Endothelin-1 (ET-1) causes death of retinal neurons through activation of nitric oxide synthase (NOS) and production of superoxide anion

Experimental Eye Research

Volumn 86, Issue 1, 2008, Pages 118-130

  Oku, Hidehiro ^a   Fukuhara, Masayuki ^a   Komori, Asako ^a   Okuno, Takashi ^a   Sugiyama, Tetsuya ^a   Ikeda, Tsunehiko ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

amacrine cell; cultured retinal neuron; endothelin; nitric oxide synthase; superoxide anion

Indexed keywords

CYCLO(DEXTRO TRYPTOPHYL DEXTRO ASPARTYLPROLYL DEXTRO VALYLLEUCYL); DIHYDRORHODAMINE 123; ENDOTHELIN 1; HYDROETHIDINE; N (2,6 DIMETHYLPIPERIDINOCARBONYL) 4 METHYLLEUCYL DEXTRO (1 METHOXYCARBONYLTRYPTOPHANYL) DEXTRO NORLEUCINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; SUPEROXIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA AMACRINE CELL; WESTERN BLOTTING;

AMACRINE CELLS; ANIMALS; CELL DEATH; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIN-1; ENZYME ACTIVATION; ENZYME INHIBITORS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PEROXYNITROUS ACID; RATS; RATS, WISTAR; RECEPTOR, ENDOTHELIN B; RETINA; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 36749052872     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2007.10.001     Document Type: Article

References (75)

1. Almeida A., Heales S.J., Bolanos J.P., and Medina J.M. Glutamate neurotoxicity is associated with nitric oxide-mediated mitochondrial dysfunction and glutathione depletion. Brain Res. 790 (1998) 209-216
2. Bindokas V.P., Jordan J., Lee C.C., and Miller R.J. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16 (1996) 1324-1336
3. Blomstrand F., Giaume C., Hansson E., and Ronnback L. Distinct pharmacological properties of ET-1 and ET-3 on astroglial gap junctions and Ca(2+) signaling. Am. J. Physiol. 277 (1999) C616-C627
4. Blomstrand F., Venance L., Siren A.L., Ezan P., Hanse E., Glowinski J., Ehrenreich H., and Giaume C. Endothelins regulate astrocyte gap junctions in rat hippocampal slices. Eur. J. Neurosci. 19 (2004) 1005-1015
5. Brown G.C., and Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 33 (2002) 1440-1450
6. Callera G.E., Tostes R.C., Yogi A., Montezano A.C., and Touyz R.M. Endothelin-1-induced oxidative stress in DOCA-salt hypertension involves NADPH-oxidase-independent mechanisms. Clin. Sci. (Lond.) 110 (2006) 243-253
7. Chun M.H., Oh S.J., Kim I.B., and Kim K.Y. Light and electron microscopical analysis of nitric oxide synthase-like immunoreactive neurons in the rat retina. Vis. Neurosci. 16 (1999) 379-389
8. Cooper C.E., and Giulivi C. Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am. J. Physiol. Cell Physiol. 292 (2007) C1993-C2003
9. Crow J.P. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1 (1997) 147-157
10. Dai X., Galligan J.J., Watts S.W., Fink G.D., and Kreulen D.L. Increased O2*-production and upregulation of ETB receptors by sympathetic neurons in DOCA-salt hypertensive rats. Hypertension 43 (2004) 1048-1054
11. Deng D., Evans T., Mukherjee K., Downey D., and Chakrabarti S. Diabetes-induced vascular dysfunction in the retina: role of endothelins. Diabetologia 42 (1999) 1228-1234
12. Duerrschmidt N., Wippich N., Goettsch W., Broemme H.J., and Morawietz H. Endothelin-1 induces NAD(P)H oxidase in human endothelial cells. Biochem. Biophys. Res. Commun. 269 (2000) 713-717
13. Elfering S.L., Sarkela T.M., and Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J. Biol. Chem. 277 (2002) 38079-38086
14. Forstermann U., and Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113 (2006) 1708-1714
15. Goto R., Doi M., Ma N., Semba R., and Uji Y. Contribution of nitric oxide-producing cells in normal and diabetic rat retina. Jpn. J. Ophthalmol. 49 (2005) 363-370
16. Greenlund L.J., Deckwerth T.L., and Johnson Jr. E.M. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14 (1995) 303-315
17. Harada N., Himeno A., Shigematsu K., Sumikawa K., and Niwa M. Endothelin-1 binding to endothelin receptors in the rat anterior pituitary gland: possible formation of an ETA-ETB receptor heterodimer. Cell Mol. Neurobiol. 22 (2002) 207-226
18. Jones B.W., Watt C.B., Frederick J.M., Baehr W., Chen C.K., Levine E.M., Milam A.H., Lavail M.M., and Marc R.E. Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol. 464 (2003) 1-16
19. de Juan J.A., Moya F.J., Fernandez-Cruz A., and Fernandez-Durango R. Identification of endothelin receptor subtypes in rat retina using subtype-selective ligands. Brain Res. 690 (1995) 25-33
20. Kallberg M.E., Brooks D.E., Garcia-Sanchez G.A., Komaromy A.M., Szabo N.J., and Tian L. Endothelin 1 levels in the aqueous humor of dogs with glaucoma. J. Glaucoma. 11 (2002) 105-109
21. Keller J.N., Kindy M.S., Holtsberg F.W., St. Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., and Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J. Neurosci. 18 (1998) 687-697
22. Kiel J.W. Endothelin modulation of choroidal blood flow in the rabbit. Exp. Eye Res. 71 (2000) 543-550
23. Kimura C., Oike M., Koyama T., and Ito Y. Impairment of endothelial nitric oxide production by acute glucose overload. Am. J. Physiol. Endocrinol. Metab. 280 (2001) E171-E178
24. Kobayashi T., Oku H., Fukuhara M., Kojima S., Komori A., Ichikawa M., Katsumura K., Kobayashi M., Sugiyama T., and Ikeda T. Endothelin-1 enhances glutamate-induced retinal cell death, possibly through ETA receptors. Invest. Ophthalmol. Vis. Sci. 46 (2005) 4684-4690
25. Kojima H., Nakatsubo N., Kikuchi K., Kawahara S., Kirino Y., Nagoshi H., Hirata Y., and Nagano T. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal. Chem. 70 (1998) 2446-2453
26. Kooy N.W., Royall J.A., Ischiropoulos H., and Beckman J.S. Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic. Biol. Med. 16 (1994) 149-156
27. Koppenol W.H., Moreno J.J., Pryor W.A., Ischiropoulos H., and Beckman J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5 (1992) 834-842
