Diet-induced obesity impairs endothelium-derived hyperpolarization via altered potassium channel signaling mechanisms

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Haddock, Rebecca E ^a,b   Hilton Grayson, T ^a   Morris, Margaret J ^a   Howitt, Lauren ^a   Chadha, Preet S ^a,c   Sandow, Shaun L ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b Biology and Environment   (Australia)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 ETHYL 2 BENZIMIDAZOLINONE; ACETYLCHOLINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMINE; BARIUM; CYCLOHEXYL [2 (3,5 DIMETHYL PYRAZOL 1 YL) 6 METHYL PYRIMIDIN 4 YL]AMINE; GAP JUNCTION PROTEIN; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; OUABAIN; POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL DIAMETER; CONTROLLED STUDY; DIET; ENZYME ACTIVATION; ENZYME INHIBITION; GAP JUNCTION; HEART MUSCLE TENSION; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; MESENTERIC ARTERY; MORPHOLOGY; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANIMAL; CELL JUNCTION; CELL MEMBRANE POTENTIAL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TISSUE DISTRIBUTION; VASODILATATION;

RATTUS;

ANIMALS; DIET; ENDOTHELIUM, VASCULAR; GAP JUNCTIONS; MEMBRANE POTENTIALS; OBESITY; POTASSIUM CHANNELS; RATS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; VASODILATION;

EID: 79251633164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016423     Document Type: Article

References (58)

