Full Access
Activity-dependent regulation of N-cadherin in DRG neurons: Differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials
Kouichi Itoh,
Miwako Ozaki,
Beth Stevens,
R. Douglas Fields,
Kouichi Itoh
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorMiwako Ozaki
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorBeth Stevens
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorCorresponding Author
R. Douglas Fields
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892Search for more papers by this authorKouichi Itoh,
Miwako Ozaki,
Beth Stevens,
R. Douglas Fields,
Kouichi Itoh
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorMiwako Ozaki
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorBeth Stevens
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Search for more papers by this authorCorresponding Author
R. Douglas Fields
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892
Unit on Neurocytology and Physiology, Laboratory of Developmental Neurobiology, UNP, National Institutes of Health, NICHD, Building 49, Room 5A38, 49 Convent Drive, Bethesda, Maryland 20892Search for more papers by this authorFirst published: 07 December 1998
Citations: 86
Abstract
Cell adhesion molecule (CAM) expression is highly regulated during nervous system development to control cell migration, neurite outgrowth, fasciculation, and synaptogenesis. Using electrical stimulation of mouse dorsal root ganglion (DRG) neurons in cell culture, this work shows that N-cadherin expression is regulated by neuronal firing, and that expression of different CAMs is regulated by distinct patterns of neural impulses. N-cadherin was down-regulated by 0.1 or 1 Hz stimulation, but NCAM mRNA and protein levels were not altered by stimulation. L1 was down-regulated by 0.1 Hz stimulation, but not by 0.3 Hz, 1 Hz, or pulsed stimulation. N-cadherin expression was lowered with faster kinetics than L1 (1 vs. 5 days), and L1 mRNA returned to higher levels after terminating the stimulus. The RSLE splice variant of L1 was not regulated by action potential stimulation, and activity-dependent influences on L1 expression were blocked by target-derived influences. The results are consistent with changes in firing pattern accompanying DRG development and suggest that functional activity can influence distinct developmental processes by regulating the relative abundance of different CAMs. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 735–748, 1997
References
- Appel, F., Holm, J., Conscience, J. F., Von Bohlenund Halbach, F., Faissner, A., James, P., and Schachner, M. (1995). Identification of the border between fibronectin type III homologous repeats 2 and 3 of the neural cell adhesion molecule L1 as a neurite outgrowth promoting and signal transducing domain. J. Neurobiol. 28: 297–312.
- Arcari, P., Martinelli, R., and Salvatore, F. (1984). The complete sequence of a full length cDNA for human liver glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res. 12: 9179–9189.
- Barami, K., Kirschenbaum, B., Lemmon, V., and Goldman, S. A. (1994). N-cadherin and Ng-CAM/8D9 are involved serially in the migration of newly generated neurons into the adult songbird brain. Neuron 13: 567–582.
- Beesley, P. W., Mummery, R., and Tibaldi, J. (1995). N-cadherin is a major glycoprotein component of isolated rat forebrain postsynaptic densities. J. Neurochem. 64: 2288–2294.
- Burden-Gulley, S. M. and Lemmon, V. (1995). Ig superfamily adhesion molecules in the vertebrate nervous system: binding partners and signal transduction during axon growth. Semin. Dev. Biol. 6: 79–87.
- Chomcynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156–159.
- Cifuentes-Diaz, C., Nicolet, M., Goudou, D., Reiger, F., and Mege, R. M. (1994). N-cadherin expression in developing, adult and denervated chicken neuromuscular system: accumulations at both the neuromuscular junction and the node of Ranvier. Development 120: 1–11.
- Dahm, L. M. and Landmesser, L. T. (1988). The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130: 621–644.
- Davis, G. O., Schuster, C. M., and Goodman, C. S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17: 669–679.
- Doherty, P., Fazeli, M. S., and Walsh, F. S. (1994). The neural cell adhesion molecule and synaptic plasticity. J. Neurobiol. 26: 437–446.
- Edelman, G. M. and Crossin, K. L. (1991). Cell adhesion molecules: implications for molecular histology. Annu. Rev. Biochem. 60: 155–190.
- Fannon, A. M. and Colman, D. R. (1996). A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 4: 423–434.
