Impaired Coronary Microvascular Dilation Correlates with Enhanced Vascular Smooth Muscle MLC Phosphorylation in Diabetes

References

• Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 1996; 271: 20246–20249
   PubMed Web of Science ®Google Scholar
• Ammar RF, Jr, Gutterman DD, Brooks LA, Dellsperger KC. Impaired dilation of coronary arterioles during increases in myocardial O2 consumption with hyperglycemia. Am J Physiol Endocrinol Metab 2000; 279: E868–E874
   Web of Science ®Google Scholar
• Bender SB, Klabunde RE. Altered role of smooth muscle endothelin receptors in coronary endothelin-1 and {alpha}1-adrenoceptor-mediated vasoconstriction in type 2 diabetes. Am J Physiol Heart Circ Physiol 2007; 293: H2281–H2288
   PubMed Web of Science ®Google Scholar
• Boodhwani M, Sodha NR, Mieno S, Xu SH, Feng J, Ramlawi B, Clements RT, Sellke FW. Functional, cellular, and molecular characterization of the angiogenic response to chronic myocardial ischemia in diabetes. Circulation 2007; 116: I31–I37
   PubMed Web of Science ®Google Scholar
• Britten MB, Zeiher AM, Schachinger V. Clinical importance of coronary endothelial vasodilator dysfunction and therapeutic options. J Intern Med 1999; 245: 315–327
   PubMed Web of Science ®Google Scholar
• Brooks BA, Franjic B, Ban CR, Swaraj K, Yue DK, Celermajer DS, Twigg SM. Diastolic dysfunction and abnormalities of the microcirculation in type 2 diabetes. Diab Obes Metab 2007; 10: 739–746
   Google Scholar
• Brooks BA, McLennan SV, Twigg SM, Yue DK. Detection and characterisation of microcirculatory abnormalities in the skin of diabetic patients with microvascular complications. Diab Vasc Dis Res 2008; 5: 30–35
   Google Scholar
• Browner NC, Dey NB, Bloch KD, Lincoln TM. Regulation of cGMP-dependent protein kinase expression by soluble guanylyl cyclase in vascular smooth muscle cells. J Biol Chem 2004; 279: 46631–46636
   Google Scholar
• Chakraphan D, Sridulyakul P, Thipakorn B, Bunnag S, Huxley VH, Patumraj S. Attenuation of endothelial dysfunction by exercise training in STZ-induced diabetic rats. Clin Hemorheol Microcirc 2005; 32: 217–226
   Google Scholar
• Chang S, Hypolite JA, DiSanto ME, Changolkar A, Wein AJ, Chacko S. Increased basal phosphorylation of detrusor smooth muscle myosin in alloxan-induced diabetic rabbit is mediated by upregulation of Rho-kinase beta and CPI-17. Am J Physiol Renal Physiol 2006; 290: F650–F656
   PubMedGoogle Scholar
• Clements RT, Minnear FL, Singer HA, Keller RS, Vincent PA. RhoA and Rho-kinase dependent and independent signals mediate TGF-beta-induced pulmonary endothelial cytoskeletal reorganization and permeability. Am J Physiol Lung Cell Mol Physiol 2005; 288: L294–L306
   Google Scholar
• Clements RT, Sodha NR, Feng J, Mieno S, Boodhwani M, Ramlawi B, Bianchi C, Sellke FW. Phosphorylation and translocation of heat shock protein 27 and alphaB-crystallin in human myocardium after cardioplegia and cardiopulmonary bypass. J Thorac Cardiovasc Surg 2007; 134: 1461–1470
   Google Scholar
• Clough GF, Bennett AR, Church MK. Measurement of nitric oxide concentration in human skin in vivo using dermal microdialysis. Exp Physiol 1998; 83: 431–434
   PubMed Web of Science ®Google Scholar
• Di Carli MF, Janisse J, Grunberger G, Ager J. Role of chronic hyperglycemia in the pathogenesis of coronary microvascular dysfunction in diabetes. J Am Coll Cardiol 2003; 41: 1387–1393
   PubMedGoogle Scholar
• Gatenby PA. The role of complement in the aetiopathogenesis of systemic lupus erythematosus. Autoimmunity 1991; 11: 61–66
   Web of Science ®Google Scholar
