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Mapping cation entry in photoreceptors and inner retinal neurons during early degeneration in the P23H-3 rat retina

Published online by Cambridge University Press:  05 April 2013

YUAN ZHU ,
STUTI MISTRA ,
LISA NIVISON-SMITH ,
MONICA L. ACOSTA ,
ERICA L. FLETCHER  and
MICHAEL KALLONIATIS
YUAN ZHU
Affiliation:
School of Optometry and Vision Science, University of New South Wales, Sydney, Australia
STUTI MISTRA
Affiliation:
Department of Optometry and Vision Science, New Zealand National Eye Centre, University of Auckland, Auckland, New Zealand
LISA NIVISON-SMITH
Affiliation:
School of Optometry and Vision Science, University of New South Wales, Sydney, Australia
MONICA L. ACOSTA
Affiliation:
Department of Optometry and Vision Science, New Zealand National Eye Centre, University of Auckland, Auckland, New Zealand
ERICA L. FLETCHER
Affiliation:
Department of Anatomy and Neuroscience, The University of Melbourne, Melbourne, Australia
MICHAEL KALLONIATIS*
Affiliation:
School of Optometry and Vision Science, University of New South Wales, Sydney, Australia Department of Optometry and Vision Science, New Zealand National Eye Centre, University of Auckland, Auckland, New Zealand Department of Anatomy and Neuroscience, The University of Melbourne, Melbourne, Australia Centre for Eye Health, University of New South Wales, Sydney, Australia
*
*Address correspondence to: Prof. Michael Kalloniatis, Centre for Eye Health, University of New South Wales, Sydney 2052, NSW, Australia. E-mail: [email protected]
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Abstract

The proline-23-histidine line 3 (P23H-3) transgenic rat carries a human opsin gene mutation leading to progressive photoreceptor loss characteristic of human autosomal dominant retinitis pigmentosa. The aim of the present study was to evaluate neurochemical modifications in the P23H-3 retina as a function of development and degeneration. Specifically, we investigated the ion channel permeability of photoreceptors by tracking an organic cation, agmatine (1-amino-4-guanidobutane, AGB), which permeates through nonspecific cation channels. We also investigated the activity of ionotropic glutamate receptors in distinct populations of bipolar, amacrine, and ganglion cells using AGB tracking in combination with macromolecular markers. We found elevated cation channel permeation in photoreceptors as early as postnatal day 12 (P12) suggesting that AGB labeling is an early indicator of impending photoreceptor degeneration. However, bipolar, amacrine, or ganglion cells displayed normal responses secondary to ionotropic glutamate receptor activation even at P138 when about one half of the photoreceptor layer was lost and apoptosis and gliosis were observed. These results suggest that possible therapeutic windows as downstream neurons in inner retina appear to retain normal function with regard to AGB permeation when photoreceptors are significantly reduced but not lost.

Keywords

AgmatineAGBTUNELRemodelingCell markerImmunocytochemistryPKCαIslet-1CalretininParvalbuminRetinitis pigmentosa
Type
Research Articles
Information
Visual Neuroscience , Volume 30 , Issue 3 , May 2013 , pp. 65 - 75
Copyright
Copyright © Cambridge University Press 2013 

