Abstract
The expression of MAP2 during rat brain development was studied by using specific antibodies and cDNA probes. MAP2 cDNAs were isolated from a rat brain λgt11 library, and their identity was confirmed by the reactivity of their fusion proteins with several independent monoclonal antibodies that recognize MAP2. Northern blot analyses of the RNA prepared from whole brains, cerebral cortex, hypothalamus, brain stem, olfactory bulbs, and cerebellum showed that the levels of MAP2 mRNA increase during the initial phase of development, reach a maximum between postnatal weeks 2 and 3, and then decrease in the adult. The time course and the kinetics of this change varied between different brain regions and appeared to reflect the pattern of morphological changes in these regions RNA blots were also analyzed with β-tubulin and β-actin cDNA probes to ensure the quality and the quantity of the RNA. The levels of MAP2 mRNA and protein showed similar changes during the initial part of brain development and suggested a transcriptional control. However, while MAP2 protein levels remained high throughout development, MAP2 mRNA levels decreased in adulthood. We suggest that the increased stability of the MAP2 molecule may be a contributing factor in the developmental regulation of steady-state levels of MAP2. *** DIRECT SUPPORT *** A07GO001 00014
Similar content being viewed by others
References
Bernhardt, R., Matus, A. (1984). Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: A difference between the dendritic and axonal cytoskeleton. J. Comp. Neurol. 226:203–221.
Binder, L.I., Frankfurter, A., Kim, H., Caceres, A., Payne, M.R., Rebhun, L.I. (1984). Heterogeneity of microtubule-associated protein during rat brain development. Proc. Natl. Acad. Sci. U.S.A. 81:5613–5617
Bond, J.F., Farmer, S.R. (1983). Regulation of tubulin and actin mRNA production in rat brain: Expression of a new beta-tubulin mRNA with development. Mol. Cell. Biol. 3:1333–1342.
Bruning, J.L., Kintz, B.L. (1977). Computational Hand-book of Statistics, 2nd ed. Forseman and Co. Glenview, IL.
Burgoyne, R.D. (1986). Microtubule proteins in neuronal differentiation. Comp. Biochem. Physiol. 83B:1–8
Burgoyne, R.D., Cumming, R. (1984). Ontogeny of microtubule-associated protein 2 in rat cerebellum: Differential expression of the double polypeptides. Neuroscience 11:156–167
Caceres, A., Banker, G., Steward, O., Binder, L., Payne, M. (1984). MAP 2 is localized to the dendrites of hippocampal neurons which develop in culture. Dev. Brain. Res. 13:314–318
Caron, J.M., Jones, A.L., Rall, L.B., Kirschner, M.W. (1985). Autoregulation of tubulin synthesis in enucleated cells. Nature 317:648–651
Chirgwin, J.M., Prezybla, A.E., MacDonald, R.J., Rutter, W.J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299
Church, G.M., Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. U.S.A. 81:1991–1995
Cleveland, D.W., Lopata, M.A., MacDonald, R.J., Cowan, N.J., Rutter, W.J., Kirschner, M.W. (1980). Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell 20:95–105
Cleveland, D.W., Lopata, M.A., Sherline, P., Kirschner, M.W. (1981). Unpolymerized tubulin modulates the levels of tubulin mRNAs. Cell 25:537–546
Couchi, D., Charriere-Bertrand, C., Nunez, J. (1988). Expression of the mRNA for tau proteins during brain development and in cultured neurons and astroglial cells. J. Neurochem. 50:1894–1899
De Camilli, P., Miller, P.E., Navone, F., Theurkauf, W.E., Vallee, R.B. (1984). Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience 11:817–846
Drubin, D.G., Kobayashi, S., Kellogg, D., Kirschner, M. (1988). Regulation of microtubule protein levels during cellular morphogenesis in nerve growth factor-treated PC12 cells. J. Cell Biol. 106:1583–1591
Fischer, I., Shea, T.B., Sapirstein, V.S., Kosik, K.S. (1986). Expression and distribution of microtubule-associated protein 2 (MAP2) in neuroblastoma and primary neuronal cells. Dev. Brain Res. 25:99–109
Fischer, I., Kosik, K.S., Sapirstein, V.S. (1987). Heterogeneity of microtubule-associated protein (MAP2) in vertebrate brains. Brain Res. 436:39–48
Fischer, I., Foutch, L.A., Safaei-Semnani R. (1988). Isolation and characterization of MAP2 cDNAs from rat brain. Trans. Am. Soc. Neurochem. 19:85
