Obesity, Insulin Resistance, and Capillary Recruitment

REFERENCES

• The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993; 329: 977–986
   PubMed Web of Science ®Google Scholar
• United Kingdom Prospective Diabetes Study (UKPDS). 13: Relative efficacy of randomly allocated diet, sulphonylurea, insulin, or metformin in patients with newly diagnosed non-insulin dependent diabetes followed for three years. Br Med J 1995; 310: 83–88
   PubMed Web of Science ®Google Scholar
• Abbink-Zandbergen E J, Vervoort G, Tack C J, Lutterman J A, Schaper N C, Smits P. The role of adenosine in insulin-induced vasodilation. J Cardiovasc Pharmacol 1999; 34: 374–380
   Google Scholar
• Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999; 257: 79–83
   PubMed Web of Science ®Google Scholar
• Baron A D. Hemodynamic actions of insulin. Am J Physiol 1994; 267: E187–E202
   PubMed Web of Science ®Google Scholar
• Baron A D, Laakso M, Brechtel G, Edelman S V. Mechanism of insulin resistance in insulin-dependent diabetes mellitus: a major role for reduced skeletal muscle blood flow. J Clin Endocrinol Metab 1991; 73: 637–643
   PubMed Web of Science ®Google Scholar
• Baron A D, Laakso M, Brechtel G, Edelman S V. Reduced capacity and affinity of skeletal muscle for insulin-mediated glucose uptake in noninsulin-dependent diabetic subjects. J Clin Invest 1991; 87: 1186–1194
   PubMed Web of Science ®Google Scholar
• Boden G, Shulman G I. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur J Clin Invest 2002; 32: 14–23
   PubMed Web of Science ®Google Scholar
• Bradley E A, Clark M G, Rattigan S. Acute effects of wortmannin on insulin's hemodynamic and metabolic actions in vivo. Am J Physiol Endocrinol Metab 2007; 292: E779–787
   Google Scholar
• Ceddia R B, Somwar R, Maida A, Fang X, Bikopoulos G, Sweeney G. Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 2005; 48: 132–139
   PubMed Web of Science ®Google Scholar
• Cersosimo E, Defronzo R A. Insulin resistance and endothelial dysfunction: the road map to cardiovascular diseases. Diabetes Metab Res Rev 2006; 22: 423–436
   PubMed Web of Science ®Google Scholar
• Chen H, Montagnani M, Funahashi T, Shimomura I, Quon M J. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 2003; 278: 45021–45026
   PubMed Web of Science ®Google Scholar
• Chen Y L, Messina E J. Dilation of isolated skeletal muscle arterioles by insulin is endothelium dependent and nitric oxide mediated. Am J Physiol 1996; 270: H2120–H2124
   PubMed Web of Science ®Google Scholar
• Clark M G, Barrett E J, Wallis M G, Vincent M A, Rattigan S. The microvasculature in insulin resistance and type 2 diabetes. Semin Vasc Med 2002; 2: 21–31
   Google Scholar
• Clark M G, Wallis M G, Barrett E J, Vincent M A, Richards S M, Clerk L H, Rattigan S. Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 2003; 284: E241–E258
   PubMed Web of Science ®Google Scholar
• Clerk L H, Rattigan S, Clark M G. Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 2002; 51: 1138–1145
   PubMed Web of Science ®Google Scholar
• Clerk L H, Vincent M A, Jahn L A, Liu Z, Lindner J R, Barrett E J. Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 2006; 55: 1436–1442
   PubMed Web of Science ®Google Scholar
• Clerk L H, Vincent M A, Lindner J R, Clark M G, Rattigan S, Barrett E J. The vasodilatory actions of insulin on resistance and terminal arterioles and their impact on muscle glucose uptake. Diabetes Metab Res Rev 2004; 20: 3–12
   PubMed Web of Science ®Google Scholar
• Coggins M, Lindner J, Rattigan S, Jahn L, Fasy E, Kaul S, Barrett E. Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 2001; 50: 2682–2690
   PubMed Web of Science ®Google Scholar
