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Ontogeny of plasma membrane Ca2+ ATPase isoforms in the neural retina of the postnatal rat

Published online by Cambridge University Press:  02 August 2005

RENÉ C. RENTERÍA ,
EMANUEL E. STREHLER ,
DAVID R. COPENHAGEN  and
DAVID KRIZAJ
RENÉ C. RENTERÍA
Affiliation:
Department of Ophthalmology, University of California, San Francisco
EMANUEL E. STREHLER
Affiliation:
Departments of Biochemistry and Molecular Biology, Mayo Clinic, Rochester
DAVID R. COPENHAGEN
Affiliation:
Department of Ophthalmology, University of California, San Francisco Department of Physiology, University of California, San Francisco
DAVID KRIZAJ
Affiliation:
Department of Ophthalmology, University of California, San Francisco Department of Physiology, University of California, San Francisco
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Abstract

Calcium ion (Ca2+) signaling has been widely implicated in developmental events in the retina, but little is known about the specific mechanisms utilized by developing neurons to decrease intracellular Ca2+. Using immunocytochemistry, we determined the expression profiles of all known isoforms of a key Ca2+ transporter, the plasma membrane Ca2+ ATPase (PMCA), in the rat retina. During the first postnatal week, the four PMCA isoforms were expressed in patterns that differed from their expression in the adult retina. At birth, PMCA1 was found in the ventricular zone and nascent cell processes in the distal retina as well as in ganglion and amacrine cells. After the first postnatal week, PMCA1 became restricted to photoreceptors and cone bipolar cells. By P10 (by postnatal day 10), most inner retinal PMCA consisted of PMCA2 and PMCA3. Prominent PMCA4 expression appeared after the first postnatal week and was confined primarily to the ON sublamina of the inner plexiform layer (IPL). The four PMCA isoforms could play distinct functional roles in the development of the mammalian retina even before synaptic circuits are established. Their expression patterns are consistent with the hypothesis that inner and outer retinal neurons have different Ca2+ handling needs.

Keywords

PMCADevelopmentDifferentiationGanglion cellPhotoreceptor
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 263 - 274
Copyright
2005 Cambridge University Press

