1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Vision Science
  4. Volume 3, 2017
  5. Article

Annual Review of Vision Science

Volume 3, 2017

Neuroprotection in Glaucoma: Animal Models and Clinical Trials

Abstract

Glaucoma is a progressive neurodegenerative disease that frequently results in irreversible blindness. Glaucoma causes death of retinal ganglion cells (RGCs) and their axons in the optic nerve, resulting in visual field deficits and eventual loss of visual acuity. Glaucoma is a complex optic neuropathy, and a successful strategy for its treatment requires not only better management of known risk factors such as elevated intraocular pressure and the development of improved tools for detecting RGC injury but also treatments that address this injury (i.e., neuroprotection). Experimental models of glaucoma provide insight into the cellular and molecular mechanisms of glaucomatous optic neuropathy and aid the development of neuroprotective therapies.

Keyword(s): animal models, clinical trials, glaucoma, neurodegeneration, neuroprotection, optic nerve
Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-102016-061422
2017-09-15
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/vision/3/1/annurev-vision-102016-061422.html?itemId=/content/journals/10.1146/annurev-vision-102016-061422&mimeType=html&fmt=ahah

Literature Cited

  1. Agostinone J, Di Polo A. 2015. Retinal ganglion cell dendrite pathology and synapse loss: implications for glaucoma. Prog. Brain Res. 220:199–216 [Google Scholar]
  2. Aihara M, Lindsey JD, Weinreb RN. 2003. Experimental mouse ocular hypertension: establishment of the model. Investig. Ophthalmol. Vis. Sci. 44:4314–20 [Google Scholar]
  3. Akopian A, Kumar S, Ramakrishnan H, Viswanathan S, Bloomfield SA. 2016. Amacrine cells coupled to ganglion cells via gap junctions are highly vulnerable in glaucomatous mouse retinas. J. Comp. Neurol. In press
  4. Albers GW, Bogousslavsky J, Bozik MA, Brass LM, Broderick JP. et al. 2001. Recommendations for clinical trial evaluation of acute stroke therapies. Stroke 32:1598–606 [Google Scholar]
  5. Almasieh M, Lieven CJ, Levin LA, Di Polo A. 2011. 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. 118:1075–86 [Google Scholar]
  6. Almasieh M, Wilson AM, Morquette B, Cueva Vargas JL, Di Polo A. 2012. The molecular basis of retinal ganglion cell death in glaucoma. Prog. Retin. Eye Res. 31:152–81 [Google Scholar]
  7. Almasieh M, Zhou Y, Kelly ME, Casanova C, Di Polo A. 2010. Structural and functional neuroprotection in glaucoma: role of galantamine-mediated activation of muscarinic acetylcholine receptors. Cell Death Dis 1:e27 [Google Scholar]
  8. Bebarta V, Luyten D, Heard K. 2003. Emergency medicine animal research: Does use of randomization and blinding affect the results?. Acad. Emerg. Med. 10:684–87 [Google Scholar]
  9. Beirowski B, Babetto E, Coleman MP, Martin KR. 2008. The WldS gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur. J. Neurosci. 28:1166–79 [Google Scholar]
  10. Bernstein SL, Guo Y, Kelman SE, Flower RW, Johnson MA. 2003. Functional and cellular responses in a novel rodent model of anterior ischemic optic neuropathy. Investig. Ophthalmol. Vis. Sci. 44:4153–62 [Google Scholar]
  11. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–73 [Google Scholar]
  12. Binley KE, Ng WS, Barde Y-A, Song B, Morgan JE. 2016. Brain-derived neurotrophic factor prevents dendritic retraction of adult mouse retinal ganglion cells. Eur. J. Neurosci. 44:2028–39 [Google Scholar]
  13. Burgoyne C. 2015a. The morphological difference between glaucoma and other optic neuropathies. J. Neuro-Ophthalmol. 35:Suppl. 1S8–21 [Google Scholar]
  14. Burgoyne CF. 2015b. The non-human primate experimental glaucoma model. Exp. Eye Res. 141:57–73 [Google Scholar]
  15. Catrinescu MM, Chan W, Mahammed A, Gross Z, Levin LA. 2012. Superoxide signaling and cell death in retinal ganglion cell axotomy: effects of metallocorroles. Exp. Eye Res. 97:31–35 [Google Scholar]
  16. Cestari DM, Gaier ED, Bouzika P, Blachley TS, De Lott LB. et al. 2016. Demographic, systemic, and ocular factors associated with nonarteritic anterior ischemic optic neuropathy. Ophthalmology 123:2446–55 [Google Scholar]
  17. Chang DS, Xu L, Boland MV, Friedman DS. 2013. Accuracy of pupil assessment for the detection of glaucoma: a systematic review and meta-analysis. Ophthalmology 120:2217–25 [Google Scholar]
  18. Chang EE, Goldberg JL. 2012. Glaucoma 2.0: neuroprotection, neuroregeneration, neuroenhancement. Ophthalmology 119:979–86 [Google Scholar]
