Pathophysiology of human glaucomatous optic nerve damage: Insights from rodent models of glaucoma

Experimental Eye Research

Volumn 93, Issue 2, 2011, Pages 156-164

  Morrison, John C ^a   Cepurna Ying Guo, William O ^a   Johnson, Elaine C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Animal models; Glaucoma; Intraocular pressure; Optic nerve head; Pressure induced optic nerve damage

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; NEUROTROPHIN RECEPTOR P75;

ARTICLE; ASTROCYTE; EXPERIMENTAL MODEL; EXTRACELLULAR MATRIX; GENE EXPRESSION; GLAUCOMA; GLIA; INTRAOCULAR PRESSURE; LAMINA CRIBROSA; NERVE FIBER; NONHUMAN; OPTIC NERVE; OPTIC NERVE DISEASE; OPTIC NERVE HEAD; OPTIC NERVE INJURY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; EYE; GLAUCOMA; INTRAOCULAR PRESSURE; MACACA; OPTIC DISK; OPTIC NERVE DISEASES; RATS;

EID: 80052810406     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2010.08.005     Document Type: Article

References (114)

1. AGIS-Investigators The advanced glaucoma intervention study (AGIS): 7. The relationship between control of intraocular pressure and visual field deterioration. The AGIS Investigators. Am. J. Ophthalmol. 2000, 130(4):429-440.
2. Ahmed F., Brown K.M., Stephan D.A., Morrison J.C., Johnson E.C., Tomarev S.I. Microarray analysis of changes in mRNA levels in the rat retina after experimental elevation of intraocular pressure. Invest. Ophthalmol. Vis. Sci. 2004, 45(4):1247-1258.
3. Ahmed F.A., Hegazy K., Chaudhary P., Sharma S.C. Neuroprotective effect of alpha(2) agonist (brimonidine) on adult rat retinal ganglion cells after increased intraocular pressure. Brain Res. 2001, 913(2):133-139.
4. Aihara M., Lindsey J.D., Weinreb R.N. Experimental mouse ocular hypertension: establishment of the model. Invest. Ophthalmol. Vis. Sci. 2003, 44(10):4314-4320.
5. Anderson D.R., Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest. Ophthalmol. 1974, 13(10):771-783.
6. Beirowski B., Babetto E., Coleman M.P., Martin K.R. The WldS gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur. J. Neurosci. 2008, 28(6):1166-1179.
7. Buckingham B.P., Inman D.M., Lambert W., Oglesby E., Calkins D.J., Steele M.R., Vetter M.L., Marsh-Armstrong N., Horner P.J. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J. Neurosci. 2008, 28(11):2735-2744.
8. Chen H., Weber A.J. BDNF enhances retinal ganglion cell survival in cats with optic nerve damage. Invest. Ophthalmol. Vis. Sci. 2001, 42(5):966-974.
9. Cheng L., Sapieha P., Kittlerova P., Hauswirth W.W., Di Polo A. TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. J. Neurosci. 2002, 22(10):3977-3986.
10. Cioffi G.A., Van Buskirk E.M. Microvasculature of the anterior optic nerve. Surv. Ophthalmol. 1994, 38(Suppl.):S107-S116. discussion S116-S117.
11. Di Polo A., Aigner L.J., Dunn R.J., Bray G.M., Aguayo A.J. Prolonged delivery of brain-derived neurotrophic factor by adenovirus-infected Muller cells temporarily rescues injured retinal ganglion cells. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(7):3978-3983.
12. Drance S.M. The collaborative normal-tension glaucoma study and some of its lessons. Can. J. Ophthalmol. 1999, 34(1):1-6.
13. Eida H., Bhutto I.A., Amemiya T. Corrosion cast demonstration of choroidal vasculature in normal Wistar Kyoto rat. Ital. J. Anat. Embryol. 2001, 106(2 Suppl. 1):245-250.
