Neuroprotective effects of brimonidine treatment in a rodent model of ischemic optic neuropathy

Experimental Eye Research

Volumn 84, Issue 2, 2007, Pages 293-301

  Danylkova, Nataliya O ^a   Alcala, Sandra R ^a   Pomeranz, Howard D ^a   McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

2 agonists; hypoxia; ischemia; neuroprotection; optic nerve

Indexed keywords

BRIMONIDINE; EYE DROPS; ROSE BENGAL; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; ISCHEMIC OPTIC NEUROPATHY; NERVE FIBER; NEUROPROTECTION; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; AXONS; CELL SURVIVAL; COLORING AGENTS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; DRUG EVALUATION, PRECLINICAL; NEUROPROTECTIVE AGENTS; OPHTHALMIC SOLUTIONS; OPTIC NEUROPATHY, ISCHEMIC; OXAZINES; QUINOXALINES; RATS; RATS, LONG-EVANS; RETINAL GANGLION CELLS;

EID: 33845658346     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2006.10.002     Document Type: Article

References (68)

1. Acheampong A.A., Shackleton M., John B., Burke J., Wheeler L., and Tang-Liu D. Distribution of brimonidine into anterior and posterior tissues of monkey, rabbit, and rat eyes. Drug Metab. Dispos. 30 (2002) 421-429
2. Acheampong A.A., Shackleton M., and Tang-Liu D.D. Comparative ocular pharmacokinetics of brimonidine after a single dose application to the eyes of albino and pigmented rabbits. Drug Metab. Dispos. 23 (1995) 708-712
3. Alcala S.R., Danylkova N., Hoekman J., Hanson L., Frey W., and McLoon L.K. Intranasal delivery of insulin-like growth factor-1 distributes to the optic nerve and retina in the rat. Investig. Ophthalmol. Vis. Sci. 47 (2006) 728 (ARVO abstract)
4. Al-Shahwan S., Al-Torbak A.A., Turkmani S., Al-Omran M., Al-Jadaan I., and Edward D.P. Side-effect profile of brimonidine tartrate in children. Ophthalmology 112 (2005) 2143
5. Aviles-Trigueros M., Mayor-Torroglosa S., Garcia-Aviles A., Lafuente M.P., Rodriguez M.E., Miralles de Imperial J., Villegas-Perez M.P., and Vidal-Sanz M. Transient ischemia of the retina results in massive degeneration of the retinotectal projection: long-term neuroprotection with brimonidine. Exp. Neurol. 184 (2003) 767-777
6. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14 (1994) 4368-4374
7. Bernstein S.L., Guo Y., Kelman S.E., Flower R.W., and Johnson M.A. Functional and cellular responses in a novel rodent model of anterior ischemic optic neuropathy. Investig. Ophthalmol. Vis. Sci. 44 (2003) 4153-4162
8. Bhandari A., Cioffi G.A., Van Buskirk E.M., Orgul S., and Wang L. Effect of brimonidine on optic nerve blood flow in rabbits. Am. J. Ophthalmol. 128 (1999) 601-605
9. BRAION Study Group, Wilhem B., Ludtke H., and Wilhem H. Efficacy and tolerability of 0.2% brimonidine tartrate for the treatment of acute non-arteritic anterior ischemic optic neuropathy (NAION): a 3-month, double-masked, randomized, placebo-controlled trial. Graefe's Arch. Clin. Exp. Ophthalmol. 244 (2006) 551-558
10. Carlsson A.M., Chauhan B.C., Lee A.A., and LeBlanc R.P. The effect of brimonidine tartrate on retinal blood flow in patients with ocular hypertension. Am. J. Ophthalmol. 129 (2000) 297-301
11. Cepurna W.O., Kayton R.J., Johnson E.C., and Morrison J.C. Age related optic nerve axonal loss in adult Brown Norway rats. Exp. Eye Res. 80 (2005) 877-884
12. Danylkova N.O., Pomeranz H.D., Alcala S.R., and McLoon L.K. Histological and morphometric evaluation of transient retinal and optic nerve ischemia in rat. Brain Res. 1096 (2006) 20-29
13. Debock F., Kurz J., Azad S.C., Parsons C.G., Hapfelmeier G., Zieglgansberger W., and Rammes G. Alpha 2-adrenoreceptor activation inhibits LTP and LTD in the basolateral amygdale: involvement of Gi-o-protein-mediated modulation of Ca2+-channels and inwardly rectifying K+-channels in LTD. Eur. J. Neurosci. 17 (2003) 1411-1424