  19. Chen H, Wei X, Cho K-S, Chen G, Sappington R. et al. 2011. Optic neuropathy due to microbead-induced elevated intraocular pressure in the mouse. Investig. Ophthalmol. Vis. Sci. 52:36–44 [Google Scholar]
  20. Chen Y-S, Green CR, Danesh-Meyer HV, Rupenthal ID. 2015. Neuroprotection in the treatment of glaucoma—a focus on connexin43 gap junction channel blockers. Eur. J. Pharm. Biopharm. 95:182–93 [Google Scholar]
  21. Chhetri J, Jacobson G, Gueven N. 2014. Zebrafish—on the move towards ophthalmological research. Eye 28:367–80 [Google Scholar]
  22. Cioffi GA. 2005. Ischemic model of optic nerve injury. Trans. Am. Ophthalmol. Soc. 103:592–613 [Google Scholar]
  23. Cordeiro MF, Guo L, Coxon KM, Duggan J, Nizari S. et al. 2010. Imaging multiple phases of neurodegeneration: a novel approach to assessing cell death in vivo. Cell Death Dis 1:e3 [Google Scholar]
  24. Cordeiro MF, Levin LA. 2011. Clinical evidence for neuroprotection in glaucoma. Am. J. Ophthalmol. 152:715–16 [Google Scholar]
  25. Cordeiro MF, Normando EM, Cardoso MJ, Miodragovic S, Jeylani S. et al. 2017. Real-time imaging of single neuronal cell apoptosis in patients with glaucoma. Brain 140:1757–67 [Google Scholar]
  26. Crish SD, Calkins DJ. 2015. Central visual pathways in glaucoma: evidence for distal mechanisms of neuronal self-repair. J. Neuro-Ophthalmol. 35:Suppl. 1S29–37 [Google Scholar]
  27. Crowston JG, Fahy ET, Fry L, Trounce IA, van Wijngaarden P. et al. 2017. Targeting retinal ganglion cell recovery. Eye 31:196–98 [Google Scholar]
  28. Cueva Vargas JL, Belforte N, Di Polo A. 2016. The glial cell modulator ibudilast attenuates neuroinflammation and enhances retinal ganglion cell viability in glaucoma through protein kinase A signaling. Neurobiol. Dis. 93:156–71 [Google Scholar]
  29. Danesh-Meyer HV. 2011. Neuroprotection in glaucoma: recent and future directions. Curr. Opin. Ophthalmol. 22:78–86 [Google Scholar]
  30. Danesh-Meyer HV, Levin LA. 2009. Neuroprotection: extrapolating from neurologic diseases to the eye. Am. J. Ophthalmol. 148:186–91 [Google Scholar]
  31. Danesh-Meyer HV, Levin LA. 2015. Glaucoma as a neurodegenerative disease. J. Neuro-Ophthalmol. 35:S22–28 [Google Scholar]
  32. Davis C-HO, Kim K-Y, Bushong EA, Mills EA, Boassa D. et al. 2014. Transcellular degradation of axonal mitochondria. PNAS 111:9633–38 [Google Scholar]
  33. De Moraes CG, Liebmann JM, Levin LA. 2017. Detection and measurement of clinically meaningful visual field progression in clinical trials for glaucoma. Prog. Retin. Eye Res. 56:107–47 [Google Scholar]
  34. Dekeyster E, Geeraerts E, Buyens T, Van den Haute C, Baekelandt V. et al. 2015. Tackling glaucoma from within the brain: an unfortunate interplay of BDNF and TrkB. PLOS ONE 10:e0142067 [Google Scholar]
  35. Della Santina L, Ou Y. 2017. Who's lost first? Susceptibility of retinal ganglion cell types in experimental glaucoma. Exp. Eye Res. 158:43–50 [Google Scholar]
  36. Dowling J. 2011. Astrocytes and glaucomatous neurodegeneration Lasker/IRRF Initiative for Innovation in Vision Science New York:
  37. Ergorul C, Levin LA. 2013. Solving the lost in translation problem: improving the effectiveness of translational research. Curr. Opin. Pharmacol. 13:108–14 [Google Scholar]
  38. Feng L, Zhao Y, Yoshida M, Chen H, Yang JF. et al. 2013. Sustained ocular hypertension induces dendritic degeneration of mouse retinal ganglion cells that depends on cell type and location. Investig. Ophthalmol. Vis. Sci. 54:1106–17 [Google Scholar]
  39. Feuerstein GZ, Zaleska MM, Krams M, Wang X, Day M. et al. 2008. Missing steps in the STAIR case: a Translational Medicine perspective on the development of NXY-059 for treatment of acute ischemic stroke. J. Cereb. Blood Flow Metab. 28:217–19 [Google Scholar]
  40. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA. et al. 2009. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40:2244–50 [Google Scholar]
  41. Fisher M, Hanley DF, Howard G, Jauch EC, Warach S. 2007. Recommendations from the STAIR V meeting on acute stroke trials, technology and outcomes. Stroke 38:245–48 [Google Scholar]
  42. Fortune B, Reynaud J, Hardin C, Wang L, Sigal IA, Burgoyne CF. 2016. Experimental glaucoma causes optic nerve head neural rim tissue compression: a potentially important mechanism of axon injury. Investig. Ophthalmol. Vis. Sci. 57:4403–11 [Google Scholar]
  43. Foxton RH, Finkelstein A, Vijay S, Dahlmann-Noor A, Khaw PT. et al. 2013. VEGF-A is necessary and sufficient for retinal neuroprotection in models of experimental glaucoma. Am. J. Pathol. 182:1379–90 [Google Scholar]
