Sealing the live part of the skin: The integrated meshwork of desmosomes, tight junctions and curvilinear ridge structures in the cells of the uppermost granular layer of the human epidermis

European Journal of Cell Biology

Volumn 83, Issue 11-12, 2004, Pages 655-665

  Schlüter, Holger ^a   Wepf, Roger ^b   Moll, Ingrid ^c   Franke, Werner W ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b BEIERSDORF AG   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Desmosomes; Epidermis; Freeze fracture; Keratinocytes; Plasma membrane; Tight junctions

Indexed keywords

OCCLUDIN;

ADULT; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; CELL CONTACT; CELL MEMBRANE; CELL STRUCTURE; DESMOSOME; ELECTRON MICROSCOPY; EPIDERMIS; FETUS; FREEZE FRACTURE; GRANULAR CELL; HUMAN; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; PERMEABILITY BARRIER; PRIORITY JOURNAL; SKIN EPITHELIUM; SQUAMOUS EPITHELIUM; STRATUM CORNEUM; TIGHT JUNCTION;

EID: 12344274098     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1078/0171-9335-00434     Document Type: Article

References (98)

1. Andersen, L., 1980. Cell junctions in squamous epithelium during wound healing in palatal mucosa of guinea pigs. Scand. J. Dent. Res. 88, 328-339.
2. Anderson, J. M., Van Itallie, C. M., Fanning, A. S., 2004. Setting up a selective barrier at the apical junction complex. Curr. Opin. Cell Biol. 16, 140-145.
3. Behr, M., Riedel, D., Schuh, R., 2003. The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev. Cell 5, 611-620.
4. Brandner, J. M., Houdek, P., Kief, S., Grund, C., Franke, W. W., Moll, I., 2000. Are there "tight junctions" in human epidermis? Abstract. Annual Meeting of the Society for Investigative Dermatology, Chicago, May 9-12, 2000. J. Invest. Dermatol. 114, 810.
5. Brandner, J. M., Kief, S., Grund, C., Rendl, M., Houdek, P., Kuhn, C., Tschachler, E., Franke, W. W., Moll, I., 2002. Organization and formation of the tight junction-system in human epidermis and cultured keratinocytes. Eur. J. Cell Biol. 81, 253-263.
6. Breathnach, A. S., 1971. An Atlas of the Ultrastructure of Human Skin. J. & A. Churchill, London.
7. Caputo, R., 1981. The junctions in skin. Am. J. Dermatopathol. 3, 315-322.
8. Caputo, R., Perlucchetti, D., 1977. The junctions of normal human epidermis. A freeze-fracture study. J. Ultrastruct. Res. 61, 44-61.
9. 2- reverses this effect. J. Membr. Biol. 134, 15-29.
10. Claude, P., Goodenough, D. A., 1973. Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J. Cell Biol. 58, 390-400.
11. Drenckhahn, D., 1994. Benninghoff Anatomie, Bd. 1. 15. Edn. Kap. 2: Zellenlehre & Kap. 4.1: Epithelgewebe. Urban & Schwarzenberg, München, pp. 9-93 & 109-117.
12. Echlin, P., 1992. Low-Temperature Microscopy and Analysis. Chapter 3. Plenum Press, New York.
13. Elias, P. M., 1996. The stratum corneum revisited. J. Dermatol. 23, 756-768.
14. Elias, P. M., Friend, D. S., 1975. The permeability barrier in mammalian epidermis. J. Cell Biol. 65, 180-191.
15. Elias, P. M., Friend, D. S., 1976. Vitamin-A-induced mucous metaplasia. An in vitro system for modulating tight and gap junction differentiation. J. Cell Biol. 68, 173-188.
16. Elias, P. M., McNutt, N. S., Friend, D. S, 1977. Membrane alterations during cornification of mammalian squamous epithelia: a freeze-fracture, tracer and thin-section study. Anal. Rec. 189, 577-594.
17. Farquhar, M. G., Palade, G. E., 1963. Junctional complexes in various epithelia. J. Cell Biol. 17, 375-412.
18. Farquhar, M. G., Palade, G. E., 1965. Cell junctions in amphibian skin. J. Cell Biol. 26, 263-291.
19. Fawcett, D. W., 1994. A Textbook of Histology. Chapman and Hall, New York.
20. Fejerskov, O., 1973. Keratinized squamous epithelium of normal and wounded palatal mucosa in guinea pigs. J. Periodont. Res. 11 (Suppl.), 1-80.
21. Ferri, S., Sesso, A., 1979. Freeze-fracture study of the epidermal cells of a teleost with particular reference to intercellular junctions and permeability to tracer. Z. Mikrosk. Anat. Forsch. 93, 497-511.
22. Fox, H., 1986. The skin of amphibia: epidermis, in: J. Bereiter-Hahn, A. G. Matoltsy, K. S. Richards (eds.), Biology of the Integument, Vol. 2 Vertebrates. Springer-Verlag, Berlin, pp. 78-110.
