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GAP-43 in the cat visual cortex during postnatal development

Published online by Cambridge University Press:  02 June 2009

Helen McIntosh
Affiliation:
Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis
Nigel Daw
Affiliation:
Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis
David Parkinson
Affiliation:
Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis

Abstract

GAP-43 levels have been determined by immunoassay in cat visual cortex during postnatal development to test the idea that GAP-43 expression could be related to the duration of the critical period for plasticity. For comparison, GAP-43 levels have also been assayed in primary motor cortex, primary somatosensory cortex, and cerebellum at each age. GAP-43 levels were high in all regions at 5 d (with concentrations ranging from 7−10 ng;/μg protein) and then declined 60−80% by 60 d of age. After 60 d of age, GAP-43 concentrations in each region continued a slow decline to adult values, which ranged from 0.5−2 ng/μg protein. To test for the involvement of GAP-43 in ocular dominance plasticity during the critical period, the effect of visual deprivation on GAP-43 levels was investigated. Monocular deprivation for 2−7 d, ending at either 27 or 35 d of age, had no effect on total membrane levels of GAP-43. The concentrations of membrane-associated GAP-43 prior to 40 d of age correlate with events that occur during postnatal development of the cat visual cortex. However, the slow decline in membrane-associated GAP-43 levels after 40 d of age may be an index of relative plasticity remaining after the peak of the critical period.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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References