14. Gross R.L., Ji J., Chang P., Pennesi M.E., Yang Z., Zhang J., Wu S.M. A mouse model of elevated intraocular pressure: retina and optic nerve findings. Trans. Am. Ophthalmol. Soc. 2003, 101:163-169. discussion 169-171.
15. Grozdanic S.D., Betts D.M., Sakaguchi D.S., Kwon Y.H., Kardon R.H., Sonea I.M. Temporary elevation of the intraocular pressure by cauterization of vortex and episcleral veins in rats causes functional deficits in the retina and optic nerve. Exp. Eye Res. 2003, 77(1):27-33.
16. Guo L., Moss S.E., Alexander R.A., Ali R.R., Fitzke F.W., Cordeiro M.F. Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Invest. Ophthalmol. Vis. Sci. 2005, 46(1):175-182.
17. Guo Y., Johnson E., Cepurna W., Jia L., Dyck J., Morrison J.C. Does elevated intraocular pressure reduce retinal TRKB-mediated survival signaling in experimental glaucoma?. Exp. Eye Res. 2009.
18. Guo Y., Cepurna W.O., Dyck J., Doser T., Johnson E.C., Morrison J.C. Retinal cell responses to elevated intraocular pressure: a gene array comparison between the whole retina and retinal ganglion cell layer. Invest. Ophthalmol. Vis. Sci. 2010.
19. Hanninen V.A., Pantcheva M.B., Freeman E.E., Poulin N.R., Grosskreutz C.L. Activation of caspase 9 in a rat model of experimental glaucoma. Curr. Eye Res. 2002, 25(6):389-395.
20. Heijl A., Leske M.C., Bengtsson B., Hyman L., Bengtsson B., Hussein M. Reduction of intraocular pressure and glaucoma progression: results from the early manifest glaucoma trial. Arch. Ophthalmol. 2002, 120(10):1268-1279.
21. Hernandez M.R. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog. Retin. Eye Res. 2000, 19(3):297-321.
22. Howell G.R., Libby R.T., Jakobs T.C., Smith R.S., Phalan F.C., Barter J.W., Barbay J.M., Marchant J.K., Mahesh N., Porciatti V., et al. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007, 179(7):1523-1537.
23. Huang W., Fileta J.B., Filippopoulos T., Ray A., Dobberfuhl A., Grosskreutz C.L. Hsp27 phosphorylation in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2007, 48(9):4129-4135.
24. Huang X.R., Knighton R.W. Altered F-actin distribution in retinal nerve fiber layer of a rat model of glaucoma. Exp. Eye Res. 2009, 88(6):1107-1114.
25. Jakobs T.C., Libby R.T., Ben Y., John S.W., Masland R.H. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 2005, 171(2):313-325.
26. Ji J., Chang P., Pennesi M.E., Yang Z., Zhang J., Li D., Wu S.M., Gross R.L. Effects of elevated intraocular pressure on mouse retinal ganglion cells. Vision Res. 2005, 45(2):169-179.
27. Ji J.Z., Elyaman W., Yip H.K., Lee V.W., Yick L.W., Hugon J., So K.F. CNTF promotes survival of retinal ganglion cells after induction of ocular hypertension in rats: the possible involvement of STAT3 pathway. Eur. J. Neurosci. 2004, 19(2):265-272.
28. Jia L., Cepurna W.O., Johnson E.C., Morrison J.C. Patterns of intraocular pressure elevation after aqueous humor outflow obstruction in rats. Invest. Ophthalmol. Vis. Sci. 2000, 41(6):1380-1385.
29. Jia L., Cepurna W.O., Johnson E.C., Morrison J.C. Effect of general anesthetics on IOP in rats with experimental aqueous outflow obstruction. Invest. Ophthalmol. Vis. Sci. 2000, 41(11):3415-3419.
