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Long-term cellular and regional specificity of the photoreceptor toxin, iodoacetic acid (IAA), in the rabbit retina

Published online by Cambridge University Press:  28 April 2008

LI LIANG
Affiliation:
Department of Anatomy & Neurobiology, Boston University School of Medicine, Boston, Massachusetts
YOSHIAKI KATAGIRI
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky
LUISA M. FRANCO
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky
YASUYUKI YAMAUCHI
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky Department of Ophthalmology, Tokyo Medical University Hospital, Tokyo, Japan
VOLKER ENZMANN
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky Department of Ophthalmology, Inselspital, University of Bern, Bern, Switzerland
HENRY J. KAPLAN
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky
JULIE H. SANDELL*
Affiliation:
Department of Anatomy & Neurobiology, Boston University School of Medicine, Boston, Massachusetts
*
Address correspondence and reprint requests to: Julie H. Sandell, Department of Anatomy & Neurobiology, Room R-1014, Boston University School of Medicine, 715 Albany Street, Boston, MA 02118. E-mail: [email protected]

Abstract

This study investigated the anatomical consequences of a photoreceptor toxin, iodoacetic acid (IAA), in the rabbit retina. Retinae were examined 2 weeks, 1, 3, and 6 months after systemic IAA injection. The retinae were processed using standard histological methods to assess the gross morphology and topographical distribution of damage, and by immunohistochemistry to examine specific cell populations in the retina. Degeneration was restricted to the photoreceptors and was most common in the ventral retina and visual streak. In damaged regions, the outer nuclear layer was reduced in thickness or eliminated entirely, with a concomitant loss of immunoreactivity for rhodopsin. However, the magnitude of the effect varied between animals with the same IAA dose and survival time, suggesting individual differences in the bioavailability of the toxin. In all eyes, the inner retina remained intact, as judged by the thickness of the inner nuclear layer, and by the pattern of immunoreactivity for protein kinase C-α (rod bipolar cells) and calbindin D-28 (horizontal cells). Müller cell stalks became immunoreactive for glial fibrillary acidic protein (GFAP) even in IAA-treated retinae that had no signs of cell loss, indicating a response of the retina to the toxin. However, no marked hypertrophy or proliferation of Müller cells was observed with either GFAP or vimentin immunohistochemistry. Thus the selective, long lasting damage to the photoreceptors produced by this toxin did not lead to a reorganization of the surviving cells, at least with survival as long as 6 months, in contrast to the remodeling of the inner retina that is observed in inherited retinal degenerations such as retinitis pigmentosa and retinal injuries such as retinal detachment.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Aonuma, H., Yamazaki, R. & Watanabe, I. (1999). Retinal cell death by light damage. Japanese Journal of Ophthalmology 43, 171179.CrossRefGoogle ScholarPubMed
Ashburn, F.S. Jr., Pilkerton, A.R., Rao, N.A. & Marak, G.E. (1980). The effects of iodate and iodoacetate on the retinal adhesion. Investigative Ophthalmology & Visual Science 19, 14271432.Google ScholarPubMed
Barnstable, C.J. (1980). Monoclonal antibodies which recognize different cell types in the rat retina. Nature 286, 231235.CrossRefGoogle ScholarPubMed
Bringmann, A., Pannicke, T., Grosche, J., Francke, M., Wiedemann, P., Skatchkov, S.N., Osborne, N.N. & Reichenbach, A. (2006). Muller cells in the healthy and diseased retina. Progress in Retinal and Eye Research 25, 397424.CrossRefGoogle ScholarPubMed
Chang, M.L., Wu, C.H., Jiang-Shieh, Y.F., Shieh, J.Y. & Wen, C.Y. (2007). Reactive changes of retinal astrocytes and Muller glial cells in kainate-induced neuroexcitotoxicity. Journal of Anatomy 210, 5465.CrossRefGoogle ScholarPubMed
DiLoreto, D.A. Jr., Martzen, M.R., del Cerro, C., Coleman, P.D. & del Cerro, M. (1995). Muller cell changes precede photoreceptor cell degeneration in the age-related retinal degeneration of the Fischer 344 rat. Brain Research 698, 114.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Sharpe, S.J. (1995). Regional topography of rod and immunocytochemically characterized “blue” and “green” cone photoreceptors in rabbit retina. Visual Neuroscience 12, 11511175.CrossRefGoogle ScholarPubMed
Fariss, R.N., Li, Z.Y. & Milam, A.H. (2000). Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. American Journal of Ophthalmology 129, 215223.CrossRefGoogle ScholarPubMed
Fisher, S.K. & Lewis, G.P. (2003). Muller cell and neuronal remodeling in retinal detachment and reattachment and their potential consequences for visual recovery: A review and reconsideration of recent data. Vision Research 43, 887897.CrossRefGoogle ScholarPubMed
Francke, M., Faude, F., Pannicke, T., Uckermann, O., Weick, M., Wolburg, H., Wiedemann, P., Reichenbach, A., Uhlmann, S. & Bringmann, A. (2005). Glial cell-mediated spread of retinal degeneration during detachment: A hypothesis based upon studies in rabbits. Vision Research 45, 22562267.CrossRefGoogle ScholarPubMed
Franco, L., Yamauchi, Y., Sandell, J., Rizzo, J., Ziv, R., Kaplan, H. & Enzmann, V. (2005). Electrophysiological and anatomical changes in the outer retina after iodoacetic acid injection in the rabbit. Association for Research in Vision and Ophthalmology 46, Abstract 1492.Google Scholar
Gargini, C., Terzibasi, E., Mazzoni, F. & Strettoi, E. (2007). Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: A morphological and ERG study. Journal of Comparative Neurology 500, 222238.CrossRefGoogle Scholar
Humayun, M.S., Prince, M., de Juan, E. Jr., Barron, Y., Moskowitz, M., Klock, I.B. & Milam, A.H. (1999). Morphometric analysis of the extramacular retina from postmortem eyes with retinitis pigmentosa. Investigative Ophthalmology & Visual Science 40, 143148.Google ScholarPubMed
Humayun, M., Sato, Y., Propst, R. & de Juan, E. Jr. (1995). Can potentials from the visual cortex be elicited electrically despite severe retinal degeneration and a markedly reduced electroretinogram? German Journal of Ophthalmology 4, 5764.Google Scholar
Juliusson, B., Bergstrom, A., Rohlich, P., Ehinger, B., van Veen, T. & Szel, A. (1994). Complementary cone fields of the rabbit retina. Investigative Ophthalmology & Visual Science 35, 811818.Google ScholarPubMed
Kohno, H., Sakai, T. & Kitahara, K. (2006). Induction of nestin, Ki-67, and cyclin D1 expression in Muller cells after laser injury in adult rat retina. Graefes Archive for Clinical and Experimental Ophthalmology 244, 9095.CrossRefGoogle ScholarPubMed
Lasansky, A. & De Robertis, E. (1959). Submicroscopic changes in visual cells of the rabbit induced by iodoacetate. Journal of Biophysics and Biochemistry Cytology 5, 245250.CrossRefGoogle ScholarPubMed
Li, Z.Y., Kljavin, I.J. & Milam, A.H. (1995). Rod photoreceptor neurite sprouting in retinitis pigmentosa. Journal of Neuroscience 15, 54295438.CrossRefGoogle ScholarPubMed
Liang, L., Rizzo, J. & Sandell, J. (2007). Chx10 and nestin labelling in retinitis pigmentosa. Investigative Ophthalmology & Visual Science 48, Abstract 3749.Google Scholar
Lyser, K.M., Li, A. & Nunez, M. (1994). Horizontal cells in the rabbit retina: Differentiation of subtypes at neonatal and postnatal stages. International Journal of Developmental Neuroscience 12, 673682.CrossRefGoogle ScholarPubMed
Marc, R.E., Jones, B.W., Watt, C.B. & Strettoi, E. (2003). Neural remodeling in retinal degeneration. Progress in Retinal Eye Research 22, 607655.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269287.CrossRefGoogle ScholarPubMed
McKechnie, N.M. & Foulds, W.S. (1980). Recovery of the rabbit retina after light damage (preliminary observations). Graefes Archive for Clinical and Experimental Ophthalmology 212, 271283.CrossRefGoogle ScholarPubMed