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References

Acosta, M.L., Bumsted O’Brien, K.M., Tan, S.S. & Kalloniatis, M. (2008). Emergence of cellular markers and functional ionotropic glutamate receptors on tangentially dispersed cells in the developing mouse retina. The Journal of Comparative Neurology 506, 506–523.CrossRefGoogle ScholarPubMed
Acosta, M.L., Chua, J. & Kalloniatis, M. (2007). Functional activation of glutamate ionotropic receptors in the developing mouse retina. The Journal of Comparative Neurology 500, 923–941.CrossRefGoogle ScholarPubMed
Acosta, M.L., Fletcher, E.L., Azizoglu, S., Foster, L.E., Farber, D.B. & Kalloniatis, M. (2005). Early markers of retinal degeneration in rd/rd mice. Molecular Vision 11, 717–728.Google ScholarPubMed
Acosta, M.L., Shin, Y.S., Ready, S., Fletcher, E.L., Christie, D.L. & Kalloniatis, M. (2010). Retinal metabolic state of the proline-23-histidine rat model of retinitis pigmentosa. American Journal of Physiology. Cell Physiology 298, C764–C774.CrossRefGoogle ScholarPubMed
Aleman, T.S., LaVail, M.M., Montemayor, R., Ying, G., Maguire, M.M., Laties, A.M., Jacobson, S.G. & Cideciyan, A.V. (2001). Augmented rod bipolar cell function in partial receptor loss: An ERG study in P23H rhodopsin transgenic and aging normal rats. Vision Research 41, 2779–2797.CrossRefGoogle ScholarPubMed
Chua, J., Fletcher, E.L. & Kalloniatis, M. (2009). Functional remodeling of glutamate receptors by inner retinal neurons occurs from an early stage of retinal degeneration. The Journal of Comparative Neurology 514, 473–491.CrossRefGoogle ScholarPubMed
Chua, J., Nivison-Smith, L., Fletcher, E.L., Trenhom, S., Awatramani, G.B. & Kalloniatis, M. (2013). Early remodelling of Müller cell in the rd/rd mouse model of retinal dystrophy. The Journal of Comparative Neurology. doi: 10.1002/cne.23307.CrossRefGoogle ScholarPubMed
Cuenca, N., Pinilla, I., Sauve, Y., Lu, B., Wang, S. & Lund, R.D. (2004). Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience 127, 301–317.CrossRefGoogle ScholarPubMed
de Souza, C.F., Kalloniatis, M., Polkinghorne, P.J., McGhee, C.N. & Acosta, M.L. (2012). Functional and anatomical remodeling in human retinal detachment. Experimental Eye Research 97, 73–89.CrossRefGoogle ScholarPubMed
Dryja, T.P., Hahn, L.B., Cowley, G.S., McGee, T.L. & Berson, E.L. (1991). Mutation spectrum of the rhodopsin gene among patients with autosomal dominant retinitis pigmentosa. Proceedings of the National Academy of Sciences of the United States of America 88, 9370–9374.CrossRefGoogle ScholarPubMed
Edwards, F.A., Konnerth, A., Sakmann, B. & Takahashi, T. (1989). A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflügers Archiv 414, 600–612.CrossRefGoogle ScholarPubMed
Elshatory, Y., Deng, M., Xie, X. & Gan, L. (2007). Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina. The Journal of Comparative Neurology 503, 182–197.CrossRefGoogle ScholarPubMed
Farber, D.B., Flannery, J.G. & Bowes-Rickman, C. (1994). The rd mouse story: Seventy years of research on an animal model of inherited retinal degeneration. Progress in Retinal and Eye Research 13, 31–64.CrossRefGoogle Scholar
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, 215–223.CrossRefGoogle ScholarPubMed
Fu, C.T. & Sretavan, D.W. (2012). Ectopic vesicular glutamate release at the optic nerve head and axon loss in mouse experimental glaucoma. Journal of Neuroscience 32, 15859–15876.CrossRefGoogle ScholarPubMed
Gavrieli, Y., Sherman, Y. & Ben-Sasson, S.A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. The Journal of Cell Biology 119, 493–501.CrossRefGoogle ScholarPubMed
Gibson, R., Fletcher, E.L., Vingrys, A.J., Zhu, Y., Vessey, K.A. & Kalloniatis, M. (2012). Functional and neurochemical development in the normal and degenerating mouse retina. The Journal of Comparative Neurology 521, 1251–1267.CrossRefGoogle Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. The Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Hartong, D.T., Berson, E.L. & Dryja, T.P. (2006). Retinitis pigmentosa. Lancet 368, 1795–1809.CrossRefGoogle ScholarPubMed
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. The Journal of Comparative Neurology 424, 1–23.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Jensen, R.J. (2012). Activation of ganglion cells in wild-type and P23H rat retinas with a small subretinal electrode. Experimental Eye Research 99, 71–77.CrossRefGoogle ScholarPubMed
Jones, B.W., Kondo, M., Terasaki, H., Lin, Y., McCall, M. & Marc, R..E. (2012). Retinal remodeling. Japanese Journal of Ophthalmology 56, 289–306.CrossRefGoogle ScholarPubMed
Jones, B.W. & Marc, R.E. (2005). Retinal remodeling during retinal degeneration. Experimental Eye Research 81, 123–137.CrossRefGoogle ScholarPubMed
Jones, B.W., Watt, C.B., Frederick, J.M., Baehr, W., Chen, C.K., Levine, E.M., Milam, A.H., Lavail, M.M. & Marc, R.E. (2003). Retinal remodeling triggered by photoreceptor degenerations. The Journal of Comparative Neurology 464, 1–16.CrossRefGoogle ScholarPubMed
Kalloniatis, M. & Fletcher, E.L. (1993). Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. The Journal of Comparative Neurology 336, 174–193.CrossRefGoogle ScholarPubMed
Kalloniatis, M., Sun, D., Foster, L., Haverkamp, S. & Wässle, H. (2004). Localization of NMDA receptor subunits and mapping NMDA drive within the mammalian retina. Visual Neuroscience 21, 587–597.CrossRefGoogle ScholarPubMed
Kalloniatis, M., Tomisich, G., Wellard, J.W. & Foster, L.E. (2002). Mapping photoreceptor and postreceptoral labelling patterns using a channel permeable probe (agmatine) during development in the normal and RCS rat retina. Visual Neuroscience 19, 61–70.CrossRefGoogle ScholarPubMed
Kuzirian, A., Meyhofer, E., Hill, L., Neary, J.T. & Alkon, D.L. (1986). Autoradiographic measurement of tritiated agmatine as an indicator of physiologic activity in Hermissenda visual and vestibular neurons. Journal of Neurocytology 15, 629–643.CrossRefGoogle ScholarPubMed
LaVail, M.M., Yasumura, D., Matthes, M.T., Drenser, K.A., Flannery, J.G., Lewin, A.S. & Hauswirth, W.W. (2000). Ribozyme rescue of photoreceptor cells in P23H transgenic rats: Long-term survival and late-stage therapy. Proceedings of the National Academy of Sciences of the United States of America 97, 11488–11493.CrossRefGoogle ScholarPubMed
Lewis, G.P., Charteris, D.G., Sethi, C.S., Leitner, W.P., Linberg, K.A. & Fisher, S.K. (2002). The ability of rapid retinal reattachment to stop or reverse the cellular and molecular events initiated by detachment. Investigative Ophthalmology and Visual Science 43, 2412–2420.Google ScholarPubMed
Lewis, G.P. & Fisher, S.K. (2003) Up-regulation of glial fibrillary acidic protein in response to retinal injury: Its potential role in glial remodeling and a comparison to vimentin expression. International Review of Cytology 230, 263–290.CrossRefGoogle Scholar
Machida, S., Kondo, M., Jamison, J.A., Khan, N.W., Kononen, L.T., Sugawara, T., Bush, R.A. & Sieving, P.A. (2000). P23H rhodopsin transgenic rat: Correlation of retinal function with histopathology. Investigative Ophthalmology and Visual Science 41, 3200–3209.Google ScholarPubMed
Marc, R.E. (1999 a). Kainate activation of horizontal, bipolar, amacrine, and ganglion cells in the rabbit retina. The Journal of Comparative Neurology 407, 65–76.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Marc, R.E. (1999 b). Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. The Journal of Comparative Neurology 407, 47–64.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Marc, R.E., Jones, B.W., Anderson, J.R., Kinard, K., Marshak, D.W., Wilson, J.H., Wensel, T. & Lucas, R.J. (2007). Neural reprogramming in retinal degeneration. Investigative Ophthalmology and Visual Science 48, 3364–3371.CrossRefGoogle ScholarPubMed
Marc, R.E., Jones, B.W., Watt, C.B. & Strettoi, E. (2003). Neural remodeling in retinal degeneration. Progress in Retinal and Eye Research 22, 607–655.CrossRefGoogle ScholarPubMed
Marc, R.E., Kalloniatis, M. & Jones, B.W. (2005). Excitation mapping with the organic cation AGB2+. Vision Research 45, 3454–3468.CrossRefGoogle ScholarPubMed
Marc, R.E., Liu, W.L., Kalloniatis, M., Raiguel, S.F. & van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 4006–4034.CrossRefGoogle ScholarPubMed
Marc, R.E., Murry, R.F. & Basinger, S.F. (1995). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.CrossRefGoogle ScholarPubMed
Mills, S.L., Massey, S.C. (2000). A series of biotinylated tracers distinguishes three types of gap junction in retina. Journal of Neuroscience 20, 8629–8636.CrossRefGoogle ScholarPubMed
Mojumder, D.K., Wensel, T.G. & Frishman, L.J. (2008). Subcellular compartmentalization of two calcium binding proteins, calretinin and calbindin-28 kDa, in ganglion and amacrine cells of the rat retina. Molecular Vision 14, 1600–1613.Google ScholarPubMed
