Abstract
The 5AII/HT7 antigen is the avian homologue of a 45-50X103 M r plasma membrane glycoprotein of the immunoglobulin super-gene family also identified in mammalian species (basigin, mouse gp42, MRC OX-47 antigen, M6 antigen). We had previously demonstrated that antibodies to this antigen interfere with heterotypic cell-to-cell interaction-dependent glial cell maturation in vitro. In this report, we sought to gain insight into its developmental role through an analysis of its distribution at various stages of avian embryogenesis. The primary mode of expression progresses from generalized staining of the undifferentiated tissue to intense labelling of specific cell types coincident with biochemical or morphological differentiation. In the retina, expression progresses from the generalized staining of the neural ectoderm, then, during neurogenesis, becomes restricted to Müller cells, photoreceptor cell bodies, the retina pigmented epithelium, the pigmented cells of the ciliary membrane and endothelia of the pecten. Similarly, the uniform staining of undifferentiated skin ectoderm progressively becomes confined to the germinative cells of the epidermis during biochemical differentiation of scutate and reticulate scales and formation of the feather follicle. During mesonephric and metanephric tubule development, labeling appears on those cells induced to form epithelia from the unlabeled mesenchyme and persists on the basal-lateral membranes of the convoluted tubules. Western blot analysis of NP-40 solubilized proteins from hatchling chicken identifies an immunoreactive polypeptide of 45-50X103 M r in tissues stained immunohistochemically and an additional band of 69X103 M r in the neural retina and pineal gland. The localization of the 5A11 antigen at boundaries typically associated with inductive interactions between cells and tissues suggests broad involvement in cell-to-cell interactions associated with cellular maturation.
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References
Albelda SM, Buck CA (1990) Integrins and other cell adhesion molecules. FASEB J 4:2868–2880
Albrecht U, Seulberger H, Schwarz H, Risau W (1990) Correlation of blood-brain barrier function and HT7 protein distribution in chick brain circumventricular organs. Brain Res 535:49–61
Atruda F, Cervella P, Gaeta ML, Daniele A, Giancotti F, Tarone G, Stefanuto G, Silengo L (1989) Cloning of cDNA for a novel mouse membrane glycoprotein (gp42): shared identity to histo-compatibility antigens, immunoglobulins and neural-cel adhesion molecules. Gene 85:445–452
Chuong CM, Edelman GM (1985) Expression of Cell-adhesion molecules in embryonic induction. I. Morphogenesis of nestling feathers. J Cell Biol 101:1009–1026
Covault J, Merlie JP, Goridis C, Sanes JR (1986) Molecular forms of N-CAM and its RNA in developing and denervated skeletal muscle. J Cell Biol 102:731–739
Crossin KL, Chuong CM, Edelman GM (1984) Expression sequnces of cell adhesion molecules. Proc Natl Acad Sci USA 82:6942–6946
Damsky CH, Richa J, Solter J, Knudsen D, Buck CA (1983) Identification and purification of a cellsurface glycoprotein mediating intracellular adhesion in embryonic and adult tissue. Cell 34:455–466
Edelman GM (1988) Morphoregulatory molecules. Biochemistry 27:3533–3543
Fadool JM, Linser PJ (1993A) The 5A11 antigen is a cell recognition molecule which is involved in neuronal-glial interactions in avian neural retina. Dev Dynamics 196:252–262
Fadool JM, Linser PJ (1993B) Differential gylcosylation of the 5A11/HT7 antigen by neural retina and epithelial tissues in the chicken. J Neurochem 60:1354–1364
Fossum S, Mallett S, Barclay AN (1991) The MRC OX-47 antigen is a mamber of the immunoglobulin superfamily with an unusual transmembrane sequence. Eur J Immunol 21:671–679
Gallin WJ, Edelman GM, Cunningham BA (1983) Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc Natl Acad Sci USA 80:1038–1042
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Hatta K, Takagi S, Fujisawa H, Takeichi M (1987) Spatial and temporal expression pattern of N-cadherin cell ashesion molecules correlated with morphogenetic processes of chick embryos. Dev Biol 120:215–227
Hyafil F, Babinet C, Jacob F (1981) Cell-Cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26:447–454