• Combs T P, Berg A H, Obici S, Scherer P E, Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest 2001; 108: 1875–1881
   PubMed Web of Science ®Google Scholar
• Crettaz M, Prentki M, Zaninetti D, Jeanrenaud B. Insulin resistance in soleus muscle from obese Zucker rats. Biochem J 1980; 186: 525–534
   PubMed Web of Science ®Google Scholar
• Dawson D, Vincent M A, Barrett E J, Kaul S, Clark A, Leong-Poi H, Lindner J R. Vascular recruitment in skeletal muscle during exercise and hyperinsulinemia assessed by contrast ultrasound. Am J Physiol Endocrinol Metab 2002; 282: E714–E720
   PubMed Web of Science ®Google Scholar
• Dohm G L, Tapscott E B, Pories W J, Dabbs D J, Flickinger E G, Meelheim D, Fushiki T, Atkinson S M, Elton C W, Caro J F. An in vitro human muscle preparation suitable for metabolic studies: decreased insulin stimulation of glucose transport in muscle from morbidly obese and diabetic subjects. J Clin Invest 1988; 82: 486–494
   PubMed Web of Science ®Google Scholar
• Engler M M, Engler M B, Malloy M J, Chiu E Y, Schloetter M C, Paul S M, Stuehlinger M, Lin K Y, Cooke J P, Morrow J D, Ridker P M, Rifai N, Miller E, Witztum J L, Mietus-Snyder M. Antioxidant vitamins C and E improve endothelial function in children with hyperlipidemia: Endothelial Assessment of Risk from Lipids in Youth (EARLY) Trial. Circulation 2003; 108: 1059–1063
   PubMed Web of Science ®Google Scholar
• Eringa E C, Stehouwer C D, Merlijn T, Westerhof N, Sipkema P. Physiological concentrations of insulin induce endothelin-mediated vasoconstriction during inhibition of NOS or PI3-kinase in skeletal muscle arterioles. Cardiovasc Res 2002; 56: 464–471
   PubMed Web of Science ®Google Scholar
• Fitzgerald S M, Kemp-Harper B K, Tare M, Parkington H C. Role of endothelium-derived hyperpolarizing factor in endothelial dysfunction during diabetes. Clin Exp Pharmacol Physiol 2005; 32: 482–487
   Google Scholar
• Fruebis J, Tsao T S, Javorschi S, Ebbets-Reed D, Erickson M R, Yen F T, Bihain B E, Lodish H F. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 2001; 98: 2005–2010
   PubMed Web of Science ®Google Scholar
• Grasby D J, Morris J L, Segal S S. Heterogeneity of vascular innervation in hamster cheek pouch and retractor muscle. J Vasc Res 1999; 36: 465–476
   Google Scholar
• Hamdy O. Lifestyle modification and endothelial function in obese subjects. Expert Rev Cardiovasc Ther 2005; 3: 231–241
   PubMedGoogle Scholar
• Henry R R, Abrams L, Nikoulina S, Ciaraldi T P. Insulin action and glucose metabolism in nondiabetic control and NIDDM subjects: comparison using human skeletal muscle cell cultures. Diabetes 1995; 44: 936–946
   PubMed Web of Science ®Google Scholar
• Hojlund K, Frystyk J, Levin K, Flyvbjerg A, Wojtaszewski J F, Beck-Nielsen H. Reduced plasma adiponectin concentrations may contribute to impaired insulin activation of glycogen synthase in skeletal muscle of patients with type 2 diabetes. Diabetologia 2006; 49: 1283–1291
   PubMed Web of Science ®Google Scholar
• Hundal H S, Marette A, Mitsumoto Y, Ramlal T, Blostein R, Klip A. Insulin induces translocation of the alpha2 and beta1 subunits of the Na+/ K+-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle. J Biol Chem 1992; 267: 5040–5043
   PubMedGoogle Scholar
• Kahn A M, Song T. Insulin inhibits dog vascular smooth muscle contraction and lowers Ca2+i by inhibiting Ca2+ influx. J Nutr 1995; 125: 1732S–1737S
   Google Scholar
• Kern P A, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 2001; 280: E745–E751
   PubMed Web of Science ®Google Scholar
• Kim J A, Montagnani M, Koh K K, Quon M J. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 2006; 113: 1888–1904
   PubMed Web of Science ®Google Scholar
