Differential progression of structural and functional alterations in distinct retinal ganglion cell types in a mouse model of glaucoma

Journal of Neuroscience

Volumn 33, Issue 44, 2013, Pages 17444-17457

  Santina, Luca Della ^a   Inman, Denise M ^a   Lupien, Caroline B ^a   Horner, Philip J ^a   Wong, Rachel O L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSTYRENE; TRANSCRIPTION FACTOR POU4F1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DENSITY; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; FEMALE; GLAUCOMA; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; SPIKE WAVE; SYNAPSE; VISUAL FIELD DEFECT; VISUAL SYSTEM FUNCTION; VISUAL THRESHOLD;

ACTION POTENTIALS; ANIMALS; CELL DEATH; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GLAUCOMA; INTRAOCULAR PRESSURE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, INVERTEBRATE; RANDOM ALLOCATION; RETINAL GANGLION CELLS;

EID: 84886678112     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5461-12.2013     Document Type: Article

References (74)

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. Bakalash S, Kipnis J, Yoles E, Schwartz M (2002) Resistance of retinal gan glion cells to an increase in intraocular pressure is immune-dependent. Invest Ophthalmol Vis Sci 43:2648-2653. Medline
3. Baltan S, Inman DM, Danilov CA, Morrison RS, Calkins DJ, Horner PJ (2010) Metabolic vulnerability disposes retinal ganglion cell axons to dysfunction in a model of glaucomatous degeneration. J Neurosci 30: 5644-5652. CrossRef Medline
4. Ben Simon GJ, Bakalash S, Aloni E, Rosner M (2006) A rat model for acute rise in intraocular pressure: immune modulation as a therapeutic strat-egy. Am J Ophthalmol 141:1105-1111. CrossRef Medline
5. 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
6. Calkins DJ (2012) Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog Retin Eye Res 31:702-719. CrossRef Medline
7. Calkins DJ, Horner PJ (2012) The cell and molecular biology of glaucoma: axonopathy and the brain. Invest Ophthalmol Vis Sci 53:2482-2484. CrossRef Medline
8. Cantrell DR, Cang J, Troy JB, Liu X (2010) Non-centered spike-triggered covariance analysis reveals neurotrophin-3 as a developmental regulator of receptive field properties of ON-OFF retinal ganglion cells. PLoS Com-put Biol 6:e1000967. CrossRef Medline
9. 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
10. Cheng JW, Cai JP, Wei RL (2009) Meta-analysis of medical intervention for normal tension glaucoma. Ophthalmology 116:1243-1249. CrossRef Medline
11. Chichilnisky EJ (2001) A simple white noise analysis of neuronal light responses. Network 12:199-213. CrossRef Medline
12. Cleland BG, Levick WR, Wässle H (1975) Physiological identification of a morphological class of cat retinal ganglion cells. J Physiol 248:151-171. Medline
13. 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
14. Crook JD, Peterson BB, Packer OS, Robinson FR, Troy JB, Dacey DM (2008) Y-cell receptive field and collicular projection of parasol ganglion cells in macaque monkey retina. J Neurosci 28:11277-11291. CrossRef Medline
15. Cuenca N, Pinilla I, Fernández-Sánchez L, Salinas-Navarro M, Alarcón-Martínez L, Avilés-Trigueros M, de la Villa P, Miralles de Imperial J, Villegas-Pérez MP, Vidal-Sanz M (2010) Changes in the inner and outer retinal layers after acute increase of the intraocular pressure in adult albino Swiss mice. Exp Eye Res 91:273-285. CrossRef Medline
16. Demas J, Eglen SJ, Wong RO (2003) Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. J Neurosci 23:2851-2860. Medline
17. Demb JB, Zaghloul K, Haarsma L, Sterling P (2001) Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J Neurosci 21:7447-7454. Medline
18. Devries SH, Baylor DA (1997) Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J Neurophysiol 78:2048-2060. Medline
19. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51. CrossRef Medline
20. 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
