Skip to main content
Log in

Alignment of desmosomes in stratifying human epidermis

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Cultured human epithelial cells stained with antibody to desmosomal proteins by indirect immunofluorescence showed linear arrays of desmosomes en face between stratified cells. To confirm that an extensive linear pattern existed on the cell surface, subconfluent cultures were viewed using scanning electron microscopy. Aligned arrays of blunt protrusions lying parallel to each other and extending in the direction of the long axis of the cell were observed on the surface of groups of superficial cells in intact cultures. That this pattern was indeed related to desmosomal distribution was verified by transmission microscopy of thin sections cut in a plane between the upper and lower surfaces of flattened stratified cells to view desmosomes directly. A similar arrangement of desmosomes was seen in intact tissue, using epidermal sheets separated from newborn foreskin. The same pattern found in flattened cells was sometimes apparent in more rounded basal cells where the cytoplasm was beginning to extend. Since desmosomal plaques are associated with keratin filaments, the alignment of desmosomes must occur in association with cytoskeletal changes as cells become flattened toward the distal epithelial surface. The primary initiation of desmosomal alignment remains to be investigated. However, the present findings demonstrate an increasingly regular membrane-cytoskeletal spatial interaction as stratified epithelial cells of skin mature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Cowin P, Garrod DR (1983) Antibodies to epithelial desmosomes show wide tissue and species cross-reactivity. Nature 302:148–149

    Google Scholar 

  • Cowin P, Mattey D, Garrod D (1984a) Distribution of desmosomal components in the tissues of vertebrates, studied by fluorescent antibody staining. J Cell Sci 66:119–132

    Google Scholar 

  • Cowin P, Mattey D, Garrod D (1984b) Identification of desmosomal surface components (desmocollins) and inhibition of desmosome formation by specific Fab'. J Cell Sci 70:41–60

    Google Scholar 

  • Cowin P, Kapprell H-P, Franke WW (1985) The complement of desmosomal plaque proteins in different cell types. J Cell Biol 101:1442–1454

    Google Scholar 

  • Cowing P, Kapprell H-P, Franke WW, Tamkun JJ, Hynes RO (1986) Plakoglobin: a protein common to different kinds of intercellular adhering junctions. Cell 46:1063–1073

    Google Scholar 

  • Cowin P, Franke WW, Grund C, Kapprell H-P, Kartenbeck J (1987) The desmosome-intermediate filament complex. In: Eldelman GM, Thiery J-P (eds) The cell in contact. Wiley and Sons, New York, pp 427–460

    Google Scholar 

  • Deganello S, Chou C (1984) The uric acid-whewellite association in human kidney stones. SEM 11:927–933

    Google Scholar 

  • Drochmans P, Freudenstein C, Wanson J-C, Laurent L, Keenan TW, Stadler J, Leloup R, Franke WW (1978) Structure and biochemical composition of desmosomes and tonofilaments isolated from calf muzzle epidermis. J Cell Biol 79:427–443

    Google Scholar 

  • Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412

    Google Scholar 

  • Franke WW, Mueller H, Mittnacht S, Kapprell H-P, Jocano JL (1983) Significance of two desmosome plaque-associated polypeptides of molecular weights 75,000 and 83,000. EMBO J 2:2211–2215

    Google Scholar 

  • Franke WW, Schiller DL, Hatzfeld M, Jacono JL, Mittnacht S, Schmid E, Cohlberg JA, Quinlan RA (1984) Cytokeratin: complex formation, biogenesis, and interactions with desmosomes. In: Levine A, Topp W, Vande Woude G, Watson JD (eds) Cancer Cell 1/The Transformed Phenotype. Cold Spring Habor Laboratory

  • Geiger B, Schmid E, Franke WW (1983) Spatial distribution of proteins specific for desmosomes and adhaerens junctions in epithelial cells demonstrated by double immunofluorescence microscopy. Differentiation 23:189–205

    Google Scholar 

  • Geiger B, Volik T, Volberg T (1985) Molecular heterogeneity of adherens junctions. J Cell Biol 101:1523–1531

    Google Scholar 

  • Geiger BT, Avnuk Z, Volberg T, Volk T (1987) Molecular domains of adherens junctions. In: Eldelman GM, Thiery J-P (eds) The Cell in contact. John Wiley and Sons New York, pp 461–489

    Google Scholar 

  • Guidice JG, Cohen SM, Patel NP, Steinberg MS (1984) Immunological comparison of desmosomal components from several bovine tissues. J Cell Biochem 26:35–45

    Google Scholar 

  • Gorbsky G, Steinberg MS (1981) Isolation of the intercellular glycoproteins of desmosomes. J Cell Biol 90:243–248

    Google Scholar 

  • Gorbsky G, Cohen SM, Shida H, Guidice GJ, Steinberg MS (1985) Isolation of the non-glycosylated proteins of desmosomes and immunolocalization of a third plaque protein: desmoplakin III. Proc Natl Acad Sci USA 82:810–814

