Summary
The cytoskeleton is important for neuronal morphogenesis. During the postnatal development of cat brain, the molecular composition of the neuronal cytoskeleton changes with maturation. Several of its proteins change in their rate of expression, in their degree of phosphorylation, in their subcellular distribution, or in their biochemical properties. It is proposed that phosphorylation is an essential mechanism to regulate the plasticity of the early, juvenile-type cytoskeleton. Among such proteins are several microtubule-associated proteins (MAPs), such as MAP5a, MAP2c or the juvenile tau proteins. Phosphorylation may also act on neurofilaments, postulated to be involved in the adult-type stabilization of axons. These observations imply that phosphorylation may affect cytoskeleton function in axons and dendrites at various developmental stages. Yet, the mechanisms of phosphorylation and its regulation cascades are largely unknown. In view of the topic of this issue on CD15, the potential role of matrix molecules being involved in the modulation of phosphorylation activity and of cytoskeletal properties is addressed.
Similar content being viewed by others
References
Almas, B., Pryme, I. F., Vedeler, V. &Hesketh, J. E. (1992) Insulin: signal transmission and short-term effects on the cytoskeleton and protein synthesis.Int. J. Biochem. 24, 183–91.
Avila, J., Serrano, L., Hernandez, M. A. &Diaz-Nido, J. (1988) Phosphorylation of neuronal microtubule proteins.Protoplasma 145, 82–99.
Baudier, J., Lee, S.-H. &Cole, R. D. (1987) Separation of the different microtubule-associated Tau protein species from bovine brain and their mode II phosphorylation by Ca2+/phospholipid-dependent protein kinase C.J. Biol. Chem. 262, 17584–90.
Bennett, V. (1990). Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm.Physiol. Rev. 70, 1029–65.
Bernhardt, R., Huber, G. &Matus, A. (1985) Differences in the developmental patterns of three microtubule-associated proteins in the rat cerebellum.J. Neurosci 5, 977–91.
Binder, L. I., Frankfurter, A., Kim, H., Caceres, A., Payne, M. R. &Rebhun, L. I. (1984) Heterogeneity of microtubule-associated protein 2 during rat brain development.Proc. Natl Acad. Sci. USA 81, 5613–7.
Binder, L. I., Frankfurter, A. &Rebhun, L. I. (1985) The distribution of tau polypeptides in the mammalian central nervous system.J. Cell Biol. 103, 1371–8.
Bloom, G. S., Schoenfeld, T. A. &Vallee, R. B. (1984) Widespread distribution of the major polypeptide component of MAP1A (microtubule-associated protein 1A) in the nervous system.J. Cell Biol. 98, 320–30.
Bloom, G. S., Luca, F. C. &Vallee, R. B. (1985) Microtubule-associated protein 1B: identification of a major component of the neuronal cytoskeleton.Proc. Natl Acad. Sci. USA 82, 5404–8.
Brion, J. P., Guilleminot, J., Couchie, D., Flament-Durand, J. &Nunez, J. (1988) Both adult and juvenile tau microtubule-associated proteins are axon specific in the developing and adult rat cerebellum.Neurosci. 25, 139–46.
Brugg, B. &Matus, A (1988) PC12 cells express juvenile microtubule-associated proteins during NGF-induced neurite outgrowth.J. Cell Biol. 107, 643–50.
Brugg, B. &Matus, A. (1991) Phosphorylation determines the binding of MAP2 to microtubules in living cells.J. Cell Biol. 114, 735–43.
Calvert, R. &Anderton, B. H. (1985) A microtubule-associated protein (MAP1) which is expressed at elevated levels during development of the rat cerebellum.EMBO J. 4, 1171–6.
Carlier, M. F., Simon, C., Cassoly, R. &Pradel, F. A. (1984) Interaction between microtubule-associated protein tau and spectrin.Biochim. 66, 305–11.
Dhermy, D. (1991) The spectrin super-family.Biol. Cell. 71, 249–54.
Diaz-Nido, J., Armas-Portela, R. &Avila, J. (1991) Addition of protease inhibitors to culture medium of neuroblastoma cells induces both neurite outgrowth and phosphorylation of microtubule-associated protein MAP1B.J. Cell Sci. 98, 409–14.
Figlewicz, D. A., Gremo, F. &Innocenti, G. M. (1988) Differential expression of neurofilament subunits in the developing corpus callosum.Dev. Brain Res. 42, 181–9.
Francon, J., Lennon, A. M., Fellous, A., Mareck, A., Pierre, M. &Nunez, J. (1982) Heterogeneity of microtubule-associated proteins and brain development.Eur. J. Biochem. 129, 465–71.
Garner, C. C. &Matus, A. (1988) Different forms of microtubule-associated protein 2 are encoded by separate mRNA transcripts.J. Cell Biol. 106, 779–83.