  44. Galassi F, Masini E, Giambene B, Fabrizi F, Uliva C. et al. 2006. A topical nitric oxide-releasing dexamethasone derivative: effects on intraocular pressure and ocular haemodynamics in a rabbit glaucoma model. Br. J. Ophthalmol. 90:1414–19 [Google Scholar]
  45. Gardiner SK, Demirel S, Goren D, Mansberger SL, Swanson WH. 2015. The effect of stimulus size on the reliable stimulus range of perimetry. Transl. Vis. Sci. Technol. 4:10 [Google Scholar]
  46. Gardiner SK, Mansberger SL. 2016. Effect of restricting perimetry testing algorithms to reliable sensitivities on test-retest variability. Investig. Ophthalmol. Vis. Sci. 57:5631–36 [Google Scholar]
  47. Garway-Heath DF, Crabb DP, Bunce C, Lascaratos G, Amalfitano F. et al. 2015. Latanoprost for open-angle glaucoma (UKGTS): a randomised, multicentre, placebo-controlled trial. Lancet 385:1295–304 [Google Scholar]
  48. Garway-Heath DF, Lascaratos G, Bunce C, Crabb DP, Russell RA, Shah A. 2013. The United Kingdom Glaucoma Treatment Study: a multicenter, randomized, placebo-controlled clinical trial: design and methodology. Ophthalmology 120:68–76 [Google Scholar]
  49. Gelatt KN, MacKay EO. 2004. Prevalence of the breed-related glaucomas in pure-bred dogs in North America. Vet. Ophthalmol. 7:97–111 [Google Scholar]
  50. Ghaffarieh A, Levin LA. 2012. Optic nerve disease and axon pathophysiology. Int. Rev. Neurobiol. 105:1–17 [Google Scholar]
  51. Gramlich OW, Beck S, von Thun Und Hohenstein-Blaul N, Boehm N, Ziegler A. et al. 2013a. Enhanced insight into the autoimmune component of glaucoma: IgG autoantibody accumulation and pro-inflammatory conditions in human glaucomatous retina. PLOS ONE 8:e57557 [Google Scholar]
  52. Gramlich OW, Bell K, von Thun Und Hohenstein-Blaul N, Wilding C, Beck S. et al. 2013b. Autoimmune biomarkers in glaucoma patients. Curr. Opin. Pharmacol. 13:90–97 [Google Scholar]
  53. Grozdanic SD, Kecova H, Harper MM, Nilaweera W, Kuehn MH, Kardon RH. 2010. Functional and structural changes in a canine model of hereditary primary angle-closure glaucoma. Investig. Ophthalmol. Vis. Sci. 51:255–63 [Google Scholar]
  54. Guo L, Moss SE, Alexander RA, Ali RR, Fitzke FW, Cordeiro MF. 2005. Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Investig. Ophthalmol. Vis. Sci. 46:175–82 [Google Scholar]
  55. Hare WA, WoldeMussie E, Lai RK, Ton H, Ruiz G. et al. 2004a. Efficacy and safety of memantine treatment for reduction of changes associated with experimental glaucoma in monkey, I: functional measures. Investig. Ophthalmol. Vis. Sci. 45:2625–39 [Google Scholar]
  56. Hare WA, WoldeMussie E, Weinreb RN, Ton H, Ruiz G. et al. 2004b. Efficacy and safety of memantine treatment for reduction of changes associated with experimental glaucoma in monkey, II: structural measures. Investig. Ophthalmol. Vis. Sci. 45:2640–51 [Google Scholar]
  57. Harwerth RS, Carter-Dawson L, Shen F, Smith ELR, Crawford ML. 1999. Ganglion cell losses underlying visual field defects from experimental glaucoma. Investig. Ophthalmol. Vis. Sci. 40:2242–50 [Google Scholar]
  58. Hattenhauer MG, Johnson DH, Ing HH, Herman DC, Hodge DO. et al. 1998. The probability of blindness from open-angle glaucoma. Ophthalmology 105:2099–104 [Google Scholar]
  59. Heijl A, Leske MC, Bengtsson B, Hyman L, Hussein M. 2002. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch. Ophthalmol. 120:1268–79 [Google Scholar]
  60. Hill MD. 2007. Stroke: the dashed hopes of neuroprotection. Lancet Neurol 6:2–3 [Google Scholar]
  61. Hood DC, Raza AS, de Moraes CG, Odel JG, Greenstein VC. et al. 2011. Initial arcuate defects within the central 10 degrees in glaucoma. Investig. Ophthalmol. Vis. Sci. 52:940–46 [Google Scholar]
  62. Hou H, Wang C, Nan K, Freeman WR, Sailor MJ, Cheng L. 2016. Controlled release of dexamethasone from an intravitreal delivery system using porous silicon dioxide. Investig. Ophthalmol. Vis. Sci. 57:557–66 [Google Scholar]
  63. Howell GR, Libby RT, Jakobs TC, Smith RS, Phalan FC. et al. 2007. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 179:1523–37 [Google Scholar]
  64. Howell GR, Soto I, Libby RT, John SW. 2013. Intrinsic axonal degeneration pathways are critical for glaucomatous damage. Exp. Neurol. 246:54–61 [Google Scholar]
  65. Jakobs TC, Libby RT, Ben Y, John SW, Masland RH. 2005. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 171:313–25 [Google Scholar]
  66. Jia L, Cepurna WO, Johnson EC, Morrison JC. 2000. Effect of general anesthetics on IOP in rats with experimental aqueous outflow obstruction. Investig. Ophthalmol. Vis. Sci. 41:3415–19 [Google Scholar]
