Comparison of retinal nerve fiber layer thickness in vivo and axonal transport after chronic intraocular pressure elevation in young versus older rats

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Abbott, Carla J ^a   Choe, Tiffany E ^a   Burgoyne, Claude F ^a   Cull, Grant ^a   Wang, Lin ^a   Fortune, Brad ^a  

^a DEVERS EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN B SUBUNIT;

ADULT; AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; GLAUCOMA; IN VIVO STUDY; INTRAOCULAR PRESSURE; MALE; NERVE FIBER TRANSPORT; NERVE INJURY; NONHUMAN; OPTIC NERVE FIBER; RAT; RETINAL NERVE FIBER LAYER THICKNESS; SCANNING LASER OPHTHALMOSCOPY; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; SUPERIOR COLLICULUS; YOUNG ADULT; AGING; ANIMAL; AXON; COMPARATIVE STUDY; CYTOLOGY; OPTIC NERVE INJURY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; RETINA GANGLION CELL;

RATTUS; RATTUS NORVEGICUS;

AGING; ANIMALS; AXONAL TRANSPORT; AXONS; INTRAOCULAR PRESSURE; MALE; OPTIC NERVE INJURIES; RATS; RETINA; RETINAL GANGLION CELLS;

EID: 84918501987     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114546     Document Type: Article

References (87)

