Tone-dependent vascular responses to astrocyte-derived signals

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 6, 2008, Pages

  Blanco, Víctor M ^a   Stern, Javier E ^a   Filosa, Jessica A ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Epoxyeicosatrienoic acid; Glia; Glutamate; Neurovascular coupling; Potassium

Indexed keywords

11,12 EPOXY 5,8,14 ICOSATRIENOIC ACID; ALKANE 1 MONOOXYGENASE; ARACHIDONIC ACID; CYCLOOXYGENASE 1; CYTOCHROME P450; EPOXYICOSATRIENOIC ACID; METABOTROPIC RECEPTOR; PHOSPHOLIPASE A2; POTASSIUM; UNCLASSIFIED DRUG; 1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 1-AMINO-1,3-DICARBOXYCYCLOPENTANE; 11,12 EPOXY 5,8,14 EICOSATRIENOIC ACID; 11,12-EPOXY-5,8,14-EICOSATRIENOIC ACID; 15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; AMINO ACID RECEPTOR STIMULATING AGENT; CALCIUM; CYCLOLEUCINE; DIHOMO GAMMA LINOLENIC ACID; DRUG DERIVATIVE; VASOCONSTRICTOR AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTERY DIAMETER; ARTICLE; ASTROCYTE; BLOOD VESSEL TONE; BRAIN SLICE; CONTROLLED STUDY; ENZYME INHIBITION; HYPEREMIA; NONHUMAN; PRIORITY JOURNAL; RAT; VASOCONSTRICTION; VASODILATATION; ANIMAL; ARTERIOLE; BRAIN CORTEX; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; IN VITRO STUDY; METABOLISM; PARACRINE SIGNALING; SPRAGUE DAWLEY RAT; VASCULARIZATION;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; 8,11,14-EICOSATRIENOIC ACID; ANIMALS; ARACHIDONIC ACID; ARTERIOLES; ASTROCYTES; CALCIUM; CEREBRAL CORTEX; CYCLOLEUCINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; PARACRINE COMMUNICATION; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION;

EID: 49249138741     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.91451.2007     Document Type: Article

References (60)

