Cerebral capillary endothelial cell mitogenesis and morphogenesis induced by astrocytic epoxyeicosatrienoic acid

Stroke

Volumn 33, Issue 12, 2002, Pages 2957-2964

  Zhang, Chenyang ^a   Harder, David R ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Angiogenesis; Capillaries; Cells, cultured; Cytochrome P 450; Gap junctions; Rats

Indexed keywords

EPOXYICOSATRIENOIC ACID; GENISTEIN; MATRIGEL; PROTEIN TYROSINE KINASE; THYMIDINE DERIVATIVE; TRITIUM;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; ARTIFACT; ASTROCYTE; BASEMENT MEMBRANE; BRAIN CAPILLARY; CAPILLARY ENDOTHELIUM; CELL ACTIVATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; COCULTURE; CULTURE MEDIUM; DNA SYNTHESIS; ENDOTHELIUM CELL; ENZYME INHIBITION; GAP JUNCTION; IMMUNOHISTOCHEMISTRY; MITOGENESIS; MORPHOGENESIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; ASTROCYTES; BRAIN; CAPILLARIES; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MITOSIS; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; THYMIDINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0036901546     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.STR.0000037787.07479.9A     Document Type: Article

References (46)

1. Araque A, Carmignoto G, Haydon PG. Dynamic signaling between astrocytes and neurons. Annu Rev Physiol. 2001;63:795-813.
2. Temburni MK, Jacob MH. New functions for glial in the brain. Proc Natl Acad Sci U S A. 2001;98:3631-3632.
3. Harder DR, Zhang C, Gebremedhin D. Astrocytes function in matching blood flow to metabolic activity. News Physiol Sci. 2002;17:27-31.
4. Ling T, Mitrofanis J, Stone J. Origin of retinal astrocytes in the rat: Evidence of migration from the optic nerve. J Comp Neurol. 1989;286: 345-352.
5. Chan-Ling T, Stone J. Factors determining the migration of astrocytes into the developing retina: Migration does not depend on intact axons or patent vessels. J Comp Neurol. 1991;303:375-386.
6. Schnitzer J. Retinal astrocytes: Their restriction to vascularized parts of the mammalian retina. Neurosci Lett. 1987;78:29-32.
7. Jiang B, Alibezhadian M, Caldwell RB. Astrocytes modulate retinal vasculogenesis: Effects on endothelial cell differentiation. Glia. 1995; 15:1-10.
8. Munzenmaier DH, Harder DR. Cerebral microvascular endothelial cell tube formation: Role of astrocytic epoxyeicosatrienoic acid release. Am J Physiol. 2000;278:H1163-H1167.
9. Alkayed NJ. Narayanan J, Gebremedhin D, Medhora M, Roman RJ, Harder DR. Molecular characterization of an arachidonic acid epoxygenase in rat brain astrocytes. Stroke. 1996;27:971-979.
10. Capdevila J, Pramanik B, Napoli JL, Manna S, Falck JR. Arachidonic acid epoxidation: Epoxyeicosatrienoic acids are endogenous constituents of rat liver. Arch Biochem Biophys. 1984;231:511-517.
11. Laniado-Schwartzman ML, Davis KL, McGiff JC, Levere RD, Abraham NG. Purification and characterization of cytochrome P-450-dependent arachidonic acid epoxygenase from human liver. J Biol Chem. 1988;263: 2536-2542.
12. Murphy S, Pearce B, Jeremy J, Dandona P. Astrocytes as eicosanoid-producing cells. Glia. 1988;1:241-245.
13. Deleted in proof.
14. 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. 1997;28:1066-1072.
15. Leffler CW, Fedinec AL. Newborn piglet cerebral microvascular response to epoxyeicosatrienoic acids. Am J Physiol. 1997;273: H333-H335.
16. Picciano PT, Johnson B, Walenga RW, Donovan M, Borman BJ, Douglas WH, Kreutzer DL. Effects of D-valine on pulmonary artery endothelial cell morphology and function in cell culture. Exp Cell Res. 1984;151: 134-147.
17. Abbott NJ, Hughes CC, Revest PA, Greenwood J. Development and characterization of a rat brain capillary endothelial culture: Towards an in vitro blood brain barrier. J Cell Sci. 1992;103:23-37.
18. Mccarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980;85: 890-902.
19. Laterra J, Christopher G, Goldstein GW. Astrocytes induce neural microvascular endothelial cells to form capillary-like structures in vitro. J Cell Physiol. 1990;144:204-215.
20. Passaniti A. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest. 1992;67:519-528.
21. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306-1309.
