Elsevier

Developmental Biology

Volume 135, Issue 2, October 1989, Pages 272-286
Developmental Biology

Full paper
Expression of L1 and N-CAM cell adhesion molecules during development of the mouse olfactory system

https://doi.org/10.1016/0012-1606(89)90179-6Get rights and content

Abstract

The expression of the neural adhesion molecules L1 and N-CAM has been studied in the embryonic and early postnatal olfactory system of the mouse in order to gain insight into the function of these molecules during development of a neural structure which retains neuronal turnover capacities throughout adulthood. N-CAM was slightly expressed and L1 was not significantly expressed in the olfactory placode on Embryonic Day 9, the earliest stage tested. Rather, N-CAM was strongly expressed in the mesenchyme underlying the olfactory placode. In the developing nasal pit, L1 and N-CAM were detectable in the developing olfactory epithelium, but not in regions developing into the respiratory epithelium. At early developmental stages, expression of the so-called embryonic form of N-CAM (E-N-CAM) coincides with the expression of N-CAM, whereas at later developmental stages and in the adult it is restricted to a smaller number of sensory cell bodies and axons, suggesting that the less adhesive embryonic form is characteristic of morphogenetically dynamic neuronal structures. Moreover, E-N-CAM is highly expressed at contact sites between olfactory axons and their target cells in the glomeruli of the olfactory bulb. L1 and N-CAM 180, the component of N-CAM that accumulates at cell contacts by interaction with the cytoskeleton are detectable as early as the first axons extend toward the primordial olfactory bulb. L1 remains prominent throughout development on axonal processes, both at contacts with other axons and with ensheathing cells. Contrary to N-CAM 180 which remains detectable on differentiating sensory neuronal cell bodies, L1 is only transiently expressed on these and is no longer detectable on primary olfactory neuronal cell bodies in the adult. Furthermore, whereas throughout development L1 has a molecular form similar to that seen in other parts of the developing and adult central nervous systems, N-CAM and, in particular, N-CAM 180 retain their highly sialylated form at least partially throughout all ages studied. These observations suggest that E-N-CAM and N-CAM 180 are characteristic of developmentally active structures and L1 may not only be involved in neurite outgrowth, but also in stabilization of contacts among fasciculating axons and between axons and ensheathing cells, as it has previously been found in the developing peripheral nervous system.

References (67)

  • I. Nagata et al.

    Neuronal influence on antigenic marker profile, cell shape and proliferation of cultured astrocytes obtained by microdissection of distinct layers from the early postnatal mouse cerebellum

    Dev. Brain Res

    (1986)
  • J. Nieke et al.

    Expression of neural cell adhesion molecules L1 and N-CAM and their common carbohydrate epitope L2-HNK-1 during development and after transection of mouse sciatic nerve

    Differentiation

    (1985)
  • G.P. Richardson et al.

    Expression of cell adhesion molecules during embryonic induction. III. Development of the otic placode

    Dev. Biol

    (1987)
  • U. Rutishauser et al.

    N-CAM: The molecule and its genetics

    Trends Genet

    (1986)
  • J. Schnitzer et al.

    Expression of Thy-1, H-2, and NS-4 cell surface antigens and tetanus toxin receptors in early postnatal and adult mouse cerebellum

    J. Neuroimmunol

    (1981)
  • W. Werz et al.

    Adhesion of neural cells to extracellular matrix constituents

    Involvement of glycosaminoglycans and cell adhesion molecules

    Dev. Brain Res

    (1988)
  • U. Bartsch et al.

    Immunohistochemical localization of the adhesion molecules L1, N-CAM and MAG in developing and adult optic nerve of mice

    J. Comp. Neurol

    (1989)
  • J.L. Bixby et al.

    Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro

    J. Cell Biol

    (1988)
  • W. Breipohl

    Ontogeny of Olfaction

    (1986)
  • S. Chang et al.

    Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins

    J. Cell Biol

    (1987)
  • C.M. Chuong et al.

    Alterations in neural cell adhesion molecules during development of different regions of the nervous system

    J. Neurosci

    (1984)
  • A. Cushieri et al.

    The development of the olfactory mucosa in the mouse: Light microscopy

    J. Anat

    (1975)
  • A. Cushieri et al.

    The development of the olfactory mucosa in the mouse: Electron microscopy

    J. Anat

    (1975)
  • G.M. Edelman

    Cell adhesion molecules in the regulation of animal form and tissue pattern

    Annu. Rev. Cell Biol

    (1986)
  • G.M. Edelman et al.

    Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice

  • G.M. Edelman et al.

    Early epochal maps of two different cell adhesion molecules

  • G.M. Edelman et al.

    The Cell in Contact

    (1985)
  • A. Faissner et al.

    The neural cell adhesion molecule L1 is distinct from the N-CAM-related group of surface antigens BSP-2 and D2

    EMBO J

    (1984)
  • A. Faissner et al.

    Biosynthesis and membrane topography of the neural cell adhesion molecule L1

    EMBO J

    (1985)
  • A.I. Farbman et al.

    Development of the olfactory epithelium in the rat

  • G. Filogamo et al.

    Neuroblasts in the olfactory pits of mammals

    Acta Anat. (Suppl)

    (1969)
  • J. Finne et al.

    An IgG monoclonal antibody to group B meningococci crossreacts with developmentally regulated polysialic acid units of glycoproteins in neural and extraneural tissues

    J. Immunol

    (1987)
  • G. Fischer et al.

    Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1

    J. Neurosci

    (1986)
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