Impairment of neurovascular coupling in type 1 diabetes mellitus in rats is linked to PKC modulation of BKca and Kir channels

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 6, 2012, Pages

  Vetri, Francesco ^a   Xu, Haoliang ^a   Paisansathan, Chanannait ^a   Pelligrino, Dale A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Cerebrovascular disease; Inward rectifier potassium channel; Large conductance calcium operated potassium channel; Pial vessels; Potassium channels; Protein kinase C

Indexed keywords

1 (2 HYDROXY 5 TRIFLUOROMETHYLPHENYL) 5 TRIFLUOROMETHYL 2(3H) BENZIMIDAZOLONE; CALPHOSTIN C; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL AGONIST; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; PHORBOL DIBUTYRATE; POTASSIUM CHANNEL STIMULATING AGENT; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN TISSUE; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; FEMALE; GRAY MATTER; INSULIN DEPENDENT DIABETES MELLITUS; NERVE STIMULATION; NEUROVASCULAR COUPLING IMPAIRMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANIMALS; ARTERIOLES; BENZIMIDAZOLES; CEREBROVASCULAR CIRCULATION; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ELECTRIC STIMULATION; ENZYME ACTIVATION; ENZYME ACTIVATORS; FEMALE; NAPHTHALENES; PHORBOL 12,13-DIBUTYRATE; PHOSPHORYLATION; PIA MATER; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; TIME FACTORS; VASODILATION;

EID: 84863275031     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01067.2011     Document Type: Article

References (47)

