Experimental Models of Glaucoma
https://doi.org/10.21516/2072-0076-2021-14-4-164-171
Abstract
Optic nerve pits are a mono- or bilateral congenital anomaly represented by optic disc depressions of various sizes. In half of the cases, the pits are complicated by edema, central retinal detachment and retinoschisis, and cause visual function decrease. Visual acuity losses can be either insignificant or pronounced. Optic discs pits have been investigated massively over the last century and a half, but their etiology is still underresearched. In recent years, however, due to the development of digital scanning and data processing technologies and the emergence of non-invasive highly informative diagnostic methods, it has become possible to reveal structural and functional changes of the optic disc in vivo, in addition to the traditional detection of histological changes in cadaveric eyes.Glaucomatous process modeling is one of the challenges in ophthalmology. And this is due primarily to the fact that, so far, the main reasons for the onset and progression of glaucoma. Numerous works on experimental research in its core model ocular. However, there are forms of glaucoma, which are independent of the level of intraocular pressure. Ideal model of glaucoma is considered a model with the development of the characteristic symptom in which a key symptom is a slowly progressive excavation of the optic nerve. But given the new knowledge in the pathogenesis of neurodegenerative changes in glaucoma in this model should be added and the opportunity to study the brain, vascular factors of progression, the level of neurotransmitters, trophic factors, etc. Therefore, we tried to make the analysis of models of glaucoma in various experimental animals and determine the most appropriate model for studying the pathogenesis of glaucoma.
About the Authors
O. N. Onufriichuk
Turner National Medical Research Center for Сhildren's Orthopedics and Trauma Surgery
Russian Federation
Russian Federation
Oleg N. Onufriichuk — Cand. of Med. Sci., ophthalmologist
64-68 Parkovaya st., Pushkin, Saint-Petersburg, 196603
I. R. Gazizova
N.P. Bekhtereva Institute of the Human Brain of the Russian Academy of Sciences (IHB RAS)
Russian Federation
Russian Federation
Ilmira R. Gazizova — Dr. of Med. Sci., head of the ophthalmological department
9, Akademika Pavlova st., 197376, Saint-Petersburg
A. V. Kuroyedov
Mandryka Central Clinical Hospital; Pirogov Russian National Research Medical University
Russian Federation
Russian Federation
Alexander V. Kuroyedov — Dr. of Med. Sci., head of the ophthalmological department, professor, chair of ophthalmology
8а, Bol’shaya Olen’ya st., Moscow, 107014
1, Ostrovitianov st., Moscow, 117997
А. V. Seleznev
Ivanovo State Medical Academy
Russian Federation
Russian Federation
Alexey V. Seleznev — Cand. of Med. Sci., assistant professor, chair of otolaryngology and ophthalmology
8, Sheremetevskiy av., Ivanovo, 153012
A. Yu. Brezhnev
Kursk State Medical University
Russian Federation
Russian Federation
Andrey Yu. Brezhnev — Cand. of Med. Sci., assistant professor, chair of ophthalmology
3, Karl Marx st., Kursk, 305041
References
1. Darenskaya N.G., Ushakov I.B., Ivanov I.V., et al. Extrapolation of experimental data on humans in physiology and radiology. Voronezh: Istoki; 2004 (in Russian).
2. Karkishchenko N.N. Alternatives to biomedicine. V. 1. Basics of biomedicine and pharmacomodelling. Moscow: Izdatel'stvo VPK; 2007 (in Russian).
3. Karkishchenko N.N. Extrapolation of experimental data on the methodology for testing drugs in the clinic. Farmakologiya i toksikologiya. 1982; 3: 22 (in Russian).
4. Krasovskiy G.N., Egorova N.A., Antonova M.G. The problem of extrapolating the results of bioassays on humans. Toksikologicheskiy vestnik. 2000; 6: 13–9 (in Russian).
