Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 May 1;102(5):1917–1930. doi: 10.1083/jcb.102.5.1917

Site-restricted expression of cytotactin during development of the chicken embryo

PMCID: PMC2114192  PMID: 2422181

Abstract

The sequential appearance of the extracellular matrix (ECM) protein, cytotactin, was examined during development of the chicken embryo by immunohistochemical techniques. Although cytotactin was identified as a molecule that mediates glia-neuron interactions, preliminary immunohistochemical localization of the molecule suggested that it was an ECM protein with a widespread but nonetheless more restricted distribution than either fibronectin or laminin. In the present study, it was found that cytotactin is first present in the gastrulating chicken embryo. It appears later in the basement membrane of the developing neural tube and notochord in a temporal sequence beginning in the cephalic regions and proceeding caudally. Between 2 and 3 d of development, the molecule is present at high levels in the early neural crest pathways (surrounding the neural tube and somites) but, in contrast to fibronectin and laminin, is not found in the lateral plate mesoderm or ectoderm. At later times, cytotactin is expressed extensively in the central nervous system, in lesser amounts in the peripheral nervous system, and in a number of nonneural sites, most prominently in all smooth muscles and in basement membranes of lung and kidney. Cytotactin appears in adult tissues with distributions that are similar to those seen in embryonic tissues. The findings raise the possibility that certain ECM proteins contribute to pattern formation in embryogenesis as a result of their restricted expression in a spatiotemporally regulated fashion at some sites but not at others.

