E11-E21.
79. Wasserman, D. H. and Halseth, A. E. (1998). An overview of muscle glucose uptake during exercise. Sites of regulation. Adv. Exp. Med. Biol. 441, 1-16.
80. Wasserman, D. H., Lickley, H. L. and Vranic, M. (1984). Interactions between glucagon and other counterregulatory hormones during normoglycemic and hypoglycemic exercise in dogs. J. Clin. Invest. 74, 1404-1413.
81. Wasserman, D. H., Lickley, H. L. and Vranic, M. (1985). Important role of glucagon during exercise in diabetic dogs. J. Appl. Physiol. 59, 1272-1281.
82. Wasserman, D. H., Spalding, J. A., Bracy, D., Lacy, D. B. and Cherrington, A. D. (1989a). Exercise-induced rise in glucagon and ketogenesis during prolonged muscular work. Diabetes 38, 799-807.
83. Wasserman, D. H., Spalding, J. A., Lacy, D. B., Colburn, C. A., Goldstein, R. E. and Cherrington, A. D. (1989b). Glucagon is a primary controller of hepatic glycogenolysis and gluconeogenesis during muscular work. Am. J. Physiol. 257, E108-E117.
84. Wasserman, D. H., Williams, P. E., Lacy, D. B., Goldstein, R. E. and Cherrington, A. D. (1989c). Exercise-induced fall in insulin and hepatic carbohydrate metabolism during muscular work. Am. J. Physiol. 256, E500-E509.
85. Wasserman, D. H., Williams, P. E., Lacy, D. B., Bracy, D. and Cherrington, A. D. (1990). Hepatic nerves are not essential to the increase in hepatic glucose production during muscular work. Am. J. Physiol. 259, E195-E203.
86. Wasserman, D. H., Geer, R. J., Rice, D. E., Bracy, D., Flakoll, P. J., Brown, L. L., Hill, J. O. and Abumrad, N. N. (1991). Interaction of exercise and insulin action in humans. Am. J. Physiol. 260, E37-E45.
87. Wasserman, D. H., Mohr, T., Kelly, P., Lacy, D. B. and Bracy, D. (1992). The impact of insulin-deficiency on glucose fluxes and muscle glucose metabolism during exercise. Diabetes 41, 1229-1238.
88. Wasserman, D. H., Lacy, D. B. and Bracy, D. P. (1993). Relationship between arterial and portal vein immunoreactive glucagon during exercise. J. Appl. Physiol. 75, 724-729.
89. Wasserman, K., Van Kessel, A. L. and Burton, G. G. (1967). Interaction of physiological mechanisms during exercise. J. Appl. Physiol. 22, 71-85.
90. Weber, J. M., Brichon, G., Zwingelstein, G., McClelland, G., Saucedo, C., Weibel, E. R. and Taylor, C. R. (1996a). Design of the oxygen and substrate pathways. IV. Partitioning energy provision from fatty acids. J. Exp. Biol. 199, 1667-1674.
91. Weber, J. M., Roberts, T. J., Vock, R., Weibel, E. R. and Taylor, C. R. (1996b). Design of the oxygen and substrate pathways. III. Partitioning energy provision from carbohydrates. J. Exp. Biol. 199, 1659-1666.
92. Weibel, E. R., Taylor, C. R. and Hoppeler, H. (1991). The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc. Natl. Acad. Sci. USA 88, 10357-10361.
93. Weibel, E. R., Taylor, C. R., Weber, J. M., Vock, R., Roberts, T. J. and Hoppeler, H. (1996). Design of the oxygen and substrate pathways. VII. Different structural limits for oxygen and substrate supply to muscle mitochondria. J. Exp. Biol. 199, 1699-1709.
94. Williams, K. V., Price, J. C. and Kelley, D. E. (2001). Interactions of impaired glucose transport and phosphorylation in skeletal muscle insulin resistance: a dose-response assessment using positron emission tomography. Diabetes 50, 2069-2079.
95. Witczak, C. A., Jessen, N., Warro, D. M., Toyoda, T., Fujii, N., Anderson, M. E., Hirshman, M. F. and Goodyear, L. J. (2010). CaMKII regulates contraction-but not insulin-induced glucose uptake in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 298, E1150-E1160.
96. Wolfe, R. R., Nadel, E. R., Shaw, J. H., Stephenson, L. A. and Wolfe, M. H. (1986). Role of changes in insulin and glucagon in glucose homeostasis in exercise. J. Clin. Invest. 77, 900-907.
97. Zierath, J. R., Houseknecht, K. L., Gnudi, L. and Kahn, B. B. (1997). High-fat feeding impairs insulin-stimulated GLUT4 recruitment via an early insulin-signaling defect. Diabetes 46, 215-223.
98. Zinker, B. A., Lacy, D. B., Bracy, D., Jacobs, J. and Wasserman, D. H. (1993a). Regulation of glucose uptake and metabolism by working muscle. An in vivo analysis. Diabetes 42, 956-965.
99. Zinker, B. A., Lacy, D. B., Bracy, D. P. and Wasserman, D. H. (1993b). Role of glucose and insulin loads to the exercising limbs in glucose uptake and metabolism. J. Appl. Physiol. 74, 2915-2921.