Acute retinal ischemia inhibits endothelium-dependent nitric oxide-mediated dilation of retinal arterioles via enhanced superoxide production

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 1, 2012, Pages 30-36

  Hein, Travis W ^a   Ren, Yi ^a   Potts, Luke B ^a   Yuan, Zhaoxu ^a   Kuo, Enoch ^a   Rosa, Robert H ^a   Kuo, Lih ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; NITRIC OXIDE; SODIUM CHLORIDE; SUPEROXIDE; TEMPOL;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; INTRAOCULAR PRESSURE; MALE; NONHUMAN; PRIORITY JOURNAL; RETINA ISCHEMIA; SWINE; VASCULAR ENDOTHELIUM; VASODILATATION;

EID: 84855306513     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8753     Document Type: Article

References (52)

1. Osborne N, Casson R, Wood J, et al. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Ret Eye Res. 2004;23:91-147.
2. Hayreh SS. Acute retinal arterial occlusive disorders. Prog Ret Eye Res. 2011;30:359-394.
3. Bek T. Inner retinal ischaemia: current understanding and needs for further investigations. Acta Ophthalmol. 2009;87:362-367.
4. Gidday JM, Zhu Y. Endothelium-dependent changes in retinal blood flow following ischemia. Curr Eye Res. 1998;17:798-807.
5. Lin J, Roth S. Ischemic preconditioning attenuates hypoperfusion after retinal ischemia in rats. Invest Ophthalmol Vis Sci. 1999;40: 2925-2931.
6. Goldstein IM, Ostwald P, Roth S. Nitric oxide: a review of its role in retinal function and disease. Vis Res. 1996;36:2979-2994.
7. Polak K, Luksch A, Frank B, et al. Regulation of human retinal blood flow by endothelin-1. Exp Eye Res. 2003;76:633-640.
8. Donati G, Pournaras C, Pizzolato G, Tsacopoulos M. Decreased nitric oxide production accounts for secondary arteriolar constriction after retinal branch occlusion. Invest Ophthalmol Vis Sci. 1997;38:1450-1457.
9. Bonne C, Muller A, Villain M. Free radicals in retina ischemia. Gen Pharmacol. 1998;30:275-280.
10. Gryglewski RJ, Palmer RMJ, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature. 1986;320:454-456.
11. Smith G, Baird C. Survival time of retinal cells when deprived of their blood supply by increased intraocular pressure. Am J Ophthalmol. 1952;35:133-136.
12. Büchi E, Suivaizdis I, Fu J. Pressure-induced retinal ischemia in rats: an experimental model for quantitative study. Ophthalmologica. 1991;203:138-147.
13. Dollery C, Henkind P, Kohner E, Paterson J. Effect of raised intraocular pressure on the retinal and choroidal circulation. Invest Ophthalmol Vis Sci. 1968;7:191-198.
14. Parrish R, Gass J, Anderson D. Outer retina ischemic infarction-a newly recognized complication of cataract extraction and closed vitrectomy. Part 2. An animal model. Ophthalmology. 1982;89: 1472-1477.
15. Cao W, Drumheller A, Zaharia M, et al. Effects of experimentally induced ischemia on dopamine metabolism in rabbit retina. Invest Ophthalmol Vis Sci. 1993;34:3140-3146.
16. Hein TW, Yuan Z, Rosa RH Jr, Kuo L. Requisite roles of A2A receptors, nitric oxide, and KATP channels in retinal arteriolar dilation in response to adenosine. Invest Ophthalmol Vis Sci. 2005;46:2113-2119.
17. Kulkarni P, Joshua IG, Roberts AM, Barnes G. A novel method to assess reactivities of retinal microcirculation. Microvasc Res. 1994; 48:39-49.
18. Nagaoka T, Takahashi A, Sato E, et al. Effect of systemic administration of simvastatin on retinal circulation. Arch Ophthalmol. 2006;124:665-670.
19. Jeppesen P, Aalkjaer C, Bek T. Bradykinin relaxation in small porcine retinal arterioles. Invest Ophthalmol Vis Sci. 2002;43: 1891-1896.
20. Nagaoka T, Hein TW, Yoshida A, Kuo L. Simvastatin elicits dilation of isolated porcine retinal arterioles: role of nitric oxide and mevalonate- Rho kinase pathways. Invest Ophthalmol Vis Sci. 2007; 48:825-832.
21. Hein TW, Xu W, Kuo L. Dilation of retinal arterioles in response to lactate: role of nitric oxide, guanylyl cyclase, and ATP-sensitive potassium channels. Invest Ophthalmol Vis Sci. 2006;47:693-699.
22. Zhang C, Hein TW, Wang W, Kuo L. Divergent roles of angiotensin II AT1 and AT2 receptors in modulating coronary microvascular function. Circ Res. 2003;92:322-329.
23. Bloodworth JJ, Gutgesell HJ, Engerman R. Retinal vasculature of the pig. Light and electron microscope studies. Exp Eye Res. 1965;4:174-178.
24. Rootman J. Vascular system of the optic nerve head and retina in the pig. Br J Ophthalmol. 1971;55:808-819.
25. Beauchemin ML. The fine structure of the pig's retina. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1974;190:27-45.
26. Simoens P, De Schaepdrijver L, Lauwers H. Morphologic and clinical study of the retinal circulation in the miniature pig. A: Morphology of the retinal microvasculature. Exp Eye Res. 1992; 54:965-973.
