Epoxyeicosatrienoic acids are endogenous regulators of vasoactive neuropeptide release from trigeminal ganglion neurons

Journal of Neurochemistry

Volumn 115, Issue 6, 2010, Pages 1530-1542

  Iliff, Jeffrey J ^a,b   Fairbanks, Stacy L ^a   Balkowiec, Agnieszka ^b   Alkayed, Nabil J ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

calcitonin gene related peptide; cytochrome P450 epoxygenase; epoxyeicosatrienoic acid; perivascular nerves; substance P; transient receptor potential vanilloid 1

Indexed keywords

14,15 EPOXY 5,8,11 ICOSATRIENOIC ACID; CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; CYTOCHROME P450 2J2; CYTOCHROME P450 2J3; CYTOCHROME P450 2J4; EPOXYICOSATRIENOIC ACID; NEUROPEPTIDE; SUBSTANCE P; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOCYTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MEMBRANE DEPOLARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TRIGEMINUS GANGLION;

RATTUS;

EID: 78649984660     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07059.x     Document Type: Article

References (51)

1. Alkayed N. J., Narayanan J., Gebremedhin D., Medhora M., Roman R. J., and, Harder D. R., (1996) Molecular characterization of an arachidonic acid epoxygenase in rat brain astrocytes. Stroke 27, 971-979.
2. Alkayed N. J., Birks E. K., Narayanan J., Petrie K. A., Kohler-Cabot A. E., and, Harder D. R., (1997) Role of P-450 arachidonic acid epoxygenase in the response of cerebral blood flow to glutamate in rats. Stroke 28, 1066-1072.
3. Benemei S., Nicoletti P., Capone J. A., and, Geppetti P., (2007) Pain pharmacology in migraine: focus on CGRP and CGRP receptors. Neurol. Sci. 28 (Suppl. 2), S89-S93.
4. Buldyrev I., Tanner N. M., Hsieh H. Y., Dodd E. G., Nguyen L. T., and, Balkowiec A., (2006) Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J. Neurochem. 99, 1338-1350.
5. Canonico P. L., Judd A. M., Koike K., Valdenegro C. A., and, MacLeod R. M., (1985) Arachidonate stimulates prolactin release in vitro: a role for the fatty acid and its metabolites as intracellular regulator(s) in mammotrophs. Endocrinology 116, 218-225.
6. Capdevila J., Chacos N., Falck J. R., Manna S., Negro-Vilar A., and, Ojeda S. R., (1983) Novel hypothalamic arachidonate products stimulate somatostatin release from the median eminence. Endocrinology 113, 421-423.
7. Cashman J. R., (1989) 5,6-Epoxyeicosatrienoic acid stimulates growth hormone release in rat anterior pituitary cells. Life Sci. 44, 1387-1393.
8. Cashman J. R., and, Snowdowne K. W., (1992) Prolactin secretion in anterior pituitary cells: effect of eicosanoids. Eicosanoids 5, 153-161.
9. Cashman J. R., Hanks D., and, Weiner R. I., (1987) Epoxy derivatives of arachidonic acid are potent stimulators of prolactin secretion. Neuroendocrinology 46, 246-251.
10. Chen L., Liu C., and, Liu L., (2008) The modulation of voltage-gated potassium channels by anisotonicity in trigeminal ganglion neurons. Neuroscience 154, 482-495.
11. Chen L., Liu C., Liu L., and, Cao X., (2009) Changes in osmolality modulate voltage-gated sodium channels in trigeminal ganglion neurons. Neurosci. Res. 64, 199-207.
12. Durham P. L., (2006) Calcitonin gene-related peptide (CGRP) and migraine. Headache 46 (Suppl. 1), S3-S8.
13. Durham P. L., (2008) Inhibition of calcitonin gene-related peptide function: a promising strategy for treating migraine. Headache 48, 1269-1275.
14. Earley S., Heppner T. J., Nelson M. T., and, Brayden J. E., (2005) TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ. Res. 97, 1270-1279.
15. Edvinsson L., and, Uddman R., (2005) Neurobiology in primary headaches. Brain Res. Brain Res. Rev. 48, 438-456.
