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Differential staining of neurons in the human retina with antibodies to protein kinase C isozymes

Published online by Cambridge University Press:  02 June 2009

Helga Kolb ,
Li Zhang  and
Laura Dekorver
Helga Kolb
Affiliation:
Physiology and Ophthalmology Departments, University of Utah, Salt Lake City
Li Zhang
Affiliation:
Physiology and Ophthalmology Departments, University of Utah, Salt Lake City
Laura Dekorver
Affiliation:
Physiology and Ophthalmology Departments, University of Utah, Salt Lake City
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Abstract

Monoclonal antibodies to the three isozymes of protein kinase C (PKC) (α, β, and γ) were applied to postmortem human retina. Immunostaining was done on wholemount, or cryostat-sectioned retina, and visualized after ABC/DAB procedures by light (LM) and electron (EM) microscopy.

The PCK-α antibody stained rod bipolar cells throughout the retina. EM analysis confirmed they were PKC-α-immunoreactive (IR) on their characteristic dendritic and axonal synaptology. Putative blue cone bipolar cells with wide-field axon terminals, stratifying in s5 of the inner plexiform layer (IPL), were also PKC-α-IR, and EM showed them to engage in narrow-cleft ribbon junctions in blue cone pedicles.

The PKC-β antibody stained cone bipolar cells, many amacrine cells, and most ganglion cells. Cone bipolar cells were stained all the way into the foveal center: both midget and diffuse varieties were included. The IPL was densely PKC-IR and individual neurons could not be identified on stratification patterns. EM of the outer plexiform layer (OPL) revealed that both flat and invaginating cone bipolar types were IR and that IR axon terminals were presynaptic in all strata of the IPL. The occurrence of PKC-β-IR bipolar axons in stratum 2 of the IPL suggests that OFF-center as well as ON-center types were included.

The PKC-γ antibody gave inferior staining compared with results from the other two antibodies; however, two varieties of wide-field monostratified amacrine cell and a large-bodied ganglion cell type were discernible.

PKC in one form or another appears to be a second messenger used in neurotransmission by both rod and cone systems and ON- and OFF-center systems in the human retina.

Keywords

Rod bipolar cellCone bipolar cellAmacrine cellGanglion cellPKC–αPKC–βPKC–γ
Type
Research Article
Information
Visual Neuroscience , Volume 10 , Issue 2 , March 1993 , pp. 341 - 351
Copyright
Copyright © Cambridge University Press 1993

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References

Ahnelt, P.K., Keri, C. & Kolb, H. (1990). Identification of pedicles of putative blue sensitive cones in human and primate retina. Journal of Comparative Neurology 293, 39–53CrossRefGoogle Scholar
Ahnelt, P.K. & Kolb, H. (1993). Horizontal cells and cone photoreceptors in human retina: A Golgi electron-microscope study of spectral connectivity. Journal of Comparative Neurology (submitted).Google Scholar
Ahnelt, P.K., Kolb, H. & Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. Journal of Comparative Neurology 255, 18–34CrossRefGoogle ScholarPubMed
Aleman, V., Osorio, B. & Camacho, J.L. (1989). Reciprocal interactions between m-receptor and protein kinase C in cultured neurons from hippocampus. Society for Neuroscience Abstracts 15, 1218.Google Scholar
Barrie, A.P., Niccolls, D.G., Sanchez-Prieto, J. & Sihra, T.S. (1991). An ion channel locus for the protein kinase C potentiation of transmitter glutamate release from guinea pig cerebrocortical synaptosomes. Journal of Neurochemistry 57, 1398–1404CrossRefGoogle ScholarPubMed
Boycott, B.B. & Hopkins, J.M. (1991). Cone bipolar cells and cone synapses in the primate retina. Visual Neuroscience 7, 49–60CrossRefGoogle ScholarPubMed
Browning, M.D., Bureau, M., Barnes, E. & Olsen, R. (1989). Protein kinase C and cAMP-dependent protein kinase phosphorylate the purified GABAA receptor. Society for Neuroscience Abstracts 15, 830.Google Scholar
Coussens, L., Parker, P.L., Phee, L., Yang-Feng, T.L., Chen, E., Waterfield, M.D., Franke, U. & Ulrich, A. (1986). Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. Science 233, 859–866CrossRefGoogle ScholarPubMed
Crook, R.B., Lehman, N.L. & Polansky, J.R. (1992). Protein kinase C stimulates turnover of receptor-bound atrionatriuretic peptide in fetal human NPE cells. Investigative Ophthalmology and Visual Science (Suppl.) 15, 903.Google Scholar
Cuenca, N., Fernandez, E. & Kolb, H. (1990). Distribution of immunoreactivity to protein kinase C in the turtle retina. Brain Research 532, 278–287CrossRefGoogle ScholarPubMed
Curcio, C., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, l.B. & Millam, A.H. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. Journal of Comparative Neurology 312, 610–624CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 1267–1269CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E. & Hollyfield, J.G. (1984). Glycinergic neurons in the human retina. Journal of Comparative Neurology 227, 159–172CrossRefGoogle ScholarPubMed
Gouras, P. (1971). The function of the midget system in primate color vision. Vision Research (Suppl.) 3, 397–410CrossRefGoogle Scholar
Grimes, P.A., Li, H. & Stramm, L. (1992). Localization of protein kinase-C-like immunoreactivity in rat retinal neurons with antibodies recognizing alpha, beta-I, beta-II, and gamma isozymes. Investigative Ophthalmology and Visual Science (Suppl.) 33, 940.Google Scholar
Gruünert, U., Greferath, U. & Wäassle, H. (1989). Rod bipolar cells show protein kinase C-like immunoreactivity in the cat and other mammalian retinae. Abstracts Society for Neuroscience 15, 1209.Google Scholar
Gruünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 2742–2758CrossRefGoogle Scholar
Hopkins, J.M. & Boycott, B.B. (1992). Synaptic contacts of a two-cone flat bipolar cell in a primate retina. Visual Neuroscience 8, 379–384CrossRefGoogle Scholar
Kaneko, A., De La Villa, P. & Kurahashi, T. (1992). L-glutamateinduced responses in isolated cat bipolar cells the subtype of which was identified by PKC-like immunoreactivity. Investigative Ophthalmology and Visual Science (Suppl.) 33, 752.Google Scholar
Koda, Y., Yanagihara, N., Wada, A., Uezono, Y., Kobayashi, H. & Izumi, F. (1989). Cis-unsaturated fatty acids stimulate catecholamine secretion, tyrosine hydroxylase, and protein kinase C in bovine adrenal medullary cells. Society for Neuroscience Abstracts 15, 1228.Google Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261–283Google ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron-microscopic observations. Journal of Neurocytology 8, 295–329CrossRefGoogle ScholarPubMed
Kolb, H. (1984). Cone pathways in the mammalian retina. Molecular and Cellular Basis of Visual Acuity, ed., Hilfer, S.R. & Sheffield, J.B., pp. 56–78. New York: Springer-Verlag.Google Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992 a). The neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. Progress in Retinal Research 3, 21–60CrossRefGoogle Scholar
Kolb, H., Zhang, L. & Dekorver, L. (1991). Staining of the human retina with monoclonal antibodies to protein kinase C isozymes. Abstracts for the Society for Neuroscience 17, 1564.Google Scholar
Kolb, H., Zhang, L. & Dekorver, L. (1992 b). Staining of the human retina with antisera to protein kinase C isozymes. Investigative Ophthalmology and Visual Science (Suppl.) 15, 1173.Google Scholar
Kouyama, N. & Marshak, D.W. (1992). Bipolar cells specific for blue cones in the macaque retina. Journal of Neuroscience 12, 1233–1252CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W.-S. (1985). Glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241–260CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984). Bipolar cells in monkey retina selective for cones likely to be blue-sensitive. Nature 308, 184–186CrossRefGoogle ScholarPubMed
Marshak, D.W., Aldrich, L.B., Valle, J.Del & Yamada, T. (1990). Localization of immunoreactive cholecystokinin precursor to amacrine cells and bipolar cells of the macaque monkey retina. Journal of Neuroscience 10, 3045–3055CrossRefGoogle ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425CrossRefGoogle Scholar
Muüller, B. & Peichl, L. (1991). Rod bipolars in the cone-dominated retina of the tree shrew, Tupaia belangeri. Visual Neuroscience 6, 629–640CrossRefGoogle Scholar
Nathans, J., Thomas, D. & Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding the blue, green, and red pigments. Science 232, 193–202CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1989). Immunocytochemical localization of protein kinase C in some vertebrate retinas. In Neurobiology of the Inner Retina. NAT ASI Series, Vol. H31, ed. Weiler, R. & Osborne, N., pp. 425–436. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell of the rod system in the retina of the cat. Journal of Neurophysiology 54, 592–614CrossRefGoogle ScholarPubMed
Osborne, N.N., Barnett, N.L., Morris, N.J. & Huang, F.L. (1992). The occurrence of three isozymes of protein kinase C (aα, Bβ, and rγ) in retinas of different species. Brain Research 570, 161–166CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist (3H)muscimol: A combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 25–35CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1988 a). Substance P-like immunoreactive amacrine cells in the cat retina. Journal of Comparative Neurology 275, 542–552CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1988 b). Colocalization of substance P and rγ-aminobutyric acid in amacrine cells of the cat retina. Brain Research 447, 164–168CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the monkey retina. Journal of Cell Biology 65, 192–222CrossRefGoogle Scholar
Schiller, P.H. (1992). The ON and OFF channels of the visual system. Trends in Neuroscience 15, 86–92CrossRefGoogle ScholarPubMed
Scholz, W.K. & Palfrey, H.C. (1991). Glutamate-stimulated protein phosphorylation in cultured hippocampal pyramidal neurons. Journal of Neuroscience 11, 2422–2432CrossRefGoogle ScholarPubMed
Siegel, E. & Bauer, R. (1988). Activation of protein kinase C differentially modulates neuronal Na+, Ca2+, and rγ-aminobutyrate type A channels. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6192–6196CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182–184CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1983). An excitatory amino acid antagonist blocks cone input to sign-conserving second-order retinal neurons. Science 219, 1230–1232CrossRefGoogle ScholarPubMed
Suzuki, S. & Kaneko, A. (1990). Identification of bipolar cell subtypes by protein kinase C-like immunoreactivity in the goldfish retina. Visual Neuroscience 5, 223–230CrossRefGoogle ScholarPubMed
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, 1241–1247CrossRefGoogle ScholarPubMed
Vaccarino, F., Guidotti, A. & Costa, E. (1987). Ganglioside inhibition of glutamate-mediated protein kinase C translocation in primary cultures of cerebellar neurons. Proceedings of the National Academy of Sciences of the U.S.A. 84, 8707–8711CrossRefGoogle ScholarPubMed
Vaccarino, F.M., Liljequist, S. & Tallman, J.F. (1991). Modulation of protein kinase C translocation by excitatory and inhibitory amino acids in primary cultures of neurons. Journal of Neurochemistry 57, 391–396CrossRefGoogle ScholarPubMed
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112CrossRefGoogle ScholarPubMed
Yazulla, S. & Studholme, K.M. (1992). Light dependent plasticity of Mb bipolar cell synaptic terminals. Investigative Ophthalmology and Visual Science (Suppl.) 15, 1172.Google Scholar
Young, H.M. & Vaney, D.I. (1991). The retinae of Prototherian mammals possess neuronal types that are characteristic of nonmammalian retinae. Visual Neuroscience 5, 61–66CrossRefGoogle Scholar
Zhang, L., Dekorver, L. & Kolb, H. (1992). Light and electron microscopy of immunostaining for protein kinase C and its isozymes in the turtle retina. Journal of Neurocytology (in press).CrossRefGoogle Scholar
Zrenner, E. (1983). Neurophysiological Aspects of Color Vision in Primates. Berlin: Springer.CrossRefGoogle Scholar