14. Donello J.E., Padillo E.U., Webster M.L., Wheeler L.A., and Gil D.W. Alpha (2)-adrenoceptor agonists inhibit vitreal glutamate and aspartate accumulation and preserve retinal function after transient ischemia. J. Pharmacol. Exp. Ther. 296 (2001) 216-223
15. El-Asrar A.M., Morse P.H., Maimone D., Torczynski E., and Reder A.T. MK-801 protects retinal neurons from hypoxia and the toxicity of glutamate and aspartate. Investig. Ophthalmol. Vis. Sci. 33 (1992) 3463-3468
16. Elena P.P., Kosina-Boix M., Denis P., Moulin G., and Lapalus P. Alpha 2-adrenergic receptors in rat and rabbit eye: a tritium-sensitive film autoradiography. Ophthalmic. Res. 21 (1989) 309-314
17. Evans D.W., Hosking S.L., Gherghel D., and Barlett J.D. Contrast sensitivity improves after brimonidine therapy in primary open angle glaucoma: a case for neuroprotection. Br. J. Ophthalmol. 87 (2003) 1463-1465
18. Faber J.E., and Meininger G.A. Selective interaction of alpha-adrenoreceptors with myogenic regulation of microvascular smooth muscle. Am. J. Physiol. 259 (1990) H1126-H1133
19. Faktorovich E.G., Steinberg R.H., Yasumura D., Matthes M.T., and LaVail M.M. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J. Neurosci. 12 (1992) 3554-3567
20. Faktorovich E.G., Steinberg R.H., Yasumura D., Matthes M.T., and LaVail M.M. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature 347 (1990) 83-86
21. Fazzone H.E., Kupersmith M.J., and Leibman J. Does topical brimonidine tartrate help NAION?. Br. J. Ophthalmol. 87 (2003) 1193-1194
22. Ferencz J.R., Gilady G., Harel O., Belkin M., and Assia E.I. Topical brimonidine reduces collateral damage caused by laser photocoagulation for choroidal neovascularization. Graefe's Arch. Clin. Exp. Ophthalmol. 243 (2005) 877-880
23. Gandolfi S.A., Cimino L., and Mora P. Effect of brimonidine on intraocular pressure in normal tension glaucoma: a short term clinical trial. Eur. J. Ophthalmol. 13 (2003) 611-615
24. Gao H., Qiao X., Cantor L.B., and WuDunn D. Up-regulation of brain-derived neurotrophic factor expression by brimonidine in rat retinal ganglion cells. Arch. Ophthalmol. 120 (2002) 797-803
25. Goldenberg-Cohen N., Guo Y., Margolis F., Cohen Y., Miller N.R., and Bernstein S.L. Oligodendrocyte dysfunction after induction of experimental anterior optic nerve ischemia. Investig. Ophthalmol. Vis. Sci. 46 (2005) 2716-2725
26. Greenfield D.S., Liebmann J.M., and Ritch R. Brimonidine: a new alpha 2-adrenoreceptor agonist for glaucoma treatment. J. Glaucoma 6 (1997) 250-258
27. Han Y., and Wu S.M. NMDA-evoked [Ca2+] increase in salamander retinal ganglion cells: modulation by PKA and adrenergic receptors. Vis. Neurosci. 19 (2002) 249-256
28. Hayreh S.S. Inter-individual variation in blood supply of the optic nerve head. Its importance in various ischemic disorders of the optic nerve head, and glaucoma, low-tension glaucoma and allied disorders. Doc. Ophthalmol. 59 (1985) 217-246
29. Hayreh S.S. Acute ischemic disorders of the optic nerve: pathogenesis, clinical manifestations and management. Ophthalmol. Clin. North Am. 9 (1996) 407-442
30. Huang Y., Gil D.W., Vanscheeuwijck P., Stamer W.D., and Regan J.W. Localization of alpha 2-adrenergic receptor subtypes in the anterior segment of the human eye with selective antibodies. Investig. Ophthalmol. Vis. Sci. 36 (1995) 2729-2739
31. Jakobs K.H. Inhibition of adenylate cyclase by hormones and neurotransmitters. Mol. Cell Endocrinol. 16 (1979) 147-156
32. Katsimpris J.M., Siganos D., Konstas A.G., Kozobolis V., and Georgiadis N. Efficacy of brimonidine 0.2% in controlling acute postoperative intraocular pressure elevation after phacoemulsification. J. Cataract Refract. Surg. 29 (2003) 2288-2294
