Alterations in photoreceptor-bipolar cell signaling following ischemia/reperfusion in the rat retina

Journal of Comparative Neurology

Volumn 505, Issue 1, 2007, Pages 131-146

  Sun, Daniel ^a   Bui, Bang V ^b   Vingrys, Algis J ^b   Kalloniatis, Michael ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

AGB; Agmatine; AII amacrine cells; B wave; Cholinergic amacrine cells; Electroretinogram; Glutamate; Metabotropic glutamate receptors; Neurochemical truth point; Oscillatory potentials

Indexed keywords

2 AMINO 4 PHOSPHONOBUTYRIC ACID; AGMATINE; CATION CHANNEL; GLUTAMATE RECEPTOR; GLUTAMIC ACID; METABOTROPIC RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; BRAIN NERVE CELL; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL POPULATION; CELL SUBPOPULATION; CONTROLLED STUDY; ELECTRORETINOGRAM; MOLECULAR PROBE; NEUROCHEMISTRY; NONHUMAN; OSCILLATORY POTENTIAL; PHOTORECEPTOR; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RAT; RECEPTOR SENSITIVITY; REPERFUSION; RETINA; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA ISCHEMIA; RETINA NERVE CELL; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; ELECTRORETINOGRAPHY; NERVE TISSUE PROTEINS; PHOTORECEPTORS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RETINA; RETINAL BIPOLAR CELLS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 35948986794     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21470     Document Type: Article

References (116)

1. Ames A 3rd, Li YY. 1992. Energy requirements of glutamatergic pathways in rabbit retina. J Neurosci 12:4234-4242.
2. Attwell D, Laughlin SB. 2001. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
3. Barnett NL, Grozdanic SD. 2004. Glutamate transporter localization does not correspond to the temporary functional recovery and late degeneration after acute ocular ischemia in rats. Exp Eye Res 79:513-524.
4. Barnett NL, Osborne NN. 1995. Prolonged bilateral carotid artery occlusion induces electrophysiological and immunohistochemical changes to the rat retina without causing histological damage. Exp Eye Res 61:83-90.
5. Barnett NL, Pow DV, Robinson SR. 2000. Inhibition of Muller cell glutamine synthetase rapidly impairs the retinal response to light. Glia 30:64-73.
6. Bayer AU, Danias J, Brodie S, Maag KP, Chen B, Shen F, Podos SM, Mittag TW. 2001. Electroretinographic abnormalities in a rat glaucoma model with chronic elevated intraocular pressure. Exp Eye Res 72:667-677.
7. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ. 1994. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14:4368-4374.
8. Birch DG, Hood DC, Nusinowitz S, Pepperberg DR. 1995. Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Invest Ophthalmol Vis Sci 36:1603-1614.
9. Block F, Schwarz M. 1998. The b-wave of the electroretinogram as an index of retinal ischemia. Gen Pharmacol 30:281-287.
10. Block F, Schwarz M, Sontag KH. 1992. Retinal ischemia induced by occlusion of both common carotid arteries in rats as demonstrated by electroretinography. Neurosci Lett 144:124-126.
11. Brunette JR, Olivier P, Zaharia M, Blondeau P, Lafond G. 1986. Rod-cone differences in response to retinal ischemia in rabbit. Doc Ophthalmol 63:359-365.
12. Buchi ER. 1992a. Cell death in the rat retina after a pressure-induced ischemia-reperfusion insult: an electron microscopic study. I. Ganglion cell layer and inner nuclear layer. Exp Eye Res 55:605-613.
13. Buchi ER. 1992b. Cell death in rat retina after pressure-induced ischemia-reperfusion insult: electron microscopic study. II. Outer nuclear layer. Jpn J Ophthalmol 36:62-68.
14. Buchi ER, Suivaizdis I, Fu J. 1991. Pressure-induced retinal ischemia in rats: an experimental model for quantitative study. Ophthalmologica 203:138-147.
15. Bui BV, Fortune B. 2004. Ganglion cell contributions to the rat full-field electroretinogram. J Physiol 555(Pt 1):153-173.
16. Bui BV, Armitage JA, Vingrys AJ. 2002. Extraction and modeling of oscillatory potentials. Doc Ophthalmol 104:17-36.
17. Bui BV, Kalloniatis M, Vingrys AJ. 2004a. Retinal function loss after monocarboxylate transport inhibition. Invest Ophthalmol Vis Sci 45:584-593.
