Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T12:25:57.027Z Has data issue: false hasContentIssue false

Developmental expression of protein kinase C immunoreactivity in rod bipolar cells of the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Giovanni Casini
Affiliation:
Department of Environmental Sciences, Tuscia University, 01100 Viterbo, Italy
Achille Grassi
Affiliation:
Department of Environmental Sciences, Tuscia University, 01100 Viterbo, Italy
Luigi Trasarti
Affiliation:
Department of Environmental Sciences, Tuscia University, 01100 Viterbo, Italy
Paola Bagnoli
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56125 Pisa, Italy

Abstract

Rod bipolar cells constitute the second-order neuron in the rod pathway. Previous investigations of the rabbit retina have evaluated the development of other components of the rod pathway, namely the dopaminergic and All amacrine cell populations. To gain further insights into the maturation of this retinal circuitry, we studied the development of rod bipolar cells, identified with antibodies directed to the α isoform of protein kinase C (PKC), in the rabbit retina. Lightly immunostained PKC-immunoreactive (IR) somata are first observed at postnatal day (PND) 6 in the distal inner nuclear layer (INL). Immunostaining is also observed in the outer plexiform layer (OPL), indicating the presence of PKC-IR dendrites. PKC-IR axons are present in the INL oriented toward the inner plexiform layer (IPL). Several of them terminate with enlarged structures resembling growth cones. At PND 8, some immunostained terminal bulbs, characteristic of rod bipolar cells, are detected in the proximal IPL. PKC-IR cells at PND 11 (eye opening) display stronger immunostaining and more mature characteristics than at earlier ages. The dendritic arborizations of these cells in the OPL and their axon terminals in the IPL attain mature morphology at later ages (PND 30 or older). The density of PKC-IR cells shows a peak at PND 11 followed by a drastic decrease up to adulthood. The total number of PKC-IR cells increases from PND 6 to PND 11 and then it remains almost unchanged until adulthood. The mosaic of PKC-IR cells is nonrandom in some retinal locations at PND 6, but the overall regularity index at PND 6 is lower than at older ages. The present data provide a comprehensive evaluation of the development of rod bipolar cells in the postnatal rabbit retina and are consistent with those previously reported for dopaminergic and All amacrine cell populations, indicating that different components of the rod pathway follow a similar pattern of maturation, presumably allowing the rod pathway to be functional at eye opening.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, R. & Hatlee, M. (1989). Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 243, 391393.CrossRefGoogle ScholarPubMed
Bovolenta, P. & Mason, C. (1987). Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. Journal of Neuroscience 7, 14471460.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1893). La rétine des vertébrés. La Céllule 9, 119257.Google Scholar
Cameron, D.A. & Easter, S.S. Jr., (1995). Cone photoreceptor regeneration in adult fish retina: Phenotypic determination and mosaic pattern formation. Journal of Neuroscience 15, 22552271.CrossRefGoogle ScholarPubMed
Casini, G. & Brecha, N.C. (1992 a). Postnatal development of tyro-sine hydroxylase immunoreactive amacrine cells in the rabbit retina. I. Morphological characterization. Journal of Comparative Neurology 326, 283301.CrossRefGoogle Scholar
Casini, G. & Brecha, N.C. (1992 b). Postnatal development of tyro-sine hydroxylase immunoreactive amacrine cells in the rabbit retina. II. Quantitative analysis. Journal of Comparative Neurology 326, 302313.CrossRefGoogle Scholar
Casini, G., Molnar, M. & Brecha, N.C. (1994 a). Vasoactive intestinal polypeptide/peptide histidine isoleucine mRNA in the rat retina: Adult distribution and developmental expression. Neuroscience 58, 657667.CrossRefGoogle ScholarPubMed
Casini, G., Grassi, A., Trasarti, L. & Bagnoli, P. (1994 b). Protein kinase C immunoreactivity in rod bipolar cells of the developing rabbit retina. Society for Neuroscience Abstracts 20, 769.Google Scholar
Casini, G., Rickman, D.W. & Brecha, N.C. (1995). An amacrine cell population in the rabbit retina: Identification by parvalbumin immunoreactivity. Journal of Comparative Neurology 356, 132142.CrossRefGoogle ScholarPubMed