27. De Schaepdrijver L, Simoens P, Pollet L, Lauwers H, De Laey JJ. Morphologic and clinical study of the retinal circulation in the miniature pig. B: Fluorescein angiography of the retina. Exp Eye Res. 1992;54:975-985.
28. Chandler MJ, Smith PJ, Samuelson DA, MacKay EO. Photoreceptor density of the domestic pig retina. Vet Ophthalmol. 1999;2:179-184.
29. Yang P, Chen L, Zwart R, Kijlstra A. Immune cells in the porcine retina: distribution, characterization and morphological features. Invest Ophthalmol Vis Sci. 2002;43:1488-1492.
30. Hein TW, Rosa RH Jr, Yuan Z, Roberts E, Kuo L. Divergent roles of nitric oxide and Rho kinase in vasomotor regulation of human retinal arterioles. Invest Ophthalmol Vis Sci. 2010;51:1583-1590.
31. Wurm A, Iandiev I, Uhlmann S, et al. Effects of ischemia-reperfusion on physiological properties of Muller glial cells in the porcine retina. Invest Ophthalmol Vis Sci. 2011;52:3360-3367.
32. Kyhn MV, Warfvinge K, Scherfig E, et al. Acute retinal ischemia caused by controlled low ocular perfusion pressure in a porcine model. Electrophysiological and histological characterisation. Exp Eye Res. 2009;88:1100-1106.
33. Kyhn MV, Klassen H, Johansson UE, et al. Delayed administration of glial cell line-derived neurotrophic factor (GDNF) protects retinal ganglion cells in a pig model of acute retinal ischemia. Exp Eye Res. 2009;89:1012-1020.
34. Gesslein B, Hakansson G, Carpio R, et al. Mitogen-activated protein kinases in the porcine retinal arteries and neuroretina following retinal ischemia-reperfusion. Mol Vis. 2010;16:392-407.
35. Gesslein B, Hakansson G, Gustafsson L, Ekstrom P, Malmsjo M. Tumor necrosis factor and its receptors in the neuroretina and retinal vasculature after ischemia-reperfusion injury in the pig retina. Mol Vis. 2010;16:2317-2327.
36. Margalit E, Sadda S. Retinal and optic nerve diseases. Artif Organs. 2003;27:963-974.
37. Rosa Jr RH, Hein TW, Yuan Z, et al. Brimonidine evokes heterogeneous vasomotor response of retinal arterioles: diminished nitric oxide-mediated vasodilation when size goes small. Am J Physiol Heart Circ Physiol. 2006;291:H231-H238.
38. Kamiya T, Katayama Y, Kashiwagi F, Terashi A. The role of bradykinin in mediating ischemic brain edema in rats. Stroke. 1993;24: 571-575.
39. Pan HL, Chen SR, Scicli GM, Carretero OA. Cardiac interstitial bradykinin release during ischemia is enhanced by ischemic preconditioning. Am J Physiol Heart Circ Physiol. 2000;279:H116-H121.
40. Hayreh SS, Weingeist TA. Experimental occlusion of the central artery of the retina. IV: Retinal tolerance time to acute ischaemia. Br J Ophthalmol. 1980;64:818-825.
41. Hayreh SS, Weingeist TA. Experimental occlusion of the central artery of the retina. I. Ophthalmoscopic and fluorescein fundus angiographic studies. Br J Ophthalmol. 1980;64:896-912.
42. Hayreh SS, Kolder HE, Weingeist TA. Central retinal artery occlusion and retinal tolerance time. Ophthalmology. 1980;87:75-78.
43. Szabo ME, Droy-Lefaix MT, Doly M, Carre C, Braquet P. Ischemia and reperfusion-induced histologic changes in the rat retina. Demonstration of a free radical-mediated mechanism. Invest Ophthalmol Vis Sci. 1991;32:1471-1478.
44. Delaey C, Van de Voorde J. Regulatory mechanisms in the retinal and choroidal circulation. Ophthalmic Res. 2000;32:249-256.
45. Brazitikos PD, Pournaras CJ, Munoz JL, Tsacopoulos M. Microinjection of L-lactate in the preretinal vitreous induces segmental vasodilation in the inner retina of miniature pigs. Invest Ophthalmol Vis Sci. 1993;34:1744-1752.
46. Ido Y, Chang K, Williamson JR. NADH augments blood flow in physiologically activated retina and visual cortex. Proc Nat Acad Sci U S A. 2004;101:653-658.
47. Garhofer G, Zawinka C, Resch H, et al. Effect of intravenous administration of sodium-lactate on retinal blood flow in healthy subjects. Invest Ophthalmol Vis Sci. 2003;44:3972-3976.
48. Garhofer G, Kopf A, Polska E, et al. Influence of exercise induced hyperlactatemia on retinal blood flow during normo-and hyperglycemia. Curr Eye Res. 2004;28:351-358.
49. Veriac S, Tissie G, Bonne C. Oxygen free radicals adversely affect the regulation of vascular tone by nitric oxide in the rabbit retina under high intraocular pressure. Exp Eye Res. 1993;56:85-88.
50. Muller A, Pietri S, Villain M, et al. Free radicals in rabbit retina under ocular hyperpressure and functional consequences. Exp Eye Res. 1997;64:637-643.
51. Li J, Shah A. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1014-R1030.
52. Du XL, Edelstein D, Dimmeler S, et al. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest. 2001;108:1341-1348.