Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T11:53:59.016Z Has data issue: false hasContentIssue false
  • English
  • Français

Agrin mRNA expression in the developing chick Edinger-Westphal nucleus

Published online by Cambridge University Press:  02 June 2009

Michael McAvoy ,
Martin A. Smith  and
Joanne T. Fujii
Michael McAvoy
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
Martin A. Smith
Affiliation:
Department of Anatomy and Neurobiology, University of California at Irvine, Irvine
Joanne T. Fujii
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
Get access Rights & Permissions [Opens in a new window]

Abstract

Agrin is a large extracellular matrix protein that directs the accumulation of acetylcholine receptors at the neuromuscular junction. Recent evidence suggests that agrin may be involved in organizing synapses in the visual system as well. Focussing on the pathway that controls accommodation and pupilloconstriction, this study examined the temporal pattern of agrin expression with reference to the organization of cholinergic synapses between embryonic chick Edinger-Westphal and ciliary ganglion neurons. In situ hybridization with an S35-labeled agrin cRNA probe was used to characterize agrin expression in the Edinger-Westphal nucleus during development. Agrin mRNA was detected in the Edinger-Westphal nucleus at all time points studied, from embryonic day 7 (E7, Hamburger and Hamilton stage 31) through newly hatched chicks. Throughout this period, agrin mRNA expression in Edinger-Westphal neurons was lower than in nearby oculomotor and trochlear neurons, suggesting that cells projecting to neuronal targets may require less agrin than those projecting to muscle. Agrin mRNA expression in the Edinger-Westphal nucleus at E7, E8, E9, and E10 was significantly higher than at E12. The early appearance of agrin mRNA coincides with the period during which acetylcholine receptors are being organized on ciliary ganglion neurons, consistent with the possibility that agrin contributes to neuron-neuron synapse formation in this pathway.