18. Bui BV, Vingrys AJ, Kalloniatis M. 2004b. Monocarboxylate transport inhibition alters retinal function and cellular amino acid levels. Eur J Neurosci 20:1525-1537.
19. 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.
20. Bush RA, Sieving PA. 1994. A proximal retinal component in the primate photopic ERG a-wave. Invest Ophthalmol Vis Sci 35:635-645.
21. Chen H, Wu D, Huang S, Yan H. 2006. The photopic negative response of the flash electroretinogram in retinal vein occlusion. Doc Ophthalmol 113:53-59.
22. Chiao CC, Masland RH. 2002. Starburst cells nondirectionally facilitate the responses of direction-selective retinal ganglion cells. J Neurosci 22:10509-10513.
23. Chua J, Fletcher EL, Kalloniatis M. 2007. AMPA/Kainate activates depolarizing cone bipolar cells in the rdl mouse retina. Invest Ophthalmol Vis Sci 48:1346 E-Abstract.
24. Dijk F, Kamphuis W. 2004a. Ischemia-induced alterations of AMPA-type glutamate receptor subunit. Expression patterns in the rat retina - an immunocytochemical study. Brain Res 997:207-221.
25. Dijk F, Kamphuis W. 2004b. An immunocytochemical study on specific amacrine cell subpopulations in the rat retina after ischemia. Brain Res 1026:205-217.
26. Dijk F, Leeuwen SV, Kamphuis W. 2004a. Differential effects of ischemia/reperfusion on amacrine cell subtype-specific transcript levels in the rat retina. Brain Res 1026:194-204.
27. Dijk F, Kraal-Muller E, Kamphuis W. 2004b. Ischemia-induced changes of AMPA-type glutamate receptor subunit expression pattern in the rat retina: a real-time quantitative PCR study. Invest Ophthalmol Vis Sci 45:330-341.
28. Dureau P, Bonnel S, Menasche M, Dufier JL, Abitbol M. 2001. Quantitative analysis of intravitreal injections in the rat. Curr Eye Res 22:74-77.
29. Edwards JG, Michel WC. 2002. Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. J Comp Neurol 454:294-209.
30. Ekesten B, Gouras P, Moschos M. 1998-1999. Cone properties of the light-adapted murine ERG. Doc Ophthalmol 97:23-31.
31. Euler T, Wässle H. 1995. Immunocytochemical identification of cone bipolar cells in the rat retina. J Comp Neurol 361:461-478.
32. Famiglietti EV. 2002. A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Vis Neurosci 19:145-162.
33. Feghali JG, Jin JC, Odom JV. 1991. Effect of short-term intraocular pressure elevation on the rabbit electroretinogram. Invest Ophthalmol Vis Sci 32:2184-2189.
34. Friedburg C, Allen CP, Mason PJ, Lamb TD. 2004. Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J Physiol 556:819-834.
35. Gascon S, Deogracias R, Sobrado M, Roda JM, Renart J, Rodriguez-Pena A, Diaz-Gierra M. 2005. Transcription of the NR1 subunit of the N-methyl-D-aspartate receptor is down-regulated by excitotoxic stimulation and cerebral ischemia. J Biol Chem 280:35018-35027.
36. Gehlbach PL, Purple RL. 1994. A paired comparison of two models of experimental retinal ischemia. Curr Eye Res 13:597-602.
37. Ghosh KK, Haverkamp S, Wässle H. 2001. Glutamate receptors in the rod pathway of the mammalian retina. J Neurosci 21:8636-8647.
38. Goebel DJ, Poosch MS. 2001. Transient down-regulation of NMDA receptor subunit gene expression in the rat retina following NMDA-induced neurotoxicity is attenuated in the presence of the non-competitive NMDA receptor antagonist MK-801. Exp Eye Res 72:547-558.
39. Granit R. 1933. Components of the retinal action potential in mammals and their relations to the discharge in the optic nerve. J Physiol 77:207-238.
40. Green DG, Kapousta-Bruneau NV. 1999. A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs. Vis Neurosci 16:727-741.
41. Greferath U, Grünert U, Wässle H. 1990. Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 301:433-442.
42. Gurevich L, Slaughter MM. 1993. Comparison of the wave-forms of the on bipolar neuron and the b-wave of the electroretinogram. Vison Res 33:2431-2435.