  67. John SW, Smith RS, Savinova OV, Hawes NL, Chang B. et al. 1998. Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Investig. Ophthalmol. Vis. Sci. 39:951–62 [Google Scholar]
  68. Johnson EC, Deppmeier LMH, Wentzien SKF, Hsu I, Morrison JC. 2000. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Investig. Ophthalmol. Vis. Sci. 41:431–42 [Google Scholar]
  69. Johnson EC, Morrison JC, Farrell S, Deppmeier L, Moore CG, McGinty MR. 1996. The effect of chronically elevated intraocular pressure on the rat optic nerve head extracellular matrix. Exp. Eye Res. 62:663–74 [Google Scholar]
  70. Ju W-K, Kim K-Y, Noh Y-H, Hoshijima M, Lukas TJ. et al. 2015. Increased mitochondrial fission and volume density by blocking glutamate excitotoxicity protect glaucomatous optic nerve head astrocytes. Glia 63:736–53 [Google Scholar]
  71. Kaja S, Payne AJ, Naumchuk Y, Levy D, Zaidi DH. et al. 2015. Plate reader-based cell viability assays for glioprotection using primary rat optic nerve head astrocytes. Exp. Eye Res. 138:159–66 [Google Scholar]
  72. Kanamori A, Catrinescu MM, Belisle JM, Costantino S, Levin LA. 2012. Retrograde and Wallerian axonal degeneration occur synchronously after retinal ganglion cell axotomy. Am. J. Pathol. 181:62–73 [Google Scholar]
  73. Kanamori A, Catrinescu MM, Kanamori N, Mears KA, Beaubien R, Levin LA. 2010a. Superoxide is an associated signal for apoptosis in axonal injury. Brain 133:2612–25 [Google Scholar]
  74. Kanamori A, Catrinescu MM, Traistaru M, Beaubien R, Levin LA. 2010b. In vivo imaging of retinal ganglion cell axons within the nerve fiber layer. Investig. Ophthalmol. Vis. Sci. 51:2011–18 [Google Scholar]
  75. Kardon RH, Kirkali PA, Thompson HS. 1991. Automated pupil perimetry. Pupil field mapping in patients and normal subjects. Ophthalmology 98:485–95 [Google Scholar]
  76. Kass MA, Heuer DK, Higginbotham EJ, Johnson CA, Keltner JL. et al. 2002. 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. 120:701–13 [Google Scholar]
  77. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. 2010. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLOS Biol 8:e1000412 [Google Scholar]
  78. Kimura A, Namekata K, Guo X, Harada C, Harada T. 2017. Dock3-NMDA receptor interaction as a target for glaucoma therapy. Histol. Histopathol. 32:215–21 [Google Scholar]
  79. Klopstock T, Metz G, Yu-Wai-Man P, Buchner B, Gallenmuller C. et al. 2013. Persistence of the treatment effect of idebenone in Leber's hereditary optic neuropathy. Brain 136:e230 [Google Scholar]
  80. Klopstock T, Yu-Wai-Man P, Dimitriadis K, Rouleau J, Heck S. et al. 2011. A randomized placebo-controlled trial of idebenone in Leber's hereditary optic neuropathy. Brain 134:2677–86 [Google Scholar]
  81. Kompella UB, Kadam RS, Lee VH. 2010. Recent advances in ophthalmic drug delivery. Ther. Deliv. 1:435–56 [Google Scholar]
  82. Krupin T, Liebmann JM, Greenfield DS, Ritch R, Gardiner S. 2011. A randomized trial of brimonidine versus timolol in preserving visual function: results from the Low-Pressure Glaucoma Treatment Study. Am. J. Ophthalmol. 151:671–81 [Google Scholar]
  83. Kuehn MH, Fingert JH, Kwon YH. 2005. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol. Clin. North Am. 18:383–95 [Google Scholar]
  84. Lebrun-Julien F, Duplan L, Pernet V, Osswald I, Sapieha P. et al. 2009. Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism. J. Neurosci. 29:5536–45 [Google Scholar]
  85. Lee J-W, Morales E, Sharifipour F, Amini N, Yu F. et al. 2017. The relationship between central visual field sensitivity and macular ganglion cell/inner plexiform layer thickness in glaucoma. Br. J. Ophthalmol. 101:1052–58 [Google Scholar]
  86. Lee MS, Grossman D, Arnold AC, Sloan FA. 2011. Incidence of nonarteritic anterior ischemic optic neuropathy: increased risk among diabetic patients. Ophthalmology 118:959–63 [Google Scholar]
  87. Levin LA. 2001. Animal and culture models of glaucoma for studying neuroprotection. Eur. J. Ophthalmol. 11:Suppl. 2S23–29 [Google Scholar]
  88. Levin LA. 2005. Neuroprotection and regeneration in glaucoma. Ophthalmol. Clin. North Am. 18:585–96 [Google Scholar]
  89. Levin LA. 2016. Translational pharmacology in glaucoma neuroprotection. Handbook of Experimental Pharmacology1–22 Berlin: Springer Berlin Heidelberg [Google Scholar]
  90. Levin LA, Danesh-Meyer HV. 2010. Lost in translation: bumps in the road between bench and bedside. JAMA 303:1533–34 [Google Scholar]