1. Haslam D (2010) Obesity and diabetes: the links and common approaches. Prim Care Diabetes 4: 105-112.
2. Vanhoutte PM, Feletou M, Taddei S (2005) Endothelium-dependent contractions in hypertension. Br J Pharmacol 144: 449-458.
3. Feletou M (2009) Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br J Pharmacol 156: 545-562.
4. Sandow SL, Tare M (2007) C-type natriuretic peptide: a new endotheliumderived hyperpolarizing factor? Trends Pharmacol Sci 28: 61-67.
5. Sandow SL, Haddock RE, Hill CE, Chadha PS, Kerr PM, et al. (2009) What's where and why at a vascular myoendothelial microdomain signalling complex? Clin Exp Pharmacol Physiol 36: 67-76.
6. Feletou M, Vanhoutte PM (2004) EDHF: new therapeutic targets? Pharmacol Res 49: 565-580.
7. McGuire JJ, Ding H, Triggle CR (2001) Endothelium-derived relaxing factors: a focus on endothelium-derived hyperpolarizing factor(s). Can J Physiol Pharmacol 79: 443-470.
8. Fukao M, Hattori Y, Kanno M, Sakuma I, Kitabatake A (1997) Sources of Ca2+ in relation to generation of acetylcholine-induced endothelium-dependent hyperpolarization in rat mesenteric artery. Br J Pharmacol 120: 1328-1334.
9. 2+ -release. Arch Pharm Res 28: 709-715.
10. Ca) and connexins: possible relationship to vasodilator function? J Anat 209: 689-698.
11. Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC (2002) Involvement of myoendothelial gap junctions in the actions of endotheliumderived hyperpolarizing factor. Circ Res 90: 1108-1113.
12. Mather S, Dora KA, Sandow SL, Winter P, Garland CJ (2005) Rapid endothelial cell-selective loading of connexin 40 antibody blocks endotheliumderived hyperpolarizing factor dilation in rat small mesenteric arteries. Circ Res 97: 399-407.
13. Dora KA, Gallagher NT, McNeish A, Garland CJ (2008) Modulation of endothelial cell KCa3.1 channels during endothelium-derived hyperpolarizing factor signaling in mesenteric resistance arteries. Circ Res 102: 1247-1255.
14. + channel in porcine coronary artery endothelium: relevance to EDHF. Br J Pharmacol 135: 1133-1143.
15. Young EJ, Hill MA, Wiehler WB, Triggle CR, Reid JJ (2008) Reduced EDHF responses and connexin activity in mesenteric arteries from the insulin-resistant obese Zucker rat. Diabetologia 51: 872-881.
16. Ca and myoendothelial gap junctions to maintain endothelial vasodilator function. Journal of Pharmacology and Experimental Therapeutics 335: 284-293.
17. Fenger-Gron J, Mulvany MJ, Christensen KL (1995) Mesenteric blood pressure profile of conscious, freely moving rats. J Physiol 488: 753-760.
18. Frisbee JC, Maier KG, Stepp DW (2002) Oxidant stress-induced increase in myogenic activation of skeletal muscle resistance arteries in obese Zucker rats. Am J Physiol 283: H2160-2168.
19. Hayashi K, Kanda T, Homma K, Tokuyama H, Okubo K, et al. (2002) Altered renal microvascular response in Zucker obese rats. Metabolism 51: 1553-1561.
20. Erdei N, Toth A, Pasztor ET, Papp Z, Edes I, et al. (2006) High-fat diet-induced reduction in nitric oxide-dependent arteriolar dilation in rats: role of xanthine oxidase-derived superoxide anion. Am J Physiol 291: H2107-2115.
21. Jebelovszki E, Kiraly C, Erdei N, Feher A, Pasztor ET, et al. (2008) High-fat diet-induced obesity leads to increased NO sensitivity of rat coronary arterioles: role of soluble guanylate cyclase activation. Am J Physiol 294: H2558-2564.
22. de Kreutzenberg SV, Puato M, Kiwanuka E, Del Prato S, Pauletto P, et al. (2003) Elevated non-esterified fatty acids impair nitric oxide independent vasodilation, in humans: evidence for a role of inwardly rectifying potassium channels. Atherosclerosis 169: 147-153.
23. Beltowski J (2006) Leptin and atherosclerosis. Atherosclerosis 189: 47-60.
24. Hansen MJ, Jovanovska V, Morris MJ (2004) Adaptive responses in hypothalamic neuropeptide Y in the face of prolonged high-fat feeding in the rat. J Neurochem 88: 909-916.
25. Chen H, Simar D, Morris MJ (2009) Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS One 4: e6259.
26. Velkoska E, Cole TJ, Morris MJ (2005) Early dietary intervention: long-term effects on blood pressure, brain neuropeptide Y, and adiposity markers. Am J Physiol 288: E1236-1243.
27. Sandow SL (2004) Factors, fiction and endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol 31: 563-570.
28. + channels. Br J Pharmacol 151: 655-665.
29. Ca channels and of downstream hyperpolarizing pathways in mesenteric arteries from spontaneously hypertensive rats. Br J Pharmacol 160: 836-843.
30. Kusama N, Kajikuri J, Yamamoto T, Watanabe Y, Suzuki Y, et al. (2005) Reduced hyperpolarization in endothelial cells of rabbit aortic valve following chronic nitroglycerine administration. Br J Pharmacol 146: 487-497.
31. + channels in rat mesenteric arteries. J Pharmacol Exp Ther 333: 210-217.
32. Brondum E, Kold-Petersen H, Simonsen U, Aalkjaer C (2010) NS309 restores EDHF-type relaxation in mesenteric small arteries from type 2 diabetic ZDF rats. Br J Pharmacol 159: 154-165.
