Skip to main content

Immunocytological characterization of the expression of cell adhesion molecule L1 during early innervation of mouse otocysts

Cell and Tissue Research volume 255, pages 81–88 (1989)Cite this article

Summary

Doubts exist as to whether afferent nerve fibers exert a neurotrophic effect on the differentiation of sensory cells in the developing vestibular neuroepithelium. To determine whether innervation of hair cells precedes their differentiation, we have used the L1 adhesion molecule as a marker for axons. The detection of L1 on afferent axons in the otic vesicle of mouse embryos on gestation day 11 shows that nerve fibers penetrate the neuroepithelium before the sensory cells differentiate. L1-immunoreactivity of nerve endings also reveals the considerable fiber ramification on gestation days 14 and 15, i.e., corresponding to the first stages of sensory cell differentiation. The expression of L1 at successive stages of nerve fiber growth in the neuroepithelium, such as fasciculation and ramification, is not consistent with the previous role proposed for L1 as a fascicule-promoting factor and raises the possibility that other mechanisms are involved in L1 mediaded adhesion.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Acheson A, Rutishauser U (1988) Neural cell adhesion molecule regulates cell contact-mediated changes in choline acetyltransferase activity of embryonic chick sympathetic neurons. J Cell Biol 106:479–486

    Google Scholar 

  • Acheson AL, Thoenen H (1983) Cell contact-mediated regulation of tyrosine hydroxylase synthesis in cultured bovine adrenal chromaffin cells. J Cell Biol 97:925–928

    Google Scholar 

  • Anniko M, Nordemar H, Van de Water TR (1979) Embryogenesis of the inner ear. I. Development and differentiation of the mammalian crista ampullaris in vitro and in vivo. Arch Oto-Rhino-Laryngol 224:285–299

    Google Scholar 

  • Beasley L, Stallcup WB (1987) The nerve growth factor-inducible large external (NILE) glycoprotein and neural cell adhesion molecule (N-CAM) have distinct patterns of expression in the developing rat central nervous system. J Neurosci 7:708–715

    Google Scholar 

  • Bock E, Richter-Landsberg C, Faissner A, Schachner M (1985) Demonstration of immunochemical identity between the nerve growth factor inducible large external (NILE) glycoprotein and the cell adhesion molecule L1. EMBO J 4:2765–2768

    Google Scholar 

  • Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353–358

    Google Scholar 

  • Dechesne CJ, Sans A, Keller A (1985) Onset and development of neuron-specific enolase immunoreactivity in the peripheral vestibular system of the mouse. Neurosci Lett 61:299–304

    Google Scholar 

  • Edelman G (1984) Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu Rev Neurosci 7:339–377

    Google Scholar 

  • Faissner A, Kruse J, Nieke J, Schachner M (1984) Expression of neural cell adhesion molecule L1 during development, in neurological mutants and in the peripheral nervous system. Dev Brain Res 15:69–82

    Google Scholar 

  • Fischer G, Kunemünd K, Schachner M (1986) Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to cell surface glycoprotein L1. J Neurosci 6:605–612

    Google Scholar 

  • Fushiki S, Schachner M (1986) Immunocytological localization of cell adhesion molecules L1 and N-CAM and the shared carbohydrate epitope L2 during development of the mouse neocortex. Dev Brain Res 24:153–167

    Google Scholar 

  • Gil-Loyzaga P, Pujol R (1987) Trophic interactions between spiral ganglion neurons and the cochlear epithelium during in vitro development. 10th Midwinter Research meeting ARO, Clearwater beach (Florida), Feb. 1–5, 223

    Google Scholar 

  • Ginzberg R, Gilula N (1980) Synaptogenesis in the vestibular sensory epithelium of the chick embryo. J Neurocytol 9:405–424

    Google Scholar 

  • Goridis C, De Agostini-Bazin H, Hirn M, Hirsch MR, Rougon G, Sadoul R, Langley OK, Gombos G, Finne J (1983) Neural surface antigens during nervous system development. Cold Spring Harbor Symposium on Quantitative Biology 48:527–538

    Google Scholar 

  • Grumet M, Edelman GM (1988) Neuron-glia cell adhesion molecule interacts with neurons and astroglia via different binding mechanisms. J Cell Biol 106:487–503

    Google Scholar 

  • Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissue that mediates glia-neuron interaction. Proc Natl Acad Sci USA 82:8075–8079

    Google Scholar 

  • Jorgensen JM, Flock A (1976) Non-innervated sense organs of the lateral line: development in the regenerating tail of the salamander Ambystoma mexicanum. J Neurocytol 5:33–41

    Google Scholar 

  • Knowlton VY (1967) Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers of the chick embryo. J Morphol 121:179–208

    Google Scholar 

  • König N, Wilkie NB, Lauder JM (1988) Tyrosine hydroxylase and serotonin containing cells in embryonic rat rhombencephalon: A whole-mount immunocytochemical study. J Neurosci Res 20:212–223

    Google Scholar 

  • Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Schachner M (1984) Neural cell adhesion molecules and myelinassociated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311:153–155

    Google Scholar 

  • Kruse J, Keilhauer G, Faissner A, Timpl R, Schachner M (1985) The J1 glycoprotein —a novel nervous system cell adhesion molecule of L2/HNK-1 family. Nature 316:146–148

    Google Scholar 

  • Li CW, Van de Water TR, Ruben RJ (1978) The fate mapping of the eleventh and twelfth day mouse otocyst: An “in vitro” study of the sites of origin of the embryonic inner ear sensory structures. J Morphol 157:249–268

    Google Scholar 

  • Lindner J, Rathjen F, Schachner M (1983) L1 mono-and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427–430