22. Lange A. Gebremedhin D, Narayanan J, Harder D. 20-Hydroxyeicosatetraenoic acid-induced vasoconstriction and inhibition of potassium current in cerebral vascular smooth muscle is dependent on activation of protein kinase C. J Biol Chem. 1997;272:27345-27352.
23. Suarez I, Bodega G, Rubio M, Garcia-Segura LM, Fernandez B. Astroglial induction of in vivo angiogenesis. J Neural Transplant Plast. 1994;5:1-10.
24. O'Callaghan JP. Quantitative features of reactive gliosis following toxicant-induced damage of the CNS. Ann N Y Acad Sci. 1993;679: 195-210.
25. Rakic P. Limits of neurogenesis in primates. Science. 1985;227: 1054-1056.
26. Sellmayer A, Uedelhoven WM, Weber PC, Bonventre JV. Endogenous non-cyclooxygenase metabolites of arachidonic acid modulate growth and mRNA levels of immediate-early response genes in rat mesangial cells. J Biol Chem. 1991;266:3800-3807.
27. 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. 1993;61:150-159.
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. 2001;298:327-336.
29. Burns KD, Capdevila J, Wei S, Breyer MD, Homma T, Harris RC. Role of cytochrome P-450 epoxygenase metabolites in EGF signaling in renal proximal tubule. Am J Physiol. 1995;269:C831-C840.
30. + exchange and are mitogenic in cultured rat glomerular mesangial cells. J Cell Physiol. 1990;144:429-437.
31. Homma T, Zhang JY, Shimizu T, Prakash C, Blair IA, Harris RC, Cyclooxygenase-derived metabolites of 8,9-epoxyeicosatrienoic acid are potent mitogens for cultured rat glomerular mesangial cells. Biochem Biophys Res Commun. 1993;191:282-288.
32. Chen JK, Falck JR, Reddy KM, Capdevila J, Harris RC. Epoxyeicosatrienoic acids and their sulfonamide derivatives stimulate tyrosine phosphorylation and induce mitogenesis in renal epithelial cells. J Biol Chem. 1998;273:29254-29261.
33. Ment LR, Stewart WB, Fronc R, Seashore C, Mahooti S, Scaramuzzino D, Madri JA. Vascular endothelial growth factor mediates reactive angiogenesis in the developing brain. Brain Res Dev Brain Res. 1997;100: 52-61.
34. Stone J, Ltin A, Gnessin H, Chan-Ling T, Pe'er Y, Keshet R. Normal retinal vascularisation is mediated by the hypoxia-induced expression of vascular endothelial growth factor by retinal glia. Exp Eye Res. 1994; 59:S65. Abstract.
35. Plate KH. Mechanism of angiogenesis in the brain. J Neuropathol Exp Neurol. 1999;58:313-320.
36. Mart HH, Risau W. Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci U S A. 1998;95:15809-15814.
37. Bbardwaj 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. 2000;279:H1616-H1624.
38. Harder DR, Alkayed NJ, Lange AR, Gebremedhin D, Roman RJ. Functional hyperemia in the brain: Hypothesis for astrocyte-derived vasodilator metabolites. Stroke. 1998;29:229-234.
39. Borowsky IW, Collins RC. Metabolic anatomy of brain: A comparison of regional capillary density, glucose metabolism, and enzyme activities. J Comp Neurol. 1989;288:401-413.
40. Isaacs KR, Anderson BJ, Alcantara AA, Black JE, Greenough WT. Exercise and the brain: Angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J Cereb Blood Flow Metab. 1992;12:110-119.
41. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ Res. 1996;78:415-423.
42. Harder DR, Roman RJ, Gebremedbin D. Molecular mechanisms controlling nutritive blood flow: Role of cytochrome P450 enzymes. Acta Physiol Scand. 2000;168:543-549.
43. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL, Jain RK. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci U S A. 2001;98:2604-2609.
44. Chen JK, Wang DW, Falck JR, Capdevila J, Harris RC. Transfection of an active cytochrome P450 arachidonic acid epoxygenase indicates that 14, 15-epoxyeicosatrienoic acid functions as an intracellular second messenger in response to epidermal growth factor. J Biol. Chem. 1999;274: 4764-4769.
45. Chen JK, Capdevila J, Harris RC. Overexpression of C-terminal Src kinase blocks 14,15-epoxyeicosatrienoic acid-induced tyrosine phosphorylation and mitogenesis. J Biol Chem. 2000;275:13789-13792.
46. Shivachar AC, Willoughby KA, Ellis EF. Effect of protein kinase C modulation on 14,15-epoxyeicosatrienoic acid incorporation into astroglial phospholipids. J Neurochem. 1995;65:338-346.