Contribution of nitric oxide synthase isoforms to cholinergic vasodilation in murine retinal arterioles

Experimental Eye Research

Volumn 109, Issue , 2013, Pages 60-66

  Gericke, Adrian ^a   Goloborodko, Evgeny ^a   Sniatecki, Jan J ^a   Steege, Andreas ^b   Wojnowski, Leszek ^a   Pfeiffer, Norbert ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Acetylcholine; Cholinergic; Gene targeted mouse; Nitric oxide synthase; Retinal arteriole; Vasodilation

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; ACETYLCHOLINE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NEURONAL NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BRAIN; CONTROLLED STUDY; GENOTYPE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA; RETINA BLOOD VESSEL; VASOCONSTRICTION; VASODILATATION; VIDEO MICROSCOPY; WILD TYPE;

ACETYLCHOLINE; ANIMALS; ARTERIOLES; BRAIN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; NITROPRUSSIDE; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL VESSELS; RNA, MESSENGER; VASODILATION; VASODILATOR AGENTS;

EID: 84874781834     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.01.012     Document Type: Article

References (55)

1. Bardell A.L., MacLeod K.M. Evidence for inducible nitric-oxide synthase expression and activity in vascular smooth muscle of streptozotocin-diabetic rats. J. Pharmacol. Exp. Ther. 2001, 296:252-259.
2. Berra A., Ganzinelli S., Saravia M., Borda E., Sterin-Borda L. Inducible nitric oxide synthase subserves cholinergic vasodilation in retina. Vis. Neurosci. 2005, 22:371-377.
3. Bhagat K., Hingorani A.D., Palacios M., Charles I.G., Vallance P. Cytokine-induced venodilatation in humans in vivo: eNOS masquerading as iNOS. Cardiovasc. Res. 1999, 41:754-764.
4. Bhutto I.A., Baba T., Merges C., McLeod D.S., Lutty G.A. Low nitric oxide synthases (NOSs) in eyes with age-related macular degeneration (AMD). Exp. Eye Res. 2010, 90:155-167.
5. Boulanger C.M., Heymes C., Benessiano J., Geske R.S., Levy B.I., Vanhoutte P.M. Neuronal nitric oxide synthase is expressed in rat vascular smooth muscle cells: activation by angiotensin II in hypertension. Circ. Res. 1998, 83:1271-1278.
6. Burdo J.R., Chen Q., Calcutt N.A., Schubert D. The pathological interaction between diabetes and presymptomatic Alzheimer's disease. Neurobiol. Aging 2009, 30:1910-1917.
7. de Vera M.E., Shapiro R.A., Nussler A.K., Mudgett J.S., Simmons R.L., Morris S.M., Billiar T.R., Geller D.A. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:1054-1059.
8. Dewhurst M., Stevens E.J., Tomlinson D.R. Effects of aminoguanidine and N(G)-nitro-L-arginine methyl ester on vascular responses of aortae and lungs from streptozotocin-diabetic rats. Prostaglandins Leukot. Essent. Fatty Acids 1997, 56:317-324.
9. Dorner G.T., Garhofer G., Kiss B., Polska E., Polak K., Riva C.E., Schmetterer L. Nitric oxide regulates retinal vascular tone in humans. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H631-H636.
10. Ferrari-Dileo G., Davis E.B., Anderson D.R. Biochemical evidence for cholinergic activity in retinal blood vessels. Invest. Ophthalmol. Vis. Sci. 1989, 30:473-477.
11. Forstermann U., Sessa W.C. Nitric oxide synthases: regulation and function. Eur. Heart J. 2011.
12. Garhofer G., Resch H., Lung S., Weigert G., Schmetterer L. Intravenous administration of L-arginine increases retinal and choroidal blood flow. Am. J. Ophthalmol. 2005, 140:69-76.
13. Gericke A., Sniatecki J.J., Goloborodko E., Steege A., Zavaritskaya O., Vetter J.M., Grus F.H., Patzak A., Wess J., Pfeiffer N. Identification of the muscarinic acetylcholine receptor subtype mediating cholinergic vasodilation in murine retinal arterioles. Invest. Ophthalmol. Vis. Sci. 2011, 52:7479-7484.
14. Godecke A., Decking U.K., Ding Z., Hirchenhain J., Bidmon H.J., Godecke S., Schrader J. Coronary hemodynamics in endothelial NO synthase knockout mice. Circ. Res. 1998, 82:186-194.