- Fields, R. D. and Itoh, K. (1996). Neural cell adhesion molecules in activity-dependent development and synaptic plasticity. Trends Neurosci. 19: 473–470.
- Fields, R. D. and Nelson, P. G. (1992). Activity-dependent development of the vertebrate nervous system. Int. Rev. Neurobiol. 34: 133–214.
- Fields, R. D., Neale, E. A., and Nelson, P. G. (1990). Effects of patterned electrical activity on neurite out-growth from mouse sensory neurons. J. Neurosci. 10: 2950–2964.
- Fields, R. D., Yu, C., Neale, E. A., and Nelson, P. G. (1992). Recording chambers in cell culture. In: Electrophysiological Methods for In Vitro Studies in Vertebrate Neurobiology, H. Kettenmann and R. Grantyn, Eds. New York, Liss, pp. 67–76.
- Fitzgerald, M. and Fulton, P. B. (1992). The physiological properties of developing sensory neurons. In: Sensory Neurons, S. A. Scott, Ed. Oxford University Press, New York, pp. 287–306.
- Fitzgerald, M. (1991). A physiological study of the perinatal development of cutaneous sensory inputs to dorsal horn cells in the rat. J. Physiol. Lond. 432: 473–482.
- Fitzgerald, M. (1987). Spontaneous and evoked activity of fetal primary afferents in vivo. Nature 326: 603–605.
- Fredette, B., Rutishauser, U., and Landmesser, L. (1993). Regulation and activity-dependence of N-cadherin, NCAM isoforms, and polysialic acid on chick myotubes during development. J. Cell Biol. 123: 1867–1888.
- Fulton, B. P., Miledi, R., and Takahashi, T. (1980). Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc. R. Soc. Lond. Ser. B 208: 115–120.
- Goodman, C. S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19: 341–377.
- Gumbiner, B. M. (1993). Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron 11: 551–564.
- Hahn, C. G. and Covault, J. (1992). Neural regulation of N-cadherin gene expression in developing and adult skeletal muscle. J. Neurosci. 12: 4677–4688.
- Hasegawa, M., Seto, A., Uchiyama, N., Kida, S., Ahibitory Mashima, T., and Yamashita, J. (1996). Localization of E-cadherin in peripheral glia after nerve injury and repair. J. Neuropathol. Exp. Neurol. 55: 424–434.
- Hoffman, C. G. and Edelman, G. M. (1983). Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecules. Proc. Natl. Acad. Sci. USA 80: 5762–5766.
- Honig, M. G. and Rutishauser, U. S. (1996). Changes in the segmental pattern of sensory neuron projections in the chick hindlimb under conditions of altered cell adhesion molecule function. Dev. Biol. 175: 325–337.
- Ide, C. (1996). Peripheral nerve regeneration. Neurosci. Res. 25: 101–121.
- Itoh, K., Brackenbury, R., and Akeson, R. A. (1995). Induction of L1 mRNA in PC12 cells by NGF is modulated by cell-cell contact and does not require the high affinity NGF receptor. J. Neurosci. 15: 2504–2512.
- Itoh, K., Stevens, B., Schachner, M., and Fields, R. D. (1995). Regulation of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 270: 1369–1372.
- Jorgensen, O. S. (1995). Neural cell adhesion molecule (NCAM) as a quantitative marker in synaptic remodeling. Neurochem. Res. 20: 533–547.
- Kadmon, G., Kowitz, A., Altevogt, P., and Schachner, M. (1990). Functional cooperation between neural cell adhesion molecule L1 and N-CAM is carbohydrate dependent. J. Cell. Biol. 110: 209–218.
- Kudo, N. and Yamada, T. (1987). Morphological and physiological studies of development of the monosynaptic reflex pathway in the rat lumbar cord. J. Physiol. Lond. 389: 441–459.
- Lagunowich, L. A., Stein, A. P., and Reuhl, K. R. (1994). N-cadherin in normal and abnormal brain development. Neurotoxicology 15: 123–132.
- Landmesser, L., Dahm, L., Schultz, K., and Rutishauser, U. (1988). Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev. Biol. 130: 645–670.