43. Hamano K, Kiyama H, Emson PC, Manabe R, Nakauchi M, Tohyama M. 1990. Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina. J Comp Neurol 302:417-424.
44. Hayreh SS, Klugman MR, Podhajsky P, Kolder HE. 1989. Electroretinography in central retinal vein occlusion. Graefe's Arch Clin Exp Ophthalmol 227:549-561.
45. Hood DC, Birch DG. 1992. A computational model of the amplitude and implicit time of the b-wave of the human ERG. Vis Neurosci 8:107-126.
46. Hood DC, Birch DG. 1993. Human cone receptor activity: the leading edge of the a-wave and models of receptor activity. Vis Neurosci 10:857-871.
47. Hood DC, Birch DG. 1996. Assessing abnormal rod photoreceptor activity with the a-wave of the electroretinogram: application and methods. Doc Ophthalmol 92:253-267.
48. Hsueh YP, Sheng M. 1998. Anchoring of glutamate receptors at the synapse. Prog Brain Res 116:123-131.
49. Hughes A. 1979. A schematic eye for the rat. Vision Res 19:569-588.
50. Hughes WF. 1991. Quantitation of ischemic damage in the rat retina. Exp Eye Res 53:573-582.
51. Jakobs TC, Libby RT, Ben Y, John SWM, Masland R. 2005. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 171:313-325.
52. Johnson MA, Hood DC. 1996. Rod photoreceptor transduction is affected in central retinal vein occlusion associated with iris neovascularization. J Opt Soc Am 13:572-576.
53. Johnson MA, McPhee TJ. 1993. Electroretinographic findings in iris neovascularization due to acute central retinal vein occlusion. Arch Ophthalmol 111:806-814.
54. Johnson MA, Marcus S, Elman MJ, McPhee TJ. 1988. Neovascularization in central retinal vein occlusion. Electroretinographic findings. Arch Ophthalmol 106:348-352.
55. Johnson MA, Procope J, Quinlan P. 1990. Electroretinographic oscillatory potentials and their role in predicting treatable complications in patients with central retinal vein occlusion. Opt Soc Am Techn Dig 3:62-65.
56. Ju WK, Kim KY, Hofman HD, Kim IB, Lee MY, Oh SJ, Chun MH. 2000. Selective neuronal survival and upregulation of PCNA in the rat inner retina following transient ischemia. J Neuropathol Exp Neurol 59:241-250.
57. Junk AK, Mammis A, Savitz SI, Singh M, Roth S, Malhotra S, Rosenbaum PS, Cerami A, Brines M, Rosenbaum DM. 2002. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci U S A 99:10659-10664.
58. Kalloniatis M, Sun D, Foster L, Haverkamp S, Wässle H. 2004. Localization of NMDA receptor subunits and mapping NMDA drive within the mammalian retina. Vis Neurosci 21:587-597.
59. Kamboj S, Huganir RL. 1998. Receptor clustering: activate to accumulate? Curr Biol 8:R719-721.
60. Katai N, Yoshimura N. 1999. Apoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases. Invest Ophthalmol Vis Sci 40:2697-2705.
61. Kergoat H, Lovasik JV. 1990. The effects of altered retinal vascular perfusion pressure on the white flash scotopic ERG and oscillatory potentials in man. Electroencephalogr Clin Neurophysiol 75:306-322.
62. Kuehn MH, Fingert JH, Kwon YH. 2005. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol Clin N Am 18:383-395.
63. Lafuente MP, Villegas-Pérez MP, Selles-Navarro I, Mayor-Torroglosa S, Miralies De Imperial J, Vidal-Sanz M. 2002. Retinal ganglion cell death after acute retinal ischemiais an ongoing process whose severity and duration depends on the duration of the insult. Neuroscience 109:157-168.
64. Lam TT, Abler AS, Tso MO. 1999. Apoptosis and caspases after ischemia-reperfusion injury in rat retina. Invest Ophthalmol Vis Sci 40:967-975.
65. Linn DM, Massey SC. 1991. Acetylcholine release from the rabbit retina mediated by NMDA receptors. J Neurosci 11:123-133.
66. Lipton P. 1999. Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568.
67. Liu S, Lau L, Wei J, Zhu D, Zou S, Sun HS, Fu Y, Liu F, Lu Y. 2004. Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43:43-55.