5. Karamyan A.I. Functional evolution of the brain of vertebrates. Leningrad: Nauka; 1970 (in Russian).
6. Batuev A.S. Frontal lobe evolution and integrative brain activity. Leningrad: Meditsina; 1973 (in Russian).
7. Vasilevskiy N.N. Ecological physiology of the brain. Leningrad: Meditsina; 1979 (in Russian).
8. Krushinskiy L.V. Problems of animal behavior. Selected Works. V. 1. Moscow: Nauka; 1993 (in Russian).
9. Batuev A.S. Higher integrative systems of the brain. AN SSSR. Leningrad: Nauka; 1981 (in Russian).
10. Villaseca A. The impact of intraocular pressure on the glaucomatous disk. A theoretical study based on hydrostatic principles. Arch. Ophthalmol. 1962; 67: 769–72. doi: 10.1001/archopht.1962.00960020769012
11. Novokhatskiy A.S., Ponomarchuk V.S. Eye diseases in the pathology of the autonomic nervous system. Kiev: Zdorov’ya, 1988 (in Russian).
12. Lipovetskaya E.M. The development of experimental glaucoma with prolonged intravenous administration of adrenaline. Oftal'mologicheskiy zhurnal. 1966; 3: 221–3 (in Russian).
13. Ito Y.A., Belforte N., Cueva Vargas J.L., Di Polo A. A magnetic microbead occlusion model to induce ocular hypertension-dependent glaucoma in mice. J. Vis. Exp. 2016; 3 (109): e53731. doi:10.3791/53731
14. Ficarrotta K.R., Mohamed Y.H., Passaglia C.L. Experimental glaucoma model with controllable intraocular pressure history. Sci. Rep. 2020; 10 (1): 126. doi: 10.1038/s41598-019-57022-5
15. Johnson T.V., Tomarev S.I. Rodent models of glaucoma. Brain Res. Bull. 2010; 81 (2-3): 349–58. doi: 10.1016/j.brainresbull.2009.04.004
16. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Text with EEA relevance OJ L 276, 20.10.2010; 33–79 (BG, ES, CS, DA, DE, ET, EL, EN, FR, IT, LV, LT, HU, MT, NL, PL, PT, RO, SK, SL, FI, SV). Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32010L0063
17. Denisov A.V., Cheprakova V.A., Anisin A.V., Bezrukov S.I. Ethical aspects of modern use of animals in experimental studies. Bulletin of the Russian Military Medical Academy. 2018; 63 (3): 238–42 (in Russian). doi: 10.17816/brmma12383
18. Olivier F.J., Brooks D.E., Kallberg M.E., et al. Time-specific diurnal intraocular pressure curves in Rhesus macaques (Macaca mulatta) with laser-induced ocular hypertension. Vet. Ophthalmol. 2004; 7 (1): 23–7. doi: 10.1111/j.1463-5224.2004.00316.x
19. Morrison J.C., Moore C.G., Deppmeier L.M., et al. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 1997; 64 (1): 85–96. doi: 10.1006/exer.1996.0184
20. Vecino E., Sharma S.C. Glaucoma animal models. In: Glaucoma-basic and clinical concepts. InTech. 2011; 11: 319–34. doi:10.5772/18498
21. Liu H.H., Flanagan J.G. A mouse model of chronic ocular hypertension induced by circumlimbal suture. Invest. Ophthalmol. Vis. Sci. 2017; 58 (1): 353–61. doi: 10.1167/iovs.16-20576
22. Phulke S., Kaushik S., Kaur S., Pandav S. Steroid-induced glaucoma: An avoidable irreversible blindness. J. Curr. Glaucoma Pract. 2017; 11 (2): 67–72. doi:10.5005/jp-journals-l0028-1226