21. Fortune B, Burgoyne CF, Cull GA, Reynaud J, Wang L (2012) Structural and functional abnormalities of retinal ganglion cells measured in vivo at the onset of optic nerve head surface change in experimental glaucoma. Invest Ophthalmol Vis Sci 53:393-3950. 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. Fu CT, Sretavan D (2010) Laser-induced ocular hypertension in albino CD-1 mice. Invest Ophthalmol Vis Sci 51:980-990. CrossRef Medline
24. Harada C, Namekata K, Guo X, Yoshida H, Mitamura Y, Matsumoto Y, Tanaka K, Ichijo H, Harada T (2010) ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell Death Differ 17:1751-1759. CrossRef Medline
25. Heiduschka P, Julien S, Schuettauf F, Schnichels S (2010) Loss of retinal function in aged DBA/2J mice-New insights into retinal neurodegeneration. Exp Eye Res 91:779-783. CrossRef Medline
26. Heijl A, Leske MC, Bengtsson B, Hyman L, Bengtsson B, Hussein M, Early Manifest Glaucoma Trial Group (2002) Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 120:1268-1279. CrossRef Medline
27. Howell GR, Libby RT, Jakobs TC, Smith RS, Phalan FC, Barter JW, Barbay JM, Marchant JK, Mahesh N, Porciatti V, Whitmore AV, Masland RH, John SW (2007) Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J Cell Biol 179:1523-1537. CrossRef Medline
28. 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. CrossRef Medline
29. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936-8946. Medline
30. 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
31. Kerschensteiner D, Liu H, Cheng CW, Demas J, Cheng SH, Hui CC, Chow RL, Wong RO (2008) Genetic control of circuit function: Vsx1 and Irx5 transcription factors regulate contrast adaptation in the mouse retina. J Neurosci 28:2342-2352. CrossRef Medline
32. Koehler CL, Akimov NP, Rentería RC (2011) Receptive field center size decreases and firing properties mature in ON and OFF retinal ganglion cells after eye opening in the mouse. J Neurophysiol 106:895-904. CrossRef Medline
33. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, Viola KL, Klein WL (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27:796-807. CrossRef Medline
34. Longair MH, Baker DA, Armstrong JD (2011) Simple Neurite Tracer: open source software for reconstruction, visualization and analysis of neuronal processes. Bioinformatics 27:2453-2454. CrossRef Medline
35. Luan L, Ren C, Lau BW, Yang J, Pickard GE, So KF, Pu M (2011) Y-like retinal ganglion cells innervate the dorsal raphe nucleus in the Mongolian gerbil (Meriones unguiculatus). PLoS ONE 6:e18938. CrossRef Medline
36. Luo X, Patel NB, Harwerth RS, Frishman LJ (2011) Loss of the low-frequency component of the global-flash multifocal electroretinogram in primate eyes with experimental glaucoma. Invest Ophthalmol Vis Sci 52:3792-3804. CrossRef Medline
37. Margolis DJ, Detwiler PB (2007) Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells. J Neurosci 27:5994-6005. CrossRef Medline
38. Margolis DJ, Detwiler PB (2011) Cellular origin of spontaneous ganglion cell spike activity in animal models of retinitis pigmentosa. J Ophthalmol pii: 507037. Medline
39. Margolis DJ, Gartland AJ, Euler T, Detwiler PB (2010) Dendritic calcium signaling in ON and OFF mouse retinal ganglion cells. J Neurosci 30: 7127-7138. CrossRef Medline
40. Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4:877-886. CrossRef Medline
41. Mattson DL (2001) Comparison of arterial blood pressure in different strains of mice. Am J Hypertens 14:405-408. CrossRef Medline
42. McKinnon SJ, Schlamp CL, Nickells RW (2009) Mouse models of retinal ganglion cell death and glaucoma. Exp Eye Res 88:816-824. CrossRef Medline
43. Morgan JL, Schubert T, Wong RO (2008) Developmental patterning of glutamatergic synapses onto retinal ganglion cells. Neural Dev 3:8. CrossRef Medline
44. Murphy GJ, Rieke F (2006) Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52:511-524. CrossRef Medline
45. Nadal-Nicolás FM, Jiménez-López M, Sobrado-Calvo P, Nieto-López L, Cánovas-Martínez I, Salinas-Navarro M, Vidal-Sanz M, Agudo M (2009) Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50:3860-3868. CrossRef Medline