    CAS  PubMed  Google Scholar 

  • Linnemann D, Nybroe O, Gibson A, Rohde H, Jorgensen OS, Bock E (1987) Characterization of the biosynthesis, membrane association and function of the cell adhesion molecule L1. Neurochem Int 10:113–120

    Google Scholar 

  • Lumsden AGS, Davies AM (1983) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature 306:786–788

    Google Scholar 

  • Lumsden AGS, Davies AM (1986) Chemotropic effect of specific epithelium in the developing mammalian nervous system. Nature 323:538–539

    Google Scholar 

  • Martini R, Schachner M (1986) Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J Cell Biol 103:2439–2448

    Google Scholar 

  • Mbiene JP, Favre D, Sans A (1984) The pattern of ciliary development in fetal mouse vestibular receptors. A qualitative and quantitative SEM study. Anat Embryol 170:229–238

    Google Scholar 

  • Mbiene JP, Favre D, Sans A (1988) Early innervation and differentiation in the sensory vestibular epithelia. A SEM and TEM study in mouse embryos. Anat Embryol 177:331–340

    Google Scholar 

  • Nakai Y (1970) The development of the sensory epithelium of the cristae ampullares in the rabbit. Pract Oto Rhino Laryngol 32:268–278

    Google Scholar 

  • Persohn E, Schachner M (1987) Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of mouse cerebellum. J Cell Biol 105:569–576

    Google Scholar 

  • Pollerberg EG, Burridge K, Krebs KE, Goodman SR, Schachner M (1987) The 180-KD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res 250:227–236

    Google Scholar 

  • Poltorak M, Sadoul R, Keilhauer G, Landa C, Fahrig T, Schachner M (1987) The myelin-associated glycoprotein (MAg), a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction. J Cell Biol (in press)

  • Rathjen FG, Schachner M (1984) Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J 3:1–10

    Google Scholar 

  • Raymond J (1987) In vitro differentiation of mouse embryo statoacoustic ganglion and sensory epithelium. Hearing Res 28:45–56

    Google Scholar 

  • Richardson GP, Crossin KL, Chuong C-M, Edelman GM (1987) Expression of cell adhesion molecules during embryonic induction. III. Development of the otic placode. Developmental Biology 119:217–230

    Google Scholar 

  • Ruben RJ (1967) Development of the inner ear of the mouse: A radioautographic study of terminal mitoses. Acta Oto-Laryngol [Suppl] 220:1–44

    Google Scholar 

  • Rutishauser U (1984) Developmental biology of a neural cell adhesion molecule. Nature 310:549–554

    Google Scholar 

  • Sadoul K, Sadoul R, Faissner A, Schachner M (1987) Biochemical characterization of different molecular forms of the neural cell adhesion molecule L1. J Neurochem (in press)

  • Sans A, Chat M (1982) Analysis of temporal and spatial patterns of rat vestibular hair cell differentiation by tritiated thymidine radioautography. J Comp Neurol 206:1–8

    Google Scholar 

  • Sans A, Dechesne CJ (1987) Afferent nerve endings development and synaptogenesis in the vestibular epithelium of human fetuses. Hearing Res 28:65–72

    Google Scholar 

  • Schachner M, Faissner A, Kruse J, Lindner J, Meier DH, Rathjen FG, Wernecke H (1983) Cell-type specificity and developmental expression of neural cell-surface components involved in cell interactions and of structurally related molecules. Cold Spring Harbor Symposium on Quantitative Biology 48:557–568

    Google Scholar 

  • Schachner M, Faissner A, Fischer G, Keilhauer G, Kruse J, Künemund V, Linder J, Wernecke H (1985) Functional and structural aspects of the cell surface in mammalian nervous system development. In: Edelman GM Thiery JP (eds) The Cell Contact. John Wiley and Sons, Inc, New York, pp 257–276

    Google Scholar 

  • Sher AE (1971) The embryonic and postnatal development of the inner ear of the mouse. Acta Oto-Laryngol Suppl 285:1–77

    Google Scholar 

  • Thiery JP, Duband JL, Rutishauser U, Edelman G (1982) Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci USA 79:6737–6741

    Google Scholar 

  • Thiery JP, DeLouvée A, Grumet M, Edelman G (1985) Initial appearance and regional distribution of neuron-glia cell adhesion molecule in the chick embryo. J Cell Biol 100:442–456

    Google Scholar 

  • Thor G, Pollerberg EG, Schachner M (1986) Molecular association of two neural cell adhesion molecules, L1 antigen and the 180 kd component of N-CAM, within the surface membrane of cultured neuroblastoma cells. Neurosci Lett 66:121–126

    Google Scholar 

  • Van de Water TR (1976) Effects of removal of the stato-acoustic ganglion complex upon the growing otocyst. Ann Otol Rhino Laryngol [Suppl] 85:1–32

    Google Scholar 

Download references

Author information

Affiliations

  1. INSERM — U254, Laboratoire de Neurophysiologie Sensorielle, U.S.T.L., Place Eugène Bataillon, F-34060, Montpellier, France

    J. P. Mbiene, C. J. Dechesne & A. Sans

  2. Department of Neurobiology, University of Heidelberg, Heidelberg, Germany

    M. Schachner

Authors
  1. J. P. Mbiene
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. J. Dechesne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Schachner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Sans
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mbiene, J.P., Dechesne, C.J., Schachner, M. et al. Immunocytological characterization of the expression of cell adhesion molecule L1 during early innervation of mouse otocysts. Cell Tissue Res. 255, 81–88 (1989). https://doi.org/10.1007/BF00229069

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229069

Key words

  • L1-antigen
  • Cell adhesion molecule
  • Developing vestibular neuroepithelium
  • Immunocytochemistry
  • Mouse (CBAxC57)