• Kobayashi H, Ouchi N, Kihara S, Walsh K, Kumada M, Abe Y, Funahashi T, Matsuzawa Y. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res 2004; 94: e27–e31
   PubMed Web of Science ®Google Scholar
• Kraegen E W, Cooney G J, Ye J, Thompson A L. Triglycerides, fatty acids and insulin resistance–hyperinsulinemia. Exp Clin Endocrinol Diabetes 2001; 109: S516–S526
   Google Scholar
• Laakso M, Edelman S V, Brechtel G, Baron A D. Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man. J Clin Invest 1990; 85: 1844–1852
   PubMed Web of Science ®Google Scholar
• Lau D C, Dhillon B, Yan H, Szmitko P E, Verma S. Adipokines: molecular links between obesity and atheroslcerosis. Am J Physiol Heart Circ Physiol 2005; 288: H2031–H2041
   PubMed Web of Science ®Google Scholar
• Leahy J L. Pathogenesis of type 2 diabetes mellitus. Arch Med Res 2005; 36: 197–209
   PubMed Web of Science ®Google Scholar
• LeBrasseur N K, Ruderman N B. Why might thiazolidinediones increase exercise capacity in patients with type 2 diabetes?. Diabetes Care 2005; 28: 2975–2977
   Google Scholar
• Mahajan H, Richards S M, Rattigan S, Clark M G. Local methacholine but not bradykinin potentiates insulin-mediated glucose uptake in muscle in vivo by augmenting capillary recruitment. Diabetologia 2004; 47: 2226–2234
   Google Scholar
• Moore R D. Stimulation of Na:H exchange by insulin. Biophys J 1981; 33: 203–210
   PubMed Web of Science ®Google Scholar
• Natali A, Bonadonna R, Santoro D, Galvan A Q, Baldi S, Frascerra S, Palombo C, Ghione S, Ferrannini E. Insulin resistance and vasodilation in essential hypertension: studies with adenosine. J Clin Invest 1994; 94: 1570–1576
   PubMed Web of Science ®Google Scholar
• Nawrocki A R, Rajala M W, Tomas E, Pajvani U B, Saha A K, Trumbauer M E, Pang Z, Chen A S, Ruderman N B, Chen H, Rossetti L, Scherer P E. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem 2006; 281: 2654–2660
   PubMed Web of Science ®Google Scholar
• Nolte L A, Hansen P A, Chen M M, Schluter J M, Gulve E A, Holloszy J O. Short-term exposure to tumor necrosis factor-alpha does not affect insulin-stimulated glucose uptake in skeletal muscle. Diabetes 1998; 47: 721–726
   Google Scholar
• Ohashi K, Kihara S, Ouchi N, Kumada M, Fujita K, Hiuge A, Hibuse T, Ryo M, Nishizawa H, Maeda N, Maeda K, Shibata R, Walsh K, Funahashi T, Shimomura I. Adiponectin replenishment ameliorates obesity-related hypertension. Hypertension 2006; 47: 1108–1116
   PubMed Web of Science ®Google Scholar
• Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 2004; 279: 1304–1309
   PubMed Web of Science ®Google Scholar
• Ouchi N, Ohishi M, Kihara S, Funahashi T, Nakamura T, Nagaretani H, Kumada M, Ohashi K, Okamoto Y, Nishizawa H, Kishida K, Maeda N, Nagasawa A, Kobayashi H, Hiraoka H, Komai N, Kaibe M, Rakugi H, Ogihara T, Matsuzawa Y. Association of hypoadiponectinemia with impaired vasoreactivity. Hypertension 2003; 42: 231–234
   PubMed Web of Science ®Google Scholar
• Pajvani U B, Hawkins M, Combs T P, Rajala M W, Doebber T, Berger J P, Wagner J A, Wu M, Knopps A, Xiang A H, Utzschneider K M, Kahn S E, Olefsky J M, Buchanan T A, Scherer P E. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem 2004; 279: 12152–12162
   PubMed Web of Science ®Google Scholar
• Plum L, Schubert M, Bruning J C. The role of insulin receptor signaling in the brain. Trends Endocrinol Metab 2005; 16: 59–65
   PubMed Web of Science ®Google Scholar
• Randriamboavonjy V, Schrader J, Busse R, Fleming I. Insulin induces the release of vasodilator compounds from platelets by a nitric oxide-G kinase-VAMP-3-dependent pathway. J Exp Med 2004; 199: 347–356
   PubMed Web of Science ®Google Scholar
