Dietary obesity increases NO and inhibits BKCa-mediated, endothelium-dependent dilation in rat cremaster muscle artery: Association with caveolins and caveolae

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 12, 2012, Pages 2464-2476

  Howitt, Lauren ^a   Hilton Grayson, T ^a   Morris, Margaret J ^a   Sandow, Shaun L ^a   Murphy, Timothy V ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Large conductance Ca2+ activated K+ channel; Nitric oxide

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; 1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ACETYLCHOLINE; APAMIN; CAVEOLIN; CAVEOLIN 1; CAVEOLIN 2; CAVEOLIN 3; IBERIOTOXIN; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; MONOMER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; OLIGOMER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTERIOLE; ARTERY ENDOTHELIUM; ARTICLE; BODY MASS; BODY WEIGHT; CAVEOLA; CELL COUNT; CELL DENSITY; CONTROLLED STUDY; CREMASTER MUSCLE; CREMASTER MUSCLE ARTERY; DIETARY INTAKE; DRUG INHIBITION; ENDOTHELIUM DEPENDENT DILATION; FEEDING; LIPID DIET; MALE; NONHUMAN; OBESITY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SMOOTH MUSCLE FIBER; VASODILATATION;

ACETYLCHOLINE; ANIMALS; APAMIN; ARTERIOLES; CAVEOLAE; CAVEOLIN 1; CAVEOLIN 2; DIET, HIGH-FAT; ENDOTHELIUM, VASCULAR; MALE; MUSCLE, SMOOTH; NITRIC OXIDE; NITROPRUSSIDE; OBESITY; PEPTIDES; POTASSIUM CHANNELS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; VASODILATION; VASODILATOR AGENTS;

EID: 84862546523     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00965.2011     Document Type: Article

References (76)