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References

REFERENCES

Bachman, K.M. & Balkema, G.W. (1993). Developmental expression of a synaptic ribbon antigen (B16) in mouse retina. Journal of Comparative Neurology 333, 109–117.CrossRefGoogle Scholar
Berridge, M.J., Bootman, M.D., & Roderick, H.L. (2003). Calcium signalling: Dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology 4, 517–529.CrossRefGoogle Scholar
Bindokas, V.P., Yoshikawa, M., & Ishida, A.T. (1994). Na(+)-Ca2+ exchanger-like immunoreactivity and regulation of intracellular Ca2+ levels in fish retinal ganglion cells. Journal of Neurophysiology 72, 47–55.Google Scholar
Blanks, J.C., Adinolfi, A.M., & Lolley, R.N. (1974). Synaptogenesis in the photoreceptor terminal of the mouse retina. Journal of Comparative Neurology 156, 81–93.CrossRefGoogle Scholar
Boyer, C., Art, J.J., Dechesne, C.J., Lehouelleur, J., Vautrin, J., & Sans, A. (2001). Contribution of the plasmalemma to Ca2+ homeostasis in hair cells. Journal of Neuroscience 21, 2640–2650.Google Scholar
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281–301.CrossRefGoogle Scholar
Brandt, P. & Neve, R.L. (1992). Expression of plasma membrane calcium-pumping ATPase mRNAs in developing rat brain and adult brain subregions: Evidence for stage-specific expression. Journal of Neurochemistry 59, 1566–1569.CrossRefGoogle Scholar
Brini, M., Coletto, L., Pierobon, N., Kraev, N., Guerini, D., & Carafoli, E. (2003). A comparative functional analysis of plasma membrane Ca2+ pump isoforms in intact cells. Journal of Biological Chemistry 278, 24500–24508.CrossRefGoogle Scholar
Burette, A., Rockwood, J.M., Strehler, E.E., & Weinberg, R.J. (2003). Isoform-specific distribution of the plasma membrane Ca2+ ATPase in the rat brain. Journal of Comparative Neurology 467, 464–476.CrossRefGoogle Scholar
Caride, A.J., Filoteo, A.G., Enyedi, A., Verma, A.K., & Penniston, J.T. (1996). Detection of isoform 4 of the plasma membrane calcium pump in human tissues by using isoform-specific monoclonal antibodies. Biochemistry Journal 316, 353–359.CrossRefGoogle Scholar
Caride, A.J., Penheiter, A.R., Filoteo, A.G., Bajzer, Z., Enyedi, A., & Penniston, J.T. (2001). The plasma membrane calcium pump displays memory of past calcium spikes. Differences between isoforms 2b and 4b. Journal of Biological Chemistry 276, 39797–39804.Google Scholar
Cellerino, A., Galli-Resta, L., & Colombaioni, L. (2000). The dynamics of neuronal death: A time-lapse study in the retina. Journal of Neuroscience 20, RC92.Google Scholar
Copenhagen, D.R., Hemila, S., & Reuter, T. (1990). Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise. Journal of General Physiology 95, 717–732.Google Scholar
DeMarco, S.J. & Strehler, EE. (2001). Plasma membrane Ca2+-atpase isoforms 2b and 4b interact promiscuously and selectively with members of the membrane-associated guanylate kinase family of PDZ (PSD95/Dlg/ZO-1) domain-containing proteins. Journal of Biological Chemistry 276, 21594–21600.CrossRefGoogle Scholar
Dodson, H.C. & Charalabapoulou, M. (2001). PMCA2 mutation causes structural changes in the auditory system in deafwaddler mice. Journal of Neurocytology 30, 281–292.CrossRefGoogle Scholar
Dumont, R.A., Lins, U., Filoteo, A.G., Penniston, J.T., Kachar, B., & Gillespie, P.G. (2001). Plasma membrane Ca2+-ATPase isoform 2a is the PMCA of hair bundles. Journal of Neuroscience 21, 5066–5078.Google Scholar
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461–478.CrossRefGoogle Scholar
Feller, M.B. (2002). The role of nAChR-mediated spontaneous retinal activity in visual system development. Journal of Neurobiology 53, 556–567.CrossRefGoogle Scholar
Filoteo, A.G., Elwess, N.L., Enyedi, A., Caride, A., Aung, H.H., & Penniston, J.T. (1997). Plasma membrane Ca2+ pump in rat brain. Patterns of alternative splices seen by isoform-specific antibodies. Journal of Biological Chemistry 272, 23741–23747.CrossRefGoogle Scholar
Furuta, H., Luo, L., Hepler, K., & Ryan, AF. (1998). Evidence for differential regulation of calcium by outer versus inner hair cells: Plasma membrane Ca-ATPase gene expression. Hearing Research 123, 10–26.CrossRefGoogle Scholar
Galli-Resta, L. & Ensini, M. (1996). An intrinsic time limit between genesis and death of individual neurons in the developing retinal ganglion cell layer. Journal of Neuroscience 16, 2318–2324.Google Scholar
Gu, X., Olson, E.C., & Spitzer, N.C. (1994). Spontaneous neuronal calcium spikes and waves during early differentiation. Journal of Neuroscience 14, 6325–6335.Google Scholar
Guerini, D. (1998). The significance of the isoforms of plasma membrane calcium ATPase. Cell and Tissue Research 292, 191–197.CrossRefGoogle Scholar
Guerini, D., Garcia-Martin, E., Gerber, A., Volbracht, C., Leist, M., Merino, C.G., & Carafoli, E. (1999). The expression of plasma membrane Ca2+ pump isoforms in cerebellar granule neurons is modulated by Ca2+. Journal of Biological Chemistry 274, 1667–1676.CrossRefGoogle Scholar
Hammes, A., Oberdorf, S., Strehler, E.E., Stauffer, T., Carafoli, E., Vetter, H., & Neyses, L. (1994). Differentiation-specific isoform mRNA expression of the calmodulin-dependent plasma membrane Ca(2+)-ATPase. FASEB Journal 8, 428–435.Google Scholar
Haverkamp, S., Ghosh, K.K., Hirano, A.A., & Wassle, H. (2003). Immunocytochemical description of five bipolar cell types of the mouse retina. Journal of Comparative Neurology 455, 463–476.CrossRefGoogle Scholar
Heidelberger, R., Heinemann, C., Neher, E., & Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515.CrossRefGoogle Scholar
Hicks, D. & Barnstable, C.J. (1987). A phosphorylation-sensitive anti-rhodopsin monoclonal antibody reveals light-induced phosphorylation of rhodopsin in the photoreceptor cell body. European Journal of Cell Biology 44, 341–347.Google Scholar
Hilfiker, H., Guerini, D., & Carafoli, E. (1994). Cloning and expression of isoform 2 of the human plasma membrane Ca2+ ATPase. Functional properties of the enzyme and its splicing products. Journal of Biological Chemistry 269, 26178–26183.Google Scholar
Hurtado, J., Borges, S., & Wilson, M. (2002). Na(+)-Ca(2+) exchanger controls the gain of the Ca(2+) amplifier in the dendrites of amacrine cells. Journal of Neurophysiology 88, 2765–2777.CrossRefGoogle Scholar
Jasoni, C.L. & Reh, T.A. (1996). Temporal and spatial pattern of MASH-1 expression in the developing rat retina demonstrates progenitor cell heterogeneity. Journal of Comparative Neurology 369, 319–327.3.0.CO;2-C>CrossRefGoogle Scholar
Kobayashi, K. & Tachibana, M. (1995). Ca2+ regulation in the presynaptic terminals of goldfish retinal bipolar cells. Journal of Physiology 483, 79–94.CrossRefGoogle Scholar
Kozel, P.J., Friedman, R.A., Erway, L.C., Yamoah, E.N., Liu, L.H., Riddle, T., Duffy, J.J., Doetschman, T., Miller, M.L., Cardell, E.L., & Shull, G.E. (1998). Balance and hearing deficits in mice with a null mutation in the gene encoding plasma membrane Ca2+-ATPase isoform 2. Journal of Biological Chemistry 273, 18693–18696.CrossRefGoogle Scholar
Krizaj, D. & Copenhagen, D.R. (1998). Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 21, 249–256.CrossRefGoogle Scholar
Krizaj, D. & Copenhagen, D.R. (2002). Calcium regulation in photoreceptors. Frontiers in Bioscience 7, 2023–2044.CrossRefGoogle Scholar
Krizaj, D., Demarco, S.J., Johnson, J., Strehler, E.E., & Copenhagen, D.R. (2002). Cell-specific expression of plasma membrane calcium ATPase isoforms in retinal neurons. Journal of Comparative Neurology 451, 1–21.Google Scholar
Krizaj, D., Liu, X., & Copenhagen, D.R. (2004). Expression of calcium transporters in the retina of the tiger salamander (Ambystoma tigrinum). Journal of Comparative Neurology 475, 463–480.CrossRefGoogle Scholar
Lohmann, C., Myhr, K.L., & Wong, R.O. (2002). Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418, 177–181.CrossRefGoogle Scholar
Morgans, C.W., El Far, O., Berntson, A., Wässle, H., & Taylor, W.R. (1998). Calcium extrusion from mammalian photoreceptor terminals. Journal of Neuroscience 18, 2467–2474.Google Scholar
Penn, A.A., Riquelme, P.A., Feller, M.B., & Shatz, C.J. (1998). Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108–2112.CrossRefGoogle Scholar
Pozzan, T., Rizzuto, R., Volpe, P., & Meldolesi, J. (1994). Molecular and cellular physiology of intracellular calcium stores. Physiological Reviews 74, 595–636.Google Scholar
Protti, D.A. & Llano, I. (1998). Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. Journal of Neuroscience 18, 3715–3724.Google Scholar
Redmond, L., Kashani, A.H., & Ghosh, A. (2002). Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34, 999–1010.CrossRefGoogle Scholar
Rich, K.A., Zhan, Y., & Blanks, J.C. (1997). Migration and synaptogenesis of cone photoreceptors in the developing mouse retina. Journal of Comparative Neurology 388, 47–63.3.0.CO;2-O>CrossRefGoogle Scholar
Rörig, B. & Grantyn, R. (1993). Glutamatergic and GABAergic synaptic currents in ganglion cells from isolated retinae of pigmented rats during postnatal development. Brain Research Developmental Brain Research 74, 98–110.CrossRefGoogle Scholar