  91. Levin LA, Peeples P. 2008. History of neuroprotection and rationale as a therapy for glaucoma. Am. J. Manag. Care 14:S11–14 [Google Scholar]
  92. Levkovitch-Verbin H, Quigley HA, Martin KR, Valenta D, Baumrind LA, Pease ME. 2002. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Investig. Ophthalmol. Vis. Sci. 43:402–10 [Google Scholar]
  93. Liao HW, Ren X, Peterson BB, Marshak DW, Yau KW. et al. 2016. Melanopsin-expressing ganglion cells on macaque and human retinas form two morphologically distinct populations. J. Comp. Neurol. 524:2845–72 [Google Scholar]
  94. Lieven CJ, Hoegger MJ, Schlieve CR, Levin LA. 2006. Retinal ganglion cell axotomy induces an increase in intracellular superoxide anion. Investig. Ophthalmol. Vis. Sci. 47:1477–85 [Google Scholar]
  95. Lorber B, Tassoni A, Bull ND, Moschos MM, Martin KR. 2012. Retinal ganglion cell survival and axon regeneration in WldS transgenic rats after optic nerve crush and lens injury. BMC Neurosci 13:56 [Google Scholar]
  96. Mabuchi F, Aihara M, Mackey MR, Lindsey JD, Weinreb RN. 2003. Optic nerve damage in experimental mouse ocular hypertension. Investig. Ophthalmol. Vis. Sci. 44:4321–30 [Google Scholar]
  97. Maddess T, Essex RW, Kolic M, Carle CF, James AC. 2013. High- versus low-density multifocal pupillographic objective perimetry in glaucoma. Clin. Exp. Ophthalmol. 41:140–47 [Google Scholar]
  98. Makadia HK, Siegel SJ. 2011. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3:1377–97 [Google Scholar]
  99. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266–80 [Google Scholar]
  100. May CA, Lutjen-Drecoll E. 2002. Morphology of the murine optic nerve. Investig. Ophthalmol. Vis. Sci. 43:2206–12 [Google Scholar]
  101. McLellan GJ, Miller PE. 2011. Feline glaucoma—a comprehensive review. Vet. Ophthalmol. 14:Suppl. 115–29 [Google Scholar]
  102. Merani R, Hunyor AP. 2015. Endophthalmitis following intravitreal anti-vascular endothelial growth factor (VEGF) injection: a comprehensive review. Int. J. Retina Vitreous 1:9 [Google Scholar]
  103. Mishra GP, Bagui M, Tamboli V, Mitra AK. 2011. Recent applications of liposomes in ophthalmic drug delivery. J. Drug. Deliv 2011:863734 [Google Scholar]
  104. Moore CG, Johnson EC, Morrison JC. 1996. Circadian rhythm of intraocular pressure in the rat. Curr. Eye Res. 15:185–91 [Google Scholar]
  105. Morquette JB, Di Polo A. 2008. Dendritic and synaptic protection: is it enough to save the retinal ganglion cell body and axon?. J. Neuro-Ophthalmol. 28:144–54 [Google Scholar]
  106. Morrison JC, Jia L, Cepurna W, Guo Y, Johnson E. 2009. Reliability and sensitivity of the TonoLab rebound tonometer in awake Brown Norway rats. Investig. Ophthalmol. Vis. Sci. 50:2802–8 [Google Scholar]
  107. Morrison JC, Johnson EC, Cepurna W, Jia L. 2005. Understanding mechanisms of pressure-induced optic nerve damage. Prog. Retin. Eye Res. 24:217–40 [Google Scholar]
  108. Morrison JC, Moore CG, Deppmeier LM, Gold BG, Meshul CK, Johnson EC. 1997. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 64:85–96 [Google Scholar]
  109. Mozaffarieh M, Grieshaber MC, Flammer J. 2008. Oxygen and blood flow: players in the pathogenesis of glaucoma. Mol. Vis. 14:224–33 [Google Scholar]
  110. Nadal-Nicolás FM, Sobrado-Calvo P, Jiménez-López M, Vidal-Sanz M, Agudo-Barriuso M. 2015. Long-term effect of optic nerve axotomy on the retinal ganglion cell layer. Investig. Ophthalmol. Vis. Sci. 56:6095–112 [Google Scholar]
  111. Neufeld AH, Sawada A, Becker B. 1999. Inhibition of nitric-oxide synthase 2 by aminoguanidine provides neuroprotection of retinal ganglion cells in a rat model of chronic glaucoma. PNAS 96:9944–48 [Google Scholar]
  112. Newman NJ, Biousse V, David R, Bhatti MT, Hamilton SR. et al. 2005. Prophylaxis for second eye involvement in Leber hereditary optic neuropathy: an open-labeled, nonrandomized multicenter trial of topical brimonidine purite. Am. J. Ophthalmol. 140:407–15 [Google Scholar]
  113. Nguyen JV, Soto I, Kim K-Y, Bushong EA, Oglesby E. et al. 2011. Myelination transition zone astrocytes are constitutively phagocytic and have synuclein dependent reactivity in glaucoma. PNAS 108:1176–81 [Google Scholar]
  114. Nickells RW, Howell GR, Soto I, John SWM. 2012. Under pressure: cellular and molecular responses during glaucoma, a common neurodegeneration with axonopathy. Annu. Rev. Neurosci. 35:153–79 [Google Scholar]
  115. Oliver JE, Hattenhauer MG, Herman D, Hodge DO, Kennedy R. et al. 2002. Blindness and glaucoma: a comparison of patients progressing to blindness from glaucoma with patients maintaining vision. Am. J. Ophthalmol. 133:764–72 [Google Scholar]
