Abstract
The developmental appearance of cell-adhesion molecules (CAMs) was mapped during the morphogenesis of the adult chicken feather. Neural CAM (N-CAM), liver CAM (L-CAM), and neuron-glia CAM (Ng-CAM), as well as substrate molecules (laminin and fibronectin), were compared in newborn chicken skin by immunohistochemical means. N-CAM was found to be enriched in the dermal papilla, which was closely apposed to L-CAM- positive papillar ectoderm. The two CAMs were then co-expressed in cells of the collar epithelium. Subsequently generated barb epithelia expressed only L-CAM, but N-CAM reappeared periodically on cells between developing barbs and barbules. N-CAM first appeared on a single L-CAM-positive basilar cell located in each valley flanked by two adjacent barb ridges. Subsequently, the expression of N-CAM extended one cell after another to include the whole basilar layer. N-CAM also appeared in the L-CAM-positive axial-plate epithelia, beginning in a single cell located at the ridge base. The two collectives of N-CAM- positive epithelia constituting the marginal and axial plates then disintegrated, leaving interdigitating spaces between keratinized structures that had previously expressed L-CAM. The morphological transformation from an epithelial cylinder to a three-level branched feather pattern is thus achieved by coupling alternating CAM expression in linked cell collectives with specific differentiation events, such as keratinization. During all of these morphogenetic processes, laminin and fibronectin formed a continuous basement membrane separating pulp from feather epithelia, and were excluded from the sites involved in periodic appearances of N-CAM. The same staining pattern described for developing chickens persisted in the feather follicles of adult chicken tissue that have gone through several cycles of molting. Cyclic expression of the two different CAMs underlies each of the different morphological events that are generated epigenetically during feather morphogenesis.
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Selected References
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- 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]
- Chuong C. M., Edelman G. M. Expression of cell-adhesion molecules in embryonic induction. I. Morphogenesis of nestling feathers. J Cell Biol. 1985 Sep;101(3):1009–1026. doi: 10.1083/jcb.101.3.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Edelman G. M. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. doi: 10.1126/science.6823544. [DOI] [PubMed] [Google Scholar]
- 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]
- Edelman G. M. Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu Rev Neurosci. 1984;7:339–377. doi: 10.1146/annurev.ne.07.030184.002011. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Gallin W. J., Prediger E. A., Edelman G. M., Cunningham B. A. Isolation of a cDNA clone for the liver cell adhesion molecule (L-CAM). Proc Natl Acad Sci U S A. 1985 May;82(9):2809–2813. doi: 10.1073/pnas.82.9.2809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Haake A. R., König G., Sawyer R. H. Avian feather development: relationships between morphogenesis and keratinization. Dev Biol. 1984 Dec;106(2):406–413. doi: 10.1016/0012-1606(84)90240-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Kitamura K. Distribution of endogenous beta-galactoside-specific lectin, fibronectin and type I and III collagens during dermal condensation in chick embryos. J Embryol Exp Morphol. 1981 Oct;65:41–56. [PubMed] [Google Scholar]
- Mauger A., Demarchez M., Herbage D., Grimaud J. A., Druguet M., Hartmann D., Sengel P. Immunofluorescent localization of collagen types I and III, and of fibronectin during feather morphogenesis in the chick embryo. Dev Biol. 1982 Nov;94(1):93–105. doi: 10.1016/0012-1606(82)90072-0. [DOI] [PubMed] [Google Scholar]
- Murray B. A., Hemperly J. J., Gallin W. J., MacGregor J. S., Edelman G. M., Cunningham B. A. Isolation of cDNA clones for the chicken neural cell adhesion molecule (N-CAM). Proc Natl Acad Sci U S A. 1984 Sep;81(17):5584–5588. doi: 10.1073/pnas.81.17.5584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sengel P. Role of extracellular matrix in the development of skin and cutaneous appendages. Prog Clin Biol Res. 1985;171:123–135. [PubMed] [Google Scholar]
- 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]
- 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]