1. Alkayed NJ, Birks EK, Narayanan J, Petrie KA, Kohler-Cabot AE, Harder DR. Role of P-450 arachidonic acid epoxygenase in the response of cerebral blood flow to glutamate in rats. Stroke 28: 1066-1072, 1997.
2. Alkayed NJ, Narayanan J, Gebremedhin D, Medhora M, Roman RJ, Harder DR. Molecular characterization of an arachidonic acid epoxygenase in rat brain astrocytes. Stroke 27: 971-979, 1996.
3. Armstead WM, Mirro R, Busija DW, Leffler CW. Vascular responses to vasopressin are tone-dependent in the cerebral circulation of the newborn pig. Circ Res 64: 136-144, 1989.
4. Barman SA, Zhu S, Han G, White RE. cAMP activates BKCa channels in pulmonary arterial smooth muscle via cGMP-dependent protein kinase. Am J Physiol Lung Cell Mol Physiol 284: L1004-L1011, 2003.
5. Bhardwaj A, Northington FJ, Carhuapoma JR, Falck JR, Harder DR, Traystman RJ, Koehler RC. P-450 epoxygenase and NO synthase inhibitors reduce cerebral blood flow response to N-methyl-D-aspartate. Am J Physiol Heart Circ Physiol 279: H1616-H1624, 2000.
6. Blanco VM, Filosa JA. The Influence of Resting Arteriolar Tone on Vascular Responses to Glial Activation: Neuroscience Meeting Planner. San Diego, CA: Soc Neurosci, program no. 479.12, 2007.
7. + channels in 11,12-epoxyeicosatrienoic acid-induced vasodilation of parenchymal arterioles: possible role of astrocytes. FASEB J 21: 748-744, 2007.
8. Brahma B, Forman RE, Stewart EE, Nicholson C, Rice ME. Ascorbate inhibits edema in brain slices. J Neurochem 74: 1263-1270, 2000.
9. Brekke JF, Gokina NI, Osol G. Vascular smooth muscle cell stress as a determinant of cerebral artery myogenic tone. Am J Physiol Heart Circ Physiol 283: H2210-H2216, 2002.
10. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24: 8940-8949, 2004.
11. Chuquet J, Hollender L, Nimchinsky EA. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J Neurosci 27: 4036-4044, 2007.
12. Cipolla MJ, Li R, Vitullo L. Perivascular innervation of penetrating brain parenchymal arterioles. J Cardiovasc Pharmacol 44: 1-8, 2004.
13. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27: 4452-4459, 2007.
14. 2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279, 2005.
15. Esguerra M, Wang J, Foster CD, Adelman JP, North RA, Levitan IB. Cloned Ca(2+)-dependent K+ channel modulated by a functionally associated protein kinase. Nature 369: 563-565, 1994.
16. Fang X, Faraci FM, Kaduce TL, Harmon S, Modrick ML, Hu S, Moore SA, Falck JR, Weintraub NL, Spector AA. 20-Hydroxyeicosatetraenoic acid is a potent dilator of mouse basilar artery: role of cyclooxygenase. Am J Physiol Heart Circ Physiol 291: H2301-H2307, 2006.
17. Fang X, Weintraub NL, Stoll LL, Spector AA. Epoxyeicosatrienoic acids increase intracellular calcium concentration in vascular smooth muscle cells. Hypertension 34: 1242-1246, 1999.
18. Faraci FM, Heistad DD. Regulation of the cerebral circulation: role of endothelium and potassium channels. Physiol Rev 78: 53-97, 1998.
19. Filosa JA, Blanco VM. Neurovascular coupling in the mammalian brain. Exp Physiol 92: 641-646, 2007.
20. Filosa JA, Bonev AD, Nelson MT. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res 95: e73-e81, 2004.
21. 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.
22. Gebremedhin D, Lange AR, Lowry TF, Taheri MR, Birks EK, Hudetz AG, Narayanan J, Falck JR, Okamoto H, Roman RJ, Nithipatikom K, Campbell WB, Harder DR. Production of 20-HETE and its role in autoregulation of cerebral blood flow. Circ Res 87: 60-65, 2000.
23. Gebremedhin D, Ma YH, Falck JR, Roman RJ, VanRollins M, Harder DR. Mechanism of action of cerebral epoxyeicosatrienoic acids on cerebral arterial smooth muscle. Am J Physiol Heart Circ Physiol 263: H519-H525, 1992.
24. Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100: 328-335, 2006.
25. 2 Determines the Polarity of Astrocyte-mediated Vasomotor Responses: Neuroscience Meeting Planner. San Diego, CA: Soc Neurosci, program no. 148.8, 2007.
26. Harder DR, Alkayed NJ, Lange AR, Gebremedhin D, Roman RJ. Functional hyperemia in the brain: hypothesis for astrocyte-derived vasodilator metabolites. Stroke 29: 229-234, 1998.
27. Harder DR, Narayanan J, Birks EK, Liard JF, Imig JD, Lombard JH, Lange AR, Roman RJ. Identification of a putative microvascular oxygen sensor. Circ Res 79: 54-61, 1996.
28. Haydon PG, Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86: 1009-1031, 2006.
29. Holthoff K, Witte OW. Directed spatial potassium redistribution in rat neocortex. Glia 29: 288-292, 2000.