- Lawson, S. N., Harper, A. A., Harper, E. I., Garson, J. A., and Anderton, B. H. (1984). A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurons. J. Comp. Neurol. 228: 263–272.
- Lemmon, V., Burden, S. M., Payne, H. R., Elmslie, G. J., and Hlavin, M. L. (1992). Neurite outgrowth on different substrates: permissive versus instructive influences and the role of adhesive strength. J. Neurosci. 12: 818–826.
- Lin, D. M. and Goodman, C. S. (1995). Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13: 507–523.
- Luthl, A., Laurent, J. P., Figurov, A., Muller, D., and Schachner, M. (1994). Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372: 777–779.
- Magyar-Lehmann, S., Frei, T., and Schachner, M. (1995). Fasciculation of granule cell neurites is responsible for the perpendicular orientation of small inhibitory interneurons in mouse cerebellar microexplant cultures in vitro. Eur. J. Neurosci. 7: 1460–1471.
- Matsunaga, M., Hatta, K., and Takeichi, M. (1988). Role of N-cadherin cell adhesion molecules in histogenesis of neural retina. Neuron 1: 289–295.
- Mayford, M., Barzilai, A., Keller, F., Schacher, S., and Kandel, E. R. (1992). Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity In Aplysia. Science 256: 638–644.
- McKerracher, L., Chamoux, M., and Arregul, C. O. (1996). Role of laminin and integrin interactions in growth cone guidance. Mol. Neurobiol. 12: 95–116.
- Miura, M., Kobayashi, M., Asou, H., and Uyemura, K. (1991). Molecular cloning of cDNA encoding the rate neural cell adhesion molecule L1: two L1 isoforms in the cytoplasmic region are produced by differential splicing. FEBS Lett. 289: 91–95.
- Miyatani, S., Shimamurak, K., Hatta, M., Nugafuchi, A., Nose, A., Matsunaga, M., Hatta, K., and Takeichi, M. (1989). Neural cadherin: role in selective cell-cell adhesion. Science 245: 631–635.
- Moos, M., Tacke, R., Scherer, H., Teplow, D., Fruh, K., and Schachner, M. (1988). Neural cell adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334: 701–703.
- Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G., and Kiss, J. Z. (1996). PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17: 413–422.
- Nakagawa, S. and Takeichi, M. (1995). Neural crest cell–cell adhesion controlled by sequential and sub-population-specific expression of novel cadherins. Development 121: 1321–1332.
- Nathke, S. I., Hinck, L., and Nelson, W. J. (1995). The cadherin/catenin complex: connections to multiple cellular processes involved in cell adhesion, proliferation and morphogenesis. Semin. Dev. Biol. 6: 89–95.
- Nelson, P. G., Yu, C., Fields, R. D., and Neale, E. A. (1989). Competition between convergent inputs in vitro: electrical activity modulates efficacy and number of synapses. Science 244: 585–587.
- Peter, N., Aronoff, B., Wu, F., and Schacher, S. (1994). Decrease in growth cone-neurite fasciculation by sensory and motor cells in vitro accompanies down-regulation of Aplysia cell adhesion molecules by neurotransmitters. J. Neurosci. 14: 1413–1421.
- Rafuse, V. F. and Landmesser, L. (1996). Contractile activity regulates isoform expression and polysialylation of NCAM in cultured myotubes: involvement of calcium and protein kinase C. J. Cell Biol. 132: 969–983.
- Ranscht, B. (1994). Cadherins and catenins: interactions and functions in embryonic development. Curr. Opin. Cell. Biol. 6: 740–746.
- Redies, C. (1995). Cadherin expression in the developing vertebrate CNS: from neuromeres to brain nuclei and neural circuits. Exp. Cell Res. 220: 243–256.
- Reynolds, M. L., Fitzgerald, M., and Benowitz, L. I. (1991). GAP-43 expression in the developing rat hind(1991). GAP-43 expression in the developing rat hindlimb. Neuroscience 41: 201–211.
- Riehl, R., Johnson, K., Bradley, R., Grunwald, G. B., Cornel, E., Lilienbaum, A., and Holt, C. E. (1996). Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17: 837–848.
- Rutishauser, U. and Landmesser, L. (1996). Polysialic acid in vertebrate nervous system: a promoter of plasticity in cell–cell interactions. Trends Neurosci. 19: 422–427.
- Sakimura, K., Kushiya, E., Obinata, M., Odani, S., and Takahashi, Y. (1985). Molecular cloning and the nucleotide sequence of cDNA for neuron-specific enolase messenger RNA of rat brain. Proc. Natl. Acad. Sci. USA 82: 7453–7457.
- Santoni, M. J., Barthels, D., Vopper, G., Boned, A., Goridis, C., and Wille, W. (1989). Differential exon usage involving an unusual splicing mechanism generates at least eight subtypes of NCAM cDNA in mouse brain. EMBO J. 8: 385–392.
- Schachner, M. (1992). Neural recognition molecules and their influence on cellular functions. In: The Nerve Growth Cone, P. C. Letourneau, S. B. Kater, and E. R. Macagno, Eds. Raven Press, New York, pp. 237–254.
- Scherer, M., Heller, M., and Schachner, M. (1992). Expression of the neural recognition molecule L1 by cultured neural cells is influenced by K+ and the glutamate receptor agonist NMDA. Eur. J. Neurosci. 4: 554–562.
-
Scherer, S. S.
(1996).
Molecular specializtions at nodes and paranodes in peripheral nerve.
Microsc. Res. Technol.
34:
452–461.
10.1002/(SICI)1097-0029(19960801)34:5<452::AID-JEMT5>3.0.CO;2-O CAS PubMed Web of Science® Google Scholar
- Schuster, C. M., Davis, G. W., Fetter, R. D., and Goodman, C. S. (1996a). Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synapse stabilization and growth. Neuron 17: 655–667.
- Seilheimer, B., Persohn, E., and Schachner, M. (1989). Antibodies to the L1 adhesion molecule inhibit Schwann cell ensheathment of nerves in vitro. J. Cell Biol. 109: 3095–3103.
- Seilheimer, B. and Schachner, M. (1988). Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J. Cell Biol. 107: 341–351.
- Shibuya, Y., Mizoguchi, A., Takeichi, M., Shimada, K., and Ide, C. (1995). Localization of N-cadherin in the normal and regenerating nerve fibers of the chicken peripheral nervous system. Neuroscience 67: 253–261.
- Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77: 627–638.
- Sretavan, D. W., Feng, L., Pure, E., and Reichardt, L. F. (1994). Embryonic neurons of the developing optic chiasm express L1 and CD44, cell surface molecules with opposing effects on retinal axon growth. Neuron 12: 975–975.
- Takeda, Y., Asou, H., Murakami, Y., Miura, M., Kobayashi, M., and Uyemura, K. (1996). A nonneuronal isoform of cell adhesion molecule L1: tissue-specific expression and functional analysis. J. Neurochem. 66: 2338–2349.
- Takeichi, M. (1990). Cadherins: a molecular family important in selective cell–cell adhesion. Annu. Rev. Biochem. 59: 237–252.
- Uchida, N., Honjo, Y., Johnson, K. R., Wheelock, M. J., and Takeichi, M. (1996). The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J. Cell Biol. 135: 767–779.
- Von Bohlenund Halbach, F., Taylor, J., and Schachner, M. (1992). Cell type-specific effects of the neural adhesion molecules L1 and N-CAM on diverse second messenger systems. Eur. J. Neurosci. 4: 896–909.
- Walsh, F. S., Skakper, S. D., and Doherty, P. (1994). Cell adhesion molecule (NCAM and N-cadherin)-dependent neurite outgrowth is modulated by gangliosides. Prog. Brain Res. 101: 113–118.
- Wood, P. M., Schachner, M., and Bunge, R. P. (1990). Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule. J. Neurosci. 10: 3635–3645.
- Ziskind-Conhaim, L. (1990). NMDA receptors mediate poly- and monosynaptic potentials in motoneurons of rat embryos. J. Neurosci. 10: 125–135.
- Zomzely-Neurath, C. E. (1983). In Handbook of eurobiology, 2nd ed., Vol. 4. A. Lajtha, Ed. Plenum Press, New York, pp. 403–433.