Keywords

Acetylcholine receptorsAccommodationCiliary ganglionPupilloconstrictionSynapse developmentSynaptic molecules
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 293 - 301
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akert, K., Glickman, M.A., Lang, W., Grob, P. & Huber, A. (1980). The Edinger-Westphal nucleus in the monkey. A retrograde tracer study. Brain Research 184, 491–498.CrossRefGoogle ScholarPubMed
Biroc, S.L., Payan, D.G. & Fisher, J.M. (1993). Isoforms of agrin are widely expressed in the developing rat and may function as protease inhibitors. Developmental Brain Research 75, 119–129.CrossRefGoogle ScholarPubMed
Bowe, M.A. & Fallon, J.F. (1995). The role of agrin in synapse formation. Annual Review of Neuroscience 18, 443–462.CrossRefGoogle ScholarPubMed
Burde, R.M. & Loewy, A.D. (1980). Central origin of oculomotor parasympathetic neurons in the monkey. Brain Research 198, 434–439.CrossRefGoogle ScholarPubMed
Fitzgerald, M.E.C., Vana, B.A. & Reiner, A. (1990). Control of choroidal blood flow by the Nucleus of Edinger-Westphal in pigeons: A laser doppler study. Investigative Ophthalmology and Visual Science 31(12), 2483–2492.Google ScholarPubMed
Godfrey, E.W., Nitkin, R.M., Wallace, B.G., Rubin, L.L. & McMahan, U.J. (1984). Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. Journal of Cell Biology 99, 615–627.CrossRefGoogle ScholarPubMed
Hamburger, V. & Hamilton, H.L. (1951). A series of normal stages in the development of the chick embryo. Journal of Morphology 88, 49–92.CrossRefGoogle ScholarPubMed
Jacob, M.H. (1991). Acetylcholine receptor expression in developing chick ciliary ganglion neurons. Journal of Neuroscience 11(6), 1701–1712.CrossRefGoogle ScholarPubMed
Landmesser, L. & Pilar, G. (1972). The onset and development of transmission in the chick ciliary ganglion. Journal of Physiology 222, 691–713.CrossRefGoogle ScholarPubMed
Ma, E., Morgan, R. & Godfrey, E.W. (1994). Distribution of agrin mRNAs in the chick embryo nervous system. Journal of Neuroscience 14(5), 2943–2952.CrossRefGoogle ScholarPubMed
Magill-Solc, C. & McMahan, U.J. (1988). Motor neurons contain agrin-like molecules. Journal of Cell Biology 107, 1825–1833.CrossRefGoogle ScholarPubMed
McMahan, U.J. (1990). The agrin hypothesis. Cold Spring Harbor Symposia on Quantitative Biology 55, 407–418.CrossRefGoogle ScholarPubMed
Meriney, S.D. & Pilar, G. (1987). Cholinergic innervation of the smooth muscle cells in the choroid coat of the chick eye and its development. Journal of Neuroscience 7(12), 3827–3829.CrossRefGoogle ScholarPubMed
Nitkin, R.M., Smith, M.A., Fallon, J.R., Yao, Y.-M., Wallace, B.G. & McMahan, U.J. (1987). Identification of agrin, a synaptic organizing molecule from torpedo electric organ. Journal of Cell Biology 105, 2471–2478.CrossRefGoogle Scholar
O'Connor, L.T., Lauterborn, J.C., Gall, C.M. & Smith, M.A. (1994). Localization and alternative splicing of agrin mRNA in adult rat brain: Transcripts encoding isoforms that aggregate acetylcholine receptors are not restricted to cholinergic regions. Journal of Neuroscience 14(3), 1141–1252.CrossRefGoogle Scholar
Pilar, G., Nunez, R., McLennan, I.S. & Meriney, S.D. (1987). Muscarinic and nicotinic synaptic activation of the developing chick iris. Journal of Neuroscience 7, 3813–3826.CrossRefGoogle Scholar
Reiner, A., Erichsen, J.T., Cabot, J.B., Evinger, C., Fitzgerald, M.E.C. & Karten, H.J. (1991). Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion. Visual Neuroscience 6, 451–472.CrossRefGoogle Scholar
Reiner, A., Karten, H.J., Gamlin, P.D. & Erichsen, J.T. (1983). Para-sympathetic ocular control: Functional subdivisions and circuitry of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6(4), 140–145.CrossRefGoogle Scholar
Ruegg, M.A., Tsim, K.W.K., Horton, S.E., Kroger, S. & McMahan, U.J. (1992). The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron 8, 691–699.CrossRefGoogle ScholarPubMed
Rupp, F., Payan, D.G., Magill-Solc, C., Cowan, D.M. & Scheller, R.H. (1991). Structure and expression of rat agrin. Neuron 6, 811–823.CrossRefGoogle ScholarPubMed
Smith, M.A., Magill-Solc, C., Rupp, R., Yao, Y.-M.M., Schilling, J.W., Snow, P. & McMahan, U.J. (1992). Isolation and characterization of an agrin homolog in the marine ray. Molecular and Cellular Neuroscience 3, 406–417.CrossRefGoogle ScholarPubMed
Smith, A.M. & O'Dowd, D.K. (1994). Cell-specific regulation of agrin RNA splicing in the chick ciliary ganglion. Neuron 12, 795–804.CrossRefGoogle ScholarPubMed
Thomas, W.S., O'Dowd, D.K. & Smith, M.A. (1993). Developmental expression and alternative splicing of chick agrin mRNA. Developmental Biology 158, 523–535.CrossRefGoogle Scholar
Tsen, G., Halfter, W., Kroger, S. & Cole, G.J. (1995). Agrin is a heparan sulfate proteoglycan. Journal of Biological Chemistry 270, 3392–3399.CrossRefGoogle ScholarPubMed
Tsim, K.W.K., Ruegg, M.A., Escher, G., Kroger, S. & McMahan, U.J. (1992). cDNA that encodes active agrin. Neuron 8, 677–689.CrossRefGoogle ScholarPubMed