30. Jiang C., Moore M.J., Zhang X., Klassen H., Langer R., Young M. Intravitreal injections of GDNF-loaded biodegradable microspheres are neuroprotective in a rat model of glaucoma. Mol. Vis. 2007, 13:1783-1792.
31. John S.W. Mechanistic insights into glaucoma provided by experimental genetics the cogan lecture. Invest. Ophthalmol. Vis. Sci. 2005, 46(8):2649-2661.
32. John S.W., Smith R.S., Savinova O.V., Hawes N.L., Chang B., Turnbull D., Davisson M., Roderick T.H., Heckenlively J.R. Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Invest. Ophthalmol. Vis. Sci. 1998, 39(6):951-962.
33. Johnson E.C., Morrison J.C. Friend or foe? Resolving the impact of glial responses in glaucoma. J. Glaucoma 2009, 18(5):341-353.
34. Johnson E.C., Guo Y., Cepurna W.O., Morrison J.C. Neurotrophin roles in retinal ganglion cell survival: lessons from rat glaucoma models. Exp. Eye Res. 2009, 88(4):808-815.
35. Johnson E.C., Deppmeier L.M., Wentzien S.K., Hsu I., Morrison J.C. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Invest. Ophthalmol. Vis. Sci. 2000, 41(2):431-442.
36. Johnson E.C., Jia L., Cepurna W.O., Doser T.A., Morrison J.C. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 2007, 48(7):3161-3177.
37. Johnson E.C., Morrison J.C., Farrell S., Deppmeier L., Moore C.G., McGinty M.R. The effect of chronically elevated intraocular pressure on the rat optic nerve head extracellular matrix. Exp. Eye Res. 1996, 62(6):663-674.
38. Johnson T.V., Tomarev S.I. Rodent models of glaucoma. Brain Res. Bull. 2009, 81(2-3):349-358.
39. Ju W.K., Kim K.Y., Lindsey J.D., Angert M., Duong-Polk K.X., Scott R.T., Kim J.J., Kukhmazov I., Ellisman M.H., Perkins G.A., et al. Intraocular pressure elevation induces mitochondrial fission and triggers OPA1 release in glaucomatous optic nerve. Invest. Ophthalmol. Vis. Sci. 2008, 49(11):4903-4911.
40. Kalesnykas G., Niittykoski M., Rantala J., Miettinen R., Salminen A., Kaarniranta K., Uusitalo H. The expression of heat shock protein 27 in retinal ganglion and glial cells in a rat glaucoma model. Neuroscience 2007, 150(3):692-704.
41. Kass M.A., Heuer D.K., Higginbotham E.J., Johnson C.A., Keltner J.L., Miller J.P., Parrish R.K., Wilson M.R., Gordon M.O. The ocular hypertension treatment study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch. Ophthalmol. 2002, 120(6):701-713. discussion 829-830.
42. Kim C.Y., Kuehn M.H., Clark A.F., Kwon Y.H. Gene expression profile of the adult human retinal ganglion cell layer. Mol. Vis. 2006, 12:1640-1648.
43. Klein B.E., Klein R., Sponsel W.E., Franke T., Cantor L.B., Martone J., Menage M.J. Prevalence of glaucoma. The Beaver Dam Eye Study. Ophthalmology 1992, 99(10):1499-1504.
44. Kwong J.M., Lam T.T., Caprioli J. Hyperthermic pre-conditioning protects retinal neurons from N-methyl-D-aspartate (NMDA)-induced apoptosis in rat. Brain Res. 2003, 970(1-2):119-130.
45. Kwong J.M., Lalezary M., Nguyen J.K., Yang C., Khattar A., Piri N., Mareninov S., Gordon L.K., Caprioli J. Co-expression of heat shock transcription factors 1 and 2 in rat retinal ganglion cells. Neurosci. Lett. 2006, 405(3):191-195.
46. Levkovitch-Verbin H., Quigley H.A., Martin K.R., Valenta D., Baumrind L.A., Pease M.E. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest. Ophthalmol. Vis. Sci. 2002, 43(2):402-410.