68. Lyubarsky AL, Pugh EN Jr. 1996. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci 16:563-571.
69. Machida S, Gotoh Y, Tanaka M, Tazawa Y. 2004. Predominant loss of the photopic negative response in central retinal artery occlusion. Am J Ophthalmol 137:938-940.
70. Marc RE. 1999a. Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. J Comp Neurol 407:47-64.
71. Marc RE. 1999b. Kainate activation of horizontal, bipolar, amacrine, and ganglion cells in the rabbit retina. J Comp Neurol 407:65-76.
72. Marc RE, Liu WL, Kalloniatis M, Raiguel SF, van Haesendonck E. 1990. Patterns of glutamate immunoreactivity in the goldfish retina. J Neurosci 10:4006-4034.
73. Marc RE, Basinger SF, Murry RF. 1995. Pattern recognition of amino acid signatures in retinal neurons. J Neurosci 15:5106-5129.
74. Marc RE, Kalloniatis M, Jones BW. 2005. Excitation mapping with the organic cation AGB2+. Vision Res 45:3454-3468.
75. Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH, Wensel T, Lucas RJ. 2007. Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci 48:3364-3371.
76. Matute C, Streit P. 1986. Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry 86:147-157.
77. Moon JI, Kim IB, Gwon JS, Park MH, Kang TH, Lim EJ, Choi KR, Chun MH. 2005. Changes in retinal neuronal populations in the DBA/2J mice. Cell Tissue Res 320:51-59.
78. Morkve SH, Veruki ML, Hartveit E. 2002. Functional characteristics of non-NMDA-type ionotropic glutamate receptor channel in AII amacrine cells in rat retina. J Physiol 542:147-165.
79. Naarendorp F, Sato Y, Cajdric A, Hubbard NP. 2001. Absolute and relative sensitivity of the scotopic system of rat: electroretinography and behaviour. Vis Neurosci 18:641-656.
80. Nakatani K, Yau KW. 1988. Calcium and light adaptation in retinal rods and cones. Nature 334:69-71.
81. Nawy S. 1999. The metabotropic receptor mGluR6 may signal through G(o), but not phosphodiesterase, in retinal bipolar cells. J Neurosci 19:2938-2944.
82. Nickells RW. 1996. Retinal ganglion cell death in glaucoma: the how, the why, and the maybe. J Glaucoma 5:345-356.
83. Nixon PJ, Bui BV, Armitage JA, Vingrys AJ. 2001. The contribution of cone responses to rat electroretinograms. Clin Experiment Ophthalmol 29:193-196.
84. Noh KM, Yokota H, Mashiko T, Castillo PE, Zukin RS, Bennett MV. 2005. Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc Natl Acad Sci U S A 102:12230-12235.
85. Opitz T, Grooms SY, Bennett MV, Zukin RS. 2000. Remodeling of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia. Proc Natl Acad Sci U S A 97:13360-13365.
86. Osborne NN, Larsen A, Barnett NL. 1995. Influence of excitatory amino acids and ischemia on rat retinal choline acetyltransferase-containing cells. Invest Ophthalmol Vis Sci 36:1692-1700.
87. Osborne NN, Casson RJ, Wood JP, Chidlow G, Graham M, Melena J. 2004. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Ret Eye Res 23:91-147.
88. Parker PJ, Coussens L, Totty N, Rhee L, Young S, Chen E, Stabel S, Waterfield MD, Ulrich A. 1986. The complete primary structure of protein kinase C - the major phorbol ester receptor. Science 233:853-859.
89. Paschen W, Schmitt J, Uto A. 1996. RNA editing of glutamate receptor subunits GluR2, GluR5 and GluR6 in transient cerebral ischemia in the rat. J Cereb Blood Flow Metab 16:548-556.
90. Pasteels B, Rogers J, Blachier F, Pochet R. 1990. Calbindin and calretinin localization in retina from different species. Vis Neurosci 5:1-16.
91. Peichl L, Gonzalez-Soriano J. 1994. Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis Neurosci 11:501-517.
92. Peng PL, Zhong X, Tu W, Soundarapandian MM, Molner P, Zhu D, Lau L, Liu S, Liu F, Lu Y. 2006. ADAR-2 dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49:719-733.