  116. Ou Y, Jo RE, Ullian EM, Wong ROL, Della Santina L. 2016. Selective vulnerability of specific retinal ganglion cell types and synapses after transient ocular hypertension. J. Neurosci. 36:9240–52 [Google Scholar]
  117. Pang I-H, Johnson EC, Jia L, Cepurna WO, Shepard AR. et al. 2005. Evaluation of inducible nitric oxide synthase in glaucomatous optic neuropathy and pressure-induced optic nerve damage. Investig. Ophthalmol. Vis. Sci. 46:1313–21 [Google Scholar]
  118. Paula JS, O'Brien C, Stamer WD. 2016. Life under pressure: the role of ocular cribriform cells in preventing glaucoma. Exp. Eye Res. 151:150–59 [Google Scholar]
  119. Pease ME, Cone FE, Gelman S, Son JL, Quigley HA. 2011. Calibration of the TonoLab tonometer in mice with spontaneous or experimental glaucoma. Investig. Ophthalmol. Vis. Sci. 52:858–64 [Google Scholar]
  120. Perel P, Roberts I, Sena E, Wheble P, Briscoe C. et al. 2007. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 334:197 [Google Scholar]
  121. Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I. 2004. Where is the evidence that animal research benefits humans?. BMJ 328:514–17 [Google Scholar]
  122. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. 2000. A novel human opsin in the inner retina. J. Neurosci. 20:600–5 [Google Scholar]
  123. Quigley HA. 2005. Glaucoma: macrocosm to microcosm the Friedenwald lecture. Investig. Ophthalmol. Vis. Sci. 46:2662–70 [Google Scholar]
  124. Quigley HA. 2012. Clinical trials for glaucoma neuroprotection are not impossible. Curr. Opin. Ophthalmol. 23:144–54 [Google Scholar]
  125. Raghava S, Hammond M, Kompella UB. 2004. Periocular routes for retinal drug delivery. Expert Opin. Drug Deliv. 1:99–114 [Google Scholar]
  126. Rathod LV, Kapadia R, Sawant KK. 2017. A novel nanoparticles impregnated ocular insert for enhanced bioavailability to posterior segment of eye: in vitro, in vivo and stability studies. Mater. Sci. Eng. C 71:529–40 [Google Scholar]
  127. Reinstein S, Rankin A, Allbaugh R. 2009. Canine glaucoma: pathophysiology and diagnosis. Compendium 31:450–52 [Google Scholar]
  128. Roberts I, Yates D, Sandercock P, Farrell B, Wasserberg J. et al. 2004. Effect of intravenous corticosteroids on death within 14 days in 10,008 adults with clinically significant head injury (MRC CRASH trial): randomised placebo-controlled trial. Lancet 364:1321–28 [Google Scholar]
  129. Rogers R, Dharsee M, Ackloo S, Flanagan JG. 2012. Proteomics analyses of activated human optic nerve head lamina cribrosa cells following biomechanical strain. Investig. Ophthalmol. Vis. Sci. 53:3806–16 [Google Scholar]
  130. Rossi EA, Granger CE, Sharma R, Yang Q, Saito K. et al. 2017. Imaging individual neurons in the retinal ganglion cell layer of the living eye. PNAS 114:586–91 [Google Scholar]
  131. Ruiz-Ederra J, García M, Hernández M, Urcola H, Hernández-Barbáchano E. et al. 2005. The pig eye as a novel model of glaucoma. Exp. Eye Res. 81:561–69 [Google Scholar]
  132. Russo R, Varano GP, Adornetto A, Nucci C, Corasaniti MT. et al. 2016. Retinal ganglion cell death in glaucoma: exploring the role of neuroinflammation. Eur. J. Pharmacol. 787:134–42 [Google Scholar]
  133. Salt TE, Nizari S, Cordeiro MF, Russ H, Danysz W. 2014. Effect of the Aβ aggregation modulator MRZ-99030 on retinal damage in an animal model of glaucoma. Neurotox. Res 26:440–46 [Google Scholar]
  134. Samsel PA, Kisiswa L, Erichsen JT, Cross SD, Morgan JE. 2011. A novel method for the induction of experimental glaucoma using magnetic microspheres. Investig. Ophthalmol. Vis. Sci. 52:1671–75 [Google Scholar]
  135. Sanes JR, Masland RH. 2015. The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38:221–46 [Google Scholar]
  136. Sappington RM, Carlson BJ, Crish SD, Calkins DJ. 2010. The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Investig. Ophthalmol. Vis. Sci. 51:207–16 [Google Scholar]
  137. Savitz SI. 2007. A critical appraisal of the NXY-059 neuroprotection studies for acute stroke: a need for more rigorous testing of neuroprotective agents in animal models of stroke. Exp. Neurol. 205:20–25 [Google Scholar]
  138. Schultz CL, Poling TR, Mint JO. 2009. A medical device/drug delivery system for treatment of glaucoma. Clin. Exp. Optom. 92:343–48 [Google Scholar]
  139. Semba K, Namekata K, Guo X, Harada C, Harada T, Mitamura Y. 2014. Renin-angiotensin system regulates neurodegeneration in a mouse model of normal tension glaucoma. Cell Death Dis 5:e1333 [Google Scholar]