    Google Scholar 

  • Green KJ, Geiger B, Jones JCR, Talian JC, Goldman RD (1987) The relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes. J Cell Biol 104:1389–1402

    Google Scholar 

  • Holbrook KA, Hennings H (1983) Phenotypic expression of epidermal cells in vitro: A review. J Invest Dermatol 81S:11S-24S

    Google Scholar 

  • Jones JCR, Goldman RD (1985) Intermediate filaments and the initiation of desmosome assembly. J Cell Biol 101:506–517

    Google Scholar 

  • Jones JCR, Hokoo KM, Goldman RD (1986a) Further analysis of pemphigus autoantibodies and their use in studies on heterogeneity, structure and function of desmosomes. J Cell Biol 102:1109–1117

    Google Scholar 

  • Jones JCR, Hokoo KM, Goldman RD (1986b) A cell surface desmosome-associated component: identification of a tissue-specific cell adhesion molecule. Proc Natl Acad Sci USA 83:7282–7286

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A-138A

    Google Scholar 

  • Kelly DE, Kuda AM (1981) Traversing filaments in desmosomal and hemidesmosomal attachments; freeze-fracture approaches toward their characterization. Anat Rec 199:1–14

    Google Scholar 

  • Klymkowsky MW, Miller RH, Lane EB (1983) Morphology, behavior and interaction of cultured epithelial cells after the antibody-induced disruption of keratin filament organization. J Cell Biol 96:494–509

    Google Scholar 

  • Krawczyk WS, Wilgram GF (1973) Hemidesmosomes and desmosomes morphogenesis during epidermal wound healing. J Ultrastruct Res 45:93–101

    Google Scholar 

  • Ma AS-P, Lorincz AL (1988) Immunofluorescence localization of peripheral proteins in cultured human keratinocytes. J Invest Dermatol 90:331–335

    Google Scholar 

  • Ma AS-P, Sun T-T (1986) Differentiation-dependent changes in the solubility of a 195-kD protein in human epidermal keratinocytes. J Cell Biol 103:41–48

    Google Scholar 

  • Matoltsy AG (1975) Desmosomes, filaments and keratohyaline granules: their role in stabilization of the epidermis. J Invest Dermatol 65:127–142

    Google Scholar 

  • O'Keefe EJ, Briggaman RA, Herman B (1987) Calcium-induced assembly of adherens junctions in keratinocytes. J Cell Biol 105:807–817

    Google Scholar 

  • Overton J (1973) Experimental manipulation of desmosome formation. J Cell Biol 56:636–646

    Google Scholar 

  • Overton J (1974) Cell junctions and their development. Prog Surf Membr Sci 8:161–208

    Google Scholar 

  • Overton J (1977) Formation of junctions and cell sorting in aggregates of chick and mouse cells. Dev Biol 55:103–116

    Google Scholar 

  • Overton J (1980) Inhibition of desmosomes formation in aggregating embryonic chick cells. Dev Biol 92:66–72

    Google Scholar 

  • Owaribe K, Masuda H (1986) Organization of microfilaments and intermediate filaments in retinal pigmented epithelial cells. In: Ishikawa H, Hatano S, Sato H (eds) Cell Motility: Mechanism and Regulation. Yamada Science Foundation, pp 507–514

  • Penn E, Hobson C, Rees D, Magee A (1987) Structure and assembly of desmosome junctions: biosynthesis, processing and transport of the major proteins and glycoprotein compartments in cultured epithelial cells. J Cell Biol 105:57–68

    Google Scholar 

  • Rheinwald J, Green H (1975) Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 66:331–334

    Google Scholar 

  • Skerrow CJ, Skerrow D (1980) Desmosomes and filaments in mammalian epidermis. In: Curtis ASG, Pitts JD (eds) Cell Adhesion and Motility. Third Symposium of the British Society for Cell Biology, Cambridge University Press, Cambridge, pp 445–464

    Google Scholar 

  • Steinberg MS, Shida H, Giudice GJ, Shida M, Patel NH, Blaschuk OW (1987) On the molecular organization, diversity and functions of desmosomal proteins. In: Bork G, Clark S (eds) Junctional Complexes of Epithelial Cells. CIBA Foundation Symposium 125. John Wiley and Sons New York, pp 3–77

    Google Scholar 

  • Watt FM (1984) Selective migration of terminally differentiating cells from the basal layer of cultured human epidermis. J Cell Biol 98:16–21

    Google Scholar 

  • Watt FM, Mattey DL, Garrod DR (1984) Calcium-induced reorganization of desmosomal components in cultured human keratinocytes. J Cell Biol 99:2211–2215

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ma, A.S.P., Bystol, M.E. & Overton, J. Alignment of desmosomes in stratifying human epidermis. Cell Tissue Res. 254, 585–592 (1988). https://doi.org/10.1007/BF00226508

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00226508

Key words

Navigation