33. Kent A.R., Nussdorf J.D., David R., Tyson F., Small D., and Fellows D. Vitreous concentration of topically applied brimonidine tartrate 0.2%. Ophthalmology 108 (2001) 784-787
34. Lachkar Y., Migdal C., and Dhanjil S. Effect of brimonidine tartrate on ocular hemodynamic measurements. Arch. Ophthalmol. 116 (1998) 1591-1594
35. Lafuente Lopez-Herrera M.P., Mayor-Torroglosa S., Miralles de Imperial J., Villegas-Perez M.P., and Vidal-Sanz M. Transient ischemia of the retina results in altered retrograde axoplasmic transport: neuroprotection with brimonidine. Exp. Neurol. 178 (2002) 243-258
36. Lafuente M.P., Villegas-Perez M.P., Sobrado-Calvo P., Garcia-Aviles A., Miralles de Imperial J., and Vidal-Sanz M. Neuroprotective effects of alpha (2)-selective adrenergic agonists against ischemia-induced retinal ganglion cell death. Investig. Ophthalmol. Vis. Sci. 42 (2001) 2074-2084
37. Lai R.K., Chun T., Hasson D., Lee S., Mehrbod F., and Wheeler L. Alpha 2 adrenoreceptor agonist protects retinal function after a retinal ischemic injury in the rat. Vis. Neurosci. 19 (2002) 175-185
38. Levin L.A., and Louhab A. Apoptosis of retinal ganglion cells in anterior ischemic optic neuropathy. Arch. Ophthalmol. 114 (1996) 488-491
39. Maier C., Steinberg G.K., Sun G.H., Zhi G.T., and Maze M. Neuroprotection by the alpha 2-adrenoreceptor agonist dexmedetomidine in a focal model of cerebral ischemia. Anesthesiology 79 (1993) 306-312
40. Matsuo T., and Cynader M.S. Localization of alpha-2 adrenergic receptors in the human eye. Ophthalmic Res. 24 (1992) 213-219
41. McGillivray-Anderson K.M., and Faber J.E. Effect of reduced blood flow on alpha 1- and alpha 2-adrenoceptor constriction of rat skeletal muscle microvessels. Circ. Res. 69 (1991) 165-173
42. Mondal L.K., Baidya K.P., Bhattacharya B., Chatterjee P.R., and Bhaduri G. The efficacy of topical administration of brimonidine to reduce ischaemia in the very early stage of diabetic retinopathy in good controlled type-2 diabetes mellitus. J. Indian Med. Assoc. 102 (2004) 724-725
43. Morrison J.C., Johnson E.C., Cepurna W.O., and Funk R.H.W. Microvasculature of the rat optic nerve head. Investig. Ophthalmol. Vis. Sci. 40 (1999) 1702-1709
44. Onda E., Cioffi G.A., Bacon D.R., and Van Buskirk E.M. Microvasculature of the human optic nerve. Am. J. Ophthalmol. 120 (1995) 92-102
45. Osborne N.N. Inhibition of cAMP production by alpha 2-adrenoceptor stimulation in rabbit retina. Brain Res. 553 (1991) 84-88
46. Reitsamer H.A., Posey M., and Kiel J.W. Effects of a topical alpha 2 adrenergic agonist on ciliary blood flow and aqueous production in rabbits. Exp. Eye Res. 82 (2005) 405-415
47. Risco J.M., Grimson B.S., and Johnson P.T. Angioarchitecture of the ciliary artery of the posterior pole. Arch. Ophthalmol. 99 (1981) 864-868
48. Rosa Jr. R.H., Hein T.W., Yuan Z., Xu W., Pechal M.I., Geraets R.L., Newman J.M., and Kuo L. Brimonidine evokes heterogeneous vasomotor response of retinal arterioles: diminished nitric oxide-mediated vasodilation when size goes small. Am. J. Physiol. Heart Circ. Physiol. (2006) (Feb 17 Epub ahead of print)
49. Salazar J.J., Ramirez A.I., de Hoz R., Rojas B., Trivino A., and Ramirez J.M. Apoptosis in ischemic optic neuropathy. Arch. Soc. Esp. Oftalmol. 75 (2000) 819-824
50. Sievers J., Hausmann B., Unsicker K., and Berry M. Fibroblast growth factors promote the survival of adult rat retinal ganglion cells after transection of the optic nerve. Neurosci. Lett. 76 (1987) 157-162