16. Ellis E. F., Police R. J., Yancey L., McKinney J. S., and, Amruthesh S. C., (1990) Dilation of cerebral arterioles by cytochrome P-450 metabolites of arachidonic acid. Am. J. Physiol. 259, H1171-H1177.
17. Ellis E. F., Amruthesh S. C., Police R. J., and, Yancey L. M., (1991) Brain synthesis and cerebrovascular action of cytochrome P-450/monooxygenase metabolites of arachidonic acid. Adv. Prostaglandin Thromboxane Leukot. Res. 21A, 201-204.
18. Fang X., Weintraub N. L., McCaw R. B., Hu S., Harmon S. D., Rice J. B., Hammock B. D., and, Spector A. A., (2004) Effect of soluble epoxide hydrolase inhibition on epoxyeicosatrienoic acid metabolism in human blood vessels. Am. J. Physiol. Heart Circ. Physiol. 287, H2412-H2420.
19. Gauthier K. M., Deeter C., Krishna U. M., Reddy Y. K., Bondlela M., Falck J. R., and, Campbell W. B., (2002) 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.
20. Grant A. D., Cottrell G. S., Amadesi S., et al. (2007) Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J. Physiol. 578, 715-733.
21. Gross G. J., Gauthier K. M., Moore J., Campbell W. B., Falck J. R., and, Nithipatikom K., (2009) Evidence for role of epoxyeicosatrienoic acids in mediating ischemic preconditioning and postconditioning in dog. Am. J. Physiol. Heart Circ. Physiol. 297, H47-H52.
22. Hwang S. W., Cho H., Kwak J., et al. (2000) Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl Acad. Sci. USA 97, 6155-6160.
23. Iliff J. J., Close L. N., Selden N. R., and, Alkayed N. J., (2007) A novel role for P450 eicosanoids in the neurogenic control of cerebral blood flow in the rat. Exp. Physiol. 92, 653-658.
24. Iliff J. J., Wang R., Zeldin D. C., and, Alkayed N. J., (2009) Epoxyeicosanoids as mediators of neurogenic vasodilation in cerebral vessels. Am. J. Physiol. Heart Circ. Physiol. 296, H1352-H1363.
25. Inceoglu B., Schmelzer K. R., Morisseau C., Jinks S. L., and, Hammock B. D., (2007) Soluble epoxide hydrolase inhibition reveals novel biological functions of epoxyeicosatrienoic acids (EETs). Prostaglandins Other Lipid Mediat. 82, 42-49.
26. Keseru B., Barbosa-Sicard E., Popp R., et al. (2008) Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J. 22, 4306-4315.
27. Koehler R. C., Gebremedhin D., and, Harder D. R., (2006) Role of astrocytes in cerebrovascular regulation. J. Appl. Physiol. 100, 307-317.
28. Larsen B. T., Miura H., Hatoum O. A., Campbell W. B., Hammock B. D., Zeldin D. C., Falck J. R., and, Gutterman D. D., (2006) Epoxyeicosatrienoic and dihydroxyeicosatrienoic acids dilate human coronary arterioles via BK(Ca) channels: implications for soluble epoxide hydrolase inhibition. Am. J. Physiol. Heart Circ. Physiol. 290, H491-H499.
29. Liu X., Li C., Falck J. R., Roman R. J., Harder D. R., and, Koehler R. C., (2008) Interaction of nitric oxide, 20-HETE, and EETs during functional hyperemia in whisker barrel cortex. Am. J. Physiol. Heart Circ. Physiol. 295, H619-H631.
30. Luini A. G., and, Axelrod J., (1985) Inhibitors of the cytochrome P-450 enzymes block the secretagogue-induced release of corticotropin in mouse pituitary tumor cells. Proc. Natl Acad. Sci. USA 82, 1012-1014.
31. Luini A., Corda D., and, Axelrod J., (1985) Secretagogues elevate cytosolic calcium by stimulating cyclic AMP formation in a corticotropin secreting cell line. Regul. Pept. Suppl. 4, 49-52.
32. Medhora M., Narayanan J., and, Harder D., (2001) Dual regulation of the cerebral microvasculature by epoxyeicosatrienoic acids. Trends Cardiovasc. Med. 11, 38-42.
