Advances in retinal ganglion cell imaging

Eye (Basingstoke)

Volumn 29, Issue 10, 2015, Pages 1260-1269

  Balendra, S I ^a   Normando, E M ^a,b   Bloom, P A ^b   Cordeiro, M F ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; TRACER;

ARTICLE; DIAGNOSTIC IMAGING; GLAUCOMA; HUMAN; IN VIVO STUDY; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; OPTICS; RETINA GANGLION CELL; SCANNING LASER OPHTHALMOSCOPY; SENSITIVITY AND SPECIFICITY; TRANSGENIC ORGANISM; APOPTOSIS; AXON; OPTIC DISK; OPTIC NERVE DISEASES; PATHOLOGY; PROCEDURES; VISUAL SYSTEM EXAMINATION;

APOPTOSIS; AXONS; DIAGNOSTIC IMAGING; DIAGNOSTIC TECHNIQUES, OPHTHALMOLOGICAL; GLAUCOMA; HUMANS; OPTIC DISK; OPTIC NERVE DISEASES; RETINAL GANGLION CELLS;

EID: 84943392717     PISSN: 0950222X     EISSN: 14765454     Source Type: Journal    
DOI: 10.1038/eye.2015.154     Document Type: Article

References (98)

1. Pascolini D, Mariotti SP. Global estimates of visual impairment: 2010. Br J Ophthalmol 2011; 96(5): 614-618.
2. Foster PJ, Buhrmann R, Quigley HA, Johnson GJ. The definition and classification of glaucoma in prevalence surveys. Br J Ophthalmol 2002; 86(2): 238-242.
3. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 2006; 90(3): 262-267.
4. Garcia-Valenzuela E, Shareef S, Walsh J, Sharma SC. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp Eye Res 1995; 61(1): 33-44.
5. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci 1995; 36(5): 774-786.
6. Humayun MS, Prince M, De Juan Jr E, Barron Y, Moskowitz M, Klock IB et al. Morphometric analysis of the extramacular retina from postmortem eyes with retinitis pigmentosa. Invest Ophthalmol Vis Sci 1999; 40(1): 143-148.
7. Medeiros NE, Curcio CA. Preservation of ganglion cell layer neurons in age-related macular degeneration. Invest Ophthalmol Vis Sci 2001; 42(3): 795-803.
8. Fischer U, Schulze-Osthoff K. New approaches and therapeutics targeting apoptosis in disease. Pharmacol Rev 2005; 57(2): 187-215.
9. Quigley HA. Glaucoma. Lancet 2011; 377(9774): 1367-1377.
10. Cordeiro MF, Guo L, Luong V, Harding G, Wang W, Jones HE et al. Real-time imaging of single nerve cell apoptosis in retinal neurodegeneration. Proc Natl Acad Sci USA 2004; 101(36): 13352-13356.
11. Harwerth RS, Carter-Dawson L, Shen F, Smith EL 3rd, Crawford ML. Ganglion cell losses underlying visual field defects from experimental glaucoma. Invest Ophthalmol Vis Sci 1999; 40(10): 2242-2250.
12. Kerrigan-Baumrind LA, Quigley HA, Pease ME, Kerrigan DF, Mitchell RS. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest Ophthalmol Vis Sci 2000; 41(3): 741-748.
13. Guo L, Duggan J, Cordeiro MF. Alzheimer's disease and retinal neurodegeneration. Curr Alzheimer Res 2010; 7(1): 3-14.
14. Heaton GR, Davis BM, Turner LA, Cordeiro MF. Ocular biomarkers of Alzheimer's disease. Cent Nerv Syst Agents Med Chem 2015; 15(2): 117-125.
15. Massey SC. Functional Anatomy of the Mammalian Retina. In: Sjrrhpsp Wilkinson (ed). Retina 4th edn, Chapter 4. Mosby: Edinburgh, Scotland, 2006, pp. 43-82. Available from: http: //www. sciencedirect. com/science/article/pii/ B9780323025980500100.
16. Jakobs TC, Libby RT, Ben Y, John SWM, Masland RH. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 2005; 171(2): 313-325.
17. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28 (1): 41-51.
18. Gray DC, Merigan W, Wolfing JI, Gee BP, Porter J, Dubra A et al. In vivo fluorescence imaging of primate retinal ganglion cells and retinal pigment epithelial cells. Opt Express 2006; 14 (16): 7144-7158.
19. Kerrison JB, Duh EJ, Yu Y, Otteson DC, Zack DJ. A system for inducible gene expression in retinal ganglion cells. Invest Ophthalmol Vis Sci 2005; 46(8): 2932-2939.
20. Guo L, Salt TE, Maass A, Luong V, Moss SE, Fitzke FW et al. Assessment of neuroprotective effects of glutamate modulation on glaucoma-related retinal ganglion cell apoptosis in vivo. Invest Ophthalmol Vis Sci 2006; 47(2): 626-633.
21. Guo L, Salt TE, Luong V, Wood N, Cheung W, Maass A et al. Targeting amyloid-beta in glaucoma treatment. Proc Natl Acad Sci USA 2007; 104(33): 13444-13449.
22. Krupin T, Liebmann JM, Greenfield DS, Rosenberg LF, Ritch R, Yang JW. The Low-pressure Glaucoma Treatment Study (LoGTS): study design and baseline characteristics of enrolled patients. Ophthalmology 2005; 112(3): 376-385.
23. Garway-Heath DF, Crabb DP, Bunce C, Lascaratos G, Amalfitano F, Anand N et al. Latanoprost for open-angle glaucoma (UKGTS): a randomised, multicentre, placebocontrolled trial. Lancet 2014; 385(9975): 1295-1304.
24. Harwerth RS, Wheat JL, Rangaswamy NV. Age-related losses of retinal ganglion cells and axons. Invest Ophthalmol Vis Sci 2008; 49(10): 4437-4443.
25. Curcio CA, Allen KA. Topography of ganglion cells in human retina. J Comp Neurol 1990; 300(1): 5-25.
26. Spear PD, Kim CBY, Ahmad A, Tom BW. Relationship between numbers of retinal ganglion cells and lateral geniculate neurons in the rhesus monkey. Vis Neurosci 1996; 13(01): 199-203.
27. Williams RW, Strom RC, Rice DS, Goldowitz D. Genetic and environmental control of variation in retinal ganglion cell number in mice. J Neurosci 1996; 16(22): 7193-7205.
28. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W et al. Optical coherence tomography. Science 1991; 254(5035): 1178-1181.
29. Van Velthoven MEJ, Verbraak FD, Yannuzzi LA, Rosen RB, Podoleanu AGH, de Smet MD. Imaging the retina by en face optical coherence tomography. Retina 2006; 26(2): 129-136.
30. Costa RA, Skaf M, Melo LASJ, Calucci D, Cardillo JA, Castro JC et al. Retinal assessment using optical coherence tomography. Prog Retin Eye Res 2006; 25(3): 325-353.
31. Chauhan BC, Stevens KT, Levesque JM, Nuschke AC, Sharpe GP, O'Leary N et al. Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice. PloS One 2012; 7(6): e40352.
32. Guo L, Normando EM, Nizari S, Lara D, Cordeiro MF. Tracking longitudinal retinal changes in experimental ocular hypertension using the cSLO and spectral domain-OCT. Invest Ophthalmol Vis Sci 2010; 51(12): 6504-6513.
33. Bussel II, Wollstein G, Schuman JS. OCT for glaucoma diagnosis, screening and detection of glaucoma progression. Br J Ophthalmol 2014; 98(Suppl 2): ii15-ii19.
34. Schuman JS. Spectral domain optical coherence tomography for glaucoma (an AOS thesis). Trans Am Ophthalmol Soc 2008; 106: 426-458.
35. Werkmeister RM, Dragostinoff N, Pircher M, Gotzinger E, Hitzenberger CK, Leitgeb RA et al. Bidirectional Doppler Fourier-domain optical coherence tomography for measurement of absolute flow velocities in human retinal vessels. Opt Lett 2008; 33(24): 2967-2969.
36. Pircher M, Hitzenberger CK, Schmidt-Erfurth U. Polarization sensitive optical coherence tomography in the human eye. Prog Retin Eye Res 2011; 30(6): 431-451.
37. Keane PA, Ruiz-Garcia H, Sadda SR. Clinical applications of long-wavelength (1, 000-nm) optical coherence tomography. Ophthalmic Surg Lasers Imaging 2011; 42(Suppl): S67-S74.
38. Webb RH, Hughes GW, Pomerantzeff O. Flying spot TV ophthalmoscope. Appl Opt 1980; 19(17): 2991-2997.
39. Chauhan BC. Confocal scanning laser tomography. Can J Ophthalmol 1996; 31(3): 152-156.
40. Webb RH, Hughes GW, Delori FC. Confocal scanning laser ophthalmoscope. Appl Opt 1987; 26(8): 1492-1499.
41. Zangwill LM, Bowd C. Retinal nerve fiber layer analysis in the diagnosis of glaucoma. Curr Opin Ophthalmol 2006; 17(2): 120-131.
42. Leung CKS, Lindsey JD, Crowston JG, Ju W-K, Liu Q, Bartsch D-U et al. In vivo imaging of murine retinal ganglion cells. J Neurosci Methods 2008; 168(2): 475-478.
43. Cordeiro MF, Migdal C, Bloom P, Fitzke FW, Moss SE. Imaging apoptosis in the eye. Eye 2011; 25(5): 545-553.
44. Higashide T, Kawaguchi I, Ohkubo S, Takeda H, Sugiyama K. In vivo imaging and counting of rat retinal ganglion cells using a scanning laser ophthalmoscope. Invest Ophthalmol Vis Sci 2006; 47(7): 2943-2950.
45. Maass A, von Leithner PL, Luong V, Guo L, Salt TE, Fitzke FW et al. Assessment of rat and mouse RGC apoptosis imaging in vivo with different scanning laser ophthalmoscopes. Curr Eye Res 2007; 32(10): 851-861.
46. Cilkova M, Matlach J, Chopra R, Rider A, Shah N, Mulholland P et al. Repeatability and inter-observer variability of in vivo retinal cone imaging using a modified Heidelberg Retinal Angiography (HRA2) in normal subjects.
47. High Resolution Photoreceptor Imaging, 2015. Available from http: //www. arvo. org/webs/am2015/abstract/471. pdf.
48. Miller DT, Kocaoglu OP, Wang Q, Lee S. Adaptive optics and the eye (super resolution OCT). Eye 2011; 25(3): 321-330.
49. Liang J, Grimm B, Goelz S, Bille JF. Objective measurement of wave aberrations of the human eye with the use of a Hartmann-Shack wave-front sensor. J Opt Soc Am A Opt Image Sci Vis 1994; 11(7): 1949-1957.
50. Chen TC, Cense B, Pierce MC, Nassif N, Park BH, Yun SH et al. Spectral domain optical coherence tomography: ultra-high speed, ultra-high resolution ophthalmic imaging. Arch Ophthalmol 2005; 123(12): 1715-1720.
51. Truong SN, Alam S, Zawadzki RJ, Choi SS, Telander DG, Park SS et al. High resolution Fourier-domain optical coherence tomography of retinal angiomatous proliferation. Retina 2007; 27(7): 915-925.
52. Biss DP, Sumorok D, Burns SA, Webb RH, Zhou Y, Bifano TG et al. In vivo fluorescent imaging of the mouse retina using adaptive optics. Opt Lett 2007; 32(6): 659-661.
53. Williams DR. Imaging single cells in the living retina. Vision Res 2011; 51(13): 1379-1396.
54. Chen MF, Chui TYP, Alhadeff P, Rosen RB, Ritch R, Dubra A et al. Adaptive optics imaging of healthy and abnormal regions of retinal nerve fiber bundles of patients with glaucoma. Invest Ophthalmol Vis Sci 2015; 56(1): 674-681.
55. Battu R, Dabir S, Khanna A, Kumar AK, Roy AS. Adaptive optics imaging of the retina. Indian J Ophthalmol 2014; 62(1): 60-65.
56. Köbbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S. Current concepts in neuroanatomical tracing. Prog Neurobiol 2000; 62(4): 327-351.
57. Thanos S, Fischer D, Pavlidis M, Heiduschka P, Bodeutsch N. Glioanatomy assessed by cell-cell interactions and phagocytotic labelling. J Neurosci Methods 2000; 103(1): 39-50.
58. Gray DC, Wolfe R, Gee BP, Scoles D, Geng Y, Masella BD et al. In vivo imaging of the fine structure of rhodaminelabeled macaque retinal ganglion cells. Invest Ophthalmol Vis Sci 2008; 49(1): 467-473.
59. Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci 2002; 43(9): 2962-2968.
60. Thanos S, Naskar R, Heiduschka P. Regenerating ganglion cell axons in the adult rat establish retinofugal topography and restore visual function. Exp Brain Res 1997; 114(3): 483-491.
61. Thanos S, Indorf L, Naskar R. In vivo FM: using conventional fluorescence microscopy to monitor retinal neuronal death in vivo. Trends Neurosci 2002; 25(9): 441-444.
62. Thanos S, Naskar R. Correlation between retinal ganglion cell death and chronically developing inherited glaucoma in a new rat mutant. Exp Eye Res 2004; 79(1): 119-129.
63. Leak RK, Moore RY. Identification of retinal ganglion cells projecting to the lateral hypothalamic area of the rat. Brain Res 1997; 770(1-2): 105-114.
64. Cordeiro MF, Guo L, Coxon KM, Duggan J, Nizari S, Normando EM et al. Imaging multiple phases of neurodegeneration: a novel approach to assessing cell death in vivo. Cell Death Dis 2010; 1: e3.
65. Sabel BA, Engelmann R, Humphrey MF. In vivo confocal neuroimaging (ICON) of CNS neurons. Nat Med 1997; 3(2): 244-247.
66. Vidal-Sanz M, Salinas-Navarro M, Nadal-Nicolas FM, Alarcon-Martinez L, Valiente-Soriano FJ, de Imperial JM et al. Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog Retin Eye Res 2012; 31(1): 1-27.
67. Salinas-Navarro M, Jiménez-López M, Valiente-Soriano FJ, Alarcón-Martínez L, Avilés-Trigueros M, Mayor S et al. Retinal ganglion cell population in adult albino and pigmented mice: a computerized analysis of the entire population and its spatial distribution. Vision Res 2009; 49(6): 637-647.
68. Salinas-Navarro M, Mayor-Torroglosa S, Jiménez-López M, Avilés-Trigueros M, Holmes TM, Lund RD et al. A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Res 2009; 49(1): 115-126.
69. Bodeutsch N, Thanos S. Migration of phagocytotic cells and development of the murine intraretinal microglial network: an in vivo study using fluorescent dyes. Glia 2000; 32(1): 91-101.
70. Wang X, Archibald ML, Stevens K, Baldridge WH, Chauhan BC. Cyan fluorescent protein (CFP) expressing cells in the retina of Thy1-CFP transgenic mice before and after optic nerve injury. Neurosci Lett 2010; 468(2): 110-114.
71. Hermann B, Fernandez EJ, Unterhuber A, Sattmann H, Fercher AF, Drexler W et al. Adaptive-optics ultrahighresolution optical coherence tomography. Opt Lett 2004; 29(18): 2142-2144.
72. Leung CK, Weinreb RN, Li ZW, Liu S, Lindsey JD, Choi N et al. Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells. Invest Ophthalmol Vis Sci 2011; 52(3): 1539-1547.
73. Leung CKS, Lindsey JD, Chen L, Liu Q, Weinreb RN. Longitudinal profile of retinal ganglion cell damage assessed with blue-light confocal scanning laser ophthalmoscopy after ischaemic reperfusion injury. Br J Ophthalmol 2009; 93(7): 964-968.
74. Leung CK, Lindsey JD, Crowston JG, Lijia C, Chiang S, Weinreb RN. Longitudinal profile of retinal ganglion cell damage after optic nerve crush with blue-light confocal scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci 2008; 49(11): 4898-4902.
75. Dezawa M, Takano M, Negishi H, Mo X, Oshitari T, Sawada H. Gene transfer into retinal ganglion cells by in vivo electroporation: a new approach. Micron 2002; 33(1): 1-6.
76. Zheng QA, Chang DC. High-efficiency gene transfection by in situ electroporation of cultured cells. Biochim Biophys Acta 1991; 1088(1): 104-110.
77. Nickerson JM, Goodman P, Chrenek MA, Johnson CJ, Berglin L, Redmond TM et al. Subretinal delivery and electroporation in pigmented and nonpigmented adult mouse eyes. Methods Mol Biol 2012; 884: 53-69.
78. Garcia-Frigola C, Carreres MI, Vegar C, Herrera E. Gene delivery into mouse retinal ganglion cells by in utero electroporation. BMC Dev Biol 2007; 7: 103.
79. Nickerson JM, Getz SE, Sellers JT, Chrenek MA, Goodman P, Bernal CJ et al. DNA delivery in adult mouse eyes: An update with corneal endothelium outcomes. Methods Mol Biol 2014; 1121: 165-177.