• Rattigan S, Clark M G, Barrett E J. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 1997; 46: 1381–1388
   PubMedGoogle Scholar
• Rattigan S, Clark M G, Barrett E J. Acute vasoconstriction-induced insulin resistance in rat muscle in vivo. Diabetes 1999; 48: 564–569
   PubMed Web of Science ®Google Scholar
• Rattigan S, Zhang L, Mahajan H, Kolka C M, Richards S M, Clark M G. Factors influencing the hemodynamic and metabolic effects of insulin in muscle. Curr Diab Rev 2006; 2: 61–70
   Google Scholar
• Reaven G M. Pathophysiology of insulin resistance in human disease. Physiol Rev 1995; 75: 473–486
   PubMed Web of Science ®Google Scholar
• Sarabi M, Lind L, Millgard J, Hanni A, Hagg A, Berne C, Lithell H. Local vasodilatation with metacholine, but not with nitroprusside, increases forearm glucose uptake. Physiol Res 1999; 48: 291–295
   Google Scholar
• Schalkwijk C G, Stehouwer C D. Vascular complications in diabetes mellitus: the role of endothelial dysfunction. Clin Sci 2005; 109: 143–159
   PubMed Web of Science ®Google Scholar
• Schroeder C AJ, Chen Y L, Messina E J. Inhibition of NO synthesis or endothelium removal reveals a vasoconstrictor effect of insulin on isolated arterioles. Am J Physiol 1999; 276: H815–H820
   Google Scholar
• Serne E H, IJzerman R G, Gans R O, Nijveldt R, De Vries G, Evertz R, Donker A J, Stehouwer C D. Direct evidence for insulin-induced capillary recruitment in skin of healthy subjects during physiological hyperinsulinemia. Diabetes 2002; 51: 1515–1522
   PubMed Web of Science ®Google Scholar
• Shetty G K, Economides P A, Horton E S, Mantzoros C S, Veves A. Circulating adiponectin and resistin levels in relation to metabolic factors, inflammatory markers, and vascular reactivity in diabetic patients and subjects at risk for diabetes. Diabetes Care 2004; 27: 2450–2457
   PubMed Web of Science ®Google Scholar
• Shibata R, Ouchi N, Kihara S, Sato K, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis in response to tissue ischemia through stimulation of amp-activated protein kinase signaling. J Biol Chem 2004; 279: 28670–28674
   PubMed Web of Science ®Google Scholar
• Shklyaev S, Aslanidi G, Tennant M, Prima V, Kohlbrenner E, Kroutov V, Campbell-Thompson M, Crawford J, Shek E W, Scarpace P J, Zolotukhin S. Sustained peripheral expression of transgene adiponectin offsets the development of diet-induced obesity in rats. Proc Natl Acad Sci U S A 2003; 100: 14217–14222
   PubMed Web of Science ®Google Scholar
• Steinberg H O, Brechtel G, Johnson A, Fineberg N, Baron A D. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent: a novel action of insulin to increase nitric oxide release. J Clin Invest 1994; 94: 1172–1179
   PubMed Web of Science ®Google Scholar
• Steppan C M, Lazar M A. The current biology of resistin. J Intern Med 2004; 255: 439–447
   PubMed Web of Science ®Google Scholar
• Vicent D, Ilany J, Kondo T, Naruse K, Fisher S J, Kisanuki Y Y, Bursell S, Yanagisawa M, King G L, Kahn C R. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest 2003; 111: 1373–1380
   PubMedGoogle Scholar
• Vincent M A, Barrett E J, Lindner J R, Clark M G, Rattigan S. Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 2003; 285: E123–E129
   PubMed Web of Science ®Google Scholar
• Vincent M A, Clerk L H, Lindner J R, Klibanov A L, Clark M G, Rattigan S, Barrett E J. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 2004; 53: 1418–1423
   PubMed Web of Science ®Google Scholar
• Vincent M A, Clerk L H, Lindner J R, Price W J, Jahn L A, Leong-Poi H, Barrett E J. Mixed meal and light exercise each recruit muscle capillaries in healthy humans. Am J Physiol Endocrinol Metab 2006; 290: E1191–E1197
   PubMed Web of Science ®Google Scholar