1. Quigley HA (1996) Number of people with glaucoma worldwide. Br J Ophthalmol 80: 389-393.
2. Quigley HA (1999) Neuronal death in glaucoma. Prog Retin Eye Res 18: 39-57.
3. Howell GR, Soto I, Libby RT, John SW (2013) Intrinsic axonal degeneration pathways are critical for glaucomatous damage. Exp Neurol 246: 54-61.
4. Anderson DR, Hendrickson A (1974) Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest Ophthalmol Vis Sci 13: 771-783.
5. Quigley H, Anderson DR (1976) The dynamics and location of axonal transport blockade by acute intraocular pressure elevation in primate optic nerve. Invest Ophthalmol Vis Sci 15: 606-616.
6. Quigley HA, Anderson DR (1977) Distribution of axonal transport blockade by acute intraocular pressure elevation in the primate optic nerve head. Invest Ophthalmol Vis Sci 16: 640-644.
7. Minckler DS, Bunt AH, Johanson GW (1977) Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci 16: 426-441.
8. Johansson JO (1986) Retrograde axoplasmic transport in rat optic nerve in vivo. What causes blockage at increased intraocular pressure? Exp Eye Res 43: 653-660.
9. Quigley HA, McKinnon SJ, Zack DJ, Pease ME, Kerrigan-Baumrind LA, et al. (2000) Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci 41: 3460-3466.
10. 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: 313-325.
11. Balaratnasingam C, Morgan WH, Bass L, Matich G, Cringle SJ, et al. (2007) Axonal transport and cytoskeletal changes in the laminar regions after elevated intraocular pressure. Invest Ophthalmol Vis Sci 48: 3632-3644.
12. 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: 1523-1537.
13. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson EDO, et al. (2008) Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci 28: 548-561.
14. Buckingham BP, Inman DM, Lambert W, Oglesby E, Calkins DJ, et al. (2008) Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci 28: 2735-2744.
15. Salinas-Navarro M, Alarcón-Martínez L, Valiente-Soriano FJ, Ortín-Martínez A, Jiménez-López M, et al. (2009) Functional and morphological effects of laser-induced ocular hypertension in retinas of adult albino Swiss mice. Mol Vis 15: 2578-2598.
16. Salinas-Navarro M, Alarcón-Martínez L, Valiente-Soriano FJ, Jiménez-López M, Mayor-Torroglosa S, et al. (2010) Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration. Exp Eye Res 90: 168-183.
17. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ (2010) Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci USA 107: 5196-5201.
18. Soto I, Pease ME, Son JL, Shi X, Quigley HA, et al. (2011) Retinal ganglion cell loss in a rat ocular hypertension model is sectorial and involves early optic nerve axon loss. Invest Ophthalmol Vis Sci 52: 434-441.
19. Chidlow G, Ebneter A, Wood JPM, Casson RJ (2011) The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta Neuropathol 121: 737-751.
20. Vidal-Sanz M, Salinas-Navarro M, Nadal-Nicolás FM, Alarcón-Martínez L, Valiente-Soriano FJ, et al. (2012) Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog Retin Eye Res 31: 1-27.
21. Agudo-Barriuso M, Villegas-Pérez M, de Imperial JM, Vidal-Sanz M (2013) Anatomical and functional damage in experimental glaucoma. Curr Opin Ophthalmol 13: 5-11.
22. Johansson JO (1988) Inhibition and recovery of retrograde axoplasmic transport in rat optic nerve during and after elevated IOP in vivo. Exp Eye Res 46: 223-227.
23. Abbott CJ, Choe TE, Lusardi TA, Burgoyne CF, Wang L, et al. (2014) Evaluation of retinal nerve fiber layer thickness and axonal transport 1-and 2-weeks after 8-hours of acute intraocular pressure elevation in rats. Invest Ophthalmol Vis Sci doi: 10.1167/iovs.13-12811
24. Kitazawa Y, Horie T (1975) Diurnal variation of intraocular pressure in primary open-angle glaucoma. Am J Ophthalmol 79: 557-566.
25. Brubaker RF (2003) Targeting outflow facility in glaucoma management. Surv Ophthalmol 48: S17-S20.
26. Sung VC, Barton K (2004) Management of inflammatory glaucomas. Curr Opin Ophthalmol 15: 136-140.
27. Joos KM, Li C, Sappington RM (2010) Morphometric changes in the rat optic nerve following short-term intermittent elevations in intraocular pressure. Invest Ophthalmol Vis Sci 51: 6431-6440.
28. Gramlich OW, Lueckner TC, Kriechbaum M, Teister J, Tao X, et al. (2014) Dynamics, Alterations, and Consequences of Minimally Invasive Intraocular Pressure Elevation in Rats. Invest Ophthalmol Vis Sci 55: 600-611.
29. Bui BV, He Z, Vingrys AJ, Nguyen CT, Wong VH, et al. (2013) Using the electroretinogram to understand how intraocular pressure elevation affects the rat retina. J Ophthalmol 2013: 1-15.
30. Coleman AL, Miglior S (2008) Risk factors for glaucoma onset and progression. Surv Ophthalmol 53: S3-S10.
31. Rudnicka AR, Mt-Isa S, Owen CG, Cook DG, Ashby D (2006) Variations in primary open-angle glaucoma prevalence by age, gender, and race: a Bayesian meta-analysis. Invest Ophthalmol Vis Sci 47: 4254-4261.
32. Leske MC, Heijl A, Hussein M, Bengtsson B, Hyman L, et al. (2003) Factors for glaucoma progression and the effect of treatment: the early manifest glaucoma trial. Arch Ophthalmol 121: 48-56.
