Characteristic patterns of dendritic remodeling in early-stage glaucoma: Evidence from genetically identified retinal ganglion cell types

Journal of Neuroscience

Volumn 35, Issue 6, 2015, Pages 2329-2343

  El Danaf, Rana N ^a,b,c   Huberman, Andrew D ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEUROBIOLOGY SECTION   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Dendrites; Glaucoma; Retinal ganglion cells

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN HISTOLOGY; CELL LOSS; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; EARLY STAGE GLAUCOMA; EPIFLUORESCENCE MICROSCOPY; FEMALE; GLAUCOMA; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; LATERAL GENICULATE BODY; MALE; MOUSE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; SUPERIOR COLLICULUS; ANIMAL; BRAIN; C57BL MOUSE; CELL DEATH; CELL SIZE; DENDRITE; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BRAIN; CELL DEATH; CELL SIZE; DENDRITES; DISEASE PROGRESSION; FEMALE; GLAUCOMA; INTRAOCULAR PRESSURE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RETINA; RETINAL GANGLION CELLS;

EID: 84922572484     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1419-14.2015     Document Type: Article

References (59)

1. Ahmed FA, Chaudhary P, Sharma SC (2001) Effects of increased intraocular pressure on rat retinal ganglion cells. Int J Dev Neurosci 19: 209-218. CrossRef Medline.
2. Almasieh M, MacIntyre JN, Pouliot M, Casanova C, Vaucher E, Kelly ME, Di Polo A (2013) Acetylcholinesterase inhibition promotes retinal vasoprotection and increases ocular blood flow in experimental glaucoma. Invest Ophthalmol Vis Sci 54: 3171-3183. CrossRef Medline.
3. Beier KT, Borghuis BG, El-Danaf RN, Huberman AD, Demb JB, Cepko CL (2013) Transsynaptic tracing with vesicular stomatitis virus reveals novel retinal circuitry. J Neurosci 33: 35-51. CrossRef Medline.
4. Berson DM (2008) Retinal ganglion cell types and their central projection. In: The senses: a comprehensive reference (Masland R, ed). Oxford: Elsevier.
5. Berson DM, Castrucci AM, Provencio I (2010) Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol 518: 2405-2422. CrossRef Medline.
6. Bleckert A, Schwartz GW, Turner MH, Rieke F, Wong RO (2014) Visual space is represented by nonmatching topographies of distinct mouse retinal ganglion cell types. Curr Biol 24: 310-315. CrossRef Medline.
7. Bouhenni RA, Dunmire J, Sewell A, Edward DP (2012) Animal models of glaucoma. J Biomed Biotechnol 2012: 692609. CrossRef Medline.
8. Buckingham BP, Inman DM, Lambert W, Oglesby E, Calkins DJ, Steele MR, Vetter ML, Marsh-Armstrong N, Horner PJ (2008) Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci 28: 2735-2744. CrossRef Medline.
9. Calkins DJ (2012) Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog Retin Eye Res 31: 702-719. CrossRef Medline.
10. Casson RJ, Chidlow G, Wood JP, Crowston JG, Goldberg I (2012) Definition of glaucoma: clinical and experimental concepts. Clin Experiment Ophthalmol 40: 341-349. CrossRef Medline.
11. Chen H, Wei X, Cho KS, Chen G, Sappington R, Calkins DJ, Chen DF (2011) Optic neuropathy due to microbead-induced elevated intraocular pressure in the mouse. Invest Ophthalmol Vis Sci 52: 36-44. CrossRef Medline.
12. 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. CrossRef Medline.
13. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ (2010) Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci U S A 107: 5196-5201. CrossRef Medline.
14. Cruz-Martín A, El-Danaf RN, Osakada F, Sriram B, Dhande OS, Nguyen PL, Callaway EM, Ghosh A, Huberman AD (2014) A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507: 358-361. CrossRef Medline.
15. Cuthbertson RA, Mandel TE (1986) Anatomy of the mouse retina. Endothelial cell-pericyte and capillary distribution. Invest Ophthalmol Vis Sci 27: 1659-1664. Medline.
16. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma and dialectics. Lancet Neurol 3: 184-190. CrossRef Medline.