47. Levkovitch-Verbin H., Quigley H.A., Martin K.R., Harizman N., Valenta D.F., Pease M.E., Melamed S. The transcription factor c-jun is activated in retinal ganglion cells in experimental rat glaucoma. Exp. Eye Res. 2005, 80(5):663-670.
48. Li R., Liu J.H. Telemetric monitoring of 24h intraocular pressure in conscious and freely moving C57BL/6J and CBA/CaJ mice. Mol. Vis. 2008, 14:745-749.
49. Li Y., Schlamp C.L., Poulsen K.P., Nickells R.W. Bax-dependent and independent pathways of retinal ganglion cell death induced by different damaging stimuli. Exp. Eye Res. 2000, 71(2):209-213.
50. Libby R.T., Li Y., Savinova O.V., Barter J., Smith R.S., Nickells R.W., John S.W. Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage. PLoS Genet. 2005, 1(1):17-26.
51. Libby R.T., Howell G.R., Pang I.H., Savinova O.V., Mehalow A.K., Barter J.W., Smith R.S., Clark A.F., John S.W. Inducible nitric oxide synthase, Nos2, does not mediate optic neuropathy and retinopathy in the DBA/2J glaucoma model. BMC Neurosci. 2007, 8(1):108.
52. Libby R.T., Anderson M.G., Pang I.H., Robinson Z.H., Savinova O.V., Cosma I.M., Snow A., Wilson L.A., Smith R.S., Clark A.F., et al. Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis. Neurosci. 2005, 22(5):637-648.
53. Lindsey J.D., Weinreb R.N. Elevated intraocular pressure and transgenic applications in the mouse. J. Glaucoma 2005, 14(4):318-320.
54. Mabuchi F., Aihara M., Mackey M.R., Lindsey J.D., Weinreb R.N. Regional optic nerve damage in experimental mouse glaucoma. Invest. Ophthalmol. Vis. Sci. 2004, 45(12):4352-4358.
55. Martin K.R., Quigley H.A., Zack D.J., Levkovitch-Verbin H., Kielczewski J., Valenta D., Baumrind L., Pease M.E., Klein R.L., Hauswirth W.W. Gene therapy with brain-derived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 2003, 44(10):4357-4365.
56. May C.A. The optic nerve head region of the aged rat: an immunohistochemical investigation. Curr. Eye Res. 2003, 26(6):347-354.
57. May C.A., Lutjen-Drecoll E. Morphology of the murine optic nerve. Invest. Ophthalmol. Vis. Sci. 2002, 43(7):2206-2212.
58. May C.A., Mittag T. Optic nerve degeneration in the DBA/2NNia mouse: is the lamina cribrosa important in the development of glaucomatous optic neuropathy?. Acta Neuropathol. 2006, 111(2):158-167.
59. McKinnon S.J., Schlamp C.L., Nickells R.W. Mouse models of retinal ganglion cell death and glaucoma. Exp. Eye Res. 2009, 88(4):816-824.
60. McLaren J.W., Brubaker R.F., FitzSimon J.S. Continuous measurement of intraocular pressure in rabbits by telemetry. Invest. Ophthalmol. Vis. Sci. 1996, 37(6):966-975.
61. Mittag T.W., Danias J., Pohorenec G., Yuan H.M., Burakgazi E., Chalmers-Redman R., Podos S.M., Tatton W.G. Retinal damage after 3 to 4 months of elevated intraocular pressure in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 2000, 41(11):3451-3459.
62. Miyahara T., Kikuchi T., Akimoto M., Kurokawa T., Shibuki H., Yoshimura N. Gene microarray analysis of experimental glaucomatous retina from cynomologous monkey. Invest. Ophthalmol. Vis. Sci. 2003, 44(10):4347-4356.