Full Text

The Full Text of this article is available as a PDF (6.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brackenbury R., Thiery J. P., Rutishauser U., Edelman G. M. Adhesion among neural cells of the chick embryo. I. An immunological assay for molecules involved in cell-cell binding. J Biol Chem. 1977 Oct 10;252(19):6835–6840. [PubMed] [Google Scholar]
  2. Chuong C. M., Edelman G. M. Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci. 1984 Sep;4(9):2354–2368. doi: 10.1523/JNEUROSCI.04-09-02354.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Covault J., Sanes J. R. Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4544–4548. doi: 10.1073/pnas.82.13.4544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crossin K. L., Chuong C. M., Edelman G. M. Expression sequences of cell adhesion molecules. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6942–6946. doi: 10.1073/pnas.82.20.6942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  6. Edelman G. M. Cell adhesion and morphogenesis: the regulator hypothesis. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1460–1464. doi: 10.1073/pnas.81.5.1460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelman G. M. Cell adhesion and the molecular processes of morphogenesis. Annu Rev Biochem. 1985;54:135–169. doi: 10.1146/annurev.bi.54.070185.001031. [DOI] [PubMed] [Google Scholar]
  8. Edelman G. M. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. doi: 10.1126/science.6823544. [DOI] [PubMed] [Google Scholar]
  9. Edelman G. M., Chuong C. M. Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc Natl Acad Sci U S A. 1982 Nov;79(22):7036–7040. doi: 10.1073/pnas.79.22.7036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Edelman G. M. Expression of cell adhesion molecules during embryogenesis and regeneration. Exp Cell Res. 1985 Nov;161(1):1–16. doi: 10.1016/0014-4827(85)90485-9. [DOI] [PubMed] [Google Scholar]
  11. Edelman G. M., Gallin W. J., Delouvée A., Cunningham B. A., Thiery J. P. Early epochal maps of two different cell adhesion molecules. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4384–4388. doi: 10.1073/pnas.80.14.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Edelman G. M. Surface modulation in cell recognition and cell growth. Science. 1976 Apr 16;192(4236):218–226. doi: 10.1126/science.769162. [DOI] [PubMed] [Google Scholar]
  13. Gallin W. J., Edelman G. M., Cunningham B. A. Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1038–1042. doi: 10.1073/pnas.80.4.1038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grumet M., Edelman G. M. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule. J Cell Biol. 1984 May;98(5):1746–1756. doi: 10.1083/jcb.98.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grumet M., Hoffman S., Chuong C. M., Edelman G. M. Polypeptide components and binding functions of neuron-glia cell adhesion molecules. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7989–7993. doi: 10.1073/pnas.81.24.7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grumet M., Hoffman S., Crossin K. L., Edelman G. M. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075–8079. doi: 10.1073/pnas.82.23.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grumet M., Hoffman S., Edelman G. M. Two antigenically related neuronal cell adhesion molecules of different specificities mediate neuron-neuron and neuron-glia adhesion. Proc Natl Acad Sci U S A. 1984 Jan;81(1):267–271. doi: 10.1073/pnas.81.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hatta K., Okada T. S., Takeichi M. A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. Proc Natl Acad Sci U S A. 1985 May;82(9):2789–2793. doi: 10.1073/pnas.82.9.2789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hoffman S., Edelman G. M. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5762–5766. doi: 10.1073/pnas.80.18.5762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hoffman S., Sorkin B. C., White P. C., Brackenbury R., Mailhammer R., Rutishauser U., Cunningham B. A., Edelman G. M. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J Biol Chem. 1982 Jul 10;257(13):7720–7729. [PubMed] [Google Scholar]
  21. Hyafil F., Morello D., Babinet C., Jacob F. A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell. 1980 Oct;21(3):927–934. doi: 10.1016/0092-8674(80)90456-0. [DOI] [PubMed] [Google Scholar]
  22. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
  23. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  24. Lindner J., Rathjen F. G., Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. 1983 Sep 29-Oct 5Nature. 305(5933):427–430. doi: 10.1038/305427a0. [DOI] [PubMed] [Google Scholar]
  25. Newgreen D., Thiery J. P. Fibronectin in early avian embryos: synthesis and distribution along the migration pathways of neural crest cells. Cell Tissue Res. 1980;211(2):269–291. doi: 10.1007/BF00236449. [DOI] [PubMed] [Google Scholar]
  26. Peyriéras N., Hyafil F., Louvard D., Ploegh H. L., Jacob F. Uvomorulin: a nonintegral membrane protein of early mouse embryo. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6274–6277. doi: 10.1073/pnas.80.20.6274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pollerberg E. G., Sadoul R., Goridis C., Schachner M. Selective expression of the 180-kD component of the neural cell adhesion molecule N-CAM during development. J Cell Biol. 1985 Nov;101(5 Pt 1):1921–1929. doi: 10.1083/jcb.101.5.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol. 1971 Mar;141(3):283–312. doi: 10.1002/cne.901410303. [DOI] [PubMed] [Google Scholar]
  29. Rieger F., Grumet M., Edelman G. M. N-CAM at the vertebrate neuromuscular junction. J Cell Biol. 1985 Jul;101(1):285–293. doi: 10.1083/jcb.101.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rothbard J. B., Brackenbury R., Cunningham B. A., Edelman G. M. Differences in the carbohydrate structures of neural cell-adhesion molecules from adult and embryonic chicken brains. J Biol Chem. 1982 Sep 25;257(18):11064–11069. [PubMed] [Google Scholar]
  31. Rutishauser U., Watanabe M., Silver J., Troy F. A., Vimr E. R. Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol. 1985 Nov;101(5 Pt 1):1842–1849. doi: 10.1083/jcb.101.5.1842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shirayoshi Y., Okada T. S., Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell. 1983 Dec;35(3 Pt 2):631–638. doi: 10.1016/0092-8674(83)90095-8. [DOI] [PubMed] [Google Scholar]
  33. Silver J., Rutishauser U. Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Dev Biol. 1984 Dec;106(2):485–499. doi: 10.1016/0012-1606(84)90248-3. [DOI] [PubMed] [Google Scholar]
  34. Thiery J. P., Delouvée A., Gallin W. J., Cunningham B. A., Edelman G. M. Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol. 1984 Mar;102(1):61–78. doi: 10.1016/0012-1606(84)90175-1. [DOI] [PubMed] [Google Scholar]
  35. Thiery J. P., Delouvée A., Grumet M., Edelman G. M. Initial appearance and regional distribution of the neuron-glia cell adhesion molecule in the chick embryo. J Cell Biol. 1985 Feb;100(2):442–456. doi: 10.1083/jcb.100.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thiery J. P., Duband J. L., Rutishauser U., Edelman G. M. Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6737–6741. doi: 10.1073/pnas.79.21.6737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tucker G. C., Aoyama H., Lipinski M., Tursz T., Thiery J. P. Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ. 1984 Aug;14(3):223–230. doi: 10.1016/0045-6039(84)90049-6. [DOI] [PubMed] [Google Scholar]
  39. Vincent M., Duband J. L., Thiery J. P. A cell surface determinant expressed early on migrating avian neural crest cells. Brain Res. 1983 Aug;285(2):235–238. doi: 10.1016/0165-3806(83)90058-5. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES