Modeling glaucoma in rats by sclerosing aqueous outflow pathways to elevate intraocular pressure

Experimental Eye Research

Volumn 141, Issue , 2015, Pages 23-32

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

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Aqueous outflow; Experimental models; Glaucoma; Hypertonic saline; Intraocular pressure; Optic nerve injury; Tonometry; Trabecular meshwork

Indexed keywords

SODIUM CHLORIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; AQUEOUS HUMOR; AQUEOUS HUMOR OUTFLOW; ARTICLE; AXONAL INJURY; CONTROLLED STUDY; FEMALE; GLAUCOMA; INTRAOCULAR PRESSURE; INTRAOCULAR PRESSURE ABNORMALITY; NONHUMAN; OPTIC NERVE; OPTIC NERVE INJURY; OPTIC NERVE LESION; PRIORITY JOURNAL; RAT; TRABECULAR MESHWORK; ANIMAL; DISEASE MODEL; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AQUEOUS HUMOR; DISEASE MODELS, ANIMAL; GLAUCOMA; HUMANS; INTRAOCULAR PRESSURE; RATS; SALINE SOLUTION, HYPERTONIC;

EID: 84945491485     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.05.012     Document Type: Article

References (81)

1. Abdul Y., Akhter N., Husain S. Delta-opioid agonist SNC-121 protects retinal ganglion cell function in a chronic ocular hypertensive rat model. Invest Ophthalmol. Vis. Sci. 2013, 54:1816-1828.
2. Almasieh M., Lieven C.J., Levin L.A., Di Polo A. A cell-permeable phosphine-borane complex delays retinal ganglion cell death after axonal injury through activation of the pro-survival extracellular signal-regulated kinases 1/2 pathway. J. Neurochem. 2011, 118:1075-1086.
3. Almasieh M., MacIntyre J.N., Pouliot M., Casanova C., Vaucher E., Kelly M.E., Di Polo A. Acetylcholinesterase inhibition promotes retinal vasoprotection and increases ocular blood flow in experimental glaucoma. Invest Ophthalmol. Vis. Sci. 2013, 54:3171-3183.
4. Almasieh M., Zhou Y., Kelly M.E., Casanova C., Di Polo A. Structural and functional neuroprotection in glaucoma: role of galantamine-mediated activation of muscarinic acetylcholine receptors. Cell Death Dis. 2010, 1:e27.
5. Anderson D.R. Ultrastructure of human and monkey lamina cribrosa and optic nerve head. Arch. Ophthalmol. 1969, 82:800-814.
6. Anderson D.R. Ultrastructure of the optic nerve head. Arch. Ophthalmol. 1970, 83:63-73.
7. Burgoyne C.F. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp. Eye Res. 2010, 93:120-132.
8. Burgoyne C.F., Downs J.C., Bellezza A.J., Hart R.T. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol. Vis. Sci. 2004, 45:4388-4399.
9. Cepurna W.O., Kayton R.J., Johnson E.C., Morrison J.C. Age related optic nerve axonal loss in adult Brown Norway rats. Exp. Eye Res. 2005, 80:877-884.
10. Chauhan B.C., Pan J., Archibald M.L., LeVatte T.L., Kelly M.E., Tremblay F. Effect of intraocular pressure on optic disc topography, electroretinography, and axonal loss in a chronic pressure-induced rat model of optic nerve damage. Invest Ophthalmol. Vis. Sci. 2002, 43:2969-2976.
11. Colafrancesco V., Coassin M., Rossi S., Aloe L. Effect of eye NGF administration on two animal models of retinal ganglion cells degeneration. Ann. Ist. Super. Sanita 2011, 47:284-289.
12. Cone-Kimball E., Nguyen C., Oglesby E.N., Pease M.E., Steinhart M.R., Quigley H.A. Scleral structural alterations associated with chronic experimental intraocular pressure elevation in mice. Mol. Vis. 2013, 19:2023-2039.
13. Cordeiro M.F., Guo L., Luong V., Harding G., Wang W., Jones H.E., Moss S.E., Sillito A.M., Fitzke F.W. Real-time imaging of single nerve cell apoptosis in retinal neurodegeneration. Proc. Natl. Acad. Sci. U S A 2004, 101:13352-13356.
14. Dai C., Khaw P.T., Yin Z.Q., Li D., Raisman G., Li Y. Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure. Glia 2012, 60:13-28.
15. Fechtner R.D., Weinreb R.N. Mechanisms of optic nerve damage in primary open angle glaucoma. Surv. Ophthalmol. 1994, 39:23-42.
16. Fortune B., Bui B.V., Morrison J.C., Johnson E.C., Dong J., Cepurna W.O., Jia L., Barber S., Cioffi G.A. Selective ganglion cell functional loss in rats with experimental glaucoma. Invest Ophthalmol. Vis. Sci. 2004, 45:1854-1862.
17. Fu C.T., Sretavan D. Laser-induced ocular hypertension in albino CD-1 mice. Invest Ophthalmol. Vis. Sci. 2010, 51:980-990.
18. Gaasterland D., Kupfer C. Experimental glaucoma in the rhesus monkey. Invest Ophthalmol. 1974, 13:455-457.
19. Grozdanic S.D., Betts D.M., Sakaguchi D.S., Allbaugh R.A., Kwon Y.H., Kardon R.H. Laser-induced mouse model of chronic ocular hypertension. Invest Ophthalmol. Vis. Sci. 2003, 44:4337-4346.
20. 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, 46:175-182.
21. Guo Y., Cepurna W.O., Dyck J.A., Doser T.A., 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, 51:3003-3018.
22. Guo Y., Johnson E.C., Cepurna W.O., Dyck J.A., Doser T., Morrison J.C. Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model. Invest Ophthalmol. Vis. Sci. 2011, 52:1460-1473.
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, 48:4129-4135.
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, 88:1107-1114.
25. 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, 41:3415-3419.
26. 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, 41:1380-1385.
27. Johnson E.C., Cepurna W.O., Choi D., Choe T.E., Morrison J.C. Radiation Pretreatment does not protect the rat optic nerve from elevated intraocular pressure-induced injury. Invest Ophthalmol. Vis. Sci. 2014, 56:412-419.
28. 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, 41:431-442.
29. Johnson E.C., Doser T.A., Cepurna W.O., Dyck J.A., Jia L., Guo Y., Lambert W.S., Morrison J.C. Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma. Invest Ophthalmol. Vis. Sci. 2011, 52:504-518.
30. 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, 48:3161-3177.
31. Kipfer-Kauer A., McKinnon S.J., Frueh B.E., Goldblum D. Distribution of amyloid precursor protein and amyloid-beta in ocular hypertensive C57BL/6 mouse eyes. Curr. Eye Res. 2010, 35:828-834.
32. Kompass K.S., Agapova O.A., Li W., Kaufman P.L., Rasmussen C.A., Hernandez M.R. Bioinformatic and statistical analysis of the optic nerve head in a primate model of ocular hypertension. BMC Neurosci. 2008, 9:93.
33. Kwong J.M., Vo N., Quan A., Nam M., Kyung H., Yu F., Piri N., Caprioli J. The dark phase intraocular pressure elevation and retinal ganglion cell degeneration in a rat model of experimental glaucoma. Exp. Eye Res. 2013, 112:21-28.
34. 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, 80:663-670.
35. 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, 43:402-410.
36. Li R., Liu J.H. Telemetric monitoring of 24 h intraocular pressure in conscious and freely moving C57BL/6J and CBA/CaJ mice. Mol. Vis. 2008, 14:745-749.
37. Lozano D.C., Hartwick A.T., Twa M.D. Circadian rhythm of intraocular pressure in the adult rat. Chronobiol. Int. 2015, 1-11.
38. Moore C.G., Epley D., Milne S.T., Morrison J.C. Long-term non-invasive measurement of intraocular pressure in the rat eye. Curr. Eye Res. 1995, 14:711-717.
39. Moore C.G., Johnson E.C., Morrison J.C. Circadian rhythm of intraocular pressure in the rat. Curr. Eye Res. 1996, 15:185-191.
40. Moore C.G., Milne S.T., Morrison J.C. Noninvasive measurement of rat intraocular pressure with the Tono-Pen. Invest Ophthalmol. Vis. Sci. 1993, 34:363-369.
41. 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, 60:127-135.
42. Morrison J.C. Elevated intraocular pressure and optic nerve injury models in the rat. J. Glaucoma 2005, 14:315-317.
43. Morrison J.C., Cepurna Ying Guo W.O., Johnson E.C. Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma. Exp. Eye Res. 2011, 93:156-164.
44. Morrison J.C., DeFrank M.P., Van Buskirk E.M. Comparative microvascular anatomy of mammalian ciliary processes. Invest Ophthalmol. Vis. Sci. 1987, 28:1325-1340.
45. Morrison J.C., Fraunfelder F.W., Milne S.T., Moore C.G. Limbal microvasculature of the rat eye. Invest Ophthalmol. Vis. Sci. 1995, 36:751-756.
46. Morrison J.C., Jia L., Cepurna W., Guo Y., Johnson E. Reliability and sensitivity of the TonoLab rebound tonometer in awake Brown Norway rats. Invest Ophthalmol. Vis. Sci. 2009, 50:2802-2808.
47. Morrison J.C., Johnson E.C., Cepurna W., Jia L. Understanding mechanisms of pressure-induced optic nerve damage. Prog. Retin Eye Res. 2005, 24:217-240.
48. Morrison J.C., Johnson E.C., Cepurna W.O., Funk R.H. Microvasculature of the rat optic nerve head. Invest Ophthalmol. Vis. Sci. 1999, 40:1702-1709.
49. 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, 64:85-96.
50. 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, 96:9944-9948.
51. Nguyen J.V., Soto I., Kim K.Y., Bushong E.A., Oglesby E., Valiente-Soriano F.J., Yang Z., Davis C.H., Bedont J.L., Son J.L., Wei J.O., Buchman V.L., Zack D.J., Vidal-Sanz M., Ellisman M.H., Marsh-Armstrong N. Myelination transition zone astrocytes are constitutively phagocytic and have synuclein dependent reactivity in glaucoma. Proc. Natl. Acad. Sci. U S A 2011, 108:1176-1181.