• Goodfellow J. Microvascular heart disease in diabetes mellitus. Diabetologia 1997; 40(Suppl 2)S130–S133
   Google Scholar
• Heitzer T, Krohn K, Albers S, Meinertz T. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with type II diabetes mellitus. Diabetologia 2000; 43: 1435–1438
   PubMed Web of Science ®Google Scholar
• Hofmann F. The biology of cyclic GMP-dependent protein kinases. J Biol Chem 2005; 280: 1–4
   PubMed Web of Science ®Google Scholar
• Hsueh WA, Quinones MJ. Role of endothelial dysfunction in insulin resistance. Am J Cardiol 2003; 92: 10–17
   PubMed Web of Science ®Google Scholar
• Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, Creager MA. Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 1993; 88: 2510–2516
   PubMed Web of Science ®Google Scholar
• Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) [see comments]. Science 1996; 273: 245–248
   PubMed Web of Science ®Google Scholar
• Koltai MZ, Hadhazy P, Posa I, Kocsis E, Winkler G, Rosen P, Pogatsa G. Characteristics of coronary endothelial dysfunction in experimental diabetes. Cardiovasc Res 1997; 34: 157–163
   Google Scholar
• Lee JH, Ragolia L. AKT phosphorylation is essential for insulin-induced relaxation of rat vascular smooth muscle cells. Am J Physiol Cell Physiol 2006; 291: C1355–C1365
   PubMed Web of Science ®Google Scholar
• Liu S, Ma X, Gong M, Shi L, Lincoln T, Wang S. Glucose down-regulation of cGMP-dependent protein kinase I expression in vascular smooth muscle cells involves NAD(P)H oxidase-derived reactive oxygen species. Free Rad Biol Med 2007; 42: 852–863
   PubMed Web of Science ®Google Scholar
• McVeigh GE, Brennan GM, Johnston GD, McDermott BJ, McGrath LT, Henry WR, Andrews JW, Hayes JR. Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1992; 35: 771–776
   PubMed Web of Science ®Google Scholar
• Milsom AB, Jones CJ, Goodfellow J, Frenneaux MP, Peters JR, James PE. Abnormal metabolic fate of nitric oxide in type I diabetes mellitus. Diabetologia 2002; 45: 1515–1522
   Google Scholar
• Miura H, Wachtel RE, Loberiza FR, Jr, Saito T, Miura M, Nicolosi AC, Gutterman DD. Diabetes mellitus impairs vasodilation to hypoxia in human coronary arterioles: reduced activity of ATP-sensitive potassium channels. Circ Res 2003; 92: 151–158
   PubMed Web of Science ®Google Scholar
• Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr Rev 2007; 28: 463–491
   PubMed Web of Science ®Google Scholar
• Munzel T, Daiber A, Ullrich V, Mulsch A. Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase. Arterioscler Thromb Vasc Biol 2005; 25: 1551–1557
   PubMed Web of Science ®Google Scholar
• Nahser PJ, Jr, Brown RE, Oskarsson H, Winniford MD, Rossen JD. Maximal coronary flow reserve and metabolic coronary vasodilation in patients with diabetes mellitus. Circulation 1995; 91: 635–640
   PubMedGoogle Scholar
• Nakamura M, Ichikawa K, Ito M, Yamamori B, Okinaka T, Isaka N, Yoshida Y, Fujita S, Nakano T. Effects of the phosphorylation of myosin phosphatase by cyclic GMP-dependent protein kinase. Cell Sign 1999; 11: 671–676
   Google Scholar
• Natali A, Toschi E, Baldeweg S, Casolaro A, Baldi S, Sironi AM, Yudkin JS, Ferrannini E. Haematocrit, type 2 diabetes, and endothelium-dependent vasodilatation of resistance vessels. Eur Heart J 2005; 26: 464–471
   PubMed Web of Science ®Google Scholar
• Nitenberg A, Valensi P, Sachs R, Dali M, Aptecar E, Attali JR. Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes 1993; 42: 1017–1025
   PubMed Web of Science ®Google Scholar
• Noda M, Yasuda-Fukazawa C, Moriishi K, Kato T, Okuda T, Kurokawa K, Takuwa Y. Involvement of rho in GTPgammaS-induced enhancement of phosphorylation of 20 kDa myosin light chain in vascular smooth muscle cells: inhibition of phosphatase activity. FEBS Lett 1995; 367: 246–250
   Web of Science ®Google Scholar
• Pfitzer G. Invited review: regulation of myosin phosphorylation in smooth muscle. J Appl Physiol 2001; 91: 497–503
   PubMed Web of Science ®Google Scholar
• Prior JO, Quinones MJ, Hernandez-Pampaloni M, Facta AD, Schindler TH, Sayre JW, Hsueh WA, Schelbert HR. Coronary circulatory dysfunction in insulin resistance, impaired glucose tolerance, and type 2 diabetes mellitus. Circulation 2005; 111: 2291–2298
   PubMedGoogle Scholar
• Sanz E, Fernandez N, Monge L, Martinez MA, Climent B, Dieguez G, Garcia-Villalon AL. Effects of diabetes on the vascular response to nitric oxide and constrictor prostanoids: gender and regional differences. Life Sci 2003; 72: 1537–1547
   PubMed Web of Science ®Google Scholar
• Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000; 101: 1899–1906
   PubMed Web of Science ®Google Scholar
• Simonsen U, Wadsworth RM, Buus NH, Mulvany MJ. In vitro simultaneous measurements of relaxation and nitric oxide concentration in rat superior mesenteric artery. J Physiol 1999; 516: 271–282
   Google Scholar
• Su X, Changolkar A, Chacko S, Moreland RS. Diabetes decreases rabbit bladder smooth muscle contraction while increasing levels of myosin light chain phosphorylation. Am. J Physiol Renal Physiol 2004; 287: F690–F699
   Google Scholar
• Sundell J, Laine H, Nuutila P, Ronnemaa T, Luotolahti M, Raitakari O, Knuuti J. The effects of insulin and short-term hyperglycaemia on myocardial blood flow in young men with uncomplicated type I diabetes. Diabetologia 2002; 45: 775–782
   Google Scholar
• Szerafin T, Erdei N, Fulop T, Pasztor ET, Edes I, Koller A, Bagi Z. Increased cyclo-oxygenase-2 expression and prostaglandin-mediated dilation in coronary arterioles of patients with diabetes mellitus. Circ Res 2006; 99: e12–e317
   Google Scholar
• Tofukuji M, Metais C, Li J, Hariawala MD, Franklin A, Vassileva C, Li J, Simons M, Sellke FW. Effects of ischemic preconditioning on myocardial perfusion, function, and microvascular regulation. Circulation 1998; 98: II197–II204
   Google Scholar
• Xie Z, Su W, Guo Z, Pang H, Post SR, Gong MC. Up-regulation of CPI-17 phosphorylation in diabetic vasculature and high glucose cultured vascular smooth muscle cells. Cardiovasc Res 2006; 69: 491–501
   PubMed Web of Science ®Google Scholar
• Watts GF, O'Brien SF, Silvester W, Millar JA. Impaired endothelium-dependent and independent dilatation of forearm resistance arteries in men with diet-treated non-insulin-dependent diabetes: role of dyslipidaemia. Clin Sci (Lond) 1996; 91: 567–573
   PubMed Web of Science ®Google Scholar
• Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. Impaired nitric oxide–mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 1996; 27: 567–574
   PubMed Web of Science ®Google Scholar
• Wooldridge AA, MacDonald JA, Erdodi F, Ma C, Borman MA, Hartshorne DJ, Haystead TA. Smooth muscle phosphatase is regulated in vivo by exclusion of phosphorylation of threonine 696 of MYPT1 by phosphorylation of Serine 695 in response to cyclic nucleotides. J Biol Chem 2004; 279: 34496–34504
   PubMed Web of Science ®Google Scholar
• Zhou W, Wang XL, Lamping KG, Lee HC. Inhibition of protein kinase Cbeta protects against diabetes-induced impairment in arachidonic acid dilation of small coronary arteries. J Pharmacol Exp Ther 2006; 319: 199–207
   Google Scholar