Differential effects of diet-induced obesity on BKca β1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 1, 2011, Pages

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

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Arteriolar remodeling; Large conductance calcium activated potassium channel; Myogenic tone

Indexed keywords

IBERIOTOXIN; INSULIN; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; LEPTIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTERIOLE; ARTERY DIAMETER; ARTICLE; BLOOD PRESSURE; BRAIN CIRCULATION; CONTROLLED STUDY; CREMASTER MUSCLE; HEART RATE; IMMUNOHISTOCHEMISTRY; LIPID DIET; MALE; MIDDLE CEREBRAL ARTERY; MUSCLE TONE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RESISTANCE BLOOD VESSEL; SKELETAL MUSCLE; VASCULAR SMOOTH MUSCLE;

ANIMALS; ARTERIOLES; BLOTTING, WESTERN; CEREBRAL ARTERIES; DIET; DIETARY FATS; ENERGY INTAKE; HEART RATE; HYPERINSULINISM; HYPERTENSION; IMMUNOHISTOCHEMISTRY; LEPTIN; MALE; MICROSCOPY, ELECTRON; MUSCLE TONUS; MUSCLE, SKELETAL; OBESITY; POTASSIUM CHANNELS; RATS; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WEIGHT GAIN;

EID: 79959909140     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00134.2011     Document Type: Article

References (70)