Milam, A.H., Li, Z.Y. & Fariss, R.N. (1998). Histopathology of the human retina in retinitis pigmentosa. Progress in Retinal Eye Research 17, 175205.Google ScholarPubMed
Nakajima, M., Yuge, K., Senzaki, H., Shikata, N., Miki, H., Uyama, M. & Tsubura, A. (1996). Photoreceptor apoptosis induced by a single systemic administration of N-methyl-N-nitrosourea in the rat retina. American Journal of Pathology 148, 631641.Google ScholarPubMed
Noell, W.K. (1951). The effect of iodoacetate on the vertebrate retina. Journal of Cell Physiology 37, 283307.CrossRefGoogle ScholarPubMed
Noell, W.K. (1953). Experimentally induced toxic effects on structure and function of visual cells and pigment epithelium. American Journal of Ophthalmology 36, 103116.CrossRefGoogle ScholarPubMed
Noell, W.K., Walker, V.S., Kang, B.S. & Berman, S. (1966). Retinal damage by light in rats. Investigative Ophthalmology & Visual Science 5, 450473.Google ScholarPubMed
Nork, T.M., Kim, C.B., Shanmuganayagam, D., Van Lysel, M.S., Ver Hoeve, J.N. & Folts, J.D. (2006). Measurement of regional choroidal blood flow in rabbits and monkeys using fluorescent microspheres. Archive of Ophthalmology 124, 860868.CrossRefGoogle ScholarPubMed
Orzalesi, N., Calabria, G.A. & Grignolo, A. (1970). Experimental degeneration of the rabbit retina induced by iodoacetic acid. A study of the ultrastructure, the rhodopsin cycle and the uptake of 14C-labeled iodoacetic acid. Experimental Eye Research 9, 246253.CrossRefGoogle ScholarPubMed
O'Steen, W.K., Shear, C.R. & Anderson, K.V. (1972). Retinal damage after prolonged exposure to visible light. A light and electron microscopic study. American Journal of Anatomy 134, 521.CrossRefGoogle ScholarPubMed
Pagon, R.A. (1988). Retinitis pigmentosa. Survey of Ophthalmology 33, 137177.CrossRefGoogle ScholarPubMed
Peichl, L. & Bolz, J. (1984). Kainic acid induces sprouting of retinal neurons. Science 223, 503504.CrossRefGoogle ScholarPubMed
Robinson, S.R. & Dreher, Z. (1990). Muller cells in adult rabbit retinae: Morphology, distribution and implications for function and development. Journal of Comparative Neurology 292, 178192.CrossRefGoogle ScholarPubMed
Roof, D.J., Adamian, M. & Hayes, A. (1994). Rhodopsin accumulation at abnormal sites in retinas of mice with a human P23H rhodopsin transgene. Investigative Ophthalmology & Visual Science 35, 40494062.Google ScholarPubMed
Santos, A., Humayun, M.S., de Juan, E. Jr., Greenburg, R.J., Marsh, M.J., Klock, I.B. & Milam, A.H. (1997). Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Archive of Ophthalmology 115, 511515.CrossRefGoogle ScholarPubMed
Schnitzer, J. (1985). Distribution and immunoreactivity of glia in the retina of the rabbit. Journal of Comparative Neurology 240, 128142.CrossRefGoogle ScholarPubMed
Seiler, M.J., Liu, O.L., Cooper, N.G., Callahan, T.L., Petry, H.M. & Aramant, R.B. (2000). Selective photoreceptor damage in albino rats using continuous blue light. A protocol useful for retinal degeneration and transplantation research. Graefes Archive for Clinical and Experimental Ophthalmology 238, 599607.CrossRefGoogle ScholarPubMed
Strettoi, E. & Pignatelli, V. (2000). Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proceedings of the National Academy of Science USA 97, 1102011025.CrossRefGoogle Scholar
Tyler, N.K. & Burns, M.S. (1991). Alterations in glial cell morphology and glial fibrillary acidic protein expression in urethane-induced retinopathy. Investigative Ophthalmology & Visual Science 32, 246256.Google ScholarPubMed
Wasowicz, M., Morice, C., Ferrari, P., Callebert, J. & Versaux-Botteri, C. (2002). Long-term effects of light damage on the retina of albino and pigmented rats. Investigative Ophthalmology & Visual Science 43, 813820.Google ScholarPubMed
Winkler, B.S., Sauer, M.W. & Starnes, C.A. (2003). Modulation of the Pasteur effect in retinal cells: Implications for understanding compensatory metabolic mechanisms. Experimental Eye Research 76, 715723.CrossRefGoogle ScholarPubMed
Yu, D.Y. & Cringle, S.J. (2005). Retinal degeneration and local oxygen metabolism. Experimental Eye Research 80, 745751.CrossRefGoogle ScholarPubMed