30. Iizuka K, Akahane K, Momose D, Nakazawa M, Tanouchi T, Kawamura M, Ohyama I, Kajiwara I, Iguchi Y, Okada T, Taniguchi K, Miyamoto T, Hayashi M. Highly selective inhibitors of thromboxane synthetase. 1. Imidazole derivatives. J Med Chem 24: 1139-1148, 1981.
31. 2+ oscillations. Biophys J 90: 1-23, 2006.
32. +-induced hyperpolarizations and dilatations of rat coronary and cerebral arteries involve inward rectifier K(+) channels. J Physiol 492: 419-430, 1996.
33. Koehler RC, Gebremedhin D, Harder DR. Role of astrocytes in cerebrovascular regulation. J Appl Physiol 100: 307-317, 2006.
34. Kriegler S, Chiu SY. Calcium signaling of glial cells along mammalian axons. J Neurosci 13: 4229-4245, 1993.
35. Kuschinsky W, Wahl M, Bosse O, Thurau K. Perivascular potassium and pH as determinants of local pial arterial diameter in cats. A microapplication study. Circ Res 31: 240-247, 1972.
36. Lovick TA, Brown LA, Key BJ. Neuronal activity-related coupling in cortical arterioles: involvement of astrocyte-derived factors. Exp Physiol 90: 131-140, 2005.
37. Lovick TA, Brown LA, Key BJ. Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience 92: 47-60, 1999.
38. McCarron JG, Halpern W. Potassium dilates rat cerebral arteries by two independent mechanisms. Am J Physiol Heart Circ Physiol 259: H902-H908, 1990.
39. Metea MR, Newman EA. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26: 2862-2870, 2006.
40. Miyata N, Taniguchi K, Seki T, Ishimoto T, Sato-Watanabe M, Yasuda Y, Doi M, Kametani S, Tomishima Y, Ueki T, Sato M, Kameo K. HET0016, a potent and selective inhibitor of 20-HETE synthesizing enzyme. Br J Pharmacol 133: 325-329, 2001.
41. Mosso A. Sulla circolazione del cervello dell'uomo. Atti R Accad Lincei 5: 237-358, 1880.
42. Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431: 195-199, 2004.
43. Nithipatikom K, Grall AJ, Holmes BB, Harder DR, Falck JR, Campbell WB. Liquid chromatographic-electrospray ionization-mass spectrometric analysis of cytochrome P450 metabolites of arachidonic acid. Anal Biochem 298: 327-336, 2001.
44. Niwa K, Araki E, Morham SG, Ross ME, Iadecola C. Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J Neurosci 20: 763-770, 2000.
45. Niwa K, Haensel C, Ross ME, Iadecola C. Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ Res 88: 600-608, 2001.
46. + channels in cerebral vasodilatation induced by increases in cyclic GMP and cyclic AMP in the rat. Stroke 27: 1603-1608, 1996.
47. Peng X, Carhuapoma JR, Bhardwaj A, Alkayed NJ, Falck JR, Harder DR, Traystman RJ, Koehler RC. Suppression of cortical functional hyperemia to vibrissal stimulation in the rat by epoxygenase inhibitors. Am J Physiol Heart Circ Physiol 283: H2029-H2037, 2002.
48. Peng X, Zhang C, Alkayed NJ, Harder DR, Koehler RC. Dependency of cortical functional hyperemia to forepaw stimulation on epoxygenase and nitric oxide synthase activities in rats. J Cereb Blood Flow Metab 24: 509-517, 2004.
49. Peppiatt C, Attwell D. Neurobiology: feeding the brain. Nature 431: 137-138, 2004.
50. Porter VA, Bonev AD, Knot HJ, Heppner TJ, Stevenson AS, Kleppisch T, Lederer WJ, Nelson MT. Frequency modulation of Ca2+ sparks is involved in regulation of arterial diameter by cyclic nucleotides. Am J Physiol Cell Physiol 274: C1346-C1355, 1998.
51. Regan JW. EP2 and EP4 prostanoid receptor signaling. Life Sci 74: 143-153, 2003.
52. Rosenblum WI, Nelson GH. Tone regulates opposing endothelium-dependent and -independent forces: resistance brain vessels in vivo. Am J Physiol Heart Circ Physiol 259: H243-H247, 1990.
53. Roy CS, Sherrington C. On the regulation of the blood supply of the brain. J Physiol 11: 85-108, 1890.
54. Rzigalinski BA, Willoughby KA, Hoffman SW, Falck JR, Ellis EF. Calcium influx factor, further evidence it is 5,6-epoxyeicosatrienoic acid. J Biol Chem 274: 175-182, 1999.
55. Straub SV, Bonev AD, Wilkerson MK, Nelson MT. Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J Gen Physiol 128: 659-669, 2006.
56. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9: 260-267, 2006.
57. Wang MH, Brand-Schieber E, Zand BA, Nguyen X, Falck JR, Balu N, Schwartzman ML. Cytochrome P450-derived arachidonic acid metabolism in the rat kidney: characterization of selective inhibitors. J Pharmacol Exp Ther 284: 966-973, 1998.
58. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 434-438, 2003.
59. Winship IR, Plaa N, Murphy TH. Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J Neurosci 27: 6268-6272, 2007.
60. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6: 43-50, 2003.