23. Evangelho K., Mastronardi C.A., de-la-Torre A. Experimental models of glaucoma: a powerful translational tool for the future development of new therapies for glaucoma in humans - a review of the literature. Medicina (Kaunas). 2019 Jun; 55 (6): 280. doi: 10.3390/medicina55060280
24. Qin Y., Lam S., Yam G.H., et al. A rabbit model of age-dependent ocular hypertensive response to topical corticosteroids. Acta Ophthalmol. 2012 Sep; 90 (6): 559–63. doi: 10.1111/j.1755-3768.2010.02016.x PMID: 21044276
25. Nuzzi R., Tridico F. Glaucoma: biological trabecular and neuroretinal pathology with perspectives of therapy innovation and preventive diagnosis. Front. Neurosci. 2017; 11: 494. doi: 10.3389/fnins.2017.00494
26. Iomdina E.N., Khoroshilova-Maslova I.P., Robustova O.V., et al. Mitochondriatargeted antioxidant SkQ1 reverses glaucomatous lesions in rabbits. Front. Biosci 2015; 20: 892–901. doi: 10.2741/4343
27. Rosenbaum D.M., Degterev A., David J., et al. Necroptosis, a novel form of caspase-independent cell death, contributes to neuronal damage in a retinal ischemia-reperfusion injury model. J. Neurosci. Res. 2010; 88 (7): 1569–76. doi: 10.1002/jnr.22314
28. Bouhenni R.A., Dunmire J., Sewell A., Edward D.P. Animal models of glaucoma. J. Biomed. Biotechnol. 2012; 2012: 692609. doi: 10.1155/2012/692609
29. Gelatt K.N. Animal models for glaucoma. Inv. Ophthalmol. Vis. Sci. 1977; 16 (7): 592–6.
30. Vecino E. Animal models in the study of the glaucoma: past, present and future. Arch. de la Soc. Esp. de Oftal. 2008; 83 (9): 517–9. doi: 10.4321/s0365-66912008000900001
31. Rasmussen C.A., Kaufman P.L. Primate glaucoma models. J. Glaucoma. 2005; 14 (4): 311–4. doi: 10.1097/01.ijg.0000169409.01635.bc
32. Brooks D.E. Glaucoma in the dog and cat. Vet. Clin. North Am. Small Anim. Pract. 1990; 20 (3): 775–7. doi: 10.1016/s0195-5616(90)50062-5
33. Dietrich U. Feline glaucomas. Clin. Tech. Small Anim. Pract. 2005; 20 (2): 108–16. doi: 10.1053/j.ctsap.2004.12.015
34. Ruiz-Ederra J., García M., Hernández M., et al. The pig eye as a novel model of glaucoma. Exp. Eye Res. 2005; 81 (5): 561–9. doi: 10.1016/j.exer.2005.03.014
35. Pang I.H., Wang W.H., Clark A.F. Acute effects of glaucoma medications on rat intraocular pressure. Exp. Eye Res. 2005; 80 (2): 207–14. doi: 10.1016/j.exer.2004.09.001
36. Weber A.J., Viswanathan S. The primate model of experimental glaucoma. In: Tombran-Tink J., Barnstable C.J., Shields M.B. (eds). Mechanisms of the Glaucomas. Humana Press. NY, USA. 2008: 551–77.
37. Dawson W.W., Brooks D.E., Hope G.M., et al. Primary open angle glaucomas in the rhesus monkey. Br. J. Ophthalmol. 1993; 77 (5): 302–10. doi: 10.1136/bjo.77.5.302
38. Gaasterland D., Kupfer C. Experimental glaucoma in the rhesus monkey. Invest. Ophthalmol. 1974 Jun; 13 (6): 455–7. PMID: 4208801
39. Glovinsky Y., Quigley H.A., Dunkelberger G.R. Retinal ganglion cell loss is size dependent in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 1991; 32 (3): 484–91.
