Increased skeletal muscle capillarization enhances insulin sensitivity.

Increased skeletal muscle capillarization is associated with improved glucose tolerance and insulin sensitivity. However, a possible causal relationship has not previously been identified. Therefore, we investigated whether increased skeletal muscle capillarization increases insulin sensitivity. Skeletal muscle-specific angiogenesis was induced by adding the α1-adrenergic receptor antagonist prazosin to the drinking water of Sprague-Dawley rats (n = 33), whereas 34 rats served as controls. Insulin sensitivity was measured ≥40 h after termination of the 3-wk prazosin treatment, which ensured that prazosin was cleared from the blood stream. Whole body insulin sensitivity was measured in conscious, unrestrained rats by hyperinsulinemic euglycemic clamp. Tissue-specific insulin sensitivity was assessed by administration of 2-deoxy-[(3)H]glucose during the plateau phase of the clamp. Whole body insulin sensitivity increased by ∼24%, and insulin-stimulated skeletal muscle 2-deoxy-[(3)H]glucose disposal increased by ∼30% concomitant with an ∼20% increase in skeletal muscle capillarization. Adipose tissue insulin sensitivity was not affected by the treatment. Insulin-stimulated muscle glucose uptake was enhanced independent of improvements in skeletal muscle insulin signaling to glucose uptake and glycogen synthesis, suggesting that the improvement in insulin-stimulated muscle glucose uptake could be due to improved diffusion conditions for glucose in the muscle. The prazosin treatment did not affect the rats on any other parameters measured. We conclude that an increase in skeletal muscle capillarization is associated with increased insulin sensitivity. These data point toward the importance of increasing skeletal muscle capillarization for prevention or treatment of type 2 diabetes.

[1]  D. Wasserman,et al.  Muscle-Specific Vascular Endothelial Growth Factor Deletion Induces Muscle Capillary Rarefaction Creating Muscle Insulin Resistance , 2013, Diabetes.

[2]  G. Shulman,et al.  On Diabetes: Insulin Resistance Cellular Mechanisms of Insulin Resistance , 2022 .

[3]  Masafumi Matsuda,et al.  beta-Cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. , 2005, The Journal of clinical endocrinology and metabolism.

[4]  S. Egginton,et al.  VEGF Trap Abolishes Shear Stress‐ and Overload‐Dependent Angiogenesis in Skeletal Muscle , 2006, Microcirculation.

[5]  J. Fluckey,et al.  Effect of exercise training on in vivo insulin-stimulated glucose uptake in intra-abdominal adipose tissue in rats. , 2000, American journal of physiology. Endocrinology and metabolism.

[6]  D. James,et al.  Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. , 1985, The American journal of physiology.

[7]  D. Hardie,et al.  AMPK activity and isoform protein expression are similar in muscle of obese subjects with and without type 2 diabetes. , 2004, American journal of physiology. Endocrinology and metabolism.

[8]  A. Ziada,et al.  The effect of long-term administration of alpha 1-blocker prazosin on capillary density in cardiac and skeletal muscle. , 1989, Pflugers Archiv : European journal of physiology.

[9]  E. Barrett,et al.  Insulin sensitivity of muscle capillary recruitment in vivo. , 2004, Diabetes.

[10]  T. Kodama,et al.  Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. , 2011, Cell metabolism.

[11]  C. G. Blomqvist,et al.  Hemodynamic and Neuroendocrine Responses to Acute and Chronic Alpha‐adrenergic Blockade with Prazosin and Phenoxybenzamine , 1983, Circulation.

[12]  M. Krotkiewski Physical training in the prophylaxis and treatment of obesity, hypertension and diabetes. , 1983, Scandinavian journal of rehabilitation medicine. Supplement.

[13]  P. Vollenweider,et al.  Insulin Resistance, Hyperlipidemia, and Hypertension in Mice Lacking Endothelial Nitric Oxide Synthase , 2001, Circulation.

[14]  Youngil Lee,et al.  Neutralization of tumor necrosis factor-alpha reverses insulin resistance in skeletal muscle but not adipose tissue. , 2004, American journal of physiology. Endocrinology and metabolism.

[15]  A. Baron,et al.  Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. , 2000, Diabetes.

[16]  R. DeFronzo,et al.  Effect of fatty acids on glucose production and utilization in man. , 1983, The Journal of clinical investigation.

[17]  P. Björntorp,et al.  Muscle Fiber Composition and Capillary Density in Women and Men With NIDDM , 1994, Diabetes Care.

[18]  Karim Bouzakri,et al.  Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. , 2005, Diabetes.

[19]  L. Byberg,et al.  Muscle morphology, self-reported physical activity and insulin resistance syndrome. , 2002, Acta physiologica Scandinavica.

[20]  M. Clark,et al.  Acute impairment of insulin-mediated capillary recruitment and glucose uptake in rat skeletal muscle in vivo by TNF-alpha. , 2000, Diabetes.

[21]  L. Westerkamp,et al.  Lower capillary density but no difference in VEGF expression in obese vs. lean young skeletal muscle in humans. , 2005, Journal of applied physiology.

[22]  J. Satoh,et al.  Modulation of tumor necrosis factor-α production with anti-hypertensive drugs , 2000 .

[23]  J. Satoh,et al.  Modulation of tumor necrosis factor-alpha production with anti-hypertensive drugs. , 2000, Immunopharmacology.

[24]  E. Barrett,et al.  Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. , 2003, American journal of physiology. Endocrinology and metabolism.

[25]  S. Egginton,et al.  Internal division of capillaries in rat skeletal muscle in response to chronic vasodilator treatment with α1-antagonist prazosin , 1998, Cell and Tissue Research.