Casini, G., Rickman, D.W. & Brecha, N.C. (1996). Postnatal development of rabbit All amacrine cells identified with parvalbumin immunoreactivity. Developmental Brain Research (submitted).Google Scholar
Constantine-Paton, M., Blum, A.S., Mendez-Otero, R. & Barn-Stable, C.J. (1986). A cell surface molecule distributed in a dorso-ventral gradient in the perinatal rat retina. Nature 324, 459462.CrossRefGoogle Scholar
Dacheux, R.F. & Miller, R.F. (1981 a). An intracellular electrophysi-ological study of the ontogeny of functional synapses in the rabbit retina. I. Horizontal and bipolar cells. Journal of Comparative Neurology 198, 307326.CrossRefGoogle Scholar
Dacheux, R.F. & Miller, R.F. (1981 b). An intracellular electrophysi-ological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. Journal of Comparative Neurology 198, 327334.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.CrossRefGoogle ScholarPubMed
Denis-Donini, S. (1989). Expression of dopaminergic phenotypes in the mouse olfactory bulb induced by the calcitonin gene-related pep-tide. Nature 339, 701703.CrossRefGoogle Scholar
Eberhardt, L.L. (1967). Some developments in “distance sampling.” Biometrics 23, 207216.CrossRefGoogle ScholarPubMed
Feigenspan, A., Bormann, J. & Wässle, H. (1993). Organotypic slice culture of the mammalian retina. Visual Neuroscience 10, 203217.CrossRefGoogle ScholarPubMed
French, K.A. & Kristan, W.B. Jr, (1992). Target influences on the development of leech neurons. Trends in Neurosciences 15, 169174.CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.CrossRefGoogle ScholarPubMed
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 27422758.CrossRefGoogle ScholarPubMed
Grünert, U., Martin, P.R. & Wässle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 348, 607627.CrossRefGoogle ScholarPubMed
Hampson, E.C.G.M., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 49114922.CrossRefGoogle ScholarPubMed
Hatten, M.E. & Heintz, N. (1995). Mechanisms of neural patterning and specification in the developing cerebellum. Annual Review of Neuroscience 18, 385408.CrossRefGoogle ScholarPubMed
Hirata, M., Saito, N., Kono, M. & Tanaka, C. (1991). Differential expression of the ß1- and ßII-PKC subspecies in the postnatal developing rat brain: An immunocytochemical study. Developmental Brain Research 62, 229238.CrossRefGoogle Scholar
Holt, C.E., Bertsch, T.W., Ellis, H.M. & Harris, W.A. (1988). Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1, 1526.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1989). Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Visual Neuroscience 3, 573585.CrossRefGoogle ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860876.CrossRefGoogle ScholarPubMed
Kolb, H., Zhang, L. & DeKorver, L. (1993). Differential staining of neurons in the human retina with antibodies to protein kinase C isozymes. Visual Neuroscience 10, 341351.CrossRefGoogle ScholarPubMed
Landis, S.C. (1990). Target regulation of neurotransmitter phenotype. Trends in Neurosciences 13, 344350.CrossRefGoogle ScholarPubMed
Masland, R.H. (1977). Maturation of functions in the developing rabbit retina. Journal of Comparative Neurology 175, 275286.CrossRefGoogle ScholarPubMed
Masland, R.H., Rizzo, J.F. & Sandell, J.H. (1993). Developmental variation in the structure of the retina. Journal of Neuroscience 13, 51945202.CrossRefGoogle ScholarPubMed
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253273.CrossRefGoogle ScholarPubMed
Möckel, V., Löhrke, S. & Hofmann, H.-D. (1994). Diversity of neuronal phenotypes expressed in monolayer cultures from immature rabbit retina. Visual Neuroscience 11, 629642.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247252.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1986). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Science 233, 305312.CrossRefGoogle Scholar
Pow, D.V., Crook, D.K. & Wong, R.O.L. (1994). Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunocytochemical study. Visual Neuroscience 11, 11151134.CrossRefGoogle ScholarPubMed
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73247328.CrossRefGoogle ScholarPubMed
Reh, T.A. (1987). Cell-specific regulation of neuronal production in the larval frog retina. Journal of Neuroscience 7, 33173324.CrossRefGoogle ScholarPubMed
Reh, T.A. (1992). Cellular interactions determine neuronal phenotypes in rodent retinal cultures. Journal of Neurobiology 23, 10671083.CrossRefGoogle ScholarPubMed
Reh, T.A. & Tully, T. (1986). Regulation of tyrosine hydroxylase-containing amacrine cell number in larval frog retina. Developmental Biology 114, 463469.CrossRefGoogle ScholarPubMed
