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Protein Kinase C-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study

Published online by Cambridge University Press:  02 June 2009

Danru Zhang  and
Hermes H. Yeh
Danru Zhang
Affiliation:
Department of Neurobiology and Anatomy, University of Rochester Medical Center, Rochester
Hermes H. Yeh
Affiliation:
Department of Neurobiology and Anatomy, University of Rochester Medical Center, Rochester
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Abstract

In the retina of a variety of vertebrate species, a monoclonal antibody against protein kinase C (PKC) has been shown to label preferentially bipolar cells. Although the functional consequences of PKC activation in these cells is yet to be revealed, the present study was motivated in part by the possibility that the antibody might be used as a selective marker for examining the development of bipolar cells in the rat retina. Here, the developmental pattern and the dynamic changes of retinal cells expressing PKC-like immunoreactivity (PKC-LI) were studied and analyzed throughout postnatal life until adulthood. Upon its initial detection by immunohistochemistry on postnatal day (PD)-10, faint PKC-LI was limited to the central region of the retina, labeling cell bodies located at the scleral margin of the inner nuclear layer (INL) adjacent to the outer plexiform layer (OPL). On subsequent days, PKC-LI spread progressively to the peripheral retina and axon terminal bulbs at the vitreal margin of theinner plexiform layer (IPL) began showing the first signs of immunoreactive labeling. Not until PD-15, the time of eye opening, did PKC-LI in these cells increase to the extent such that their thin axons were immunoreactive. Each of these axons traversed the entire thickness of the IPL and divided into two or three short branches before ending as enlarged terminal bulbs. The morphology and the location of PKC-LI cells in both the developing and adult retina observed in our study are consistent with them being rod bipolar cells. By the end of the fourth postnatal week, the rod bipolar cells appeared mature, resembling those found in the adult. Overall, more dynamic changes occurred at the axon terminal bulbs than at the cell bodies during the maturational process of rod bipolar cells. Interestingly, PKIC-LI was expressed precociusly in these cells when rat pups were reared in complete darkness starting from the day of birth.

Keywords

Rat retinaProtein kinase CBipolar cellsPostnatal developmentImmunohistochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 5 , May 1991 , pp. 429 - 437
Copyright
Copyright © Cambridge University Press 1991

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References

Bixby, J.L. (1989). Protein kinase C is involved in laminin stimulation of neurite outgrowth. Neuron 3, 287–297.CrossRefGoogle ScholarPubMed
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the Albino rat. American Journal of Anatomy 127, 281–302.CrossRefGoogle ScholarPubMed
Brandt, S.J., Niede, J.E., Bell, R.M. & Young, W.S. (1987). Distinct patterns of expression of different protein kinase C mRNAs in rat tissues. Cell 49, 57–63.CrossRefGoogle ScholarPubMed
Coussens, L., Parker, P.J., Rhee, L., Yang-Feng, T.L., Chen, E., Waterfield, D., Francke, U. & Ullrich, A. (1986). Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. Science 233, 859–866.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neuroscience 13, 110–115.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). Retina: An Approachable Part of the Brain. Cambridge: The Belknap Press of Harvard University Press. pp. 46–80.Google Scholar
Girard, P.R., Mazzei, G.J., Wood, J.G. & Kuo, J.F. (1985). Polyclonal antibodies to phospholipid/Ca2+-dependent protein kinase and immunocytochemical localization of the enzyme in rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3030–3034.CrossRefGoogle ScholarPubMed
Hashimoto, T., Ase, K., Sawamura, S., Kikkawa, U., Saito, N., Tanaka, C. & Nishizuka, Y. (1988). Postnatal development of a brain-specific subspecies of protein kinase C in rat. Journal of Neuroscience 8, 1678–1683.CrossRefGoogle ScholarPubMed
Horsburgh, G.M. & Sefton, J. (1987). Cellular degneration and synaptogenesis in the developing retina of the rat. Journal of Comparative Neurology 263, 553–566.CrossRefGoogle Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kikkawa, U., Kishimoto, A. & Nishizuka, Y. (1989). The protein kinase C family: heterogeneity and its implications. Annual Review of Biochemistry 58, 31–44.CrossRefGoogle ScholarPubMed
Knopf, J.L., Lee, M.-H., Sultzman, L.A., Kriz, R.W., Loomis, C.R., Hewick, R.M. & Bell, R.M. (1986). Cloning and expression of multiple protein kinase C cDNAs. Cell 46, 491–502.CrossRefGoogle ScholarPubMed
Minakuchi, R., Takai, Y., Yu, B. & Nishizuka, Y. (1981). Widespread occurrence of calcium-activated, phospholipid-dependent protein kinase in mammalian tissues. Journal of biochemistry 89, 1651–1654.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, 247–252.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1986). Studies and perspectives of protein kinase C. Science 233, 305–312.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334, 661–665.CrossRefGoogle ScholarPubMed
Ohno, S., Kawasaki, H., Imajoh, S. & Suzuki, K. (1987). Tissue-specific expression of three distinct types of rabbit protein kinase C. Nature 325, 161–166.CrossRefGoogle ScholarPubMed
Sternberger, L.A. (1979). Immunocytochemistry, 2nd edition. New York: Wiley.Google Scholar
Suzuki, S. & Kaneko, A. (1990). Identification of bipolar cell subtypes by protein kinase C-like immunoreactivity in the goldfish retina. Visual Neuroscience 5, 223–230.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, 7603–7609.CrossRefGoogle ScholarPubMed
Turner, R.S., Raynor, R.L., Mazzei, G.J., Girard, P.R. & Kuo, J.F. (1984). Developmental studies of phospholipid-sensitive Ca2+-dependent protein kinase and its substrates and of phosphoprotein phosphatases in rat brain. Procedings of the National Academy of Sciences of the U.S.A. 81, 3143–3147.CrossRefGoogle ScholarPubMed
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Cranbrook Institute of Science Bull. No. 19, Bloomfield Hills, Ml: Cranbrook Press.Google Scholar
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. Archives of Ophthalmology 79, 470–484.CrossRefGoogle ScholarPubMed
Wise, B.C., Andersson, R.G.G., Mackerlova, L., Raynor, R.L., Solomonsson, I. & Kuo, J.F. (1981). Ontogenic aspects of phospholipid-sensitive calcium-dependent protein kinase in guinea pig tissues. Biochemical Biophysical Research Communications 99, 407–413.CrossRefGoogle Scholar
Wood, J.G., Girard, P.R., Mazzei, G.J. & Kuo, J.F. (1986). Immunocytochemical localization of protein kinase C in identified neuronal compartments of rat brain. Journal of Neuroscience 6, 2571–2577.CrossRefGoogle ScholarPubMed
Wood, J.G., Hart, C.E., Mazzei, G.J., Girard, P.R. & Kuo, J.F. (1988). Distribution of protein kinase Cimmunoreactivity in rat retina. The Histochemical Journal 20, 63–68.CrossRefGoogle Scholar
Worley, P.F., Baraban, J.M. & Snyder, S.H. (1986a). Heterogeneous localization of protein kinase C in rat brain: autoradiographic analysis of phorbol ester receptor binding. Journal of Neuorscience 6, 199–207.CrossRefGoogle ScholarPubMed
Worley, P.F., Baraban, J.M., De Souza, E.B. & Snyder, S.H. (1986b). Mapping second-messenger systems in the brain: differential localizations of adenylate cyclass and protein kinase C. Proceedings of the National Academy of Sciences of the U.S.A. 83, 4053–4057.CrossRefGoogle ScholarPubMed