40. Glovinsky Y., Quigley H.A., Pease M.E. Foveal ganglion cell loss is size dependent in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 1993 Feb; 34 (2): 395–400. PMID: 8440594
41. 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 Feb; 19 (2): 137–52. PMID: 6153173
42. Quigley H.A., Hohman R.M. Laser energy levels for trabecular meshwork damage in the primate eye. Invest. Ophthalmol. Vis. Sci. 1983 Sep; 24 (9): 1305–7. PMID: 6885314
43. Quigley H.A., Sanchez R.M., Dunkelberger G.R. Chronic glaucoma selectively damages large optic nerve fibers. Invest. Ophthalmol. Vis. Sci. 1987 Jun; 28 (6): 913–20. PMID:3583630
44. Toris C.B., Zhan G.L., Wang Y.L., et al. Aqueous humor dynamics in monkeys with laser-induced glaucoma. J. Ocul. Pharmacol. Ther. 2000; 16 (1): 19–27. doi: 10.1089/jop.2000.16.19
45. 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 Feb; 19 (2): 126–36. PMID:6766124
46. Weber A.J., Zelenak D. Experimental glaucoma in the primate induced by latex microspheres. J. Neurosci. Methods. 2001; 111 (1): 39–48. doi: 10.1016/s0165-0270(01)00443-5
47. Burgoyne C.F. The non-human primate experimental glaucoma model. Exp. Eye Res. 2015; 141: 57–73. doi:10.1016/j.exer.2015.06.005
48. Borghi V., Bastia E., Guzzetta M., et al. A novel nitric oxide releasing prostaglandin analog, NCX 125, reduces intraocular pressure in rabbit, dog, and primate models of glaucoma. J. Ocul. Pharmacol. Ther. 2010; 26 (2): 125–32. doi: 10.1089/jop.2009.0120
49. Gelatt K.N., Gum G.G., Gwin R.M. Animal model of human disease. Primary open angle glaucoma. Inherited primary open angle glaucoma in the beagle. Am. J. Pathol. 1981 Feb; 102 (2): 292–5. PMID: 7468772
50. Kuchtey J., Olson L.M., Rinkoski T., et al. Mapping of the disease locus and identification of ADAMTS10 as a candidate gene in a canine model of primary open angle Glaucoma. PLoS Genet. 2011; 7 (2): e1001306. doi: 10.1371/journal.pgen.1001306
51. Hadoux J., Desterke C., Féraud O., et al. Transcriptional landscape of a RETC634Y-mutated iPSC and its CRISPR-corrected isogenic control reveals the putative role of EGR1 transcriptional program in the development of multiple endocrine neoplasia type 2A-associated cancers. Stem. Cell Res. 2018; 26: 8–16. doi: 10.1016/j.scr.2017.11.015
52. Sawaguchi K., Nakamura Y., Nakamura Y., et al. Myocilin gene expression in the trabecular meshwork of rats in a steroid-induced ocular hypertension model. Ophthalmol. Res. 2005; 37 (5): 235–42. doi: 10.1159/000086946.
53. Muldashev E.R., Kornilaeva G.G, Galimova V.U. Complicated glaucoma. Sankt-Peterburg: Izdatel'skiy dom “Neva”; 2005 (in Russian).