Garner, C. C., Brugg, B. &Matus, A. (1988) A 70 kDa microtubule-associated protein (MAP2c) related to MAP2.J. Neurochem. 50, 609–15.
Garner, C. C., Matus, A., Anderton, B. &Calvert, R. (1989) Microtubule-associated proteins MAP5 and MAP1x: closely related components of the neuronal cytoskeleton with different cytoplasmic distribution in the developing brain.Molec. Brain Res. 5, 85–92.
Goedert, M. &Jakes, R. (1990) Expression of separate isoforms of human Tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization.EMBO J. 9, 4225–30.
Goedert, M., Crowther, R. A. &Garner, C. C. (1991) Molecular characterization of microtubule-associated proteins tau and MAP2.Trends Neurosci. 14, 193–9.
Goodman, S. R., Zagon, I. S., Whitfield, C. F., Casoria, L. A., Shohet, S. B., Bernstein, S. E., Mclaughlin, P. J. &Laskiewicz, T. L. (1984) A spectrin-like protein from mouse brain membranes: phosphorylation of the 235,000-dalton subunit.Am. J. Physiol. 16, C61–73.
Goodman, S. R., Krebs, K. E., Whitfield, C. F., Riederer, B. M. &Zagon, I. S. (1988) Spectrin and related molecules.CRC Crit. Rev. Biochem. 23, 171–234.
Guadano-Ferraz, A., Riederer, B. M. &Innocenti, G. M. (1990) Developmental changes in the heavy subunit of neurofilaments in the corpus callosum of the cat.Dev. Brain Res. 56, 244–56.
Hadcock, J. R. &Malbon, C. C. (1991) Regulation of receptor expression by agonists: transcriptional and post-transcriptional controls.Trends Neurosci. 14, 242–7.
Hisanaga, S. &Hirokawa, N. (1990) Dephosphorylation-induced interactions of neurofilaments with microtubules.J. Cell Biol. 265, 21852–8.
Hoshi, M., Akiyama, T., Shinohara, Y., Miyata, Y., Ogawara, H., Nishida, E. &Sakai, H. (1988) Protein-kinase C catalyzed phosphorylation of the microtubule-binding domain of microtubule-associated protein 2 inhibits its ability to induce tubulin polymerization.Eur. J. Biochem. 174, 225–30.
Huber, G. &Matus, A. (1984) Differences in the cellular distribution of two microtubule-associated proteins, MAP1, and MAP2, in the rat brainJ. Neurosci. 4, 151–60.
Kadowaki, T., Nishida, E., Kasuga, M., Akiyama, T., Takaku, F., Ishikawa, M., Sakai, H., Kathurida, S. &Fujita-Yamaguchi, Y. (1985) Phosphorylation of fodrin (nonerythroid spectrin) by the purified insulin receptor kinase.Biochem. Biophys. Res. Com. 127, 493–500.
Kyriakis, J. M. &Avruch, J. (1990) pp54 microtubule-associated protein 2 kinase.J. Biol. Chem. 265, 17 355–63.
Lee, G. (1990) Tau protein: an update on structure and function.Cell Mot. Cytoskel. 15, 199–203.
Lindwall, G. &Cole, R. D. (1984) Phosphorylation affects the ability of tau protein to promote microtubule assemblyJ. Biol. Chem. 259, 5301–5.
Mareck, A., Fellous, A., Francon, J. &Nunez, J. (1980) Changes in composition and activity of microtubule-associated proteins during brain development.Nature 284, 353–45.
Matus, A. (1988) Microtubule-associated proteins: their potential role in determining neuronal morphology.Ann. Rev. Neurosci. 11, 29–44.
Mochly-Rosen, D., Henrich, C. J., Cheever, L., Khaner, H. &Simpson, P. C. (1990) A protein kinase C isozyme is translocated to cytoskeletal elements on activation.Cell Reg. 1, 693–706.
Murthy, A. S. &Flavin, M. (1983) Microtubule assembly using microtubule-associated protein MAP2 prepared in defined states of phosphorylation with protein kinase and phosphatase.Eur. J. Biochem. 137, 37–46.
Nestler, E. J., Walaas, S. I. &Greengard, P. (1984) Neuronal phosphoproteins: physiological and clinical implications.Science 225, 1357–64.
Nixon, R. A. &Sihag, R. (1991) Neurofilament phosphorylation: a new look at regulation and function.Trends Neurosci.14, 501–6.
Papasozomenos, S. Ch. &Binder, L. I. (1987) Phosphorylation determines two distinct species of tau in the central nervous system.Cell Motil. Cytoskel. 8, 210–26.