93. Pepperberg DR, Birch DG, Hood DC. 1997. Photoresponses of human rods in vivo derived from paired-flash electroretinograms. Vis Neurosci 14:73-82.
94. Phipps JA, Fletcher EL, Vingrys AJ. 2004. Paired-flash identification of rod and cone dysfunction in the diabetic rat. Invest Ophthalmol Vis Sci 45:4592-4600.
95. Quigley HA. 1999. Neuronal death in glaucoma. Prog Ret Eye Res 18:39-57.
96. Rosenbaum DM, Rosenbaum PS, Singh M, Gupta G, Gupta H, Li B, Roth S. 2001. Functional and morphological comparison of two methods to produce transient retinal ischemia in the rat. J Neuroophthalmol 21:62-68.
97. Sabates R, Hirose T, McMeel JW. 1983. Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol 101:232-235.
98. Selles-Navarro I, Villegas-Perez MP, Salvador-Silva M, Ruiz-Gomez JM, Vidal-Sanz M. 1996. Retinal ganglion cell death after different transient periods of pressure-induced ischemia and survival intervals. A quantitative in vivo study. Invest Ophthalmol Vis Sci 37:2002-2014.
99. Strettoi E, Pignatelli V. 2000. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc Natl Acad Sci U S A 97:11020-11025.
100. Sun D, Kalloniatis M. 2006. Mapping glutamate responses in immunocytochemically identified neurons of the mouse retina. J Comp Neurol 494:686-703.
101. Sun D, Rait JL, Kalloniatis M. 2003. Inner retinal neurons display differential responses to N-methyl-D-aspartate receptor activation. J Comp Neurol 465:38-56.
102. Sun D, Vingrys AJ, Kalloniatis M. 2007a. Metabolic and functional profiling of the normal rat retina. J Comp Neurol 505:92-113.
103. Sun D, Vingrys AJ, Kalloniatis M. 2007b. Metabolic and functional profiling of the ischemic/reperfused rat retina. J Comp Neurol 505:114-130.
104. Szabo ME, Droy-Lefaix MT, Doly M, Carre C, Braquet P. 1991. Ischemia and reperfusion-induced histologic changes in the rat retina. Invest Ophthalmol Vis Sci 32:1471-1478.
105. Takahashi T, Machida S, Masuda T, Mukaida Y, Tazawa Y. 2005. Functional changes in rod and cone pathways after photoreceptor loss in light-damaged rats. Curr Eye Res 30:703-713.
106. Tanimoto N, Usui T, Ichibe M, Takagi M, Suzuki K, Hasegawa S, Abe H. 2005. Rod and cone a-waves in central retinal vein occlusion. Jpn J Ophthalmol 49:402-410.
107. Tormene AP, Doro D, Mantovani E, Fabris S, Moro F. 1989. Electrophysiological findings in anterior ischemic optic neuropathy. Metab Pediatr Syst Ophthalmol 12:76-79.
108. Usami E. 1967. Studies on ERG of occlusion of the retinal artery and vein especially on the prognostic value. Acta Soc Ophthalmol Jpn 71:39-45.
109. Vardi N. 1998. Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells. J Comp Neurol 395:43-52.
110. Vardi N, Matesic DF, Manning DR, Liebman PA, Sterling P. 1993. Identification of a G-protein in depolarizing rod bipolar cells. Vis Neurosci 10:473-478.
111. Voigt T. 1986. Cholinergic amacrine cells in the rat retina. J Comp Neurol 248:19-35.
112. Wachtmeister L. 1998. Oscillatory potentials in the retina: what do they reveal. Prog Ret Eye Res 17:485-521.
113. Wässle H, Grünert U, Rohrenbeck J. 1993. Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. J Comp Neurol 332:407-420.
114. Winkler BS, Kapousta-Bruneau N, Arnold MJ, Green DG. 1999. Effects of inhibiting glutamine synthetase and blocking glutamate uptake on b-wave generation in the isolated rat retina. Vis Neurosci 16:345-353.
115. Young S, Rothbard J, Parker PJ. 1988. A monoclonal antibody recognizing the site of limited proteolysis of protein kinase C. Eur J Biochem 173:247-252.
116. Zhou ZJ, Fain GL. 1995. Neurotransmitter receptors of starburst amacrine cells in the rabbit retinal slices. J Neurosci 15:5334-5345.