17. Della Santina L, Inman DM, Lupien CB, Horner PJ, Wong RO (2013) Differential progression of structural and functional alterations in distinct retinal ganglion cell types in a mouse model of glaucoma. J Neurosci 33: 17444-17457. CrossRef Medline.
18. Dhande OS, Huberman AD (2014) Retinal ganglion cell maps in the brain: implications for visual processing. Curr Opin Neurobiol 24: 133-142. CrossRef Medline.
19. Dhande OS, Estevez ME, Quattrochi LE, El-Danaf RN, Nguyen PL, Berson DM, HubermanAD (2013) Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. J Neurosci 33: 17797-17813. CrossRef Medline.
20. Dumitrescu ON, Pucci FG, Wong KY, Berson DM (2009) Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. JCompNeurol 517: 226-244. CrossRef Medline.
21. Feng L, Zhao Y, Yoshida M, Chen H, Yang JF, Kim TS, Cang J, Troy JB, Liu X (2013) Sustained ocular hypertension induces dendritic degeneration of mouse retinal ganglion cells that depends on cell type and location. Invest Ophthalmol Vis Sci 54: 1106-1117. CrossRef Medline.
22. Frankfort BJ, Khan AK, Tse DY, Chung I, Pang JJ, Yang Z, Gross RL, Wu SM (2013) Elevated intraocular pressure causes inner retinal dysfunction before cell loss in a mouse model of experimental glaucoma. Invest Ophthalmol Vis Sci 54: 762-770. CrossRef Medline.
23. Glovinsky Y, Quigley HA, Dunkelberger GR (1991) Retinal ganglion cell loss is size dependent in experimental glaucoma. Invest Ophthalmol Vis Sci 32: 484-491. Medline.
24. Halliday G, Robinson SR, Shepherd C, Kril J (2000) Alzheimer's disease and inflammation: a review of cellular and therapeutic mechanisms. Clin Exp Pharmacol Physiol 27: 1-8. Medline.
25. Heijl A, Leske MC, Bengtsson B, Hyman L, Bengtsson B, Hussein M, Hussein M (2002) Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 120: 1268-1279. CrossRef Medline.
26. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA (2008) Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59: 425-438. CrossRef Medline.
27. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA (2009) Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62: 327-334. CrossRef Medline.
28. Jakobs TC, Libby RT, Ben Y, John SW, MaslandRH (2005) Retinal ganglion cell degeneration is topological but not cell type-specific in DBA/2J mice. J Cell Biol 171: 313-325. CrossRef Medline.
29. Kalesnykas G, Oglesby EN, Zack DJ, Cone FE, Steinhart MR, Tian J, Pease ME, Quigley HA (2012) Retinal ganglion cell morphology after optic nerve crush and experimental glaucoma. Invest Ophthalmol Vis Sci 53: 3847-3857. CrossRef Medline.
30. Kass MA, Heuer DK, Higginbotham EJ, Johnson CA, Keltner JL, Miller JP, Parrish RK 2nd, Wilson MR, GordonMO (2002) The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary openangle glaucoma. Arch Ophthalmol 120: 701-713; discussion 829-830. CrossRef Medline.
31. Kim M, Kim DM, Park KH, Kim TW, Jeoung JW, Kim SH (2013) Intraocular pressure reduction with topical medications and progression of normal-tension glaucoma: a 12-year mean follow-up study. Acta Ophthalmol 91: e270-5. CrossRef Medline.
32. Krahe TE, El-Danaf RE, Dilger EK, Henderson SC, Guido W (2011) Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. J Neurosci 31: 17437-17448. CrossRef Medline.
33. Li RS, Chen BY, Tay DK, Chan HH, Pu ML, So KF (2006) Melanopsinexpressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol Vis Sci 47: 2951-2958. CrossRef Medline.
34. Lichter PR (2002) Impact of intraocular pressure reduction on glaucoma progression. JAMA 288: 2607-2608. CrossRef Medline.
35. Morgan JE, Uchida H, Caprioli J (2000) Retinal ganglion cell death in experimental glaucoma. Br J Ophthalmol 84: 303-310. CrossRef Medline.
36. Morrison JC, Nylander KB, Lauer AK, Cepurna WO, Johnson E (1998) Glaucoma drops control intraocular pressure and protect optic nerves in a rat model of glaucoma. Invest Ophthalmol Vis Sci 39: 526-531. Medline.
37. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, Nguyen PL, Panagiotakos G, Inoue YU, Egusa SF, Volgyi B, Inoue T, Bloomfield SA, Barres BA, Berson DM, Feldheim DA, Huberman AD (2011) Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 71: 632-639. CrossRef Medline.
38. Pang JJ, Gao F, Wu SM (2003) Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. J Neurosci 23: 6063-6073. Medline.
39. Pascolini D, Mariotti SP (2012) Global estimates of visual impairment: 2010. Br J Ophthalmol 96: 614-618. CrossRef Medline.
40. Pavlidis M, Stupp T, Naskar R, Cengiz C, Thanos S (2003) Retinal ganglion cells resistant to advanced glaucoma: a postmortem study of human retinas with the carbocyanine dye DiI. Invest Ophthalmol Vis Sci 44: 5196-5205. CrossRef Medline.
41. Peters D, Bengtsson B, Heijl A (2014) Factors associated with lifetime risk of open-angle glaucoma blindness. Acta Ophthalmol 92: 421-425. CrossRef Medline.
42. Pournaras CJ, Rungger-Brändle E, Riva CE, Hardarson SH, Stefansson E (2008) Regulation of retinal blood flow in health and disease. Prog Retin Eye Res 27: 284-330. CrossRef Medline.
43. QuigleyHA (1999) Neuronal death in glaucoma. Prog Retin Eye Res 18: 39-57. CrossRef Medline.
44. Quigley HA, Broman AT (2006) The number of people with glaucoma in 2010 and 2020. Br J Ophthalmol 90: 262-267. CrossRef Medline.
45. Quigley HA, Sanchez RM, Dunkelberger GR, L'Hernault NL, Baginski TA (1987) Chronic glaucoma selectively damages large optic nerve fibers. Invest Ophthalmol Vis Sci 28: 913-920. Medline.
46. Quigley HA, Dunkelberger GR, Green WR (1988) Chronic human glaucoma causing selectively greater loss of large optic nerve fibers. Ophthalmology 95: 357-363. CrossRef Medline.
47. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, Barres BA, Huberman AD, Feller MB (2011) Transgenic mice reveal unexpected diversity of On-Off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 31: 8760-8769. CrossRef Medline.
48. Samuel MA, Zhang Y, Meister M, Sanes JR (2011) Age-related alterations in neurons of the mouse retina. J Neurosci 31: 16033-16044. CrossRef Medline.
49. Sappington RM, Carlson BJ, Crish SD, Calkins DJ (2010) The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest Ophthalmol Vis Sci 51: 207-216. CrossRef Medline.
50. Schwartz GW, Okawa H, Dunn FA, Morgan JL, Kerschensteiner D, Wong RO, Rieke F 2012 The spatial structure of a nonlinear receptive field. Nat Neurosci 15: 1572-1580. CrossRef Medline.
51. Shou T, Liu J, Wang W, Zhou Y, Zhao K (2003) Differential dendritic shrinkage of alpha and beta retinal ganglion cells in cats with chronic glaucoma. Invest Ophthalmol Vis Sci 44: 3005-3010. CrossRef Medline.
52. Sommer A (1989) Intraocular pressure and glaucoma. Am J Ophthalmol 107: 186-188. CrossRef Medline.
53. Venkataraman ST, Flanagan JG, Hudson C (2010) Vascular reactivity of optic nerve head and retinal blood vessels in glaucoma-a review. Microcirculation 17: 568-581. CrossRef Medline.
54. Vidal-Sanz M, Salinas-Navarro M, Nadal-Nicolás FM, Alarcó n-Martínez L, Valiente-Soriano FJ, de Imperial JM, Avilés-Trigueros M, Agudo-Barriuso M, Villegas-Pérez MP (2012) Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog Retin Eye Res 31: 1-27. CrossRef Medline.
55. Ward NJ, Ho KW, Lambert WS, Weitlauf C, Calkins DJ (2014) Absence of transient receptor potential vanilloid-1 accelerates stress-induced axonopathy in the optic projection. J Neurosci 34: 3161-3170. CrossRef Medline.
56. Weber AJ, Kaufman PL, Hubbard WC (1998) Morphology of single ganglion cells in the glaucomatous primate retina. Invest Ophthalmol Vis Sci 39: 2304-2320. Medline.
57. Weinreb RN, Khaw PT (2004) Primary open-angle glaucoma. Lancet 363: 1711-1720. CrossRef Medline.
58. Zhang Y, Stone J (1997) Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38: 1653-1666. Medline.
59. Zhao X, Stafford BK, Godin AL, KingWM, Wong KY (2014) Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J Physiol 592: 1619-1636. CrossRef Medline.