Rörig, B. & Grantyn, R. (1994). Ligand- and voltage-gated ion channels are expressed by embryonic mouse retinal neurones. Neuroreport 5, 1197–1200.CrossRefGoogle Scholar
Schmid, S. & Guenther, E. (1996). Developmental regulation of voltage-activated Na+ and Ca2+ currents in rat retinal ganglion cells. Neuroreport 7, 677–681.CrossRefGoogle Scholar
Schmid, S. & Guenther, E. (1999). Voltage-activated calcium currents in rat retinal ganglion cells in situ: Changes during prenatal and postnatal development. Journal of Neuroscience 19, 3486–3494.Google Scholar
Schwab, B.L., Guerini, D., Didszun, C., Bano, D., Ferrando-May, E., Fava, E., Tam, J., Xu, D., Xanthoudakis, S., Nicholson, D.W., Carafoli, E., & Nicotera, P. (2002). Cleavage of plasma membrane calcium pumps by caspases: A link between apoptosis and necrosis. Cell Death and Differentiation 9, 818–831.CrossRefGoogle Scholar
Singer, J.H., Mirotznik, R.R., & Feller, M.B. (2001). Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina. Journal of Neuroscience 21, 8514–8522.Google Scholar
Stacy, R.C. & Wong, R.O. (2003). Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. Journal of Comparative Neurology 456, 154–166.CrossRefGoogle Scholar
Stauffer, T.P., Guerini, D., & Carafoli, E. (1995). Tissue distribution of the four gene products of the plasma membrane Ca2+ pump. A study using specific antibodies. Journal of Biological Chemistry 270, 12184–12190.Google Scholar
Stauffer, T.P., Guerini, D., Celio, M.R., & Carafoli, E. (1997). Immunolocalization of the plasma membrane Ca2+ pump isoforms in the rat brain. Brain Research 748, 21–29.CrossRefGoogle Scholar
Strehler, E.E. & Treiman, M. (2004). Calcium pumps of plasma membrane and cell interior. Current Molecular Medicine 4, 323–325.CrossRefGoogle Scholar
Strehler, E.E. & Zacharias, D.A. (2001). Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiological Reviews 81, 21–50.Google Scholar
Sugioka, M., Fukuda, Y., & Yamashita M. (1998). Development of glutamate-induced intracellular Ca2+ rise in the embryonic chick retina. Journal of Neurobiology 34, 113–125.3.0.CO;2-5>CrossRefGoogle Scholar
Syed, M.M., Lee, S., He, S., & Zhou, Z.J. (2004). Spontaneous waves in the ventricular zone of developing mammalian retina. Journal of Neurophysiology 91, 1999–2009.CrossRefGoogle Scholar
Tang, F., Dent, E.W., & Kalil, K. (2003). Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. Journal of Neuroscience 23, 927–936.Google Scholar
Tolosa de Talamoni, N., Perez, A., Riis, R., Smith, C., Norman, M.L., & Wasserman, R.H. (2002). Comparative immunolocalization of the plasma membrane calcium pump and calbindin D28K in chicken retina during embryonic development. European Journal of Histochemistry 46, 333–340.Google Scholar
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. An electron microscopic study. Archives of Ophthalmology 79, 470–484.CrossRefGoogle Scholar
Witkovsky, P., Schmitz, Y., Akopian, A., Krizaj, D., & Tranchina, D. (1997). Gain of rod to horizontal cell synaptic transfer: relation to glutamate release and a dihydropyridine-sensitive calcium current. Journal of Neuroscience 17, 7297–7306.Google Scholar
Wong, R.O., Chernjavsky, A., Smith, S.J., & Shatz, C.J. (1995). Early functional neural networks in the developing retina. Nature 374, 716–718.CrossRefGoogle Scholar
Wong, W.T., Sanes, J.R., & Wong, RO. (1998). Developmentally regulated spontaneous activity in the embryonic chick retina. Journal of Neuroscience 18, 8839–8852.Google Scholar
Xue, J. & Cooper, N.G. (2001). The modification of NMDA receptors by visual experience in the rat retina is age dependent. Brain Research Molecular Brain Research 91, 196–203.CrossRefGoogle Scholar
Young, R.W. (1984). Cell death during differentiation of the retina in the mouse. Journal of Comparative Neurology 229, 362–373.CrossRefGoogle Scholar
Zacharias, D.A. & Kappen, C. (1999). Developmental expression of the four plasma membrane calcium ATPase (Pmca) genes in the mouse. Biochimica et Biophysica Acta 1428, 397–405.CrossRefGoogle Scholar
Zenisek, D. & Matthews, G. (2000). The role of mitochondria in presynaptic calcium handling at a ribbon synapse. Neuron 25, 229–237.CrossRefGoogle Scholar
Zirpel, L., Janowiak, M.A., Taylor, D.A., & Parks, T.N. (2000). Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis. Journal of Comparative Neurology 421, 95–106.3.0.CO;2-5>CrossRefGoogle Scholar