28. Koyama Y., Ishibashi T., Hayata K., and Baba A. Endothelins modulate dibutyryl cAMP-induced stellation of cultured astrocytes. Brain Res. 600 (1993) 81-88
29. Koyama Y., Tsujikawa K., Matsuda T., and Baba A. Endothelin-1 stimulates glial cell line-derived neurotrophic factor expression in cultured rat astrocytes. Biochem. Biophys. Res. Commun. 303 (2003) 1101-1105
30. Krishnamoorthy R., Dauphin R., Prasanna G., Johnson C., and Yorio T. Endothelin-1 acts through endothelin B (ETB) receptors to mediate apoptosis of rat retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46 (2005) E-Abstract 4656
31. Lee E.J., Kim K.Y., Gu T.H., Moon J.I., Kim I.B., Lee M.Y., Oh S.J., and Chun M.H. Neuronal nitric oxide synthase is expressed in the axotomized ganglion cells of the rat retina. Brain Res. 986 (2003) 174-180
32. Leonova J., Thorlin T., Aberg N.D., Eriksson P.S., Ronnback L., and Hansson E. Endothelin-1 decreases glutamate uptake in primary cultured rat astrocytes. Am. J. Physiol. Cell Physiol. 281 (2001) C1495-C1503
33. Lipton S.A., Choi Y.B., Pan Z.H., Lei S.Z., Chen H.S., Sucher N.J., Loscalzo J., Singel D.J., and Stamler J.S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364 (1993) 626-632
34. Loomis E.D., Sullivan J.C., Osmond D.A., Pollock D.M., and Pollock J.S. Endothelin mediates superoxide production and vasoconstriction through activation of NADPH oxidase and uncoupled nitric-oxide synthase in the rat aorta. J. Pharmacol. Exp. Ther. 315 (2005) 1058-1064
35. MacCumber M.W., and D'Anna S.A. Endothelin receptor-binding subtypes in the human retina and choroid. Arch. Ophthalmol. 112 (1994) 1231-1235
36. MacCumber M.W., Jampel H.D., and Snyder S.H. Ocular effects of the endothelins: abundant peptides in the eye. Arch. Ophthalmol. 107 (1991) 707-709
37. McPherson D.B., Kilker R.P., and Foley T.D. Superoxide activates constitutive nitric oxide synthase in a brain particulate fraction. Biochem. Biophys. Res. Commun. 296 (2002) 413-418
38. Miles A.M., Bohle D.S., Glassbrenner P.A., Hansert B., Wink D.A., and Grisham M.B. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J. Biol. Chem. 271 (1996) 40-47
39. Moncada S., and Erusalimsky J.D. Does nitric oxide modulate mitochondrial energy generation and apoptosis?. Nat. Rev. Mol. Cell Biol. 3 (2002) 214-220
40. Nambi P., Pullen M., Kincaid J., Nuthulaganti P., Aiyar N., Brooks D.P., Gellai M., and Kumar C. Identification and characterization of a novel endothelin receptor that binds both ETA- and ETB-selective ligands. Mol. Pharmacol. 52 (1997) 582-589
41. Noske W., Hensen J., and Wiederholt M. Endothelin-like immunoreactivity in aqueous humor of patients with primary open-angle glaucoma and cataract. Graefes Arch. Clin. Exp. Ophthalmol. 235 (1997) 551-552
42. Okuno T., Oku H., Sugiyama T., Goto W., and Ikeda T. Evaluation of nitric oxide synthesis in the optic nerve head in vivo using microdialysis and high-performance liquid chromatography and its interaction with endothelin-1. Ophthalmic. Res. 35 (2003) 78-83
43. Palacios-Callender M., Quintero M., Hollis V.S., Springett R.J., and Moncada S. Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 7630-7635
44. Paravicini T.M., and Touyz R.M. Redox signaling in hypertension. Cardiovasc. Res. 71 (2006) 247-258
45. Possel H., Noack H., Augustin W., Keilhoff G., and Wolf G. 2,7-Dihydrodichlorofluorescein diacetate as a fluorescent marker for peroxynitrite formation. FEBS Lett. 416 (1997) 175-178
46. Pou S., Pou W.S., Bredt D.S., Snyder S.H., and Rosen G.M. Generation of superoxide by purified brain nitric oxide synthase. J. Biol. Chem. 267 (1992) 24174-24176
47. Prasanna G., Hulet C., Desai D., Krishnamoorthy R.R., Narayan S., Brun A.M., Suburo A.M., and Yorio T. Effect of elevated intraocular pressure on endothelin-1 in a rat model of glaucoma. Pharmacol. Res. 51 (2005) 41-50
48. Prasanna G., Krishnamoorthy R., Clark A.F., Wordinger R.J., and Yorio T. Human optic nerve head astrocytes as a target for endothelin-1. Invest. Ophthalmol. Vis. Sci. 43 (2002) 2704-2713
49. Prasanna G., Narayan S., Krishnamoorthy R.R., and Yorio T. Eyeing endothelins: a cellular perspective. Mol. Cell Biochem. 253 (2003) 71-88
50. Rattner A., and Nathans J. The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J. Neurosci. 25 (2005) 4540-4549
51. Ripodas A., de Juan J.A., Roldan-Pallares M., Bernal R., Moya J., Chao M., Lopez A., Fernandez-Cruz A., and Fernandez-Durango R. Localisation of endothelin-1 mRNA expression and immunoreactivity in the retina and optic nerve from human and porcine eye. Evidence for endothelin-1 expression in astrocytes. Brain Res. 912 (2001) 137-143