15. Granstam E., Granstam S.O. Regulation of uveal and retinal blood flow in STZ-diabetic and non-diabetic rats; involvement of nitric oxide. Curr. Eye Res. 1999, 19:330-337.
16. Gunnett C.A., Chu Y., Heistad D.D., Loihl A., Faraci F.M. Vascular effects of LPS in mice deficient in expression of the gene for inducible nitric oxide synthase. Am. J. Physiol. 1998, 275:H416-H421.
17. Gunnett C.A., Lund D.D., Chu Y., Brooks R.M., Faraci F.M., Heistad D.D. NO-dependent vasorelaxation is impaired after gene transfer of inducible NO-synthase. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1281-1287.
18. Harino S., Nishimura K., Kitanishi K., Suzuki M., Reinach P. Role of nitric oxide in mediating retinal blood flow regulation in cats. J. Ocul. Pharmacol. Ther. 1999, 15:295-303.
19. Hogan M.J., Feeney L. The ultrastructure of the retinal blood vessels. I. The large vessels. J. Ultrastruct. Res. 1963, 39:10-28.
20. Huang P.L., Lo E.H. Genetic analysis of NOS isoforms using nNOS and eNOS knockout animals. Prog. Brain Res. 1998, 118:13-25.
21. Ichihara A., Hayashi M., Navar L.G., Saruta T. Inducible nitric oxide synthase attenuates endothelium-dependent renal microvascular vasodilation. J. Am. Soc. Nephrol. 2000, 11:1807-1812.
22. Izumi N., Nagaoka T., Sato E., Sogawa K., Kagokawa H., Takahashi A., Kawahara A., Yoshida A. Role of nitric oxide in regulation of retinal blood flow in response to hyperoxia in cats. Invest. Ophthalmol. Vis. Sci. 2008, 49:4595-4603.
23. Jandrasits K., Polak K., Luksch A., Stark B., Dorner G.T., Eichler H.G., Schmetterer L. Effects of atropine and propranolol on retinal vessel diameters during isometric exercise. Ophthalmic Res. 2001, 33:185-190.
24. Kitayama J., Faraci F.M., Gunnett C.A., Heistad D.D. Impairment of dilator responses of cerebral arterioles during diabetes mellitus: role of inducible NO synthase. Stroke 2006, 37:2129-2133.
25. Lamping K.G., Nuno D.W., Shesely E.G., Maeda N., Faraci F.M. Vasodilator mechanisms in the coronary circulation of endothelial nitric oxide synthase-deficient mice. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H1906-H1912.
26. Laties A.M. Central retinal artery innervation. Absence of adrenergic innervation to the intraocular branches. Arch. Ophthalmol. 1967, 77:405-409.
27. Laubach V.E., Shesely E.G., Smithies O., Sherman P.A. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:10688-10692.
28. Linden R., Martins R.A., Silveira M.S. Control of programmed cell death by neurotransmitters and neuropeptides in the developing mammalian retina. Prog. Retin. Eye Res. 2005, 24:457-491.
29. Malecki M.T., Osmenda G., Walus-Miarka M., Skupien J., Cyganek K., Mirkiewicz-Sieradzka B., damek-Guzik T.A., Guzik T.J., Sieradzki J. Retinopathy in type 2 diabetes mellitus is associated with increased intima-media thickness and endothelial dysfunction. Eur. J. Clin. Invest. 2008, 38:925-930.
30. Mann R.M., Riva C.E., Stone R.A., Barnes G.E., Cranstoun S.D. Nitric oxide and choroidal blood flow regulation. Invest. Ophthalmol. Vis. Sci. 1995, 36:925-930.
31. Masland R.H., Mills J.W. Autoradiographic identification of acetylcholine in the rabbit retina. J. Cell. Biol. 1979, 83:159-178.
32. Massey S.C., Neal M.J. The light evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by gamma-aminobutyric acid. J. Neurochem. 1979, 32:1327-1329.
33. Massey S.C., Neal M.J. Release of [3H]-acetylcholine from the isolated retina of the rat by potassium depolarization: dependence on high affinity choline uptake. Br. J. Pharmacol. 1979, 65:271-276.
34. Meng W., Ayata C., Waeber C., Huang P.L., Moskowitz M.A. Neuronal NOS-cGMP-dependent ACh-induced relaxation in pial arterioles of endothelial NOS knockout mice. Am. J. Physiol. 1998, 274:H411-H415.
35. Meng W., Ma J., Ayata C., Hara H., Huang P.L., Fishman M.C., Moskowitz M.A. ACh dilates pial arterioles in endothelial and neuronal NOS knockout mice by NO-dependent mechanisms. Am. J. Physiol. 1996, 271:H1145-H1150.