1. Alvarez EO, Beauquis J, Revsin Y, Banzan AM, Roig P, De Nicola AF, Saravia F. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav Brain Res 198: 224-230, 2009.
2. Arrick DM, Sharpe GM, Sun H, Mayhan WG. Diabetes-induced cerebrovascular dysfunction: role of poly(ADP-ribose) polymerase. Microvasc Res 73: 1-6, 2007.
3. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 468: 232-243, 2010.
4. Chavez RA, Gray AT, Zhao BB, Kindler CH, Mazurek MJ, Mehta Y, Forsayeth JR, Yost CS. TWIK-2, a new weak inward rectifying member of the tandem pore domain potassium channel family. J Biol Chem 274: 7887-7892, 1999.
5. + channel-mediated responses of the basilar artery. Stroke 33: 1692-1697, 2002.
6. Dabelea D, Bell RA, D'Agostino RB Jr, Imperatore G, Johansen JM, Linder B, Liu LL, Loots B, Marcovina S, Mayer-Davis EJ, Pettitt DJ, Waitzfelder B. Incidence of diabetes in youth in the United States. J Am Med Assoc 297: 2716-2724, 2007.
7. Das Evcimen N, King GL. The role of protein kinase C activation and the vascular complications of diabetes. Pharmacol Res 55: 498-510, 2007.
8. 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.
9. 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.
10. + channels are regulated independently by protein kinases and ATP hydrolysis. Neuron 13: 1413-1420, 1994.
11. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9: 1397-1403, 2006.
12. Geraldes P, Hiraoka-Yamamoto J, Matsumoto M, Clermont A, Leitges M, Marette A, Aiello LP, Kern TS, King GL. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat Med 106: 1319-1331, 2010.
13. 2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 107: 3811-3816, 2010.
14. Ha TS, Heo MS, Park CS. Functional effects of auxiliary beta4-subunit on rat large-conductance Ca(2+)-activated K(+) channel. Biophys J 86: 2871-2882, 2004.
15. 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.
16. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M, Sano H, Utsumi H, Nawata H. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 49: 1939-1945, 2000.
17. Kim JY, Park CS. Potentiation of large-conductance calcium-activated potassium [BK(Ca)] channels by a specific isoform of protein kinase C. Biochem Biophys Res Commun 365: 459-465, 2008.
18. + channels in vascular smooth muscle cells. J Smooth Muscle Res 44: 65-81, 2008.
19. Leffler CW, Parfenova H, Fedinec AL, Basuroy S, Tcheranova D. Contributions of astrocytes and CO to pial arteriolar dilation to glutamate in newborn pigs. Am J Physiol Heart Circ Physiol 291: H2897-H2904, 2006.
20. Lloyd EE, Crossland RF, Phillips SC, Marrelli SP, Reddy AK, Taffet GE, Hartley CJ, Bryan Disruption of K(2P)6 RM Jr.1. produces vascular dysfunction and hypertension in mice. Hypertension 58: 672-678, 2011.
21. + channel, cloned from the rat middle cerebral artery. Exp Biol Med (Maywood) 234: 1493-1502, 2009.
22. Mayhan WG, Mayhan JF, Sun H, Patel KP. In vivo properties of potassium channels in cerebral blood vessels during diabetes mellitus. Microcirculation 11: 605-613, 2004.
23. Meno JR, Nguyen TS, Jensen EM, Alexander West G, Groysman L, Kung DK, Ngai AC, Britz GW, Winn HR. Effect of caffeine on cerebral blood flow response to somatosensory stimulation. J Cereb Blood Flow Metab 25: 775-784, 2005.
24. + channel of cultured porcine coronary artery smooth muscle cells. Biochem Biophys Res Commun 190: 263-269, 1993.
25. Northam EA, Rankins D, Cameron FJ. Therapy insight: the impact of type 1 diabetes on brain development and function. Nat Clin Pract Neurol 2: 78-86, 2006.
26. + channel-related pathways in the coupling of somatosensory activation and pial arteriolar dilation. Am J Physiol Heart Circ Physiol 299: H2009-H2017, 2010.
27. + channels in rabbit coronary arterial smooth muscle cells through protein kinase C. J Cardiovasc Pharmacol 46: 681-689, 2005.
28. Pelligrino DA, Albrecht RF. Chronic hyperglycemic diabetes in the rat is associated with a selective impairment of cerebral vasodilatory responses. J Cereb Blood Flow Metab 11: 667-677, 1991.
29. Pelligrino DA, Koenig HM, Wang Q, Albrecht RF. Protein kinase C suppresses receptor-mediated pial arteriolar relaxation in the diabetic rat. Neuroreport 5: 417-420, 1994.
30. Profenno LA, Porsteinsson AP, Faraone SV. Meta-analysis of Alzheimer's Disease risk with obesity, diabetes, and related disorders. Biol Psychiatry 67: 505-512, 2010.
31. Ramakrishnan R, Sheeladevi R, Namasivayam A. Regulation of protein kinases and coregulatory interplay of S-100beta and serotonin transporter on serotonin levels in diabetic rat brain. J Neurosci Res 87: 246-259, 2009.
32. Ren Y, Xu X, Wang X. Altered mRNA expression of ATP-sensitive and inward rectifier potassium channel subunits in streptozotocin-induced diabetic rat heart and aorta. J Pharmacol Sci 93: 478-483, 2003.
33. Schubert R, Nelson MT. Protein kinases: tuners of the BKCa channel in smooth muscle. Trends Pharmacol Sci 22: 505-512, 2001.
34. Smith PD, Brett SE, Luykenaar KD, Sandow SL, Marrelli SP, Vigmond EJ, Welsh DG. KIR channels function as electrical amplifiers in rat vascular smooth muscle. J Physiol 586: 1147-1160, 2008.
35. Straub SV, Girouard H, Doetsch PE, Hannah RM, Wilkerson MK, Nelson MT. Regulation of intracerebral arteriolar tone by Kv channels: effects of glucose and PKC. Am J Physiol Cell Physiol 297: C788-C796, 2009.
36. + channels in cultured rat mesenteric artery smooth muscle cells. Biol Pharm Bull 23: 1450-1454, 2000.
37. 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.
38. Vetri F, Menicucci D, Lapi D, Gemignani A, Colantuoni A. Pial arteriolar vasomotion changes during cortical activation in rats. Neuroimage 38: 25-33, 2007.
39. Vetri F, Xu H, Mao L, Paisansathan C, Pelligrino DA. ATP hydrolysis pathways and their contributions to pial arteriolar dilation in rats. Am J Physiol Heart Circ Physiol 301: H1369-H1377, 2011.
40. Vetri F, Xu HL, Mao L, Pelligrino DA. Diabetes-related changes in neurovascular coupling in rats are gender-specific. Soc Neurosci Meet 2008, Washington, DC.
41. + channels in cerebral artery smooth muscle and alters functional conductance. Curr Neurovasc Res 7: 75-84, 2010.
42. Widmer HA, Rowe IC, Shipston MJ. Conditional protein phosphorylation regulates BK channel activity in rat cerebellar Purkinje neurons. J Physiol 552: 379-391, 2003.
43. + channels in cerebral arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 292: H1085-H1094, 2007.
44. Xu HL, Mao L, Ye S, Paisansathan C, Vetri F, Pelligrino DA. Astrocytes are a key conduit for upstream signaling of vasodilation during cerebral cortical neuronal activation in vivo. Am J Physiol Heart Circ Physiol 294: H622-H632, 2008.
45. Xu HL, Pelligrino DA. ATP release and hydrolysis contribute to rat pial arteriolar dilatation elicited by neuronal activation. Exp Physiol 92: 647-651, 2007.
46. Zaritsky JJ, Eckman DM, Wellman GC, Nelson MT, Schwarz TL. Targeted disruption of Kir2.1 and Kir22 genes reveals the essential role of the inwardly rectifying K(+) current in K(+)-mediated vasodilation. Circ Res 87: 160-166, 2000.
47. Zhou XB, Wulfsen I, Utku E, Sausbier U, Sausbier M, Wieland T, Ruth P, Korth M. Dual role of protein kinase C on BK channel regulation. Proc Natl Acad Sci USA 107: 8005-8010, 2010.