51. Sugiyama K., Gu Z.B., Kawase C., Yamamoto T., and Kitazawa Y. Optic nerve and peripapillary choroidal microvasculature of the rat eye. Investig. Ophthalmol. Vis. Sci. 40 (1999) 3084-3090
52. Szabo M.E., Droy-Lefaix M.T., Doly M., Carre C., and Braquet P. Ischemia and reperfusion-induced histologic changes in the rat retina. Demonstration of a free radical-mediated mechanism. Investig. Ophthalmol. Vis. Sci. 32 (1991) 1471-1478
53. Tatton W.G., Chalmers-Redman R.M., and Tatton N.A. Apoptosis and anti-apoptosis signaling in glaucomatous retinopathy. Eur. J. Ophthalmol. 11 Suppl. (2001) S12-S22
54. Tatton W.G., Chalmers-Redman R.M., Sud A., Podos S.M., and Mittag T.W. Maintaining mitochondrial membrane impermeability. an opportunity for new therapy in glaucoma?. Surv. Ophthalmol. 45 Suppl. 3 (2001) S277-S283
55. Toris C.B., Gleason M.L., Camras C.B., and Yablonski M.E. Effects of brimonidine on aqueous humor dynamics in human eyes. Arch. Ophthalmol. 113 (1995) 1514-1517
56. Tsai J.C., and Chang H.W. Comparison of the effects of brimonidine 0.2% and timolol 0.5% on retinal nerve fiber layer thickness in ocular hypertensive patients: a prospective, unmasked study. J. Ocul. Pharmacol. Ther. 21 (2005) 475-482
57. Vidal-Sanz M., Lafuente M.P., Mayor-Torroglosa S., Aguilera M.E., Miralles de Imperial J., and Villegas-Perez M.P. Brimonidine's neuroprotective effects against transient ischemia-induced retinal ganglion cell death. Eur. J. Ophthalmol. 11 Suppl. 2 (2001) S36-S40
58. Wen R., Cheng T., Li Y., Cao W., and Steinberg R.H. Alpha 2-adrenergic agonists induce basic fibroblast growth factor expression in photoreceptors in vivo and ameliorate light damage. J. Neurosci. 16 (1996) 5986-5992
59. Wheeler L.A., Gil D.W., and WoldeMussie E. Role of alpha-2 adrenergic receptors in neuroprotection and glaucoma. Surv. Ophthalmol. 45 Suppl. 3 (2001) S290-S294
60. Wheeler L.A., Lai R., and Woldemussie E. From the lab to the clinic: activation of an alpha-2 agonist pathway is neuroprotective in models of retinal and optic nerve injury. Eur. J. Ophthalmol. 9 Suppl. 1 (1999) S17-S21
61. Wheeler L.A., and Woldemussie E. Alpha-2 adrenergic receptor agonists are neuroprotective in experimental models of glaucoma. Eur. J. Ophthalmol. 11 Suppl. 2 (2001) S30-S35
62. WoldeMussie E., Ruiz G., Wijono M., and Wheeler L.A. Neuroprotection of retinal ganglion cells by brimonidine in rats with laser-induced chronic ocular hypertension. Investig. Ophthalmol. Vis. Sci. 42 (2001) 2849-2855
63. Wypijewski K., Duda T., and Sharma R.K. Structural, genetic and pharmacological identity of the rat alpha 2-adrenergic receptor subtype cA2-47 and its molecular characterization in rat adrenal, adrenocortical carcinoma and bovine retina. Mol. Cell Biochem. 144 (1995) 181-190
64. Yoles E., Wheeler L.A., and Schwartz M. Alpha 2-adrenoreceptor agonists are neuroprotective in a rat model of optic nerve degeneration. Investig. Ophthalmol. Vis. Sci. 40 (1999) 65-73
65. Yuan S.Z., Runold M., Hagberg H., Bona E., and Lagercrantz H. Hypoxic-ischaemic brain damage in immature rats: effects of adrenoreceptor modulation. Eur. J. Paediatr. Neurol. 5 (2001) 29-35
66. Zarbin M.A., Wamsley J.K., Palacios J.M., and Kuhar M.J. Autoradiographic localization of high affinity GABA, benzodiazepine, dopaminergic, adrenergic and muscarinic cholinergic receptors in the rat, monkey and human retina. Brain Res. 374 (1986) 75-92
67. Zhang Y. Clonidine preconditioning decreases infarct size and improves neurological outcome from transient forebrain ischemia in the rat. Neuroscience 125 (2004) 625-631
68. Zhang N., Kannan R., Okamoto C.T., Ryan S.J., Lee V.H., and Hinton D.R. Characterization of brimonidine transport in retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 47 (2006) 287-294