63. Moon J.I., Kim I.B., Gwon J.S., Park M.H., Kang T.H., Lim E.J., Choi K.R., Chun M.H. Changes in retinal neuronal populations in the DBA/2J mouse. Cell Tissue Res. 2005, 320(1):51-59.
64. Moore C.G., Johnson E.C., Morrison J.C. Circadian rhythm of intraocular pressure in the rat. Curr. Eye Res. 1996, 15(2):185-191.
65. Morgan J.E. Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye 2000, 14(Pt 3B):437-444.
66. Morrison J., Farrell S., Johnson E., Deppmeier L., Moore C.G., Grossmann E. Structure and composition of the rodent lamina cribrosa. Exp. Eye Res. 1995, 60(2):127-135.
67. Morrison J.C. Integrins in the optic nerve head: potential roles in glaucomatous optic neuropathy (an American Ophthalmological Society thesis). Trans. Am. Ophthalmol. Soc. 2006, 104:453-477.
68. Morrison J.C., Johnson E., Cepurna W.O. Rat models for glaucoma research. Prog. Brain Res. 2008, 173:285-301.
69. Morrison J.C., Jerdan J.A., Dorman M.E., Quigley H.A. Structural proteins of the neonatal and adult lamina cribrosa. Arch. Ophthalmol. 1989, 107(8):1220-1224.
70. Morrison J.C., Dorman-Pease M.E., Dunkelberger G.R., Quigley H.A. Optic nerve head extracellular matrix in primary optic atrophy and experimental glaucoma. Arch. Ophthalmol. 1990, 108(7):1020-1024.
71. Morrison J.C., Johnson E.C., Cepurna W.O., Funk R.H. Microvasculature of the rat optic nerve head. Invest. Ophthalmol. Vis. Sci. 1999, 40(8):1702-1709.
72. Morrison J.C., Johnson E.C., Cepurna W., Jia L. Understanding mechanisms of pressure-induced optic nerve damage. Prog. Retin. Eye Res. 2005, 24(2):217-240.
73. Morrison J.C., Moore C.G., Deppmeier L.M., Gold B.G., Meshul C.K., Johnson E.C. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 1997, 64(1):85-96.
74. Neufeld A.H., Hernandez M.R., Gonzalez M. Nitric oxide synthase in the human glaucomatous optic nerve head. Arch. Ophthalmol. 1997, 115(4):497-503.
75. Neufeld A.H., Sawada A., Becker B. Inhibition of nitric-oxide synthase 2 by aminoguanidine provides neuroprotection of retinal ganglion cells in a rat model of chronic glaucoma. Proc. Natl. Acad. Sci. U.S.A. 1999, 96(17):9944-9948.
76. Neufeld A.H., Das S., Vora S., Gachie E., Kawai S., Manning P.T., Connor J.R. A prodrug of a selective inhibitor of inducible nitric oxide synthase is neuroprotective in the rat model of glaucoma. J. Glaucoma 2002, 11(3):221-225.
77. Nissirios N., Chanis R., Johnson E., Morrison J., Cepurna W.O., Jia L., Mittag T., Danias J. Comparison of anterior segment structures in two rat glaucoma models: an ultrasound biomicroscopic study. Invest. Ophthalmol. Vis. Sci. 2008, 49(6):2478-2482.
78. Pang I.H., Clark A.F. Rodent models for glaucoma retinopathy and optic neuropathy. J. Glaucoma 2007, 16(5):483-505.
79. Pang I.H., Johnson E.C., Jia L., Cepurna W.O., Shepard A.R., Hellberg M.R., Clark A.F., Morrison J.C. Evaluation of inducible nitric oxide synthase in glaucomatous optic neuropathy and pressure-induced optic nerve damage. Invest. Ophthalmol. Vis. Sci. 2005, 46(4):1313-1321.
80. Park K.H., Cozier F., Ong O.C., Caprioli J. Induction of heat shock protein 72 protects retinal ganglion cells in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 2001, 42(7):1522-1530.
