Abstract
Our laboratory has previously characterized a keratan sulfate proteoglycan, named claustrin, and shown by molecular cloning that claustrin and the mouse MAP1B protein share high homology, with claustrin representing a 5′-truncated fragment of MAP1B. In the present study, we examine further the relationship between claustrin and MAP1B, and also describe the isolation of a cDNA encoding the 3′-region of MAP1B, which shares 3′-untranslated sequence, but not coding sequence, with claustrin. We call this partial cDNA 3′-MAP1B-related clone (3′-MRC), since it is homologous to the 3′-region of the mouse MAP1B sequence. We show by Northern analysis that distinct mRNAs are recognized by the claustrin and 3′-MRC cDNAs, and by RT-PCR that mRNAs encoding these distinct MAP1B-related molecules are present in embryonic chick brain and cardiac and smooth muscle. Our data also suggest a higher level of expression of claustrin mRNA in astrocyte cultures, when compared to 3′-MRC. Our data therefore provide new evidence that alternatively spliced variants of MAP1B are expressed in brain, and that at least one of these variants encodes the claustrin proteoglycan.
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References
Black M. M., Slaughter T., and Fischer I. (1994) Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons.J. Neurosci. 14, 857–870.
Bloom G. S., Luca F. C., and Vallee R. B. (1985) Microtubule associated protein 1B: identification of a major component of the neuronal cytoskeleton.Proc. Natl. Acad. Sci. USA 82, 5404–5408.
Briones E. and Wiche G. (1985)M r 205,000 sulfoglycoprotein in extracellular matrix of mouse fibroblast cells is immunologically related to high molecular weight microtubule-associated proteins.Proc. Natl. Acad. Sci. USA 82, 5776–5780.
Brugg B., Reddy D., and Matus A. (1993) Attenuation of microtubule associated protein 1B expression by antisense oligonucleotides inhibits initiation of neurite outgrowth.Neuroscience 52, 489–496.
Burg M. and Cole G. J. (1990) Characterization of cell-associated proteoglycans synthesized by embryonic neural retinal cells.Arch. Biochem. Biophys. 276, 396–404.
Burg M. A. and Cole G. J. (1994) Claustrin, an antiadhesive neural keratan sulfate proteoglycan, is structurally related to MAP1B.J. Neurobiol. 25, 1–22.
Campagnoni A. T., Pribyl T. M., Campognoni C. W., Kampf K., Amur-Umarjee S., Landry C. F. (1993) Structure and developmental regulation ofGolli-mbp, a 105-kolobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain.J. Biol. Chem. 268, 4930–4938.
Chomczynski P. and Sacchi N. (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction.Anal. Biochem. 162, 156–159.
Cole G. J. and McCabe C. F. (1991) Identification of a developmentally regulated keratan sulfate proteoglycan that inhibits cell adhesion and neurite outgrowth.Neuron 7, 1007–1018.
Ding M. and Vandre D. D. (1994) Evidence for the glycoprotein nature of high molecular weight MAPs.Mol. Biol. Cell 5:S, 167a.
Edelmann W., Zervas M., Costello P., Roback L., Rischer I., Hammarback J. A., et al. (1996) Neuronal abnormalities in microtubule-associated protein 1B mutant mice.Proc. Natl. Acad. Sci. USA 93, 1270–1275.
Eide F. F., Vining E. R., Eide B. L., Zang K., Wang X.-Y., and Reichardt L. F. (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling.J. Neurosci. 16, 3123–3129.
Faissner A., Clement A., Lochter A., Streit A., Mandl C., and Schachner M. (1994) Isolation of a neural chondroitin sulfate proteoglycan with neurite out-growth promoting properties.J. Cell Biol. 126, 783–799.
Fichard A., Verna J.-M., Olivares J., and Saxod R. (1991) Involvement of a chondroitin sulfate proteoglycan in the avoidance of chick epidermis by dorsal root ganglia fibers: a study using β-d-Xyloside.Dev. Biol. 148, 1–9.
Friedlander D. R., Milev P., Karthikeyan L., Margolis R. K., Margolis R. U., and Grumet M. (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth.J. Cell Biol. 125, 669–680.
Hammarback J. A., Obar R. A., Hughes S. M., and Vallee R. B. (1991) MAP1B is encoded as a poly-protein that is processed to form a complex N-terminal microtubule-binding domain.Neuron 7, 129–139.
