Abstract
TRANSMITTER receptors are localized to discrete cellular sites1 such that only those responses appropriate for a particular pattern of inputs are activated2–4. How neurons select between synaptic and extrasynaptic responses during development is not understood. We have investigated how contact during synapse formation between identified leech neurons5–7 selectively suppresses the modulation of extrasynaptic channels by protein kinase C8–10. A microelectrode with an isolated membrane patch containing channels from an uninnervated target neuron was 'crammed'11 into a similar cell contacted by a presynaptic partner. We report here that within a few minutes, the crammed channels were rendered insensitive to activation of protein kinase C, demonstrating the action of a cytoplasmic signal. Treatment of the neurons with selective inhibitors of tyrosine kinases12, which are signalling molecules during normal and oncogenic cellular differentiation13,14, prevented the loss of channel modulation. Thus, tyrosine kinases mediate early functional changes during specific synapse formation that are induced by neuronal contact.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Hille, B. Ionic Channels of Excitable Membranes (Sinauer, Sunderland, MA, 1992).
Gerschenfeld, H. M. Physiol. Rev. 53, 1–119 (1973).
Nicoll, R. A. Science 241, 545–551 (1988).
Nicoll, R. A., Malenka, R. C. & Kauer, J. A. Physiol. Rev. 70, 513–565 (1991).
Fuchs, P., Nicholls, J. G. & Ready, D, F. J. Physiol., Lond. 316, 203–233 (1981).
Drapeau, P. & Sanchez-Armass, S. J. Neurosci. 8, 4718–4727 (1988).
Drapeau, P., Melinyshyn, E. & Sanchez-Armass, S. J. Neurosci. 9, 2502–2508 (1989).
Merz, D. & Drapeau, P. Proc. R. Soc. B248, 129–133 (1992).
Drapeau, P. Neuron 4, 875–882 (1990).
Catarsi, S. & Drapeau, P. Neuron 8, 275–281 (1992).
Kramer, R. H. Neuron 2, 335–341 (1990).
O'Dell, T. J., Kandel, E. R. & Grant, S. G. N. Nature 353, 558–560 (1991).
Greenwald, I. & Rubin, G. M. Cell 68, 271–281 (1992).
Cantley, L. C. et al. Cell 64, 281–302 (1991).
Hamill, O. P. et al. Pflügers Arch. 391, 85–100 (1981).
Nishizuka, Y. Nature 334, 661–665 (1988).
Atashi, J. R. et al. Neuron 8, 831–842 (1992).
Qu, Z., Moritz, E. & Huganir, R. L. Neuron 2, 367–378 (1990).
Wallace, B. G., Qu, Z. & Hunanir, R. L. Neuron 6, 869–878 (1991).
Cohen, M. W., Rodriguez-Marin, E. & Wilson, E. M. J. Neurosci. 7, 2849–2861 (1987).
Bloch, R. J. & Pumplin, D. W. Am. J. Physiol. 254, C345–c364 (1988).
Katz, B. & Miledi, R. J. Physiol., Lond. 224, 665–699 (1972).
Neher, E. & Sakmann, B. J. Physiol., Lond. 258, 705–729 (1976).
Mishina, M. et al. Nature 321, 406–411 (1986).
Witzemann, V., Brenner, H.-R. & Sakmann, B. J. Cell Biol. 114, 125–141 (1991).
Drapeau, P. & Sanchez-Armass, S. J. Neurobiol. 20, 312–325 (1989).
Purves, D. & Lichtman, J. W. Principles of Neural Development (Sinauer, Sunderland, MA, 1985).
Shatz, C. J. Neuron 5, 745–756 (1990).
Dietzel, I. D., Drapeau, P. & Nicholls, J. G. J. Physiol., Lond. 372, 191–205 (1986).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Catarsi, S., Drapeau, P. Tyrosine kinase-dependent selection of transmitter responses induced by neuronal contact. Nature 363, 353–355 (1993). https://doi.org/10.1038/363353a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/363353a0
This article is cited by
-
Effect of Chronic Administration of Ethanol on the Regulation of Tyrosine Kinase Phosphorylation of the GABAA Receptor Subunits in the Rat Brain
Neurochemical Research (2007)
-
Tyrosine Kinase Phosphorylation of GABAA Receptor α1, β2 and γ2 Subunits Following Chronic Intermittent Ethanol (CIE) Exposure of Cultured Cortical Neurons of Mice
Neurochemical Research (2006)
-
Modulation and selection of neurotransmitter responses during synapse formation between identified leech neurons
Cellular and Molecular Neurobiology (1996)
-
Regulation of NMDA receptors by tyrosine kinases and phosphatases
Nature (1994)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.