81. Pease M.E., McKinnon S.J., Quigley H.A., Kerrigan-Baumrind L.A., Zack D.J. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2000, 41(3):764-774.
82. Pease M.E., Zack D.J., Berlinicke C., Bloom K., Cone F., Wang Y., Klein R.L., Hauswirth W.W., Quigley H.A. Effect of CNTF on retinal ganglion cell survival in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2009, 50(5):2194-2200.
83. Quigley H.A., Green W.R. The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. Ophthalmology 1979, 86(10):1803-1830.
84. Quigley H.A., Addicks E.M. Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest. Ophthalmol. Vis. Sci. 1980, 19(2):137-152.
85. Quigley H.A., Addicks E.M. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch. Ophthalmol. 1981, 99(1):137-143.
86. Quigley H.A., Nickells R.W., Kerrigan L.A., Pease M.E., Thibault D.J., Zack D.J. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest. Ophthalmol. Vis. Sci. 1995, 36(5):774-786.
87. Quigley H.A., McKinnon S.J., Zack D.J., Pease M.E., Kerrigan-Baumrind L.A., Kerrigan D.F., Mitchell R.S. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest. Ophthalmol. Vis. Sci. 2000, 41(11):3460-3466.
88. Quigley H.A., Addicks E.M., Green W.R., Maumenee A.E. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch. Ophthalmol. 1981, 99(4):635-649.
89. Reichstein D., Ren L., Filippopoulos T., Mittag T., Danias J. Apoptotic retinal ganglion cell death in the DBA/2 mouse model of glaucoma. Exp. Eye Res. 2007, 84(1):13-21.
90. Rudzinski M., Wong T.P., Saragovi H.U. Changes in retinal expression of neurotrophins and neurotrophin receptors induced by ocular hypertension. J. Neurobiol. 2004, 58(3):341-354.
91. Sakai M., Sakai H., Nakamura Y., Fukuchi T., Sawaguchi S. Immunolocalization of heat shock proteins in the retina of normal monkey eyes and monkey eyes with laser-induced glaucoma. Jpn. J. Ophthalmol. 2003, 47(1):42-52.
92. Salinas-Navarro M., Alarcon-Martinez L., Valiente-Soriano F.J., Ortin-Martinez A., Jimenez-Lopez M., Aviles-Trigueros M., Villegas-Perez M.P., de la Villa P., Vidal-Sanz M. Functional and morphological effects of laser-induced ocular hypertension in retinas of adult albino Swiss mice. Mol. Vis. 2009, 15:2578-2598.
93. Sappington R.M., Carlson B.J., Crish S.D., Calkins D.J. The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest. Ophthalmol. Vis. Sci. 2009, 51(1):207-216.
94. Sawada A., Neufeld A.H. Confirmation of the rat model of chronic, moderately elevated intraocular pressure. Exp. Eye Res. 1999, 69(5):525-531.
95. Schlamp C.L., Johnson E.C., Li Y., Morrison J.C., Nickells R.W. Changes in Thy1 gene expression associated with damaged retinal ganglion cells. Mol. Vis. 2001, 7:192-201.
96. Schlamp C.L., Li Y., Dietz J.A., Janssen K.T., Nickells R.W. Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci. 2006, 7(1):66.
97. Shareef S.R., Garcia-Valenzuela E., Salierno A., Walsh J., Sharma S.C. Chronic ocular hypertension following episcleral venous occlusion in rats. Exp. Eye Res. 1995, 61(3):379-382. (Letter).
98. Sommer A. Intraocular pressure and glaucoma. Am. J. Ophthalmol. 1989, 107(2):186-188.
99. Sommer A., Katz J., Quigley H.A., Miller N.R., Robin A.L., Richter R.C., Witt K.A. Clinically detectable nerve fiber atrophy precedes the onset of glaucomatous field loss. Arch. Ophthalmol. 1991, 109(1):77-83.