[26]  P. Björntorp,et al.  Interstitial Muscle Insulin and Glucose Levels in Normal and Insulin-Resistant Zucker Rats , 1997, Diabetes.

[27]  O. Hudlická,et al.  Can changes in microcirculation explain capillary growth in skeletal muscle? , 1993, International journal of experimental pathology.

[28]  J. Olefsky,et al.  Kinetics of Insulin Action In Vivo: Identification of Rate-Limiting Steps , 1995, Diabetes.

[29]  C. Berne,et al.  Application of prazosin is associated with an increase of insulin sensitivity in obese patients with hypertension , 1988, Diabetologia.

[30]  T. Skalak,et al.  Chronic Vasodilation Induces Matrix Metalloproteinase 9 (MMP‐9) Expression during Microvascular Remodeling in Rat Skeletal Muscle , 2001, Microcirculation.

[31]  B. Pedersen,et al.  Glucose ingestion during endurance training in men attenuates expression of myokine receptor , 2009, Experimental physiology.

[32]  T. Keeton,et al.  The differential effects of prazosin and hydralazine on sympathoadrenal activity in conscious rats. , 1989, European journal of pharmacology.

[33]  E. Barrett,et al.  Obesity Blunts Insulin-Mediated Microvascular Recruitment in Human Forearm Muscle , 2006, Diabetes.

[34]  J. Passonneau,et al.  A comparison of three methods of glycogen measurement in tissues. , 1974, Analytical biochemistry.

[35]  M. Rawlins,et al.  Prazosin, pharmacokinetics and concentration effect , 1979, European Journal of Clinical Pharmacology.

[36]  R. Bergman,et al.  Direct Administration of Insulin Into Skeletal Muscle Reveals That the Transport of Insulin Across the Capillary Endothelium Limits the Time Course of Insulin to Activate Glucose Disposal , 2008, Diabetes.

[37]  J. Treebak,et al.  Identification of a novel phosphorylation site on TBC1D4 regulated by AMP-activated protein kinase in skeletal muscle. , 2010, American journal of physiology. Cell physiology.

[38]  H. Lithell,et al.  Metabolic effects of doxazosin and enalapril in hypertriglyceridemic, hypertensive men. Relationship to changes in skeletal muscle blood flow. , 1996, American journal of hypertension.

[39]  L. Strindberg,et al.  Estimations of muscle interstitial insulin, glucose, and lactate in type 2 diabetic subjects. , 2000, American journal of physiology. Endocrinology and metabolism.

[40]  J. Wojtaszewski,et al.  Effects of Endurance Exercise Training on Insulin Signaling in Human Skeletal Muscle , 2007, Diabetes.

[41]  C Bogardus,et al.  Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. , 1987, The Journal of clinical investigation.

[42]  A. Pries,et al.  Endothelial NOS is main mediator for shear stress-dependent angiogenesis in skeletal muscle after prazosin administration. , 2004, American journal of physiology. Heart and circulatory physiology.

[43]  P. Björntorp,et al.  Physical training in obese women , 1984, European Journal of Applied Physiology and Occupational Physiology.

[44]  K. Tyml,et al.  Capillary adrenoceptors in rat skeletal muscle. , 1997, Microvascular research.

[45]  L. Lönn,et al.  Delayed transcapillary transport of insulin to muscle interstitial fluid in obese subjects. , 2002, Diabetes.

[46]  E. Barrett,et al.  Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. , 2004, Diabetes.

[47]  A. Ziada,et al.  The effect of long-term administration of α1-blocker prazosin on capillary density in cardiac and skeletal muscle , 1989, Pflügers Archiv.

[48]  J. Wojtaszewski,et al.  Exercise-induced AMPK activity in skeletal muscle: Role in glucose uptake and insulin sensitivity , 2013, Molecular and Cellular Endocrinology.

[49]  J. Kirwan,et al.  Progressive hyperglycemia across the glucose tolerance continuum in older obese adults is related to skeletal muscle capillarization and nitric oxide bioavailability. , 2011, The Journal of clinical endocrinology and metabolism.

[50]  B. Hansen,et al.  Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. , 2000, Diabetes.

[51]  F. Curry,et al.  Microvascular permeability. , 1999, Physiological reviews.

[52]  F. Thong,et al.  The Rab GTPase-Activating Protein AS160 Integrates Akt, Protein Kinase C, and AMP-Activated Protein Kinase Signals Regulating GLUT4 Traffic , 2007, Diabetes.

[53]  Zlatko Trajanoski,et al.  Assessment of transcapillary glucose exchange in human skeletal muscle and adipose tissue. , 2003, American journal of physiology. Endocrinology and metabolism.

[54]  O. Hudlická,et al.  The effects of long term administration of prazosin on the microcirculation in skeletal muscles. , 1989, Cardiovascular research.

[55]  C. Cobelli,et al.  In vivo glucose metabolism in the awake rat: tracer and insulin clamp studies. , 1987, Metabolism: clinical and experimental.

[56]  G. Reaven,et al.  Disparate effects of prazosin and propranolol on lipid metabolism in a rat model. , 1983, The American journal of medicine.

[57]  Yunan Tang,et al.  Overexpression of Endothelial Nitric Oxide Synthase Prevents Diet-Induced Obesity and Regulates Adipocyte Phenotype , 2012, Circulation research.

[58]  G. Pagano,et al.  Alpha 1-blocker doxazosin improves peripheral insulin sensitivity in diabetic hypertensive patients. , 1995, Metabolism: clinical and experimental.