33. Nouri-Mahdavi K, Hoffman D, Coleman AL, Liu G, Li G, et al. (2004) Predictive factors for glaucomatous visual field progression in the Advanced Glaucoma Intervention Study. Ophthalmology 111: 1627-1635.
34. Miglior S, Pfeiffer N, Torri V, Zeyen T, Cunha-Vaz J, et al. (2007) Predictive factors for open-angle glaucoma among patients with ocular hypertension in the European Glaucoma Prevention Study. Ophthalmology 114: 3-9.
35. Leske MC, Wu S-Y, Hennis A, Honkanen R, Nemesure B (2008) Risk factors for incident open-angle glaucoma: the Barbados Eye Studies. Ophthalmology 115: 85-93.
36. Manni G, Lambiase A, Centofanti M, Mattei E, De Gregorio A, et al. (1996) Histopathological evaluation of retinal damage during intraocular hypertension in rabbit: involvement of ganglion cells and nerve fiber layer. Graefes Arch Clin Exp Ophthalmol 234: S209-S213.
37. Törngren L, Lundgren B, Madsen K (2000) Intraocular pressure development in the rabbit eye after aqueous exchange with ophthalmic viscosurgical devices. J Cataract Refract Surg 26: 1247-1252.
38. Weber AJ, Zelenak D (2001) Experimental glaucoma in the primate induced by latex microspheres. J Neurosci Meth 111: 39-48.
39. Benozzi J, Nahum LP, Campanelli JL, Rosenstein RE (2002) Effect of hyaluronic acid on intraocular pressure in rats. Invest Ophthalmol Vis Sci 43: 2196-2200.
40. Ben Simon GJ, Bakalash S, Aloni E, Rosner M (2006) A rat model for acute rise in intraocular pressure: immune modulation as a therapeutic strategy. Am J Ophthalmol 141: 1105-1111.
41. 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: 429-437.
42. Ngumah QC, Buchthal SD, Dacheux RF (2006) Longitudinal non-invasive proton NMR spectroscopy measurement of vitreous lactate in a rabbit model of ocular hypertension. Exp Eye Res 83: 390-400.
43. Belforte N, Sande P, de Zavalía N, Knepper PA, Rosenstein RE (2010) Effect of chondroitin sulfate on intraocular pressure in rats. Invest Ophthalmol Vis Sci 51: 5768-5775.
44. Sappington RM, Carlson BJ, Crish SD, Calkins DJ (2010) The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest Opththalmol Vis Sci 51: 207-216.
45. Cone FE, Gelman SE, Son JL, Pease ME, Quigley HA (2010) Differential susceptibility to experimental glaucoma among 3 mouse strains using bead and viscoelastic injection. Exp Eye Res 91: 415-424.
46. Samsel PA, Kisiswa L, Erichsen JT, Cross SD, Morgan JE (2011) A novel method for the induction of experimental glaucoma using magnetic microspheres. Invest Ophthalmol Vis Sci 52: 1671-1675.
47. Ding C, Wang P, Tian N (2011) Effect of general anesthetics on IOP in elevated IOP mouse model. Exp Eye Res 92: 512-520.
48. Fortune B, Choe TE, Reynaud J, Hardin C, Cull GA, et al. (2011) Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation. Invest Ophthalmol Vis Sci 52: 6651-6661.
49. Choe TE, Abbott CJ, Piper C, Wang L, Fortune B (2014) Comparison of longitudinal in vivo measurements of retinal nerve fiber layer thickness and retinal ganglion cell density after optic nerve transection in rat. PloS one: In Press.
50. Abbott CJ, Choe TE, Lusardi TA, Burgoyne CF, Wang L, et al. (2013) Imaging axonal transport in the rat visual pathway. Biomed Opt Express 4: 364-386.
51. Moore RY, Lenn NJ (1972) A retinohypothalamic projection in the rat. J Comp Neurol 146: 1-14.
52. Land PW, Lund RD (1979) Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science 205: 698-700.
53. Reynaud J, Cull G, Wang L, Fortune B, Gardiner S, et al. (2012) Automated quantification of optic nerve axons in primate glaucomatous and normal eyes - Method and comparison to semi-automated manual quantification. Invest Ophthalmol Vis Sci 53: 2951-2959.
54. Jia L, Cepurna WO, Johnson EC, Morrison JC (2000) Patterns of intraocular pressure elevation after aqueous humor outflow obstruction in rats. Invest Ophthalmol Vis Sci 41: 1380-1385.
55. Chauhan BC, LeVatte TL, Garnier KL, Tremblay F, Pang I-H, et al. (2006) Semiquantitative optic nerve grading scheme for determining axonal loss in experimental optic neuropathy. Invest Ophthalmol Vis Sci 47: 634-640.
56. Mwanza J-C, Chang RT, Budenz DL, Durbin MK, Gendy MG, et al. (2010) Reproducibility of peripapillary retinal nerve fiber layer thickness and optic nerve head parameters measured with cirrus HD-OCT in glaucomatous eyes. Invest Ophthalmol Vis Sci 51: 5724-5730.
57. Lee SH, Kim SH, Kim T-W, Park KH, Kim DM (2010) Reproducibility of retinal nerve fiber thickness measurements using the test-retest function of spectral OCT/SLO in normal and glaucomatous eyes. J Glaucoma 19: 637-642.
58. Araie M (2013) Test-retest variability in structural parameters measured with glaucoma imaging devices. Jpn J Ophthalmol 57: 1-24.
59. Quigley HA, Addicks EM (1980) Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol Vis Sci 19: 137-152.
60. Quigley HA, Addicks EM, Green WR, Maumenee AE (1981) Optic nerve damage in human glaucoma: II. The site of injury and susceptibility to damage. Arch Ophthalmol 99: 635-649.