80. Matsuda T, Cepko CL. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci USA 2004; 101(1): 16-22.
81. Nadal-Nicolas FM, Jimenez-Lopez M, Salinas-Navarro M, Sobrado-Calvo P, Alburquerque-Bejar JJ, Vidal-Sanz M et al. Whole number, distribution and co-expression of brn3 transcription factors in retinal ganglion cells of adult albino and pigmented rats. PLoS One 2012; 7(11): e49830.
82. Surgucheva I, Weisman AD, Goldberg JL, Shnyra A, Surguchov A. Gamma-synuclein as a marker of retinal ganglion cells. Mol Vis 2008; 14: 1540-1548.
83. Surgucheva I, Surguchov A. Gamma-synuclein: cell-typespecific promoter activity and binding to transcription factors. J Mol Neurosci 2008; 35(3): 267-271.
84. Rodriguez AR, de Sevilla Müller LP, Brecha NC. The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. J Comp Neurol 2014; 522(6): 1411-1443.
85. Smith CA, Chauhan BC. Imaging retinal ganglion cells: enabling experimental technology for clinical application. Prog Retin Eye Res 2015; 44: 1-14.
86. Aman AT, Fraser S, Merritt EA, Rodigherio C, Kenny M, Ahn M et al. A mutant cholera toxin B subunit that binds GM1-ganglioside but lacks immunomodulatory or toxic activity. Proc Natl Acad Sci USA 2001; 98(15): 8536-8541.
87. Sánchez J, Holmgren J. Cholera toxin-a foe & a friend. Indian J Med Res 2011; 133(2): 153-163.
88. Bhattacharya SK, Lee RK, Grus FH The Seventh ARVO/Pfizer Ophthalmics Research Institute Conference Working Group. Molecular Biomarkers in Glaucoma. Invest Ophthalmol Vis Sci 2013; 54(1): 121-131.
89. Meers P, Mealy T. Calcium-dependent annexin V binding to phospholipids: Stoichiometry, specificity, and the role of negative charge. Biochemistry 1993; 32(43): 11711-11721.
90. Nick Wood NH, Guo L, Francesca Cordeiro M. Imaging individual ganglion cells in the human retina. In: Grehn F, Stamper R (eds). Glaucoma, Springer: Berlin, Heidelberg, Germany, 2009, pp 1-12. Available from: http: //dx. doi. org/10. 1007/978-3-540-69475-5-1.
91. D'Arceuil H, Rhine W, de Crespigny A, Yenari M, Tait JF, Strauss WH et al. 99mTc annexin V imaging of neonatal hypoxic brain injury. Stroke 2000; 31(11): 2692-2700.
92. Galvao J, Davis BM, Cordeiro MF. In vivo imaging of retinal ganglion cell apoptosis. Curr Opin Pharmacol 2013; 13(1): 123-127.
93. Guo L, Cordeiro MF. Assessment of neuroprotection in the retina with DARC. Prog Brain Res 2008; 173: 437-450.
94. Schmitz-Valckenberg S, Guo L, Maass A, Cheung W, Vugler A, Moss SE et al. Real-time in vivo imaging of retinal cell apoptosis after laser exposure. Invest Ophthalmol Vis Sci 2008; 49(6): 2773-2780.
95. Baltmr A, Duggan J, Nizari S, Salt TE, Cordeiro MF. Neuroprotection in glaucoma-is there a future role? Exp Eye Res 2010; 91(5): 554-566.
96. Maxwell D, Chang Q, Zhang X, Barnett EM, Piwnica-Worms D. An improved cell-penetrating, caspase-activatable, nearinfrared fluorescent peptide for apoptosis imaging. Bioconjug Chem 2009; 20(4): 702-709.
97. Qiu X, Johnson JR, Wilson BS, Gammon ST, Piwnica-Worms D, Barnett EM. Single-cell resolution imaging of retinal ganglion cell apoptosis in vivo using a cell-penetrating caspase-activatable peptide probe. PloS One 2014; 9(2): e88855.
98. Bullok K, Piwnica-Worms D. Synthesis and characterization of a small, membrane-permeant, caspase-activatable far-red fluorescent peptide for imaging apoptosis. J Med Chem 2005; 48(17): 5404-5407.