54. Volkov V.V. Pseudo-Normal Pressure Glaucoma: A guide for physicians. Moscow: Meditsina; 2001 (in Russian).
55. Levkovitch-Verbin H., Quigley H.A., Martin K.R.G., et al. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest. Ophthalmol. Vis. Sci. 2002 FEb; 43 (2): 402–10. PMID: 11818384
56. Shareef S.R., Garcia-Valenzuela E., Salierno A., et al. Chronic ocular hypertension following episcleral venous occlusion in rats. Exp. Eye Res. 1995; 61 (3): 379–82. doi: 10.1016/s0014-4835(05)80131-9
57. Yu S., Tanabe T., Yoshimura N. A rat model of glaucoma induced by episcleral vein ligation. Exp. Eye Res. 2006; 83 (4): 758–70. doi:10.1016/j.exer.2006.03.014
58. Moreno M.C., Aldana Marcos H.J., Croxatto J.O., et al. A new experimental model of glaucoma in rats through intracameral injections of hyaluronic acid. Exp. Eye Res. 2005; 81 (1): 71–80. doi: 10.1016/j.exer.2005.01.008
59. Daimon T., Kazama M., Miyajima Y., Nakano M. Immunocytochemical localization of thrombomodulin in the aqueous humor passage of the rat eye. Histochem. Cell Biol. 1997; 108 (2): 121–31. doi: 10.1007/s004180050153
60. Van Der Zypen E. Experimental morphological study on structure and function of the filtration angle of the rat eye. Ophthalmologica. 1977; 174 (5): 285–98. doi: 10.1159/000308617
61. Senatorov V., Malyukova I., Fariss R., et al. Expression of mutated mouse myocilin induces open-angle glaucoma in transgenic mice. J. Neurosci. 2006; 26 (46): 11903–14. doi: 10.1523/JNEUROSCI.3020-06.2006
62. Zhou Y., Grinchuk O., Tomarev S.I. Transgenic mice expressing the Tyr437His mutant of human myocilin protein develop glaucoma. Invest. Ophthalmol. Vis. Sci. 2008; 49 (5): 1932–9. doi: 10.1167/iovs.07-1339
63. Fingert J.H., Stone E.M., Sheffield V.C., Alward W.L.M. Myocilin glaucoma. Surv. Ophthalmol. 2002; 47 (6): 547–61. doi: 10.1016/s0039-6257(02)00353-3
64. Aihara M., Lindsey J.D., Weinreb R.N. Ocular hypertension in mice with a targeted type I collagen mutation. Invest. Ophthalmol. Vis. Sci. 2003; 44 (4): 1581–5. doi: 10.1167/iovs.02-0759
65. Mabuchi F., Lindsey J.D., Aihara M., et al. Optic nerve damage in mice with a targeted type I collagen mutation. Invest. Ophthalmol. Vis. Sci. 2004; 45 (6): 1841–5. doi: 10.1167/iovs.03-1008
66. Edward D.P., Bouhenni R. Anterior segment alterations and comparative aqueous humor proteomics in the buphthalmic rabbit (an American Ophthalmological Society thesis). Trans. Am. Ophthalmol. Soc. 2011; 109: 66–114.
67. Jones R., Rhee D.J. Corticosteroid-induced ocular hypertension and glaucoma: a brief review and update of the literature. Curr. Opin. Ophthalmol. 2006; 17 (2): 163–7. doi: 10.1097/01.icu.0000193079.55240.18
68. Kersey J.P., Broadway D.C. Corticosteroid-induced glaucoma: a review of the literature. Eye. 2006; 20 (4): 407–16. doi: 10.1038/sj.eye.6701895
69. Bonomi L., Perfetti S., Noya E. Experimental corticosteroid ocular hypertension in the rabbit. Albrecht Von Graefes Arch. Klin. Exp. Ophthalmol. 1978; 209 (2): 73–82. doi: 10.1007/BF00407840
70. Candia O.A., Gerometta R., Millar J.C., Podos S.M. Suppression of corticosteroid-induced ocular hypertension in sheep by anecortave. Arch. Ophthalmol. 2010; 128 (3): 338–43. doi: 10.1001/archophthalmol.2009.387
71. Gerometta R., Spiga M.G., Borrás T., Candia O.A. Treatment of sheep steroidinduced ocular hypertension with a glucocorticoid-inducible MMP1 gene therapy virus. Invest. Ophthalmol. Vis. Sci. 2010; 51 (6): 3042–8. doi: 10.1167/iovs.09-4920
72. Tektas O.Y., Hammer C.M., Danias J., et al. Morphologic changes in the outflow pathways of bovine eyes treated with corticosteroids. Invest. Ophthalmol. Vis. Sci. 2010; 51 (8): 4060–6. doi:10.1167/iovs.09-4742
73. Ticho U., Lahav M., Berkowitz S., Yoffe P. Ocular changes in rabbits with corticosteroid-induced ocular hypertension. Br. J. Ophthalmol. 1979; 63 (9): 646–50. doi:10.1136/bjo.63.9.646
74. Best M., Rabinovitz A.Z., Masket S. Experimental alphachymotrypsin glaucoma. Ann. Ophthalmol. 1975 Jun; 7 (6): 803–10. PMID: 1147507
75. Chee P., Hamasaki D.I. The basis for chymotrypsin-induced glaucoma. Arch. Ophthalmol. 1971; 85 (1): 103–6. doi:10.1001/archopht.1971.00990050105016
76. Lessell S., Kuwabara T. Experimental alpha-chymotrypsin glaucoma. Arch. Ophthalmol. 1969; 81 (6): 853–64. doi:10.1001/archopht.1969.00990010855019
77. Азнабаев Б.М., Азнабаев М.Т., Кригер Г.С., Соломатникова С.Р. Способ создания модели экспериментальной глаукомы. Патент РФ № 2164396. 1998; Бюллетень № 14. [Aznabaev B.M., Aznabaev M.T., Kriger G.S., Solomatnikova S.R. A method of creating a model of experimental glaucoma. Patent RF 2164396. 1998; Byulleten' № 14 (in Russian)].
