Epoxyeicosatrienoic acid-dependent cerebral vasodilation evoked by metabotropic glutamate receptor activation in vivo

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 2, 2011, Pages

  Liu, Xiaoguang ^a   Li, Chunyuan ^a   Gebremedhin, Debebe ^b   Hwang, Sung Hee ^c   Hammock, Bruce D ^c   Falck, John R ^d   Roman, Richard J ^e   Harder, David R ^b   Koehler, Raymond C ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Astrocyte; Cerebral blood flow; Epoxide hydrolase; Epoxygenase; Neurovascular coupling

Indexed keywords

14,15 EPOXYEICOSA 5 ENOIC ACID; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 20 HYDROXYICOSATETRAENOIC ACID; 3,5 DIHYDROXYPHENYLGLYCINE; 4 [4 (3 ADAMANTAN 1 YL UREIDO)CYCLOHEXYLOXY]BENZOIC ACID; 4 CARBOXY 2 METHYLPHENYLGLYCINE; 5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; 7 NITROINDAZOLE; ADENOSINE A2B RECEPTOR INHIBITOR; ALLOXAZINE; BRADYKININ; CHROMIUM MESOPORPHYRIN; CYCLOOXYGENASE 1 INHIBITOR; EPOXIDE HYDROLASE INHIBITOR; EPOXYICOSATRIENOIC ACID; FATTY ACID SYNTHASE INHIBITOR; GLUTAMIC ACID; HEME OXYGENASE INHIBITOR; HYDROLASE INHIBITOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; N METHYLSULFONYL 6 (2 PROPARGYLOXYPHENYL)HEXANAMIDE; NEURONAL NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; CEREBRAL VASODILATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVITY; EVOKED RESPONSE; HYPERCAPNIA; IN VIVO STUDY; LASER DOPPLER FLOWMETRY; MALE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PHARMACOLOGICAL STIMULATION; PIA ARTERY; PRIORITY JOURNAL; RAT; VASODILATATION;

8,11,14-EICOSATRIENOIC ACID; ADENOSINE A2 RECEPTOR ANTAGONISTS; ANALYSIS OF VARIANCE; ANIMALS; ARTERIOLES; BLOOD FLOW VELOCITY; CEREBRAL ARTERIES; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; EPOXIDE HYDROLASES; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GLYCINE; HEME OXYGENASE (DECYCLIZING); HYDROXYEICOSATETRAENOIC ACIDS; LASER-DOPPLER FLOWMETRY; MALE; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A2B; RECEPTORS, METABOTROPIC GLUTAMATE; REGIONAL BLOOD FLOW; RESORCINOLS; SIGNAL TRANSDUCTION; TIME FACTORS; VASODILATION; VASODILATOR AGENTS;

EID: 79961046351     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00745.2010     Document Type: Article

References (48)