Garner, C.C., Matus, A. (1988). Different forms of microtubule associated protein 2 are encoded by separate mRNA transcripts. J. Cell. Biol. 106:779–783
Garner, C.C., Brugg, B., Matus, A. (1988). A 70 kDa microtubule-associated protein (MAP2c), related to MAP2. J. Neurochem. 50:609–615
Herrmann, H., Dalton, J.M., Wiche, G. (1985). Microheterogeneity of microtubule-associated proteins, MAP 1 and MAP 2, and differential phosphorylation of individual subcomponents. J. Biol. Chem. 260:5797–5803
Hirokawa, N. (1982). Cross-linker system between neurofilaments, microtubules and membrane organelles in frog axons revealed by quick-freeze deep-etching methods. J. Cell Biol. 94:129–142
Jacobson, M. (1978). Developmental Neurobiology, 2nd ed. Plenum Press, New York
Kim, H., Binder, L.I., Rosenbaum, J.L. (1979). The periodic association of microtubule-associated proteins with brain microtubules in vitro. J. Cell Biol. 80:266–276
Krieg, P., Melton D. (1984). Functional messenger RNAs are produced by SP6 in vitro transcription of cloned DNAs. Nucleic Acids Res. 12:7057–7070
Letterier, J.F., Wong, J., Liem, R.K., Shelanski, M.L. (1984). Promotion of microtubule assembly by neurofilament-associated microtubule-associated proteins. J. Neurochem. 43:1385–1391
Lewis, S.A., Villasante, A., Sherline, P., Cowan, N. (1986). Brain specific expression of MAP 2 detected using a cloned cDNA probe. J. Cell Biol. 102:2098–2105
Lewis, S.A., Wang, D., Cowan, N.J. (1988). Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242:936–939
Maniatis, T., Fritsch, E.F., Sambrook, J. (1982). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
Matus, A. (1988). Microtubule-associated proteins: Their potential role in determining neuronal morphology. Annu. Rev. Neurosci. 11:29–44
Neve, R.L., Harris, P., Kosik, K.S., Kurnit, D.M., Donlon, T.A. (1986). Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2. Mol. Brain. Res. 1:271–280
Nunez, J. (1986). Differential expression of microtubule components during brain development. Dev. Neurosci. 8:125–141
Olmsted, J.B. (1986). Microtubule-associated proteins. Annu. Rev. Cell Biol. 2:421–457
Riederer, B., Matus, A. (1985). Differential expression of distinct microtubule-associated proteins during brain development. Proc. Natl. Acad. Sci. U.S.A. 82:6006–6009
Runge, M., Laue, T., Yphantis, D., Lifsics, M., Saito, A., Altin, M., Reinke, K., Williams, Jr., R.C. (1981). ATP-induced information of an associated complex between microtubules and neurofilaments. Proc. Natl. Acad. Sci. U.S.A. 78:1431–1435
Safaei, R., Fischer, I. (1989). Cloning of a cDNA encoding MAP1B in rat brain: Regulation of mRNA levels during development. J. Neurochem. in press
Salzer, J.L., Holmes, W.P., Colman, D.R. (1987). The amino acid sequences of myelin-associated glycoprotein: Homology to the immunoglobin gene superfamily. J. Cell Biol. 104:957–965
Selden, S.C., Pollard, T.D. (1983). Phosphorylation of microtubule-associated proteins regulates their interaction within actin filaments. J. Biol. Chem. 258:7064–7071
Shiomura, Y., Hirokawa, N. (1987). Colocalization of microtubule-associated protein 1A and microtubule-associated protein 2 on neuronal microtubules in situ revealed with double-label immunoelectron microscopy. J. Cell Biol. 104:1575–1578
Shulman, H. (1984). Phosphorylation of microtubule-associated proteins by a Ca2+/Calmodulin-dependent protein kinase. J. Cell Biol. 99:11–19
Sloboda, R.D., Dentler, W.L., Rosenbaum, J.L. (1976). Microtubule-associated proteins and the stimulation of tubulin assembly in vitro. Biochemistry 15:4497–4505
Vallee, R.B., Bloom, G.S. (1984). High molecular weight microtubule-associated proteins. Modern Cell Biol. 3:21–76
Young, R.A., Davis, R.W. (1983). Efficient isolation of genes using antibody probes. Proc. Natl. Acad. Sci. U.S.A. 80:1194–1198
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Safaei, R., Fischer, I. Regulation of microtubule-associated protein 2 (MAP2) mRNA expression during rat brain development. J Mol Neurosci 1, 189–198 (1989). https://doi.org/10.1007/BF02918906
Issue Date:
DOI: https://doi.org/10.1007/BF02918906