1. Adebiyi A, Zhao G, Cheranov SY, Ahmed A, Jaggar JH. Caveolin-1 abolishment attenuates the myogenic response in murine cerebral arteries. Am J Physiol Heart Circ Physiol 292: H1584-H1592, 2007.
2. Alioua A, Lu R, Kumar Y, Eghbali M, Kundu P, Toro L, Stefani E. Slo1 caveolin-binding motif, a mechanism of caveolin-1-Slo1 interaction regulating Slo1 surface expression. J Biol Chem 283: 4808-4817, 2008.
3. Arcaro G, Zamboni M, Rossi L, Turcato E, Covi G, Armellini F, Bosello O, Lechi A. Body fat distribution predicts the degree of endothe-lial dysfunction in uncomplicated obesity. Int J Obes Relat Metab Disord 23: 936-942, 1999.
4. Boustany-Kari CM, Gong M, Akers WS, Guo Z, Cassis LA. Enhanced vascular contractility and diminished coronary artery flow in rats made hypertensive from diet-induced obesity. Int J Obes (Lond) 31: 1652-1659, 2007.
5. Brook RD, Bard RL, Rubenfire M, Ridker PM, Rajagopalan S. Usefulness of visceral obesity (waist/hip ratio) in predicting vascular endothelial function in healthy overweight adults. Am J Cardiol 88: 1264-1269, 2001.
6. + channel-dependent EDHF responses in type II diabetic ZDF rats. Br J Pharmacol 148: 434-441, 2006.
7. + channels from arteries of type 2 diabetic Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 290: H1520-H1527, 2006.
8. Campbell WB, Fleming I. Epoxyeicosatrienoic acids and endothelium-dependent responses. Pflügers Arch 459: 881-895, 2010.
9. Chadha PS, Haddock RE, Howitt L, Morris MJ, Murphy TV, Grayson TH, Sandow SL. Obesity up-regulates intermediate conductance calcium-activated potassium channels and myoendothelial gap junctions to maintain endothelial vasodilator function. J Pharmacol Exp Ther 335: 284-293, 2010.
10. Chidlow JH Jr, Sessa WC. Caveolae, caveolins, and cavins: complex control of cellular signalling and inflammation. Cardiovasc Res 86: 219-225, 2010.
11. Contreras C, Sanchez A, Garcia-Sacristan A, Martinez MC, Andri-antsitohaina R, Prieto D. Preserved insulin vasorelaxation and up-regulation of the Akt/eNOS pathway in coronary arteries from insulin resistant obese Zucker rats. Atherosclerosis 217: 331-339.
12. Das K, Lewis RY, Scherer PE, Lisanti MP. The membrane-spanning domains of caveolins-1 and -2 mediate the formation of caveolin hetero-oligomers. Implications for the assembly of caveolae membranes in vivo. J Biol Chem 274: 18721-18728, 1999.
13. Dessy C, Feron O, Balligand JL. The regulation of endothelial nitric oxide synthase by caveolin: a paradigm validated in vivo and shared by the "endothelium-derived hyperpolarizing factor". Pflügers Arch 459: 817- 827, 2010.
14. 2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279, 2005.
15. Elmarakby AA, Imig JD. Obesity is the major contributor to vascular dysfunction and inflammation in high-fat diet hypertensive rats. Clin Sci (Lond) 118: 291-301, 2010.
16. Erdei N, Toth A, Pasztor ET, Papp Z, Edes I, Koller A, Bagi Z. High-fat diet-induced reduction in nitric oxide-dependent arteriolar dilation in rats: role of xanthine oxidase-derived superoxide anion. Am J Physiol Heart Circ Physiol 291: H2107-H2115, 2006.
17. Erdos B, Simandle SA, Snipes JA, Miller AW, Busija DW. Potassium channel dysfunction in cerebral arteries of insulin-resistant rats is mediated by reactive oxygen species. Stroke 35: 964-969, 2004.
18. Erdos B, Snipes JA, Miller AW, Busija DW. Cerebrovascular dysfunction in Zucker obese rats is mediated by oxidative stress and protein kinase C. Diabetes 53: 1352-1359, 2004.
19. Eringa EC, Stehouwer CD, Roos MH, Westerhof N, Sipkema P. Selective resistance to vasoactive effects of insulin in muscle resistance arteries of obese Zucker (fa/fa) rats. Am J Physiol Endocrinol Metab 293: E1134-E1139, 2007.
20. Feher A, Rutkai I, Beleznai T, Ungvari Z, Csiszar A, Edes I, Bagi Z. Caveolin-1 limits the contribution of BK(Ca) channel to EDHF-mediated arteriolar dilation: implications in diet-induced obesity. Cardiovasc Res 87: 732-739, 2010.
21. Feletou M. Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br J Pharmacol 156: 545-562, 2009.
22. Feletou M, Vanhoutte PM. EDHF: an update. Clin Sci (Lond) 117: 139-155, 2009.
23. Frisbee JC. Impaired dilation of skeletal muscle microvessels to reduced oxygen tension in diabetic obese Zucker rats. Am J Physiol Heart Circ Physiol 281: H1568-H1574, 2001.
24. Frisbee JC, Delp MD. Vascular function in the metabolic syndrome and the effects on skeletal muscle perfusion: lessons from the obese Zucker rat. Essays Biochem 42: 145-161, 2006.