1. 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.
2. + channels in vascular smooth muscle during hypertension. J Clin Invest 112: 717-724, 2003.
3. Amberg GC, Santana LF. Downregulation of the BK channel beta1 subunit in genetic hypertension. Circ Res 93: 965-971, 2003.
4. Borbouse L, Dick GM, Asano S, Bender SB, Dincer UD, Payne GA, Neeb ZP, Bratz IN, Sturek M, Tune JD. Impaired function of coronary BKCa channels in metabolic syndrome. Am J Physiol Heart Circ Physiol 297: H1629-H1637, 2009.
5. Brenner R, Perez GJ, Bonev AD, Eckman DM, Kosek JC, Wiler SW, Patterson AJ, Nelson MT, Aldrich RW. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 407: 870-876, 2000.
6. + channels from arteries of type 2 diabetic Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 290: H1520-H1527, 2006.
7. Busija DW, Gaspar T, Domoki F, Katakam PV, Bari F. Mitochondrialmediated suppression of ROS production upon exposure of neurons to lethal stress: mitochondrial targeted preconditioning. Adv Drug Deliv Rev 60: 1471-1477, 2008.
8. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ Res 78: 415-423, 1996.
9. 2+ spark coupling in murine arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 290: H2309-H2319, 2006.
10. Deutsch C, Portik-Dobos V, Smith AD, Ergul A, Dorrance AM. Diet-induced obesity causes cerebral vessel remodeling and increases the damage caused by ischemic stroke. Microvasc Res 78: 100-106, 2009.
11. Dick GM, Hunter AC, Sanders KM. Ethylbromide tamoxifen, a membrane-impermeant antiestrogen, activates smooth muscle calcium-activated large-conductance potassium channels from the extracellular side. Mol Pharmacol 61: 1105-1113, 2002.
12. Dick GM, Rossow CF, Smirnov S, Horowitz B, Sanders KM. Tamoxifen activates smooth muscle BK channels through the regulatory beta 1 subunit. J Biol Chem 276: 34594-34599, 2001.
13. Dick GM, Sanders KM. (Xeno)estrogen sensitivity of smooth muscle BK channels conferred by the regulatory beta1 subunit: a study of beta1 knockout mice. J Biol Chem 276: 44835-44840, 2001.
14. Dimitropoulou C, Han G, Miller AW, Molero M, Fuchs LC, White RE, Carrier GO. Potassium (BKCa) currents are reduced in microvascular smooth muscle cells from insulin-resistant rats. Am J Physiol Heart Circ Physiol 282: H908-H917, 2002.
15. Dong L, Zheng YM, Van Riper D, Rathore R, Liu QH, Singer HA, Wang YX. Functional and molecular evidence for impairment of calciumactivated potassium channels in type-1 diabetic cerebral artery smooth muscle cells. J Cereb Blood Flow Metab 28: 377-386, 2008.
16. Duling BR, Gore RW, Dacey RG Jr, Damon DN. Methods for isolation, cannulation, and in vitro study of single microvessels. Am J Physiol Heart Circ Physiol 241: H108-H116, 1981.
17. Dworetzky SI, Boissard CG, Lum-Ragan JT, McKay MC, Post-Munson DJ, Trojnacki JT, Chang CP, Gribkoff VK. Phenotypic alteration of a human BK (hSlo) channel by hSlobeta subunit coexpression: changes in blocker sensitivity, activation/relaxation and inactivation kinetics, and protein kinase A modulation. J Neurosci 16: 4543-4550, 1996.
18. Edwards G, Niederste-Hollenberg A, Schneider J, Noack T, Weston AH. Ion channel modulation by NS 1619, the putative BKCa channel opener, in vascular smooth muscle. Br J Pharmacol 113: 1538-1547, 1994.
19. Erdos B, Miller AW, Busija DW. Alterations in KATP and KCa channel function in cerebral arteries of insulin-resistant rats. Am J Physiol Heart Circ Physiol 283: H2472-H2477, 2002.
20. 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.
21. Feher A, Rutkai I, Beleznai T, Ungvari Z, Csiszar A, Edes I, Bagi Z. Caveolin-1 limits the contribution of BKCa channel to EDHF-mediated arteriolar dilation: implications in diet-induced obesity. Cardiovasc Res 87: 732-739, 2010.
22. Frisbee JC. Remodeling of the skeletal muscle microcirculation increases resistance to perfusion in obese Zucker rats. Am J Physiol Heart Circ Physiol 285: H104-H111, 2003.
23. 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.
24. Gauthier KM, Liu C, Popovic A, Albarwani S, Rusch NJ. Freshly isolated bovine coronary endothelial cells do not express the BKCa channel gene. J Physiol 545: 829-836, 2002.
25. Giangiacomo KM, Fremont V, Mullmann TJ, Hanner M, Cox RH, Garcia ML. Interaction of charybdotoxin S10A with single maxi-K channels: kinetics of blockade depend on the presence of the beta 1 subunit. Biochemistry 39: 6115-6122, 2000.
26. Gollasch M, Dubrovska G. Paracrine role for periadventitial adipose tissue in the regulation of arterial tone. Trends Pharmacol Sci 25: 647-653, 2004.
27. Grayson TH, Ohms SJ, Brackenbury TD, Meaney KR, Peng K, Pittelkow YE, Wilson SR, Sandow SL, Hill CE. Vascular microarray profiling in two models of hypertension identifies caveolin-1, Rgs2 and Rgs5 as antihypertensive targets. BMC Genomics 8: 404, 2007.
28. Gribkoff VK, Lum-Ragan JT, Boissard CG, Post-Munson DJ, Meanwell NA, Starrett JE Jr, Kozlowski ES, Romine JL, Trojnacki JT, McKay MC, Zhong J, and Dworetzky SI. Effects of channel modulators on cloned large-conductance calcium-activated potassium channels. Mol Pharmacol 50: 206-217, 1996.
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. Hill MA, Sun Z, Martinez-Lemus L, Meininger GA. New technologies for dissecting the arteriolar myogenic response. Trends Pharmacol Sci 28: 308-315, 2007.
31. Hodnett BL, Hester RL. Regulation of muscle blood flow in obesity. Microcirculation 14: 273-288, 2007.