61. Cull GA, Reynaud J, Wang L, Cioffi GA, Burgoyne CF, et al. (2012) Relationship between orbital optic nerve axon counts and retinal nerve fiber layer thickness measured by spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci 53: 7766-7773.
62. Schlamp CL, Li Y, Dietz JA, Janssen KT, Nickells RW (2006) Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci 7: 66.
63. Cepurna WO, Kayton RJ, Johnson EC, Morrison JC (2005) Age related optic nerve axonal loss in adult Brown Norway rats. Exp Eye Res 80: 877-884.
64. Calkins DJ (2013) Age-Related Changes in the Visual Pathways: Blame It on the Axon. Invest Ophthalmol Vis Sci 54: ORSF37-ORSF41.
65. Kong YXG, van Bergen N, Bui BV, Chrysostomou V, Vingrys AJ, et al. (2012) Impact of aging and diet restriction on retinal function during and after acute intraocular pressure injury. Neurobiol Aging 33: 1126. e1115-1126. e1125.
66. Charng J, Nguyen CT, Vingrys AJ, Jobling AI, Bui BV (2013) Increased Susceptibility to Injury in Older Eyes. Optom Vis Sci 90: 275-281.
67. Chrysostomou V, Trounce IA, Crowston JG (2010) Mechanisms of retinal ganglion cell injury in aging and glaucoma. Ophthalmic Res 44: 173-178.
68. Burgoyne CF (2011) A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res 93: 120-132.
69. Nguyen C, Cone FE, Nguyen TD, Coudrillier B, Pease ME, et al. (2013) Studies of scleral biomechanical behavior related to susceptibility for retinal ganglion cell loss in experimental mouse glaucoma. Invest Ophthalmol Vis Sci 54: 1767-1780.
70. Liu X, Li M, Zhong Y-M, Xiao H, Huang J-J, et al. (2010) Damage patterns of retinal nerve fiber layer in acute and chronic intraocular pressure elevation in primary angle closure glaucoma. Int J Ophthalmol 3: 152-157.
71. Fortune B, Burgoyne CF, Cull G, Reynaud J, Wang L (2013) Onset and progression of peripapillary retinal nerve fiber layer retardance changes occur earlier than RNFL thickness changes in experimental glaucoma. Invest Ophthalmol Vis Sci 54: 5653-5661.
72. Ramírez AI, Salazar JJ, de Hoz R, Rojas B, Gallego BI, et al. (2010) Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma. Invest Ophthalmol Vis Sci 51: 5690-5696.
73. Kezic JM, Chrysostomou V, Trounce IA, McMenamin PG, Crowston JG (2013) Effect of anterior chamber cannulation and acute IOP elevation on retinal macrophages in the adult mouse. Invest Ophthalmol Vis Sci 54: 3028-3036.
74. Holcombe DJ, Lengefeld N, Gole GA, Barnett NL (2008) The effects of acute intraocular pressure elevation on rat retinal glutamate transport. Acta Ophthalmol 86: 408-414.
75. Bui BV, Batcha AH, Fletcher EL, Wong VHY, Fortune B (2013) Relationship between the magnitude of intraocular pressure during an episode of acute elevation and retinal damage four weeks later in rats. PLoS One 8: e70513.
76. Buñag RD, Butterfield J (1982) Tail-cuff blood pressure measurement without external preheating in awake rats. Hypertension 4: 898-903.
77. Fortune B, Yang H, Strouthidis NG, Cull GA, Grimm JL, et al. (2009) The effect of acute intraocular pressure elevation on peripapillary retinal thickness, retinal nerve fiber layer thickness, and retardance. Invest Ophthalmol Vis Sci 50: 4719-4726.
78. Strouthidis NG, Fortune B, Yang H, Sigal IA, Burgoyne CF (2011) Effect of acute intraocular pressure elevation on the monkey optic nerve head as detected by spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci 52: 9431-9437.
79. Patel NB, Luo X, Wheat JL, Harwerth RS (2011) Retinal nerve fiber layer assessment: area versus thickness measurements from elliptical scans centered on the optic nerve. Invest Ophthalmol Vis Sci 52: 2477-2489.
80. Lozano DC, Twa MD (2013) Development of a Rat Schematic Eye from in vivo Biometry and the Correction of Lateral Magnification in SD-OCT Imaging. Invest Ophthalmol Vis Sci 54: 6446-6455.
81. Nagata A, Higashide T, Ohkubo S, Takeda H, Sugiyama K (2009) In vivo quantitative evaluation of the rat retinal nerve fiber layer with optical coherence tomography. Invest Ophthalmol Vis Sci 50: 2809-2815.
82. Thuen M, Berry M, Pedersen TB, Goa PE, Summerfield M, et al. (2008) Manganese-enhanced MRI of the rat visual pathway: Acute neural toxicity, contrast enhancement, axon resolution, axonal transport, and clearance of Mn2+. J Magn Reson Im 28: 855-865.
83. Holmgren J, Adamsson J, Anjuère F, Clemens J, Czerkinsky C, et al. (2005) Mucosal adjuvants and anti-infection and anti-immunopathology vaccines based on cholera toxin, cholera toxin B subunit and CpG DNA. Immunol Lett 97: 181-188.
84. Liang Y, Downs JC, Fortune B, Cull G, Cioffi GA, et al. (2009) Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates. Invest Ophthalmol Vis Sci 50: 2154-2160.
85. Bui BV, Edmunds B, Cioffi GA, Fortune B (2005) The gradient of retinal functional changes during acute intraocular pressure elevation. Invest Ophthalmol Vis Sci 46: 202-213.
86. Chrysostomou V, Crowston JG (2013) The Photopic Negative Response of the Mouse Electroretinogram: Reduction by Acute Elevation of Intraocular Pressure. Invest Ophthalmol Vis Sci 54: 4691-4697.
87. He Z, Bui BV, Vingrys AJ (2006) The rate of functional recovery from acute IOP elevation. Invest Ophthalmol Vis Sci 47: 4872-4880.