52. 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, 49:2478-2482.
53. Ollivier F.J., Brooks D.E., Kallberg M.E., Sapp H.L., Komaromy A.M., Stevens G.R., Dawson W.W., Sherwood M.B., Lambrou G.N. Time-specific intraocular pressure curves in Rhesus macaques (Macaca mulatta) with laser-induced ocular hypertension. Vet. Ophthalmol. 2004, 7:23-27.
54. Onda E., Cioffi G.A., Bacon D.R., Van Buskirk E.M. Microvasculature of the human optic nerve. Am. J. Ophthalmol. 1995, 120:92-102.
55. 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, 46:1313-1321.
56. Pang I.H., Wang W.H., Clark A.F. Acute effects of glaucoma medications on rat intraocular pressure. Exp. Eye Res. 2005, 80:207-214.
57. 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, 42:1522-1530.
58. Pease M.E., Cone F.E., Gelman S., Son J.L., Quigley H.A. Calibration of the TonoLab tonometer in mice with spontaneous or experimental glaucoma. Invest Ophthalmol. Vis. Sci. 2010, 52:858-864.
59. Pease M.E., Hammond J.C., Quigley H.A. Manometric calibration and comparison of TonoLab and TonoPen tonometers in rats with experimental glaucoma and in normal mice. J. Glaucoma 2006, 15:512-519.
60. 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, 50:2194-2200.
61. Prasanna G., Hulet C., Desai D., Krishnamoorthy R.R., Narayan S., Brun A.M., Suburo A.M., Yorio T. Effect of elevated intraocular pressure on endothelin-1 in a rat model of glaucoma. Pharmacol. Res. 2005, 51:41-50.
62. Quigley H.A., Addicks E.M. Chronic experimental glaucoma in primates. I. Production of elevated intraocular pressure by anterior chamber injection of autologous ghost red blood cells. Invest Ophthalmol. Vis. Sci. 1980, 19:126-136.
63. 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, 99:137-143.
64. Quigley H.A., Anderson D.R. Distribution of axonal transport blockade by acute intraocular pressure elevation in the primate optic nerve head. Invest Ophthalmol. Vis. Sci. 1977, 16:640-644.
65. Rowland J.M., Potter D.E., Reiter R.J. Circadian rhythm in intraocular pressure: a rabbit model. Curr. Eye Res. 1981, 1:169-173.
66. Samsel P.A., Kisiswa L., Erichsen J.T., Cross S.D., Morgan J.E. A novel method for the induction of experimental glaucoma using magnetic microspheres. Invest Ophthalmol. Vis. Sci. 2010, 52:1671-1675.
67. 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, 51:207-216.
68. Sawada A., Neufeld A.H. Confirmation of the rat model of chronic, moderately elevated intraocular pressure. Exp. Eye Res. 1999, 69:525-531.
69. 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, 7:66.
70. Shareef S.R., Garcia-Valenzuela E., Salierno A., Walsh J., Sharma S.C. Chronic ocular hypertension following episcleral venous occlusion in rats [letter]. Exp. Eye Res. 1995, 61:379-382.
71. Sigal I.A., Yang H., Roberts M.D., Grimm J.L., Burgoyne C.F., Demirel S., Downs J.C. IOP-induced lamina cribrosa deformation and scleral canal expansion: independent or related?. Invest Ophthalmol. Vis. Sci. 2011, 52:9023-9032.
72. 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, 40:3084-3090.
73. 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, 516:1-19.
74. Taylor S., Calder C.J., Albon J., Erichsen J.T., Boulton M.E., Morgan J.E. Involvement of the CD200 receptor complex in microglia activation in experimental glaucoma. Exp. Eye Res. 2011, 92:338-343.
75. Tehrani S., Johnson E.C., Cepurna W.O., Morrison J.C. Astrocyte processes label for filamentous actin and reorient early within the optic nerve head in a rat glaucoma model. Invest Ophthalmol. Vis. Sci. 2014, 55:6945-6952.
76. Tezel G., Yang X., Luo C., Cai J., Powell D.W. An astrocyte-specific proteomic approach to inflammatory responses in experimental rat glaucoma. Invest Ophthalmol. Vis. Sci. 2012, 53:4220-4233.
77. Valderrama C.M., Li R., Liu J.H. Direct effect of light on 24-h variation of aqueous humor protein concentration in Sprague-Dawley rats. Exp. Eye Res. 2008, 87:487-491.
78. 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, N.J) 2009, 234:918-930.
79. Wang W.H., Millar J.C., Pang I.H., Wax M.B., Clark A.F. Noninvasive measurement of rodent intraocular pressure with a rebound tonometer. Invest Ophthalmol. Vis. Sci. 2005, 46:4617-4621.
80. 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, 42:2849-2855.
81. Yang M.H., Dibas A., Tyan Y.C. Changes in retinal aquaporin-9 (AQP9) expression in glaucoma. Biosci. Rep. 2013, 33.