32. Holland M, Langton PD, Standen NB, Boyle JP. Effects of the BKCa channel activator, NS1619, on rat cerebral artery smooth muscle. Br J Pharmacol 117: 119-129, 1996.
33. Howitt L, Sandow SL, Grayson TH, Morris MJ, Murphy TV. Increased NO-dependent dilation of rat arterioles in diet-induced obesity (Abstract). Hypertension 55: 1499, 2010.
34. + channel alphasubunit. Mol Pharmacol 62: 836-846, 2002.
35. Jackson WF. Potassium channels in the peripheral microcirculation. Microcirculation 12: 113-127, 2005.
36. Jaggar JH, Porter VA, Lederer WJ, Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol 278: C235-C256, 2000.
37. Jiang Z, Wallner M, Meera P, Toro L. Human and rodent MaxiK channel beta-subunit genes: cloning and characterization. Genomics 55: 57-67, 1999.
38. Kim EY, Dryer SE. Effects of insulin and high glucose on mobilization of Slo1 BKCa channels in podocytes. J Cell Physiol. Published ahead of print; DOI:10.1002/jcp.22567.
39. Knaus HG, Eberhart A, Glossmann H, Munujos P, Kaczorowski GJ, Garcia ML. Pharmacology and structure of high conductance calciumactivated potassium channels. Cell Signal 6: 861-870, 1994.
40. + channels. J Physiol 508: 211-221, 1998.
41. 2+ signaling. Am J Physiol Heart Circ Physiol 289: H1326-H1334, 2005.
42. Lambert GW, Straznicky NE, Lambert EA, Dixon JB, Schlaich MP. Sympathetic nervous activation in obesity and the metabolic syndrome-causes, consequences and therapeutic implications. Pharmacol Ther 126: 159-172, 2010.
43. Ledoux J, Werner ME, Brayden JE, Nelson MT. Calcium-activated potassium channels and the regulation of vascular tone. Physiology (Bethesda) 21: 69-78, 2006.
44. + channels in the cerebral microcirculation of genetically hypertensive rats: evidence for their protection against cerebral vasospasm. Circ Res 82: 729-737, 1998.
45. + channels in aorta of hypertensive rats. Hypertension 30: 1403-1409, 1997.
46. Matharoo-Ball B, Ashford ML, Arulkumaran S, Khan RN. Downregulation of the alpha-and beta-subunits of the calcium-activated potassium channel in human myometrium with parturition. Biol Reprod 68: 2135-2141, 2003.
47. 2+-activated potassium beta 1 channel subunit in retinal arteriolar smooth muscle. Circ Res 100: 703-711, 2007.
48. + channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci U S A 97: 5562-5567, 2000.
49. + channels in diabetic dyslipidemic pigs is prevented by exercise. J Appl Physiol 95: 1179-1193, 2003.
50. Morris MJ. Cardiovascular and metabolic effects of obesity. Clin Exp Pharmacol Physiol 35: 416-419, 2008.
51. Murphy TV, Kotecha N, Hill MA. Endothelium-independent constriction of isolated, pressurized arterioles by Nomega-nitro-L-arginine methyl ester (L-NAME). Br J Pharmacol 151: 602-609, 2007.
52. Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, Lederer WJ. Relaxation of arterial smooth muscle by calcium sparks. Science 270: 633-637, 1995.
53. Osmond JM, Mintz JD, Dalton B, Stepp DW. Obesity increases blood pressure, cerebral vascular remodeling, and severity of stroke in the Zucker rat. Hypertension 53: 381-386, 2009.
54. Osol G, Halpern W. Myogenic properties of cerebral blood vessels from normotensive and hypertensive rats. Am J Physiol Heart Circ Physiol 249: H914-H921, 1985.
55. Parker SB, Dobrian AD, Wade SS, Prewitt RL. AT1 receptor inhibition does not reduce arterial wall hypertrophy or PDGF-A expression in renal hypertension. Am J Physiol Heart Circ Physiol 278: H613-H622, 2000.
56. Patel HH, Murray F, Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48: 359-391, 2008.
57. + channels in cerebral vasodilatation induced by increases in cyclic GMP and cyclic AMP in the rat. Stroke 27: 1603-1607, 1996.
58. 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.
59. Sadanaga T, Ohya Y, Ohtsubo T, Goto K, Fujii K, Abe I. Decreased 4-aminopyridine sensitive K[1] currents in endothelial cells from hypertensive rats. Hypertens Res 25: 589-596, 2002.
60. 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.
61. + channels. Nat Neurosci 5: 299-300, 2002.
62. 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.
63. Stepp DW, Pollock DM, Frisbee JC. Low-flow vascular remodeling in the metabolic syndrome X. Am J Physiol Heart Circ Physiol 286: H964-H970, 2004.
64. Tanaka Y, Koike K, Toro L. MaxiK channel roles in blood vessel relaxations induced by endothelium-derived relaxing factors and their molecular mechanisms. J Smooth Muscle Res 40: 125-153, 2004.
65. Tanaka Y, Meera P, Song M, Knaus HG, Toro L. Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant alpha + beta subunit complexes. J Physiol 502: 545-557, 1997.
66. Tang XD, Garcia ML, Heinemann SH, Hoshi T. Reactive oxygen species impair Slo1 BK channel function by altering cysteine-mediated calcium sensing. Nat Struct Mol Biol 11: 171-178, 2004.
67. Velkoska E, Cole TJ, Morris MJ. Early dietary intervention: long-term effects on blood pressure, brain neuropeptide Y, and adiposity markers. Am J Physiol Endocrinol Metab 288: E1236-E1243, 2005.
68. Yan J, Olsen JV, Park KS, Li W, Bildl W, Schulte U, Aldrich RW, Fakler B, Trimmer JS. Profiling the phospho-status of the BKCa channel alpha subunit in rat brain reveals unexpected patterns and complexity. Mol Cell Proteomics 7: 2188-2198, 2008.
69. 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.
70. Zhong XZ, Harhun MI, Olesen SP, Ohya S, Moffatt JD, Cole WC, Greenwood IA. Participation of KCNQ (Kv7) potassium channels in myogenic control of cerebral arterial diameter. J Physiol 588: 3277-3293, 2010.