Saito, N., Kikkawa, U., Nishizuka, Y. & Tanaka, C. (1988). Distribution of protein kinase C-like immunoreactive neurons in rat brain. Journal of Neuroscience 8, 369382.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 33313347.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303313.CrossRefGoogle ScholarPubMed
Schnitzer, J. (1990). Postnatal gliogenesis in the nerve fiber layer of the rabbit retina: An autoradiographic study. Journal of Comparative Neurology 292, 551562.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook. Sydney, Australia: Maitland Press.Google Scholar
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. Journal of Neuroscience 15, 875888.CrossRefGoogle ScholarPubMed
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449466.CrossRefGoogle ScholarPubMed
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow field, bistratified rod amacrine cells (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152168.CrossRefGoogle ScholarPubMed
Strettoi, E., Dacheux, R.F. & Raviola, E. (1994). Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. Journal of Comparative Neurology 347, 139149.CrossRefGoogle ScholarPubMed
Suzuki, S. & Kaneko, A. (1990). Identification of bipolar cell subtypes by protein kinase C-like immunoreactivity in the goldfish retina. Visual Neuroscience 5, 223230.CrossRefGoogle ScholarPubMed
Takai, Y., Kishimoto, A., Inoue, M. & Nishizuka, Y. (1977). Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues, I: Purification and characterization of an active enzyme from bovine cerebellum. Journal of Biological Chemistry 252, 76037609.CrossRefGoogle ScholarPubMed
Tanaka, C. & Saito, N. (1992). Localization of subspecies of protein kinase C in the mammalian central nervous system. Neurochemistry International 21, 499512.CrossRefGoogle ScholarPubMed
Tanaka, C. & Nishizuka, Y. (1994). The protein kinase C family for neuronal signaling. Annual Review of Neuroscience 17, 551567.CrossRefGoogle ScholarPubMed
Trisler, G.D., Schnider, M.D. & Nirenberg, M. (1981). A topographic gradient of molecules in the retina can be used to identify neuron position. Proceedings of the National Academy of Sciences of the U.S.A. 78, 21452149.CrossRefGoogle ScholarPubMed
Turner, D.L. & Cepko, C.L. (1987). A common progenitor for neurons and glia persists in rat retina late in development. Nature 238, 131136.CrossRefGoogle Scholar
Usuda, N., Kong, Y., Hagiwara, M., Uchida, C., Terasawa, M., Nagata, T. & Hidaka, H. (1991). Differential localization of protein kinase C isozymes in retinal neurons. Journal of Cell Biology 112, 12411247.CrossRefGoogle ScholarPubMed
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-signal interneurons in the rabbit retina: 2. All amacrine cells. Journal of Comparative Neurology 310, 154169.CrossRefGoogle Scholar
Walker, J.M., Homan, E.C. & Sando, J.J. (1990). Differential activation of protein kinase C isozymes by short chain phosphatidyl-serines and phosphalidylcholines. Journal of Biological Chemistry 265, 80168021.CrossRefGoogle Scholar
Wässle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 33833394.CrossRefGoogle ScholarPubMed
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society (London) 200, 441461.Google ScholarPubMed
Watanabe, T. & Raff, M. (1992). Diffusible rod-promoting signals in the developing rat retina. Development 114, 899906.CrossRefGoogle ScholarPubMed
Wetts, R. & Fraser, S.E. (1988). Multipotent precursors can give rise to all major cell types of the frog retina. Science 239, 11421145.CrossRefGoogle ScholarPubMed
Wikler, K.C. & Rakic, P. (1991). Relation of an array of early-differentiating cones to the photoreceptor mosaic in the primate retina. Nature 351, 397400.CrossRefGoogle Scholar
Wong, R.O.L. (1995). Cholinergic regulation of [Ca2+]i during cell division and differentiation in the mammalian retina. Journal of Neuroscience 15, 26962706.CrossRefGoogle ScholarPubMed
Wood, J.G., Hart, C.E., Mazzei, G.J. & Kuo, J.F. (1988). Distribution of protein kinase C immunoreactivity in rat retina. Histochemical Journal 20, 6368.CrossRefGoogle ScholarPubMed
Yoshihara, C., Saito, N., Taniyama, K. & Tanaka, C. (1991). Differential localization of four subspecies of protein kinase C in the rat striatum and substantia nigra. Journal of Neuroscience 11, 690700.CrossRefGoogle ScholarPubMed
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Neurology 310, 139153.CrossRefGoogle ScholarPubMed
Zhang, D. & Yeh, H.Y. (1991). Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study. Visual Neuroscience 6, 429437.CrossRefGoogle ScholarPubMed