• Vincent M A, Dawson D, Clark A D, Lindner J R, Rattigan S, Clark M G, Barrett E J. Skeletal muscle microvascular recruitment by physiological hyperinsulinemia precedes increases in total blood flow. Diabetes 2002; 51: 42–48
   PubMed Web of Science ®Google Scholar
• Vincent M A, Montagnani M, Quon M J. Molecular and physiologic actions of insulin related to production of nitric oxide in vascular endothelium. Curr Diab Rep 2003; 3: 279–288
   PubMedGoogle Scholar
• Visscher T L, Seidell J C. The public health impact of obesity. Annu Rev Public Health 2001; 22: 355–375
   PubMed Web of Science ®Google Scholar
• Wallis M G, Wheatley C M, Rattigan S, Barrett E J, Clark A D, Clark M G. Insulin-mediated hemodynamic changes are impaired in muscle of Zucker obese rats. Diabetes 2002; 51: 3492–3498
   PubMed Web of Science ®Google Scholar
• Wei K, Jayaweera A R, Firoozan S, Linka A, Skyba D M, Kaul S. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 1998; 97: 473–483
   PubMed Web of Science ®Google Scholar
• Wei K, Skyba D M, Firschke C, Jayaweera A R, Lindner J R, Kaul S. Interactions between microbubbles and ultrasound: in vitro and in vivo observations. J Am Coll Cardiol 1997; 29: 1081–1088
   PubMed Web of Science ®Google Scholar
• Wheatley C M, Rattigan S, Richards S M, Barrett E J, Clark M G. Skeletal muscle contraction stimulates capillary recruitment and glucose uptake in insulin-resistant obese Zucker rats. Am J Physiol Endocrinol Metab 2004; 287: E804–E809
   PubMed Web of Science ®Google Scholar
• Xi W, Satoh H, Kase H, Suzuki K, Hattori Y. Stimulated HSP90 binding to eNOS and activation of the PI3-Akt pathway contribute to globular adiponectin-induced NO production: vasorelaxation in response to globular adiponectin. Biochem Biophys Res Commun 2005; 332: 200–205
   PubMed Web of Science ®Google Scholar
• Yamauchi T, Kamon J, Waki H, Imai Y, Shimozawa N, Hioki K, Uchida S, Ito Y, Takakuwa K, Matsui J, Takata M, Eto K, Terauchi Y, Komeda K, Tsunoda M, Murakami K, Ohnishi Y, Naitoh T, Yamamura K, Ueyama Y, Froguel P, Kimura S, Nagai R, Kadowaki T. Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J Biol Chem 2003; 278: 2461–2468
   PubMed Web of Science ®Google Scholar
• Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman M L, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 2001; 7: 941–946
   PubMed Web of Science ®Google Scholar
• Yki-Jarvinen H, Utriainen T. Insulin-induced vasodilatation: physiology or pharmacology?. Diabetologia 1998; 41: 369–379
   PubMed Web of Science ®Google Scholar
• Youd J M, Rattigan S, Clark M G. Acute impairment of insulin-mediated capillary recruitment and glucose uptake in rat skeletal muscle in vivo by TNFa. Diabetes 2000; 49: 1904–1909
   PubMed Web of Science ®Google Scholar
• Yudkin J S, Eringa E, Stehouwer C D. “Vasocrine” signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet 2005; 365: 1817–1820
   PubMed Web of Science ®Google Scholar
• Zemel M B, Johnson B A, Ambrozy S A. Insulin-stimulated vascular relaxation role of Ca2+-ATPase. Am J Hypertens 1992; 5: 637–641
   PubMed Web of Science ®Google Scholar
• Zhang L, Vincent M A, Richards S M, Clerk L H, Rattigan S, Clark M G, Barrett E J. Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 2004; 53: 447–453
   PubMed Web of Science ®Google Scholar
• Zhang L, Wheatley C M, Richards S M, Barrett E J, Clark M G, Rattigan S. TNF-alpha acutely inhibits vascular effects of physiological but not high insulin or contraction. Am J Physiol Endocrinol Metab 2003; 285: E654–E660
   Web of Science ®Google Scholar
• Zimmet P, Alberti K G, Shaw J. Global and societal implications of the diabetes epidemic. Nature 2001; 414: 782–787
   PubMed Web of Science ®Google Scholar