33. Meng J., Ovsepian S. V., Wang J., Pickering M., Sasse A., Aoki K. R., Lawrence G. W., and, Dolly J. O., (2009) Activation of TRPV1 mediates calcitonin gene-related peptide release, which excites trigeminal sensory neurons and is attenuated by a retargeted botulinum toxin with anti-nociceptive potential. J. Neurosci. 29, 4981-4992.
34. Negro-Vilar A., Snyder G. D., Falck J. R., Manna S., Chacos N., and, Capdevila J., (1985) Involvement of eicosanoids in release of oxytocin and vasopressin from the neural lobe of the rat pituitary. Endocrinology 116, 2663-2668.
35. Peng X., Carhuapoma J. R., Bhardwaj A., Alkayed N. J., Falck J. R., Harder D. R., Traystman R. J., and, Koehler R. C., (2002) Suppression of cortical functional hyperemia to vibrissal stimulation in the rat by epoxygenase inhibitors. Am. J. Physiol. Heart Circ. Physiol. 283, H2029-H2037.
36. Peng X., Zhang C., Alkayed N. J., Harder D. R., and, Koehler R. C., (2004) 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.
37. Roman R. J., (2002) P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol. Rev. 82, 131-185.
38. Sadoshima S., Fujii K., Yao H., Kusuda K., Ibayashi S., and, Fujishima M., (1986) Regional cerebral blood flow autoregulation in normotensive and spontaneously hypertensive rats-effects of sympathetic denervation. Stroke J. Cereb. Circ. 17, 981-984. (Pubitemid 16000742)
39. Seubert J. M., Sinal C. J., Graves J., et al. (2006) Role of soluble epoxide hydrolase in postischemic recovery of heart contractile function. Circ. Res. 99, 442-450.
40. Sipe W. E. B., Brierley S. M., Martin C. M., et al. (2008) Transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1288-G1298.
41. Snyder G. D., Capdevila J., Chacos N., Manna S., and, Falck J. R., (1983) Action of luteinizing hormone-releasing hormone: involvement of novel arachidonic acid metabolites. Proc. Natl Acad. Sci. USA 80, 3504-3507.
42. Snyder G., Lattanzio F., Yadagiri P., Falck J. R., and, Capdevila J., (1986) 5,6-Epoxyeicosatrienoic acid mobilizes Ca2 + in anterior pituitary cells. Biochem. Biophys. Res. Commun. 139, 1188-1194.
43. Spector A. A., and, Norris A. W., (2007) Action of epoxyeicosatrienoic acids on cellular function. Am. J. Physiol. Cell Physiol. 292, C996-C1012.
44. Spector A. A., Fang X., Snyder G. D., and, Weintraub N. L., (2004) Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog. Lipid Res. 43, 55-90.
45. Vriens J., Owsianik G., Fisslthaler B., et al. (2005) Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ. Res. 97, 908-915.
46. Watanabe H., Vriens J., Prenen J., Droogmans G., Voets T., and, Nilius B., (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424, 434-438.
47. Webler A. C., Michaelis U. R., Popp R., Barbosa-Sicard E., Murugan A., Falck J. R., Fisslthaler B., and, Fleming I., (2008) Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis. Am. J. Physiol. Cell Physiol. 295, C1292-C1301.
48. Weintraub N. L., Fang X., Kaduce T. L., VanRollins M., Chatterjee P., and, Spector A. A., (1999) Epoxide hydrolases regulate epoxyeicosatrienoic acid incorporation into coronary endothelial phospholipids. Am. J. Physiol. 277, H2098-H2108.
49. Wu S., Chen W., Murphy E., et al. (1997) Molecular cloning, expression, and functional significance of a cytochrome P450 highly expressed in rat heart myocytes. J. Biol. Chem. 272, 12551-12559.
50. Yang W., Tuniki V. R., Anjaiah S., Falck J. R., Hillard C. J., and, Campbell W. B., (2008) Characterization of epoxyeicosatrienoic acid binding site in U937 membranes using a novel radiolabeled agonist, 20-125i-14,15- epoxyeicosa-8(Z)-enoic acid. J. Pharmacol. Exp. Ther. 324, 1019-1027.
51. Zeldin D. C., (2001) Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 276, 36059-36062.