78. Dumbrova N.E., Lipovetskaya E.M., Kopp O.P. Comparative ultrastructural characteristics of changes in the outflow paths of the anterior chamber angle of the eye in experimental glaucoma and transient hypertension. Oftal'mologicheskiy zhurnal. 1975; 7: 536–9 (in Russian).
79. Kryzhanovskiy G.N., Kashintseva L.T., Lipovetskaya E.M., Kopp O.P. Adrenergic mechanisms of glaucoma. Oftal'mologicheskiy zhurnal. 1983; 8: 494–7 (in Russian).
80. Mikheytseva I.N. Glaucoma models, advantages and disadvantages. Adrenaline-induced glaucoma as an adequate model of the human glaucoma process. Oftal'mologicheskiy zhurnal. 2011; 3: 89–92 (in Russian).
81. Mikheytseva I.N. The effectiveness of corvitin in the normalization of ocular blood supply and the dynamics of intraocular fluid in a model of glaucoma. Odes'kiy medichniy zhurnal. 2010; 3: 9–12 (in Russian).
82. Mikheytseva I.N., Mirnenko V.V., Shalar' T.I. Von Willebrand factor in experimental glaucoma and melatonin influence on its level. Problemy stareniya i dolgoletiya. 2012; 21 (3): 392–5 (in Russian).
83. Liao T.J., Bai C.X., Zhang L.Z. The effect of acute and persistent ocular hypertension on ultrastructure in rabbit tissues of anterior chamber angle. Zhonghua Yan Ke Za Zhi. 1994 Sep; 30 (5): 382–5 (in Chinese). PMID: 7805546
84. Alekseev V.N., Churilina N.Yu. Clinical and morphological changes of anterior segment of the eye ball in adrenalin induced glaucoma. RMZh. Klinicheskaya oftal'mologiya. 2007; 8 (3): 112–4 (in Russian).
85. Alekseev V.N., Samusenko I.A. Clinical-morphological changes in the anterior part of the eye at the experimental glaucoma. Glaucoma. 2004; 1: 3–7 (in Russian).
86. Ruiz-Ederra J., García M., Hicks D., Vecino E. Comparative study of the three neurofilament subunits within pig and human retinal ganglion cells. Mol. Vis. 2004 Feb; 10: 83–92. PMID:14961007
87. Richardson R., Tracey-White D., Webster A., Moosajee M. The zebrafish eye – A paradigm for investigating human ocular genetics. Eye. 2017; 31 (1): 68–86. doi: 10.1038/eye.2016.198
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Onufriichuk O.N., Gazizova I.R., Kuroyedov A.V., Seleznev А.V., Brezhnev A.Yu. Experimental Models of Glaucoma. Russian Ophthalmological Journal. 2021;14(4):164-171. (In Russ.) https://doi.org/10.21516/2072-0076-2021-14-4-164-171
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