36. Mishra A., Newman E.A. Inhibition of inducible nitric oxide synthase reverses the loss of functional hyperemia in diabetic retinopathy. Glia 2010, 58:1996-2004.
37. Nagaoka T., Sakamoto T., Mori F., Sato E., Yoshida A. The effect of nitric oxide on retinal blood flow during hypoxia in cats. Invest. Ophthalmol. Vis. Sci. 2002, 43:3037-3044.
38. Nakazawa T., Mori A., Saito M., Sakamoto K., Nakahara T., Ishii K. Vasodilator effects of adenosine on retinal arterioles in streptozotocin-induced diabetic rats. Naunyn Schmiedebergs Arch. Pharmacol. 2008, 376:423-430.
39. Okubo H., Gherezhiher T., Koss M.C. Long posterior ciliary arterial blood flow and systemic blood pressure. Invest. Ophthalmol. Vis. Sci. 1990, 31:819-826.
40. Patzak A., Steege A., Lai E.Y., Brinkmann J.O., Kupsch E., Spielmann N., Gericke A., Skalweit A., Stegbauer J., Persson P.B., Seeliger E. Angiotensin II response in afferent arterioles of mice lacking either the endothelial or neuronal isoform of nitric oxide synthase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R429-R437.
41. Polak K., Luksch A., Berisha F., Fuchsjaeger-Mayrl G., Dallinger S., Schmetterer L. Altered nitric oxide system in patients with open-angle glaucoma. Arch. Ophthalmol. 2007, 125:494-498.
42. Ren Y.L., Garvin J.L., Ito S., Carretero O.A. Role of neuronal nitric oxide synthase in the macula densa. Kidney Int. 2001, 60:1676-1683.
43. Resch H., Garhofer G., Fuchsjager-Mayrl G., Hommer A., Schmetterer L. Endothelial dysfunction in glaucoma. Acta Ophthalmol. 2009, 87:4-12.
44. Riva C.E., Logean E., Falsini B. Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina. Prog. Retin. Eye Res. 2005, 24:183-215.
45. Sato E., Sakamoto T., Nagaoka T., Mori F., Takakusaki K., Yoshida A. Role of nitric oxide in regulation of retinal blood flow during hypercapnia in cats. Invest. Ophthalmol. Vis. Sci. 2003, 44:4947-4953.
46. Schmetterer L., Findl O., Fasching P., Ferber W., Strenn K., Breiteneder H., Adam H., Eichler H.G., Wolzt M. Nitric oxide and ocular blood flow in patients with IDDM. Diabetes 1997, 46:653-658.
47. Shaikh M.H., Mars J.S. The acute effect of pilocarpine on pulsatile ocular blood flow in ocular hypertension. Eye (Lond.) 2001, 15:63-66.
48. Stapleton P.A., Goodwill A.G., James M.E., Frisbee J.C. Altered mechanisms of endothelium-dependent dilation in skeletal muscle arterioles with genetic hypercholesterolemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R1110-R1119.
49. Steinle J.J., Sharma S., Smith C.P., McFayden-Ketchum L.S. Normal aging involves modulation of specific inflammatory markers in the rat retina and choroid. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64:325-331.
50. Tirapelli C.R., Fukada S.Y., Yogi A., Chignalia A.Z., Tostes R.C., Bonaventura D., Lanchote V.L., Cunha F.Q., de Oliveira A.M. Gender-specific vascular effects elicited by chronic ethanol consumption in rats: a role for inducible nitric oxide synthase. Br. J. Pharmacol. 2008, 153:468-479.
51. Toda N., Nakanishi-Toda M. Nitric oxide: ocular blood flow, glaucoma, and diabetic retinopathy. Prog. Retin. Eye Res. 2007, 26:205-238.
52. Tummala S.R., Benac S., Tran H., Vankawala A., Zayas-Santiago A., Appel A., Kang Derwent J.J. Effects of inhibition of neuronal nitric oxide synthase on basal retinal blood flow regulation. Exp. Eye Res. 2009, 89:801-809.
53. Virdis A., Colucci R., Fornai M., Polini A., Daghini E., Duranti E., Ghisu N., Versari D., Dardano A., Blandizzi C., Taddei S., Del Tacca M., Monzani F. Inducible nitric oxide synthase is involved in endothelial dysfunction of mesenteric small arteries from hypothyroid rats. Endocrinology 2009, 150:1033-1042.
54. Wolff D.J., Lubeskie A. Aminoguanidine is an isoform-selective, mechanism-based inactivator of nitric oxide synthase. Arch. Biochem. Biophys. 1995, 316:290-301.
55. Zingarelli B., Southan G.J., Gilad E., O'Connor M., Salzman A.L., Szabo C. The inhibitory effects of mercaptoalkylguanidines on cyclo-oxygenase activity. Br. J. Pharmacol. 1997, 120:357-366.