1. Alkayed NJ, Birks EK, Narayanan J, Petrie KA, Kohler-Cabot AE, Harder DR. Role of P-450 arachidonic acid expoygenase 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. Amruthesh SC, Boerschel MF, McKinney JS, Willoughby KA, Ellis EF. Metabolism of arachidonic acid to epoxyeicosatrienoic acids, hydroxyeicosatetraenoic acids, and prostaglandins in cultured rat hippocampal astrocytes. J Neurochem 61: 150-159, 1993.
4. Bhardwaj A, Northington FJ, Martin LJ, Hanley DF, Traystman RJ, Koehler RC. Characterization of metabotropic glutamate receptor-mediated nitric oxide production in vivo. J Cereb Blood Flow Metab 17: 153-160, 1997.
5. Blanco VM, Stern JE, Filosa JA. Tone-dependent vascular responses to astrocyte-derived signals. Am J Physiol Heart Circ Physiol 294: H2855- H2863, 2008.
6. Brenneis C, Maier TJ, Schmidt R, Hofacker A, Zulauf L, Jakobsson PJ, Scholich K, Geisslinger G. Inhibition of prostaglandin E2 synthesis by SC-560 is independent of cyclooxygenase 1 inhibition. FASEB J 20: 1352-1360, 2006.
7. Chaudhary KR, Abukhashim M, Hwang SH, Hammock BD, Seubert JM. Inhibition of soluble epoxide hydrolase by trans-4-[4-(3-adamantan-1-yl-ureido)-cyclohexyloxy]-benzoic acid is protective against ischemiareperfusion injury. J Cardiovasc Pharmacol 55: 67-73, 2010.
8. Cholet N, Bonvento G, Seylaz J. Effect of neuronal NO synthase inhibition on the cerebral vasodilatory response to somatosensory stimulation. Brain Res 708: 197-200, 1996.
9. Dunn KM, Renic M, Flasch AK, Harder DR, Falck J, Roman RJ. Elevated production of 20-HETE in the cerebral vasculature contributes to severity of ischemic stroke and oxidative stress in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 295: H2455-H2465, 2008.
10. 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.
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. Gauthier KM, Deeter C, Krishna UM, Reddy YK, Bondlela M, Falck JR, Campbell WB. 14,15-Epoxyeicosa-5(Z)-enoic acid: a selective epoxyeicosatrienoic acid antagonist that inhibits endothelium-dependent hyperpolarization and relaxation in coronary arteries. Circ Res 90: 1028-1036, 2002.
13. 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.
14. + channels in rat hippocampal astrocytes. J Neurosci 23: 1678-1687, 2003.
15. 2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 107: 3811-3816, 2010.
16. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA. Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456: 745-749, 2008.
17. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11: 227-238, 2010.
18. Hwang SH, Tsai HJ, Liu JY, Morisseau C, Hammock BD. Orally bioavailable potent soluble epoxide hydrolase inhibitors. J Med Chem 50: 3825-3840, 2007.
19. Koehler RC, Roman RJ, Harder DR. Astrocytes and the regulation of cerebral blood flow. Trends Neurosci 32: 160-169, 2009.
20. 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.
21. Li A, Xi Q, Umstot ES, Bellner L, Schwartzman ML, Jaggar JH, Leffler CW. Astrocyte-derived CO is a diffusible messenger that mediates glutamate-induced cerebral arteriolar dilation by activating smooth muscle cell KCa channels. Circ Res 102: 234-241, 2008.
22. Lindauer U, Megow D, Matsuda H, Dirnagl U. Nitric oxide: a modulator, but not a mediator, of neurovascular coupling in rat somatosensory cortex. Am J Physiol Heart Circ Physiol 277: H799-H811, 1999.
23. Liu X, Li C, Falck JR, Roman RJ, Harder DR, Koehler RC. Interaction of nitric oxide, 20-HETE, and EETs during functional hyperemia in whisker barrel cortex. Am J Physiol Heart Circ Physiol 295: H619-H631, 2008.
24. McGiff JC, Quilley J. 20-HETE and the kidney: resolution of old problems and new beginnings. Am J Physiol Regul Integr Comp Physiol 277: R607-R623, 1999.
25. 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.
26. Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431: 195-199, 2004.
27. Newman EA. Calcium increases in retinal glial cells evoked by lightinduced neuronal activity. J Neurosci 25: 5502-5510, 2005.
28. 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.
29. 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.
30. 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.
31. Ohata H, Cao S, Koehler RC. Contribution of adenosine A2A and A2B receptors and heme oxygenase to AMPA-induced dilation of pial arterioles in rats. Am J Physiol Regul Integr Comp Physiol 291: R728-R735, 2006.
32. 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.
33. 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.
34. Pilitsis JG, Kimelberg HK. Adenosine receptor mediated stimulation of intracellular calcium in acutely isolated astrocytes. Brain Res 798: 294-303, 1998.
35. Qin X, Kwansa H, Bucci E, Roman RJ, Koehler RC. Role of 20-HETE in the pial arteriolar constrictor response to decreased hematocrit after exchange transfusion of cell-free polymeric hemoglobin. J Appl Physiol 100: 336-342, 2006.
36. Robinson JS, Fedinec AL, Leffler CW. Role of carbon monoxide in glutamate receptor-induced dilation of newborn pig pial arterioles. Am J Physiol Heart Circ Physiol 282: H2371-H2376, 2002.
37. Schoepp DD, Goldsworthy J, Johnson BG, Salhoff CR, Baker SR. 3,5-Dihydroxyphenylglycine is a highly selective agonist for phosphoinositide- linked metabotropic glutamate receptors in the rat hippocampus. J Neurochem 63: 769-772, 1994.
38. Shi Y, Liu X, Gebremedhin D, Falck JR, Harder DR, Koehler RC. Interaction of mechanisms involving epoxyeicosatrienoic acids, adenosine receptors, and metabotropic glutamate receptors in neurovascular coupling in rat whisker barrel cortex. J Cereb Blood Flow Metab 28: 111-125, 2008.
39. Stefanovic B, Bosetti F, Silva AC. Modulatory role of cyclooxygenase-2 in cerebrovascular coupling. Neuroimage 32: 23-32, 2006.
40. + channel activity and vascular tone in renal arterioles. Circ Res 83: 1069-1079, 1998.
41. 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.
42. Tsai HJ, Hwang SH, Morisseau C, Yang J, Jones PD, Kasagami T, Kim IH, Hammock BD. Pharmacokinetic screening of soluble epoxide hydrolase inhibitors in dogs. Eur J Pharm Sci 40: 222-238, 2010.
43. Wang H, Hitron IM, Iadecola C, Pickel VM. Synaptic and vascular associations of neurons containing cyclooxygenase-2 and nitric oxide synthase in rat somatosensory cortex. Cereb Cortex 15: 1250-1260, 2005.
44. 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.
45. 2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9: 816-823, 2006.
46. Yamaura K, Gebremedhin D, Zhang C, Narayanan J, Hoefert K, Jacobs ER, Koehler RC, Harder DR. Contribution of epoxyeicosatrienoic acids to the hypoxia-induced activation of Ca(2+)-activated K(+) channel current in cultured rat hippocampal astrocytes. Neuroscience 143: 703-716, 2006.
47. 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.
48. Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T, Carmignoto G. Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553: 407-414, 2003.