Akers, R.F. & Routtenberg, A. (1985). Protein kinase C phosphorylates a 47Mr protein (Fl) directly related to synaptic plasticity. Brain Research 334, 147151.Google Scholar
Alexander, K.A., Wakim, B.A., Doyle, G.S., Walsh, K.A. & Storm, D.R. (1988). Identification and characterization of the calmodulinbinding domain of neuromodulin, a neurospecific calmodulinbinding protein. Journal of Biological Chemistry 263, 75447549.Google Scholar
Aloyo, V.J., Zwiers, H. & Gispen, W.H. (1983). Phosphorylation of B-50 protein by calcium-activated, phospholipid-dependent protein kinase and B-50 protein kinase. Journal of Neurochemistry 41, 649653.CrossRefGoogle ScholarPubMed
Benowitz, L.I., Apostolides, P.J., Perrone-bizzozero, N., Finkelstein, S.P. & Zwiers, H. (1988). Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. Journal of Neuroscience 8, 339352.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Clark, M.F. & Bar-Joseph, M. (1984). Enzyme immunosorbent assays in plant virology. Methods in Virology 7, 5185.Google Scholar
Clarke, S. & Innocenti, G.M. (1986). Organization of immature intrahemispheric connections. Journal of Comparative Neurology 251, 122.Google Scholar
Cragg, B.G. (1975). The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147166.CrossRefGoogle ScholarPubMed
Cynader, M. & Mitchell, D.E. (1980). Prolonged sensitivity to monocular deprivation in dark reared cats. Journal of Neurophysiology 43, 10261040.Google Scholar
Dekker, L.V., De Graan, P.N.E., Oestreicher, A.B., Versteeg, D.H.G. & Gispen, W.H. (1989 a). Inhibition of noradrenaline release by antibodies to B-50 (GAP-43). Nature 342, 7476.Google Scholar
Dekker, L.V., De Graan, P.N.E., Versteeg, D.H.G., Oestreicher, A.B. & Gispen, W.H. (1989 b). Phosphorylation of B-50 (GAP43) is correlated with neurotransmitter release in rat hippocampal slices. Journal of Neurochemistry 52, 2430.Google Scholar
Dudek, S.M. & Bear, M.F. (1989). A biochemical correlate of the critical period for synaptic modification in the visual cortex. Science 246, 673675.CrossRefGoogle ScholarPubMed
Foote, S.L. & Morrison, J.H. (1987). Development of the noradrenergic serotonergic, and dopaminergic innervation of neocortex. In Current Topics in Developmental Biology Moscona, A.A. & Monroy, A. (series editors), Vol. 21 Hart, R.K. (vol. ed.), Chapter 15, pp. 391422. New York: Academic Press, Inc.Google Scholar
Goslin, K., Schreyer, D.J., Skene, J.H.P. & Banker, G. (1988). Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature 336, 672674.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology 206, 419436.Google Scholar
Hyman, C. & Pfenninger, K.H. (1987). Intracellular regulators of neuronal sprouting, II: Phosphorylation reactions in isolated growth cones. Journal of Neuroscience 7, 40764083.Google Scholar
Jacobson, R.D., Virag, I. & Skene, J.H.P. (1986). A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. Journal of Neuroscience 6, 18431855.Google Scholar
Johes, K.R., Spear, P.D. & Tong, L. (1984). Critical periods for effects of monocular deprivation: differences between striate and extrastriate cortex. Journal of Neuroscience 4, 25432552.Google Scholar
Karns, L.R., Ng, S.-C., Freeman, J.A. & Fishman, M.C. (1987). Cloning of complementary DNA for GAP-43, a neuronal growthrelated protein. Science 236, 597600.Google Scholar
Kasamatsu, T., Pettigrew, J.D. & Ary, M. (1981). Cortical recovery from effects of monocular deprivation: acceleration with norepinephine and suppression with 6-hydroxydopamine. Journal of Neurophysiology 45, 254266.CrossRefGoogle Scholar
Laemmli, U.K. (1970). Clevage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.Google Scholar
LeVay, S., Stryker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. Journal of Comparative Neurology 179, 223244.Google Scholar
Lovinger, D.M., Akers, R.F., Nelson, R.B., Barnes, C.A., McNaughton, B.L. & Routtenberg, A. (1985). A selective increase in phosphorylation of protein Fl, a protein kinase C substrate, directly related to three-day growth of long-term synaptic enhancement. Brain Research 343, 137143.CrossRefGoogle Scholar
McIntosh, H. & Parkinson, D. (1990). GAP-43 in adult visual cortex. Brain Research 518, 324328.Google Scholar
McIntosh, H., Parkinson, D., Meiri, K., Daw, N. & Willard, M. (1989). A GAP-43-like protein in cat visual cortex. Visual Neuroscience 2, 583591.Google Scholar
Meiri, K.F., Pfenninger, K.H. & Willard, M.B. (1986). Growthassociated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proceedings of the National Academy of Sciences of the U.S.A. 83, 35373541.Google Scholar
Meyer, G. & Ferres-Torres, R. (1984). Postnatal maturation of non- pyramidal neurons in the visual cortex of the cat. Journal of Comparative Neurology 228, 226244.Google Scholar
Mower, G.D., Caplan, C.J., Christen, W.G. & Duffy, F.H. (1985). Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. Journal of Comparative Neurology 235, 448466.Google Scholar
Nelson, R.B. & Routtenberg, A. (1985). Characterization of protein F1 (47 kDa, 4.5 p1): A kinase C substrate directly related to neural plasticity. Experimental Neurology 89, 213224.CrossRefGoogle Scholar
Neve, R.L. & Bear, M.F. (1989). Visual experience regulates gene expression in the developing striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 86, 47814784.Google Scholar
Oakley, B.R., Kirsch, D.R. & Morris, N.R. (1980). A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Analytical Biochemistry 105, 361.CrossRefGoogle ScholarPubMed
O'Farrell, P.Z., Goodman, H.M. & O'Farrell, P.H. (1977). High-resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12, 11331142.Google Scholar
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 1721.Google Scholar
Perrone-Bizzozero, N.I., & Benowitz, L.I. (1987). Expression of a 48-kD growth-associated protein in the goldfish retina. Journal of neurochemistry 48, 644652.Google Scholar
Price, D.J. & Blakemore, C. (1985). The postnatal development of the association projection from visual cortical area 17 to area 18 in the cat. Journal of Neuroscience 5, 24432452.Google Scholar
Price, D.J. & Zumbroich, T.J. (1989). Postnatal development of corticocortical efferents from area 17 in the cat's visual cortex. Journal of Neuroscience 9, 600613.Google Scholar
Schwartz, J.H. & Greenberg, S.M. (1987). Molecular mechanisms for memory: second messenger induced modifications of protein kinases in nerve cells. Annual Review of Neuroscience 10, 459476.Google Scholar
Shatz, C.J. & Luskin, M.B. (1986). The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex. Journal of Neuroscience 6, 36653668.Google Scholar
Skene, J.H.P., Jacobson, R.D., Snipes, G.J., McGuire, C.B., Norden, J.J. & Freeman, J.A. (1986). A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233, 783786.CrossRefGoogle Scholar
Skene, J.H.P. & Willard, M.B. (1981 a). Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. Journal of Cell Biology 89, 96103.Google Scholar
Skene, J.H.P. & Willard, M.B. (1981 b). Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells. Journal of Cell Biology 89, 8695.Google Scholar
Snipes, G.J., Chan, S.Y., McGuire, C.B., Costello, B.R., Norden, J.J., Freeman, J.A. & Routtenberg, A. (1987). Evidence for the coidentification of GAP-43, a growth-associated protein, and F1, a plasticity-associated protein. Journal of Neuroscience 7, 40664075.Google Scholar
Stichel, C.C. & Singer, W. (1987). Quantitative analysis of the choline acetyltransferase-immunoreactive axonal network in the cat primary visual cortex; II: Prenatal and postnatal development. Journal of Comparative Neurology 258, 99111.CrossRefGoogle Scholar
van Dongen, C.J., Zwiers, H., De Graan, P.N.E. & Gispen, W.H. (1985). Modulation of the activity of purified phosphatidylinositol 4-phosphate kinase by phosphorylated and dephosphorylated B-50 protein. Biochemical and Biophysical Research Communications 128, 12191227.Google Scholar
Van Hooff, C.O.M., De Graan, P.N.E., Oestreicher, A.B. & Gispen, W.H. (1988) B-50 phosphorylation and polyphosphoinositide metabolism in nerve growth cone membranes. Journal of Neuroscience 8, 17891795.Google Scholar
Van Lookeren Camoagne, M., Oestreicher, A.B., Van Bergen Henegouwen, P.M.P. & Gispen, W.H. (1989). Ultrastructural immunocytochemical localization of B-50/GAP43, a protein kinase C substrate, in isolated presynaptic nerve terminals and neuronal growth cones. Journal of Neurocytology 18 479489.Google Scholar
Wakim, B.T., Alexander, K.A., Masure, H.R., Cimler, B.M., Storm, D.R. & Walsh, K.A. (1987). Amino acid sequence of P-57, a neuro-specific calmodulin-binding protein. Biochemistry 26, 74667470.Google Scholar
Winfield, D.A. (1983). The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. Developmental Brain Research 9, 155169.CrossRefGoogle Scholar
Zwiers, H., Oestreicher, A.B., Bisby, M.A., De, Graan P.N.E. & Gispen, W.H. (1987). Protein kinase C substrate B-50 in adult and developing rat brain is identical to axonally transported GAP-43 in regenerating peripheral rat nerve. In Axonal Transport: Proceedings of a Satellite Symposium of the 30th Congress of the International Union of Physiological Sciences ed. Smith, R.S. & Bisby, M.A., pp. 421433. New York: Alan R. Liss, Inc.Google Scholar