Nivison-Smith, L., Sun, D., Fletcher, E., Marc, R.E. & Kalloniatis, M. (2013). Mapping kainate activation of inner neurons in the rat retina. The Journal of Comparative Neurology. doi: 10.1002./cne.23305.CrossRefGoogle ScholarPubMed
Nork, T.M., Ghobrial, M.W., Peyman, G.A. & Tso, M.O. (1986). Massive retinal gliosis. A reactive proliferation of Muller cells. Archives of Ophthalmology 104, 1383–1389.CrossRefGoogle ScholarPubMed
Park, H.S., Park, S.J., Park, S.H., Chun, M.H. & Oh, S.J. (2008). Shifting of parvalbumin expression in the rat retina in experimentally induced diabetes. Acta Neuropathologica 115, 241–248.CrossRefGoogle ScholarPubMed
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.CrossRefGoogle ScholarPubMed
Pinilla, I., Lund, R.D. & Sauve, Y. (2005). Enhanced cone dysfunction in rats homozygous for the P23H rhodopsin mutation. Neuroscience Letters 382, 16–21.CrossRefGoogle ScholarPubMed
Puthussery, T., Gayet-Primo, J., Pandey, S., Duvoisin, R.M. & Taylor, W.R. (2009). Differential loss and preservation of glutamate receptor function in bipolar cells in the rd10 mouse model of retinitis pigmentosa. The European Journal of Neuroscience 29, 1533–1542.CrossRefGoogle ScholarPubMed
Ramirez, J.M., Trivino, A., Ramirez, A.I., Salazar, J.J. & Garcia-Sanchez, J. (1994). Immunohistochemical study of human retinal astroglia. Vision Research 34, 1935–1946.CrossRefGoogle ScholarPubMed
Sanna, P.P., Keyser, K.T., Battenberg, E. & Bloom, F.E. (1990). Parvalbumin immunoreactivity in the rat retina. Neuroscience Letters 118, 136–139.CrossRefGoogle ScholarPubMed
Strettoi, E. & Pignatelli, V. (2000). Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proceedings of the National Academy of Sciences of the United States of America 97, 11020–11025.CrossRefGoogle Scholar
Strettoi, E., Pignatelli, V., Rossi, C., Porciatti, V. & Falsini, B. (2003). Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vision Research 43, 867–877.CrossRefGoogle ScholarPubMed
Strettoi, E., Porciatti, V., Falsini, B., Pignatelli, V. & Rossi, C. (2002). Morphological and functional abnormalities in the inner retina of the rd/rd mouse. Journal of Neuroscience 22, 5492–5504.CrossRefGoogle ScholarPubMed
Sun, D. & Kalloniatis, M. (2006). Mapping glutamate responses in immunocytochemically identified neurons of the mouse retina. The Journal of Comparative Neurology 494, 686–703.CrossRefGoogle ScholarPubMed
Sun, D., Rait, J.L. & Kalloniatis, M. (2003). Inner retinal neurons display differential responses to N-methyl-D-aspartate receptor activation. The Journal of Comparative Neurology 465, 38–56.CrossRefGoogle ScholarPubMed
Traverso, V., Bush, R.A., Sieving, P.A. & Deretic, D. (2002). Retinal cAMP levels during the progression of retinal degeneration in rhodopsin P23H and S334ter transgenic rats. Investigative Ophthalmology and Visual Science 43, 1655–1661.Google ScholarPubMed
Trexler, E.B., Li, W., Mills, S.L., Massey, S.C. (2001). Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. The Journal of Comparative Neurology 437, 408–422.CrossRefGoogle Scholar
Wässle, H., Grünert, U. & Rohrenbeck, J. (1993). Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. The Journal of Comparative Neurology 332, 407–420.CrossRefGoogle ScholarPubMed
Yoshikami, D. (1981). Transmitter sensitivity of neurons assayed by autoradiography. Science 212, 929–930.CrossRefGoogle ScholarPubMed
Yu, T.Y., Acosta, M.L., Ready, S., Cheong, Y.L. & Kalloniatis, M. (2007). Light exposure causes functional changes in the retina: Increased photoreceptor cation channel permeability, photoreceptor apoptosis, and altered retinal metabolic function. Journal of Neurochemistry 103, 714–724.CrossRefGoogle ScholarPubMed
Yu, D.Y. & Cringle, S.J. (2005). Retinal degeneration and local oxygen metabolism. Experimental Eye Research 80, 745–751.CrossRefGoogle ScholarPubMed
Yu, D.Y., Cringle, S., Valter, K., Walsh, N., Lee, D. & Stone, J. (2004). Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H rat. Investigative Ophthalmology and Visual Science 45, 2013–2019.CrossRefGoogle ScholarPubMed
Zhang, C., Hammassaki-Britto, D.E., Britto, L.R. & Duvoisin, R.M. (1996). Expression of glutamate receptor subunit genes during development of the mouse retina. Neuroreport 8, 335–340.CrossRefGoogle ScholarPubMed