46. Pang IH, Clark AF (2007) Rodent models for glaucoma retinopathy and optic neuropathy. J Glaucoma 16:483-505. CrossRef Medline
47. 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
48. Pascolini D, Mariotti SP (2012) Global estimates of visual impairment: 2010. Br J Ophthalmol 96:614-618. CrossRef Medline
49. 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
50. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45:4611-4616. CrossRef Medline
51. Rangarajan KV, Lawhn-Heath C, Feng L, Kim TS, Cang J, Liu X (2011) Detection of visual deficits in aging DBA/2J mice by two behavioral assays. Curr Eye Res 36:481-491. CrossRef Medline
52. Rasmussen CA, Kaufman PL (2005) Primate glaucoma models. J Glaucoma 14:311-314. CrossRef Medline
53. Ryskamp DA, Witkovsky P, Barabas P, Huang W, Koehler C, Akimov NP, Lee SH, Chauhan S, Xing W, Rentería RC, Liedtke W, Krizaj D (2011) The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci 31:7089-7101. CrossRef Medline
54. Saleh M, Nagaraju M, Porciatti V (2007) Longitudinal evaluation of retinal ganglion cell function and IOP in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 48:4564-4572. CrossRef Medline
55. Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66:15-36. CrossRef Medline
56. 2 with exposure to hydrostatic pressure. Invest Ophthalmol Vis Sci 50:717-728. Medline
57. 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
58. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. CrossRef Medline
59. Scholz M, Buder T, Seeber S, Adamek E, Becker CM, Lutjen-Drecoll E (2008) Dependency of intraocular pressure elevation and glaucomatous changes in DBA/2J and DBA/2J-Rj mice. Invest Ophthalmol Vis Sci 49:613-621. CrossRef Medline
60. Segev R, Puchalla J, Berry MJ 2nd (2006) Functional organization of ganglion cells in the salamander retina. J Neurophysiol 95:2277-2292. Medline
61. Sekirnjak C, Jepson LH, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ (2011) Changes in physiological properties of rat ganglion cells during retinal degeneration. J Neurophysiol 105:2560-2571. CrossRef Medline
62. Shareef SR, Garcia-Valenzuela E, Salierno A, Walsh J, Sharma SC (1995) Chronic ocular hypertension following episcleral venous occlusion in rats. Exp Eye Res 61:379-382. CrossRef Medline
63. Shimazawa M, Nakamura S, Miwa M, Tsuruma K, Aihara M, Nakamura K, Hara H (2013) Establishment of the ocular hypertension model using the common marmoset. Exp Eye Res 111:1-8. CrossRef Medline
64. 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
65. Sommer A (1989) Intraocular pressure and glaucoma. Am J Ophthalmol 107:186-188. Medline
66. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson ED, Steele MR, Inman DM, Vetter ML, Horner PJ, Marsh-Armstrong N (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. CrossRef Medline
67. Stasheff SF, Shankar M, Andrews MP (2011) Developmental time course distinguishes changes in spontaneous and light-evoked retinal ganglion cell activity in rd1 and rd10 mice. J Neurophysiol 105:3002-3009. CrossRef Medline
68. Tian N, Copenhagen DR (2001) Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32:439-449. CrossRef Medline
69. 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. CrossRef Medline
70. van Wyk M, Wässle H, Taylor WR (2009) Receptive field properties of ON-and OFF-ganglion cells in the mouse retina. Vis Neurosci 26:297-308. CrossRef Medline
71. Wässle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757. CrossRef Medline
72. Wax MB, Tezel G, Yang J, Peng G, Patil RV, Agarwal N, Sappington RM, Calkins DJ (2008) Induced autoimmunity to heat shock proteins elicits glaucomatous loss of retinal ganglion cell neurons via activated T-cell-derived fas-ligand. J Neurosci 28:12085-12096. CrossRef Medline
73. 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
74. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, Saido TC, Maeda J, Suhara T, Trojanowski JQ, Lee VM (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53:337-351. CrossRef Medline