  140. Shareef SR, Garcia-Valenzuela E, Salierno A, Walsh J, Sharma SC. 1995. Chronic ocular hypertension following episcleral venous occlusion in rats. Exp. Eye Res. 61:379–82 [Google Scholar]
  141. Shimazawa M, Nakamura S, Miwa M, Tsuruma K, Aihara M. et al. 2013. Establishment of the ocular hypertension model using the common marmoset. Exp. Eye Res. 111:1–8 [Google Scholar]
  142. Shindler KS, Ventura E, Dutt M, Rostami A. 2008. Inflammatory demyelination induces axonal injury and retinal ganglion cell apoptosis in experimental optic neuritis. Exp. Eye Res. 87:208–13 [Google Scholar]
  143. Shou T, Liu J, Wang W, Zhou Y, Zhao K. 2003. Differential dendritic shrinkage of α and β retinal ganglion cells in cats with chronic glaucoma. Investig. Ophthalmol. Vis. Sci. 44:3005–10 [Google Scholar]
  144. Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJ. et al. 2006. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. PNAS 103:3896–901 [Google Scholar]
  145. Sleath B, Blalock S, Covert D, Stone JL, Skinner AC. et al. 2011. The relationship between glaucoma medication adherence, eye drop technique, and visual field defect severity. Ophthalmology 118:2398–402 [Google Scholar]
  146. Snow CP. 1959. The Two Cultures and the Scientific Revolution New York: Cambridge Univ. Press
  147. Song S-K, Sun S-W, Ju W-K, Lin S-J, Cross AH, Neufeld AH. 2003. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 20:1714–22 [Google Scholar]
  148. Stankowska DL, Minton AZ, Rutledge MA, Mueller BH II, Phatak NR. et al. 2015. Neuroprotective effects of transcription factor Brn3b in an ocular hypertension rat model of glaucoma. Investig. Ophthalmol. Vis. Sci. 56:893–907 [Google Scholar]
  149. Stone J. 2013. Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision New York: Springer Sci. Bus. Media
  150. Sucher NJ, Lipton SA, Dreyer EB. 1997. Molecular basis of glutamate toxicity in retinal ganglion cells. Vis. Res. 37:3483–93 [Google Scholar]
  151. Tezel G, Wax MB. 2004. The immune system and glaucoma. Curr. Opin. Ophthalmol. 15:80–84 [Google Scholar]
  152. Thanos CG, Bell WJ, O'Rourke P, Kauper K, Sherman S. et al. 2004. Sustained secretion of ciliary neurotrophic factor to the vitreous, using the encapsulated cell therapy-based NT-501 intraocular device. Tissue Eng 10:1617–22 [Google Scholar]
  153. Tovar-Vidales T, Wordinger RJ, Clark AF. 2016. Identification and localization of lamina cribrosa cells in the human optic nerve head. Exp. Eye Res. 147:94–97 [Google Scholar]
  154. Tsuda S, Tanaka Y, Kunikata H, Yokoyama Y, Yasuda M. et al. 2016. Real-time imaging of RGC death with a cell-impermeable nucleic acid dyeing compound after optic nerve crush in a murine model. Exp. Eye Res. 146:179–88 [Google Scholar]
  155. Urcola JH, Hernández M, Vecino E. 2006. Three experimental glaucoma models in rats: comparison of the effects of intraocular pressure elevation on retinal ganglion cell size and death. Exp. Eye Res. 83:429–37 [Google Scholar]
  156. Valiente-Soriano FJ, Nadal-Nicolás FM, Salinas-Navarro M, Jiménez-López M, Bernal-Garro JM. et al. 2015. BDNF rescues RGCs but not intrinsically photosensitive RGCs in ocular hypertensive albino rat retinas. Investig. Ophthalmol. Vis. Sci. 56:1924–36 [Google Scholar]
  157. Van de Velde S, De Groef L, Stalmans I, Moons L, Van Hove I. 2015. Towards axonal regeneration and neuroprotection in glaucoma: Rho kinase inhibitors as promising therapeutics. Prog. Neurobiol. 131:105–19 [Google Scholar]
  158. Vecino E, Rodriguez FD, Ruzafa N, Pereiro X, Sharma SC. 2016. Glia–neuron interactions in the mammalian retina. Prog. Retin. Eye Res. 51:1–40 [Google Scholar]
  159. Vidal-Sanz M, Nadal-Nicolás FM, Valiente-Soriano FJ, Agudo-Barriuso M, Villegas-Pérez MP. 2015. Identifying specific RGC types may shed light on their idiosyncratic responses to neuroprotection. Neural Regen. Res. 10:1228–30 [Google Scholar]
  160. Von Thun Und Hohenstein-Blaul N, Bell K, Pfeiffer N, Grus FH. 2016. Autoimmune aspects in glaucoma. Eur. J. Pharmacol. 787:105–18 [Google Scholar]
  161. Vrabec JP, Levin LA. 2007. The neurobiology of cell death in glaucoma. Eye 21:Suppl. 1S11–14 [Google Scholar]
  162. Wakakura M, Yokoe J. 1995. Evidence for preserved direct pupillary light response in Leber's hereditary optic neuropathy. Br. J. Ophthalmol. 79:442–46 [Google Scholar]
  163. Wall M, Kutzko KE, Chauhan BC. 1997. Variability in patients with glaucomatous visual field damage is reduced using size V stimuli. Investig. Ophthalmol. Vis. Sci. 38:426–35 [Google Scholar]