Kasinrerk W, Fiebiger E, Stefanova I, Baumruker T, Knapp W, Stockinger H (1992) Human leukocyte activation antigen M6, A member of the Ig superfamily, is the species homologue of rat OX-47, mouse basigin, and chicken HT7 molecule. J Immunol 149:847–854
Knudsen KA, McElwee SA, Myers L (1990a) A role for the neural cell adhesion molecule, NCAM, in myoblast interaction during myogenesis. Dev Biol 138:159–168
Knudsen KA, Myers L, McElwee SA (1990b) A role for the Ca2+-dependent adhesion molecule, N-cadherin, in myoblast interaction during myogenesis. Exp Cell Res 188:175–184
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lemmon V, Staves EB, Perry HE, Gottlieb DI (1982) A monoclonal antibody that binds to the surface of chick brain cells and myotubes: cell selectivity and properties of the antigen. Dev Brain Res 11:191–197
Linser PJ (1987) Neural-glial interactions in retina development. Am Zool 27:161–169
Linser PJ, Moscona AA (1979) Induction of glutamine synthetase in the embryonic neural retina: localization in the Muller fibers and dependance on cell interactions. Proc Natl Acad Sci USA 76:6476–6480
Linser PJ, Moscona AA (1981) Carbonic anhydrase-C in the neural retina: transition from a generalized to glia-specific cell localization during embryonic development. Proc Natl Acad Sci USA 78:7190–7194
Linser PJ, Moscona AA (1983) Hormonal induction of glutamine synthetase in cultures of embryonic retina cells: requirement for neuron-glia contact interactions. Dev Biol 96:529–534
Linser PJ, Perkins MS (1987) Regulatory aspects of the in vitro development of retina Muller glial cells. Cell Differ 20:189–196
McNeill H, Ozawa M, Kemler R, Nelson WJ (1990) Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell 62:309–316
Miyauchi T, Masuzawa Y, Muramatsu T (1991) The basigin group of the immunoglobulin superfamily: complete conservation of a segment in and around transmembrane domains of human and mouse basigin and chicken HT7 anigen. J Biochem 110:770–774
O'Guin WM, Knapp LW, Sawyer RH (1982) Biochemical and immunohistochemical localization of alpha and beta keratins in the avian scutate scale. J Exp Zool 220:371–376
Pouliot Y, Holland PC, Blachuk OW (1990) Developmental regulation of a cadherin during the differentiation of skeletal myoblasts. Dev Biol 141:292–298
Risau W, Hallmann R, Albrecht U, Henke-Fahle S (1986) Brain induces the expression of an early cell surface marker for blood-brain barrier-specific endothelium. EMBO J 5:3179–3183
Rutishauser U, Jessell TM (1988) Cell adhesion molecules in vertebrate neural development. Biol Rev 68:819–857
Schlosshauer B, Herzog KH (1990) Neurothelin: An inducible cell surface glycoprotein of blood-brain barrier-specific endothelial cells and distinct neurons. J Cell Biol 110:1261–1274
Schwarting GA, Jungalwala FB, Chou DKH, Boyer AM, Yamamoto M (1987) Sulfated glucuronic acid-containing glycoconjugates are temporally and spatially regulated antigens in the developing mammalian nervous system. Dev Biol 120:65–76
Seulberger H, Lottspeich F, Risau W (1990) The inducible blood-brain barrier specific molecule HT7 is a novel immunoglobulin-like cell surface glycoprotein. EMBO J 9:2151–2158
Seulberger H, Unger CM, Risau W (1992) HT7, neurothelin, basigin, gp-42 and OX-47 — many names for one developmentally regulated immuno-globulin-like surface glyocprotein on blood-brain barrier endothelium, epithelial tissue barriers and neurons. Neurosci Lett 140:93–97
Soler AP, Knudsen KA (1991) Colocalization of N-CAM and N-cadherin in the avian skeletal myoblasts. Dev Biol 148:389–392
Takeichi M (1990) Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem 59:237–252
Thiery J-P, Duband J-L, Rutishauser U, Edelman GM (1982) Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci USA 79:6737–6741
Thiery JP, Delouvee A, Gallin WJ, Cunningham BA, Edelman GM (1984) Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol 102:61–78
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354
Yoshida-Noro C, Suzuki N, Takeichi M (1984) Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev Biol 101:19–27
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Fadool, J.M., Linser, P.J. Spatial and temporal expression of the 5A11/HT7 antigen in the chick embryo. Roux's Arch Dev Biol 203, 328–339 (1994). https://doi.org/10.1007/BF00457804
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DOI: https://doi.org/10.1007/BF00457804