25. Frisbee JC, Maier KG, Stepp DW. Oxidant stress-induced increase in myogenic activation of skeletal muscle resistance arteries in obese Zucker rats. Am J Physiol Heart Circ Physiol 283: H2160-H2168, 2002.
26. Frisbee JC, Stepp DW. Impaired NO-dependent dilation of skeletal muscle arterioles in hypertensive diabetic obese Zucker rats. Am J Physiol Heart Circ Physiol 281: H1304-H1311, 2001.
27. Fulop T, Jebelovszki E, Erdei N, Szerafin T, Forster T, Edes I, Koller A, Bagi Z. Adaptation of vasomotor function of human coronary arterioles to the simultaneous presence of obesity and hypertension. Arterioscler Thromb Vasc Biol 27: 2348-2354, 2007.
28. Haddock RE, Grayson TH, Morris MJ, Howitt L, Chadha PS, Sandow SL. Diet-induced obesity impairs endothelium-derived hyperpo-larization via altered potassium channel signaling mechanisms. PLos One 6: e16423, 2011.
29. Hansen MJ, Jovanovska V, Morris MJ. Adaptive responses in hypothalamic neuropeptide Y in the face of prolonged high-fat feeding in the rat. J Neurochem 88: 909-916, 2004.
30. Heygate KM, Davies J, Holmes M, James RF, Thurston H. The effect of insulin treatment and of islet transplantation on the resistance artery function in the STZ-induced diabetic rat. Br J Pharmacol 119: 495-504, 1996.
31. + channels. Am J Physiol Heart Circ Physiol 291: H216-H222, 2006.
32. Howitt L, Sandow SL, Grayson TH, Ellis ZE, Morris MJ, Murphy TV. Differential effects of diet-induced obesity on BKCa fi1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries. Am J Physiol Heart Circ Physiol 301: H29-H40, 2011.
33. Iwakiri Y, Tsai MH, McCabe TJ, Gratton JP, Fulton D, Groszmann RJ, Sessa WC. Phosphorylation of eNOS initiates excessive NO production in early phases of portal hypertension. Am J Physiol Heart Circ Physiol 282: H2084-H2090, 2002.
34. Jackson WF. Potassium channels in the peripheral microcirculation. Microcirculation 12: 113-127, 2005.
35. Je HD, Gallant C, Leavis PC, Morgan KG. Caveolin-1 regulates contractility in differentiated vascular smooth muscle. Am J Physiol Heart Circ Physiol 286: H91-H98, 2004.
36. Jebelovszki E, Kiraly C, Erdei N, Feher A, Pasztor ET, Rutkai I, Forster T, Edes I, Koller A, Bagi Z. High-fat diet-induced obesity leads to increased NO sensitivity of rat coronary arterioles: role of soluble guanylate cyclase activation. Am J Physiol Heart Circ Physiol 294: H2558-H2564, 2008.
37. Kagota S, Chia E, McGuire JJ. Preserved arterial vasodilation via endothelial protease-activated receptor-2 in obese type 2 diabetic mice. Br J Pharmacol 164: 358-371, 2011.
38. Karagiannis J, Reid JJ, Darby I, Roche P, Rand MJ, Li CG. Impaired nitric oxide function in the basilar artery of the obese Zucker rat. J Cardiovasc Pharmacol 42: 497-505, 2003.
39. Katakam PV, Domoki F, Snipes JA, Busija AR, Jarajapu YP, Busija DW. Impaired mitochondria-dependent vasodilation in cerebral arteries of Zucker obese rats with insulin resistance. Am J Physiol Regul Integr Comp Physiol 296: R289-R298, 2009.
40. Li C, Ruan L, Sood SG, Papapetropoulos A, Fulton D, Venema RC. Role of eNOS phosphorylation at Ser-116 in regulation of eNOS activity in endothelial cells. Vascul Pharmacol 47: 257-264, 2007.
41. Li PL, Zou AP, Campbell WB. Regulation of potassium channels in coronary arterial smooth muscle by endothelium-derived vasodilators. Hypertension 29: 262-267, 1997.
42. Makimattila S, Mantysaari M, Groop PH, Summanen P, Virkamaki A, Schlenzka A, Fagerudd J, Yki-Jarvinen H. Hyperreactivity to nitro-vasodilators in forearm vasculature is related to autonomic dysfunction in insulin-dependent diabetes mellitus. Circulation 95: 618-625, 1997.
43. McSherry IN, Sandow SL, Campbell WB, Falck JR, Hill MA, Dora KA. A role for heterocellular coupling and EETs in dilation of rat cremaster arteries. Microcirculation 13: 119-130, 2006.
44. Mehebik-Mojaat N, Ribiere C, Niang F, Forest C, Jaubert AM. Leptin and insulin induce mutual resistance for nitric oxide synthase III activation in adipocytes. J Cell Biochem 108: 982-988, 2009.
45. Michell BJ, Chen Z, Tiganis T, Stapleton D, Katsis F, Power DA, Sim AT, Kemp BE. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem 276: 17625-17628, 2001.
46. Monier S, Parton RG, Vogel F, Behlke J, Henske A, Kurzchalia TV. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 6: 911-927, 1995.
47. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, Rodriguez-Boulan E. Caveolin-2 localizes to the golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 274: 25708-25717, 1999.
48. ω-nitro-L-arginine methyl ester (l-NAME). Br J Pharmacol 151: 602-609, 2007.