Payrastre, B., Van Bergen En Hennegouwen, P. M. P., Breton, M., Hartigh, J. C., Plantavid, M., Verkleij, A. J. &Boonstra, J. (1991) Phosphoinositide kinase, diacylglycerol kinase and phospholipase C activities associated to the cytoskeleton: effect of epidermal growth factor.J. Cell Biol. 115, 121–8.
Pollerberg, E., Burridge, K., Krebs, K., Goodman, S. &Schachner, M. (1987) The 180 kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions.Cell Tissue Res. 250, 227–36.
Riederer, B. M. (1990) Some aspects of the neuronal cytoskeleton in development.Eur. J. Morphol. 28, 347–78.
Riederer, B. M. &Innocenti, G. M. (1991), Differential distribution of tau proteins in developing cat cerebral cortex and corpus callosum.Eur. J. Neurosci. 3, 1134–45.
Riederer, B.M. & Innocenti, G.M. (1992) MAP2 isoforms in developing cat cerebral cortex and corpus callosum.Eur. J. Neurosci. (in press).
Riederer, B. &Matus, A. (1985) Differential expression of distinct microtubule-associated proteins during brain development.Proc. Natl. Acad. Sci. USA,82, 6006–9.
Riederer, B., Cohen, R. &Matus, A., (1986) MAP5: a novel brain microtubule-associated protein under strong developmental regulation.J. Neurocytol. 15, 763–75.
Riederer, B. M., Zagon, I. S. &Goodman, S. R. (1987) Brain spectrin (240/235) and brain spectrin (240/235E): differential expression during mouse brain development.J. Neurosci. 7, 864–74.
Riederer, B. M., Guadano-Ferraz, A. &Innocenti, G. M. (1990) Difference in distribution of microtubule-associated protein 5a and 5b during the development of cerebral cortex and corpus callosum in cats: dependence on phosphorylation.Dev. Brain Res. 56, 235–43.
Riederer, B. M., Monnet-Tschudi, F. &Honegger, P. (1992) Development of the neuronal cytoskeleton in aggregated cell cultures of fetal rat telencephalon and influence of elevated K+ concentrations.J. Neurochem. 58, 649–58.
Robinson, P. A. &Anderton, B. H. (1988) Neurofilament probes—a review of neurofilament distribution and biology.Rev. Neurosci. 2, 1–40.
Sano, M., Nishiyama, K. &Kitajiama, S. (1990) A nerve growth factor-dependent protein kinase that phosphorylated microtubule-associated proteins in vitro: possible involvement of its activity in the outgrowth of neurites form PC12 cells.J. Neurochem. 55, 427–35.
Seger, R., Ahn, N. G., Boulton, T. G., Yancopoulos, G. D., Panayotatos, N., Radziejewska, E., Ericson, L., Bratlien, R. L., Cobb, M. H. &Krebs, E. G. (1991) Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation of both tyrosine and threonine residues: implications for their mechanism of activation.Proc. Natl Acad. Sci. USA 88, 6142–6.
Stefanova, I., Horejsi, V., Ansotegui, I. J., Knapp, W. &Stockinger, H. (1991) GPI-anchored cell-surface molecules complexed to protein tyrosine kinases.Science 254, 1016–9.
Steiner, B., Mandelkow, E. M., Biernat, J., Guske, N., Meyer, H. E., Schmidt, B., Mieskes, G., Soelling, H. D., Drechsel, D., Kirschner, M. W., Goedert, M. &Mandelkow, E. (1990) Phosphorylation of microtubule-associated protein tau: identification of the site for Ca2+-calmodulin dependent kinase and the relationship with tau phosphorylation in Alzheimer tangles.EMBO J. 9, 3539–44.
Theurkauf, W. &Vallee, R. B. (1983) Extensive cAMP-dependent and cAMP-independent phosphorylation of microtubule-associated protein 2.J. Biol. Chem. 258, 7883–6.
Tucker, R. P., Binder, L. I. &Matus, A. I. (1988a) Neuronal microtubule-associated proteins in the embryonic avian spinal cord.J. Comp. Neurol. 271, 44–55.
Tucker, R. P., Binder, L. I., Viereck, C., Hemmings, B. A. &Matus, A. I. (1988b) The sequential appearance of low and high-molecular-weight forms of MAP2 in the developing cerebellum.J. Neurosci. 8, 4503–12.
Vallee, R. B. (1982) A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs).J. Cell Biol. 92, 435–42.
Yamamoto, H., Fukunaga, K., Tanaka, E. &Miyamoto, E. (1983) Ca2+-and calmodulin-dependent phosphorylation of microtubule-associated protein 2 and tau factor, and inhibition of microtubule assembly.J. Neurochem. 41, 1119–25.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Riederer, B.M. Differential phosphorylation of some proteins of the neuronal cytoskeleton during brain development. Histochem J 24, 783–790 (1992). https://doi.org/10.1007/BF01046350
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01046350