100. Steele M.R., Inman D.M., Calkins D.J., Horner P.J., Vetter M.L. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest. Ophthalmol. Vis. Sci. 2006, 47(3):977-985.
101. Sugiyama K., Gu Z.B., Kawase C., Yamamoto T., Kitazawa Y. Optic nerve and peripapillary choroidal microvasculature of the rat eye. Invest. Ophthalmol. Vis. Sci. 1999, 40(13):3084-3090.
102. Sun D., Lye-Barthel M., Masland R.H., Jakobs T.C. The morphology and spatial arrangement of astrocytes in the optic nerve head of the mouse. J. Comp. Neurol. 2009, 516(1):1-19.
103. Takeda M., Kato H., Takamiya A., Yoshida A., Kiyama H. Injury-specific expression of activating transcription factor-3 in retinal ganglion cells and its colocalized expression with phosphorylated c-Jun. Invest. Ophthalmol. Vis. Sci. 2000, 41(9):2412-2421.
104. Tuulonen A., Airaksinen P.J. Initial glaucomatous optic disk and retinal nerve fiber layer abnormalities and their progression. Am. J. Ophthalmol. 1991, 111(4):485-490.
105. Ueda J., Sawaguchi S., Hanyu T., Yaoeda K., Fukuchi T., Abe H., Ozawa H. Experimental glaucoma model in the rat induced by laser trabecular photocoagulation after an intracameral injection of India ink. Jpn. J. Ophthalmol. 1998, 42(5):337-344.
106. Urcola J.H., Hernandez M., Vecino E. Three experimental glaucoma models in rats: comparison of the effects of intraocular pressure elevation on retinal ganglion cell size and death. Exp. Eye Res. 2006, 83(2):429-437.
107. Walsh M.M., Yi H., Friedman J., Cho K.I., Tserentsoodol N., McKinnon S., Searle K., Yeh A., Ferreira P.A. Gene and protein expression pilot profiling and biomarkers in an experimental mouse model of hypertensive glaucoma. Exp. Biol. Med. (Maywood) 2009, 234(8):918-930.
108. Wax M.B., Tezel G. Immunoregulation of retinal ganglion cell fate in glaucoma. Exp. Eye Res. 2009, 88(4):825-830.
109. Weber A.J., Harman C.D. Structure-function relations of parasol cells in the normal and glaucomatous primate retina. Invest. Ophthalmol. Vis. Sci. 2005, 46(9):3197-3207.
110. Weber A.J., Kaufman P.L., Hubbard W.C. Morphology of single ganglion cells in the glaucomatous primate retina. Invest. Ophthalmol. Vis. Sci. 1998, 39(12):2304-2320.
111. Weber A.J., Viswanathan S., Ramanathan C., Harman C.D. Combined application of BDNF to the eye and brain enhances ganglion cell survival and function in the cat after optic nerve injury. Invest. Ophthalmol. Vis. Sci. 2009, 51(1):327-334.
112. WoldeMussie E., Ruiz G., Wijono M., Wheeler L.A. Neuroprotection of retinal ganglion cells by brimonidine in rats with laser-induced chronic ocular hypertension. Invest. Ophthalmol. Vis. Sci. 2001, 42(12):2849-2855.
113. Yang Z., Quigley H.A., Pease M.E., Yang Y., Qian J., Valenta D., Zack D.J. Changes in gene expression in experimental glaucoma and optic nerve transection: the equilibrium between protective and detrimental mechanisms. Invest. Ophthalmol. Vis. Sci. 2007, 48(12):5539-5548.
114. Zhou Y., Pernet V., Hauswirth W.W., Di Polo A. Activation of the extracellular signal-regulated kinase 1/2 pathway by AAV gene transfer protects retinal ganglion cells in glaucoma. Mol. Ther. 2005, 12(3):402-412.