49. Naderali EK, Brown MJ, Pickavance LC, Wilding JP, Doyle PJ, Williams G. Dietary obesity in the rat induces endothelial dysfunction without causing insulin resistance: a possible role for triacylglycerols. Clin Sci (Lond) 101: 499-506, 2001.
50. Patel HH, Murray F, Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48: 359-391, 2008.
51. Paterno R Faraci FM, Heistad DD. Role of Ca(2+)-dependent K+ channels in cerebral vasodilatation induced by increases in cyclic GMP and cyclic AMP in the rat. Stroke 27: 1603-1607; discussion 1607-1608, 1996.
52. Pieper GM. Enhanced, unaltered and impaired nitric oxide-mediated endothelium-dependent relaxation in experimental diabetes mellitus: importance of disease duration. Diabetologia 42: 204-213, 1999.
53. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 113: 898-918, 2006.
54. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev 54: 431-467, 2002.
55. Rybin VO, Grabham PW, Elouardighi H, Steinberg SF. Caveolae-associated proteins in cardiomyocytes: caveolin-2 expression and interactions with caveolin-3. Am J Physiol Heart Circ Physiol 285: H325-H332, 2003.
56. Sandow SL. Factors, fiction and endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol 31: 563-570, 2004.
57. Sandow SL, Goto K, Rummery NM, Hill CE. Developmental changes in myoendothelial gap junction mediated vasodilator activity in the rat saphenous artery. J Physiol 556: 875-886, 2004.
58. Sandow SL, Grayson TH. Limits of isolation and culture: intact vascular endothelium and BKCa. Am J Physiol Heart Circ Physiol 297: H1-H7, 2009.
59. Sandow SL, Haddock RE, Hill CE, Chadha PS, Kerr PM, Welsh DG, Plane F. What's where and why at a vascular myoendothelial microdo-main signalling complex. Clin Exp Pharmacol Physiol 36: 67-76, 2009.
60. Sandow SL, Neylon CB, Chen MX, Garland CJ. Spatial separation of endothelial small- and intermediate-conductance calcium-activated potassium channels [K(Ca)] and connexins: possible relationship to vasodilator function? J Anat 209: 689-698, 2006.
61. Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC. Involvement of myoendothelial gap junctions in the actions of endothelium-derived hyperpolarizing factor. Circ Res 90: 1108-1113, 2002.
62. Sargiacomo M, Scherer PE, Tang Z, Kubler E, Song KS, Sanders MC, Lisanti MP. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci USA 92: 9407-9411, 1995.
63. Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J Cell Biol 140: 795-806, 1998.
64. Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, Lisanti MP. Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272: 29337-29346, 1997.
65. Schubert AL, Schubert W, Spray DC, Lisanti MP. Connexin family members target to lipid raft domains and interact with caveolin-1. Biochemistry 41: 5754-5764, 2002.
66. Schulz E, Jansen T, Wenzel P, Daiber A, Munzel T. Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal 10: 1115-1126, 2008.
67. Spurrell BE, Murphy TV, Hill MA. Intraluminal pressure stimulates MAPK phosphorylation in arterioles: temporal dissociation from myogenic contractile response. Am J Physiol Heart Circ Physiol 285: H1764-H1773, 2003.
68. Sweazea KL, Walker BR. High fat feeding impairs endothelin-1 mediated vasoconstriction through increased iNOS-derived nitric oxide. Horm Metab Res 43: 470-476.
69. Tesauro M, Cardillo C. Obesity, blood vessels and metabolic syndrome. Acta Physiol (Oxf) 203: 279-286, 2011.
70. Thengchaisri N, Kuo L. Hydrogen peroxide induces endothelium-depen-dent and -independent coronary arteriolar dilation: role of cyclooxygenase and potassium channels. Am J Physiol Heart Circ Physiol 285: H2255- H2263, 2003.
71. Thomas SR, Chen K, Keaney JF Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 277: 6017-6024, 2002.
72. Toro L, Wallner M, Meera P, Tanaka Y. Maxi-K(Ca), a unique member of the voltage-gated K channel superfamily. News Physiol Sci 13: 112-117, 1998.
73. Villalba N, Martinez P, Briones AM, Sanchez A, Salaices M, Garcia-Sacristan A, Hernandez M, Benedito S, Prieto D. Differential structural and functional changes in penile and coronary arteries from obese Zucker rats. Am J Physiol Heart Circ Physiol 297: H696-H707, 2009.
74. Wary KK, Mariotti A, Zurzolo C, Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634, 1998.
75. Yang Y, Murphy TV, Ella SR, Grayson TH, Haddock R, Hwang YT, Braun AP, Peichun G, Korthuis RJ, Davis MJ, Hill MA. Heterogeneity in function of small artery smooth muscle BKCa: involvement of the beta1-subunit. J Physiol 587: 3025-3044, 2009.
76. Zou MH, Shi C, Cohen RA. Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109: 817-826, 2002.