  164. Wall M, McDermott MP, Kieburtz KD, Corbett JJ, Feldon SE. et al. 2014. Effect of acetazolamide on visual function in patients with idiopathic intracranial hypertension and mild visual loss: the idiopathic intracranial hypertension treatment trial. JAMA 311:1641–51 [Google Scholar]
  165. Wallace DM, O'Brien CJ. 2016. The role of lamina cribrosa cells in optic nerve head fibrosis in glaucoma. Exp. Eye Res. 142:102–9 [Google Scholar]
  166. Wang DL, Raza AS, de Moraes CG, Chen M, Alhadeff P. et al. 2015. Central glaucomatous damage of the macula can be overlooked by conventional OCT retinal nerve fiber layer thickness analyses. Transl. Vis. Sci. Technol. 4:4 [Google Scholar]
  167. Wang N, Zhang Y, Wu L, Wang Y, Cao Y. et al. 2014. Puerarin protected the brain from cerebral ischemia injury via astrocyte apoptosis inhibition. Neuropharmacology 79:282–89 [Google Scholar]
  168. Wang RF, Schumer RA, Serle JB, Podos SM. 1998. A comparison of argon laser and diode laser photocoagulation of the trabecular meshwork to produce the glaucoma monkey model. J. Glaucoma 7:45–49 [Google Scholar]
  169. Wässle H. 2004. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5:747–57 [Google Scholar]
  170. Wax MB, Tezel G. 2009. Immunoregulation of retinal ganglion cell fate in glaucoma. Exp. Eye Res. 88:825–30 [Google Scholar]
  171. Weber AJ, Zelenak D. 2001. Experimental glaucoma in the primate induced by latex microspheres. J. Neurosci. Methods 111:39–48 [Google Scholar]
  172. Wheeler LA, WoldeMussie E. 2001. Alpha-2 adrenergic receptor agonists are neuroprotective in experimental models of glaucoma. Eur. J. Ophthalmol. 11:Suppl. 2S30–35 [Google Scholar]
  173. White AJR, Heller JP, Leung J, Tassoni A, Martin KR. 2015. Retinal ganglion cell neuroprotection by an angiotensin II blocker in an ex vivo retinal explant model. J. Renin-Angiotensin-Aldosterone Syst. 16:1193–201 [Google Scholar]
  174. Williams PA, Howell GR, Barbay JM, Braine CE, Sousa GL. et al. 2013. Retinal ganglion cell dendritic atrophy in DBA/2J glaucoma. PLOS ONE 8:e72282 [Google Scholar]
  175. Williams PA, Tribble JR, Pepper KW, Cross SD, Morgan BP. et al. 2016. Inhibition of the classical pathway of the complement cascade prevents early dendritic and synaptic degeneration in glaucoma. Mol. Neurodegener. 11:26 [Google Scholar]
  176. WoldeMussie E, Ruiz G, Wijono M, Wheeler LA. 2001. Neuroprotection of retinal ganglion cells by brimonidine in rats with laser-induced chronic ocular hypertension. Investig. Ophthalmol. Vis. Sci. 42:2849–55 [Google Scholar]
  177. WoldeMussie E, Yoles E, Schwartz M, Ruiz G, Wheeler LA. 2002. Neuroprotective effect of memantine in different retinal injury models in rats. J. Glaucoma 11:474–80 [Google Scholar]
  178. Yoles E, Wheeler LA, Schwartz M. 1999. α2-Adrenoreceptor agonists are neuroprotective in a rat model of optic nerve degeneration. Investig. Ophthalmol. Vis. Sci. 40:65–73 [Google Scholar]
  179. Yücel YH, Gupta N, Zhang Q, Mizisin AP, Kalichman MW, Weinreb RN. 2006. Memantine protects neurons from shrinkage in the lateral geniculate nucleus in experimental glaucoma. Arch. Ophthalmol. 124:217–25 [Google Scholar]
  180. Zhao L, Chen G, Li J, Fu Y, Mavlyutov TA. et al. 2017. An intraocular drug delivery system using targeted nanocarriers attenuates retinal ganglion cell degeneration. J. Control. Release 247:153–66 [Google Scholar]
  181. Zhu H, Crabb DP, Ho T, Garway-Heath DF. 2015. More accurate modeling of visual field progression in glaucoma: ANSWERS. Investig. Ophthalmol. Vis. Sci. 56:6077–83 [Google Scholar]
  182. Zhu H, Russell RA, Saunders LJ, Ceccon S, Garway-Heath DF, Crabb DP. 2014. Detecting changes in retinal function: Analysis with Non-Stationary Weibull Error Regression and Spatial enhancement (ANSWERS). PLOS ONE 9:e85654 [Google Scholar]
  183. Zhu Y, Zhang L, Sasaki Y, Milbrandt J, Gidday JM. 2013. Protection of mouse retinal ganglion cell axons and soma from glaucomatous and ischemic injury by cytoplasmic overexpression of Nmnat1. Investig. Ophthalmol. Vis. Sci. 54:25–36 [Google Scholar]
  184. Zhu Y, Zhang L, Schmidt JF, Gidday JM. 2012. Glaucoma-induced degeneration of retinal ganglion cells prevented by hypoxic preconditioning: a model of glaucoma tolerance. Mol. Med. 18:697–706 [Google Scholar]
/content/journals/10.1146/annurev-vision-102016-061422
Loading
Neuroprotection in Glaucoma: Animal Models and Clinical Trials
Annual Review of Vision Science 3, 91 (2017); https://doi.org/10.1146/annurev-vision-102016-061422
/content/journals/10.1146/annurev-vision-102016-061422
/content/journals/10.1146/annurev-vision-102016-061422
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error