33. Boettger MK, Till S, Chen MX, Anand U, Otto WR, et al. (2002) Calciumactivated potassium channel SK1- and IK1-like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors. Brain 125: 252-263.
34. + channels confer distinctive patterns of distribution in human tissues and differential cellular localisation in the colon and corpus cavernosum. Naunyn Schmiedebergs Arch Pharmacol 369: 602-615.
35. Mongan LC, Hill MJ, Chen MX, Tate SN, Collins SD, et al. (2005) The distribution of small and intermediate conductance calcium-activated potassium channels in the rat sensory nervous system. Neuroscience 131: 161-175.
36. Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, et al. (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273: 1709-1714.
37. Ca channel diversity and smooth muscle cell function. Circ Res 85: e33-e43.
38. Giachini FR, Carneiro FS, Lima VV, Carneiro ZN, Dorrance A, et al. (2009) Upregulation of intermediate calcium-activated potassium channels counterbalance the impaired endothelium-dependent vasodilation in stroke-prone spontaneously hypertensive rats. Transl Res 154: 183-193.
39. + channel-dependent EDHF responses in Type II diabetic ZDF rats. Br J Pharmacol 148: 434-441.
40. Garland CJ, Plane F, Kemp BK, Cox TM (1995) Endothelium-dependent hyperpolarization: a role in the control of vascular tone. Trends Pharmacol Sci 16: 23-30.
41. Leuranguer V, Gluais P, Vanhoutte PM, Verbeuren TJ, Feletou M (2008) Openers of calcium-activated potassium channels and endothelium-dependent hyperpolarizations in the guinea pig carotid artery. Naunyn Schmiedebergs Arch Pharmacol 377: 101-109.
42. Dalsgaard T, Kroigaard C, Misfeldt M, Bek T, Simonsen U (2010) Openers of small conductance calcium-activated potassium channels selectively enhance NO-mediated bradykinin vasodilatation in porcine retinal arterioles. Br J Pharmacol 160: 1496-1508.
43. Giachini FR, Chiao CW, Carneiro FS, Lima VV, Carneiro ZN, et al. (2009) Increased activation of stromal interaction molecule-1/Orai-1 in aorta from hypertensive rats: a novel insight into vascular dysfunction. Hypertension 53: 409-416.
44. McNamee CJ, Kappagoda CT, Kunjara R, Russell JC (1994) Defective endothelium-dependent relaxation in the JCR:LA-corpulent rat. Circ Res 74: 1126-1132.
45. Figueroa XF, Duling BR (2009) Gap junctions in the control of vascular function. Antioxid Redox Signal 11: 251-266.
46. Sandow SL, Goto K, Rummery N, Hill CE (2004) Developmental changes in myoendothelial gap junction mediated vasodilator activity in the rat saphenous artery. J Physiol 556: 875-886.
47. Bund SJ, Lee RM (2003) Arterial Structural Changes in Hypertension: A Consideration of Methodology, Terminology and Functional Consequence. J Vasc Res 40: 547-557.
48. Mulvany MJ, Baumbach GL, Aalkjaer C, Heagerty AM, Korsgaard N, et al. (1996) Vascular remodeling. Hypertension 28: 505-506.
49. Grassi G, Seravalle G, Scopelliti F, Dell'Oro R, Fattori L, et al. (2010) Structural and functional alterations of subcutaneous small resistance arteries in severe human obesity. Obesity 18: 92-98.
50. Tare M, Coleman HA, Parkington HC (2002) Glycyrrhetinic derivatives inhibit hyperpolarization in endothelial cells of guinea pig and rat arteries. Am J Physiol 282: H335-341.
51. + currents underlying the action of endothelium-derived hyperpolarizing factor in guinea-pig, rat and human blood vessels. J Physiol 531: 359-373.
52. Haddock RE, Grayson TH, Brackenbury TD, Meaney KR, Neylon CB, et al. (2006) Endothelial coordination of cerebral vasomotion via myoendothelial gap junctions containing connexins37 and 40. American Journal of Physiology 291: H2047-H2056.
53. Matchkov VV, Rahman A, Peng H, Nilsson H, Aalkjaer C (2004) Junctional and nonjunctional effects of heptanol and glycyrrhetinic acid derivates in rat mesenteric small arteries. BrJPharmacol 142: 961-972.
54. Ellis A, Goto K, Chaston DJ, Brackenbury TD, Meaney KR, et al. (2009) Enalapril treatment alters the contribution of epoxyeicosatrienoic acids but not gap junctions to endothelium-derived hyperpolarizing factor activity in mesenteric arteries of spontaneously hypertensive rats. J Pharmacol Exp Ther 330: 413-422.
55. Sandow SL, Looft-Wilson RC, Grayson TH, Segal SS, Hill CE (2003) Expression of homocellular and heterocellular gap junctions in hamster arterioles and feed arteries. Cardiovasc Res 60: 643-653.
56. Murphy TV, Kotecha N, Hill MA (2007) Endothelium-independent constriction of isolated, pressurized arterioles by Nomega-nitro-L-arginine methyl ester (LNAME). Br J Pharmacol 151: 602-609.
57. Neild TO (1989) Measurement of arteriole diameter changes by analysis of television images. Blood Vessels 26: 48-52.
58. Rummery NM, Grayson TH, Hill CE (2005) Angiotensin-converting enzyme inhibition restores endothelial but not medial connexin expression in hypertensive rats. J Hyperten 23: 317-328.