52. Rogers S.D., Demaster E., Catton M., Ghilardi J.R., Levin L.A., Maggio J.E., and Mantyh P.W. Expression of endothelin-B receptors by glia in vivo is increased after CNS injury in rats, rabbits, and humans. Exp. Neurol. 145 (1997) 180-195
53. Rogers S.D., Peters C.M., Pomonis J.D., Hagiwara H., Ghilardi J.R., and Mantyh P.W. Endothelin B receptors are expressed by astrocytes and regulate astrocyte hypertrophy in the normal and injured CNS. Glia 41 (2003) 180-190
54. Rosenberg P.A., Li Y., Ali S., Altiok N., Back S.A., and Volpe J.J. Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J. Neurochem. 73 (1999) 476-484
55. Sasaki Y., Takimoto M., Oda K., Fruh T., Takai M., Okada T., and Hori S. Endothelin evokes efflux of glutamate in cultures of rat astrocytes. J. Neurochem. 68 (1997) 2194-2200
56. Shaw P.J. Molecular and cellular pathways of neurodegeneration in motor neuron disease. J. Neurol. Neurosurg. Psychiatr. 76 (2005) 1046-1057
57. Siren A.L., Lewczuk P., Hasselblatt M., Dembowski C., Schilling L., and Ehrenreich H. Endothelin B receptor deficiency augments neuronal damage upon exposure to hypoxia-ischemia in vivo. Brain Res. 945 (2002) 144-149
58. Stanimirovic D.B., Ball R., Mealing G., Morley P., and Durkin J.P. The role of intracellular calcium and protein kinase C in endothelin-stimulated proliferation of rat type I astrocytes. Glia 15 (1995) 119-130
59. Stokely M.E., Brady S.T., and Yorio T. Effects of endothelin-1 on components of anterograde axonal transport in optic nerve. Invest. Ophthalmol. Vis. Sci. 43 (2002) 3223-3230
60. Syed H., Safa R., Chidlow G., and Osborne N.N. Sulfisoxazole, an endothelin receptor antagonist, protects retinal neurons from insults of ischemia/reperfusion or lipopolysaccharide. Neurochem. Int. 48 (2006) 708-717
61. Taniguchi T., Shimazawa M., Sasaoka M., Shimazaki A., and Hara H. Endothelin-1 impairs retrograde axonal transport and leads to axonal injury in rat optic nerve. Curr. Neurovasc. Res. 3 (2006) 81-88
62. Tezel G., Kass M.A., Kolker A.E., Becker B., and Wax M.B. Plasma and aqueous humor endothelin levels in primary open-angle glaucoma. J. Glaucoma 6 (1997) 83-89
63. Torbidoni V., Iribarne M., Ogawa L., Prasanna G., and Suburo A.M. Endothelin-1 and endothelin receptors in light-induced retinal degeneration. Exp. Eye Res. 81 (2005) 265-275
64. Torreilles F., Salman-Tabcheh S., Guerin M., and Torreilles J. Neurodegenerative disorders: the role of peroxynitrite. Brain Res. Brain Res. Rev. 30 (1999) 153-163
65. Troy C.M., and Shelanski M.L. Down-regulation of copper/zinc superoxide dismutase causes apoptotic death in PC12 neuronal cells. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 6384-6387
66. Vasquez-Vivar J., Kalyanaraman B., Martasek P., Hogg N., Masters B.S., Karoui H., Tordo P., and Pritchard Jr. K.A. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9220-9225
67. Waelti E.R., and Barton M. Rapid endocytosis of copper-zinc superoxide dismutase into human endothelial cells: role for its vascular activity. Pharmacology 78 (2006) 198-201
68. Wang L., Fortune B., Cull G., Dong J., and Cioffi G.A. Endothelin B receptor in human glaucoma and experimentally induced optic nerve damage. Arch. Ophthalmol. 124 (2006) 717-724
69. Williams R.R., Cusato K., Raven M.A., and Reese B.E. Organization of the inner retina following early elimination of the retinal ganglion cell population: effects on cell numbers and stratification patterns. Vis. Neurosci. 18 (2001) 233-244
70. Yagami T., Ueda K., Asakura K., Kuroda T., Hata S., Sakaeda T., Kambayashi Y., and Fujimoto M. Effects of endothelin B receptor agonists on amyloid beta protein (25-35)-induced neuronal cell death. Brain Res. 948 (2002) 72-81
71. Yamada H., and Kurokawa K. Histochemical studies on endothelin and the endothelin-A receptor in the hypothalamus. J. Cardiovasc. Pharmacol. 31 (1998) S215-S218
72. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., and Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332 (1988) 411-415
73. Yorio T., Krishnamoorthy R., and Prasanna G. Endothelin: is it a contributor to glaucoma pathophysiology?. J. Glaucoma 11 (2002) 259-270
74. Zhao H., Joseph J., Fales H.M., Sokoloski E.A., Levine R.L., Vasquez-Vivar J., and Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 5727-5732
75. Zhou Q.L., Strichartz G., and Davar G. Endothelin-1 activates ET(A) receptors to increase intracellular calcium in model sensory neurons. Neuroreport 12 (2001) 3853-3857