Hamre K. M., Chepenik K. P., and Goldowitz D. (1995) The annexing: specific markers of midline structures and sensory neurons in the developing murine central nervous system.J. Comp. Neurol. 352, 421–435.
Kelly M. M., Phanhthourath C., Brees D. K., McCabe C. F., and Cole G. J. (1995) Molecular characterization of EAP-300: a high molecular weight, embryonic polypeptide containing an amino acid repeat comprised of multiple leucine-zipper motifs.Dev. Brain Res. 85, 31–47.
Margolis R. K. and Margolis R. U. (1993) Nervous tissue proteoglycans.Experimentia 49, 429–446.
McCabe C. F. and Cole G. J. (1992) Expression of the barrier-associated proteins EAP-300 and claustrin in the developing central nervous system.Dev. Brain Res. 70, 9–24.
McKeon R. J., Schreiber R. C., Rudge J. S., and Silver J. (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes.J. Neurosci. 11, 3398–3411.
Ngsee J. K. and Scheller R. H. (1989) Isolation and characterization of two homologous cDNA clones from Torpedo electromotor neurons.DNA 8, 555–561.
Noble M., Lewis S. A., and Cowan N. J. (1989) The microtubule-binding domain of microtubule-associated protein MAP1B contain a repeated sequence motif unrelated to that of MAP2 and tauf.J. Cell Biol. 109, 3367–3376.
Perris R. and Johansson S. (1987) Amphibian neural crest cell migration on purified ECM components: a chondroitin sulfate proteoglycan inhibits locomotion on fibronectin substrates.J. Cell Biol. 105, 2511–2521.
Pettway Z., Guillory G., and Bronner-Fraser M. (1990) Absence of neural crest cells from the region surrounding implanted notochordsin situ.Dev. Biol. 142, 335–345.
Rienitz A., Grennigloh G., Hermans-Borg-Meyer J., Kirsch J., Littauer U. Z., Prior P., et al. (1989) Neuraxin, a novel putative structural protein of the rat central nervous system that is immunologically related to microtubule-associated protein 5.EMBO J. 8, 2879–2888.
Sanger F., Nicklen S., and Coulson A. R. (1977) DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA 74, 5463–5467.
Silver J., Poston M., and Rutishauser U. (1987) Axon pathway boundaries in the developing brain. I. Cellular and molecular determinants that separate the optic and olfactory projections.J. Neurosci. 7, 2264–2272.
Silver J., Edwards M. A., and Levitt P. (1993) Immunocytochemical demonstration of early appearing astroglial structures that form boundaries and pathways along axon tracts in the fetal brain.J. Comp. Neurol. 328, 415–436.
Snow D. M., Lemmon V., Carrino D. A., Carplan A. I., and Silver J. (1990a) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro.Exp. Neurol. 109, 111–130.
Snow D. M., Steindler D. A., and Silver J. (1990b) Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier.Dev. Biol. 138, 359–376.
Steindler D. A. (1993) Glial boundaries in the developing nervous system.Ann. Rev. Neurosci. 16, 445–470.
Takei Y., Kondo S., Harada A., Inomata S., Noda T., and Hirokawa N. (1997) Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene.J. Cell Biol. 137, 1615–1626.
Tucker R. P. (1990) The roles of microtubule-associated proteins in brain morphogenesis: a review.Brain Res. Rev. 15, 101–120.
Ulloa L., Ibarrola N., Avila J., and Diez-Guerra F. J. (1994) Microtubule-associated protein 1B (MAP1B) is present in glial cells phosphorylated different than in neurones.Glia 10, 266–275.
Yuan Y., Lee J.-A., Napier A., and Cole G. J. (1997) Molecular cloning of a new intermediate filament protein expressed by radial glia and demonstration of alternative splicing in a novel heptad repeat region located in the carboxy-terminal tail domain.Mol. Cell. Neurosci. 10, 71–86.
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Burg, M.A., Lee, JA. & Cole, G.J. An alternatively spliced, 5′-truncated MAP1B isoform is expressed in the developing chick nervous system. J Mol Neurosci 9, 177–186 (1997). https://doi.org/10.1007/BF02800500
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DOI: https://doi.org/10.1007/BF02800500