23. Friend, D. S., Gilula, N. B., 1972. Variations in tight and gap junctions in mammalian tissues. J. Cell Biol. 53, 758-776.
24. Fujimoto, K., 1995. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J. Cell Sci. 108, 3443-3449.
25. Furuse, M., Fujimoto, K., Sato, N., Hirase, T., Tsukita, Sa., Tsukita, Sh., 1996. Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures. J. Cell Sci. 109, 429-435.
26. Furuse, M., Sasaki, H., Fujimoto, K., Tsukita, S., 1998. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell Biol. 143, 391-401.
27. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A., Tsukita, S., 2002. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 156, 1099-1111.
28. Ghadially, F. N., t988. Ultrastructural Pathology of the Cell and Matrix, Vol. 2. 3. Edn. Butterworths, London.
29. Goodenough, D. A., Gilula, N. B., 1974. The splitting of hepatocyte gap junctions and zonulae occludentes with hypertonic disaccharides. J. Cell Biol. 61, 575-590.
30. Green, C. R., 1984. Intercellular junctions, in: J. Bereiter-Hahn, A. G. Matoltsy, K. S. Richards (eds.), Biology of the Integument. 2. Vertebrates. Springer-Verlag, Berlin, pp. 5-16.
31. Green, K. J., Gaudry, C. A., 2000. Are desmosomes more than tethers for intermediate filaments? Nat. Rev. Mol. Cell Biol. 1, 208-216.
32. Hashimoto, K., 1971. Intercellular spaces of the human epidermis as demonstrated with lanthanum. J. Invest. Dermatol. 57, 17-31.
33. Henderson, D. W., Papadimitriou, J. M., Coleman, M., 1986. Ultrastructural Appearances of Tumours. Diagnosis and Classification of Human Neoplasia by Electron Microscopy. 2. Edn. Churchill Livingstone, Edinburgh.
34. Herrmann, T., van der Hoeven, F., Gröne, H.-J., Stewart, A. F., Langbein, L., Kaiser, I., Liebisch, G., Gosch, I., Buchkremer, F., Drbonik, W., Schmitz, G., Stremmel, W., 2003. Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy. J. Cell Biol. 161, 1105-1115.
35. Holbrook, K. A., Dale, B. A., Witt, D. R., Hayden, M. R., Toriello, H. V., 1987. Arrested epidermal morphogenesis in three newborn infants with a fatal genetic disorder (restrictive dermopathy). J. Invest. Dermatol. 88, 330-339.
36. Holland, V. F., Zampighi, G. A., Simon, S. A., 1989. Morphology of fungiform papillae in canine lingual epithelium: location of intercellular junctions in the epithelium. J. Comp. Neurol. 279, 13-27.
37. Horak, E., Lelkes, G., Sugar, J., 1984. Intercellular junctions of methylcholanthrene-induced rat skin basocellular and squamous carcinomas. Br. J. Cancer 49, 637-644.
38. Hürter, T., Behrens, H., 1980. Freeze-etch studies of the chick embryonic skin with special consideration of cell junctions. Acta Histochem. 67, 272-282.
39. Katz, U., 1986. The role of amphibian epidermis in osmoregulation and its adaptive response to changing environment, in: J. Bereiter-Hahn, A. G. Matoltsy, K. S. Richards (eds.), Biology of the Integument, Vol. 2 Vertebrates. Springer-Verlag, Berlin, pp. 78-110.
40. Kerjaschki, D., Krisch, K., Sleyter, U. B., Umrath, W., Kakesz, R., Depisch, D., Kokoschka, R., Horandner, H., 1979. The structure of tight junctions in human thyroid tumors. A systematic freeze-fracture study. Am. J. Pathol. 96, 207-225.
41. Kimura, Y., Shiozaki, H., Hirao, M., Maeno, Y., Doki, Y., Inoue, M., Monden, T., Ando-Akatsuka, Y., Furuse, M., Tsukita, S., Monden, M., 1997. Expression of occludin, tight-junction-associated protein, in human digestive tract. Am. J. Pathol. 151, 45-54.
42. Kitajima, Y., Mori, S., 1980. Freeze-fracture study of the occurrence of plasma membrane differentiations in human basal cell carcinoma. J. Dermatol. 7, 389-396.
43. Kitajima, Y., Eguchi, K., Ohno, T., Mori, S., Yaoita, H., 1983. Tight junctions of human keratinocytes in primary culture: a freeze-fracture study. J. Ultrastruct. Res. 82, 309-313.
44. Landmann, L., 1985. Permeabilitätsbarriere der Epidermis. Grosse Scripta 9. Grosse Verlag, Berlin.
45. Landmann, L., 1986. The skin of reptiles: epidermis and dermis, in: J. Bereiter-Hahn. A. G. Matoltsy, K. S. Richards (eds.), Biology of the Integument. 2. Vertebrates. Springer-Verlag, Berlin, pp. 150-187.
46. Landmann, L., Stolinski, C., Martin, B., 1981. The permeability barrier in the epidermis of the grass snake during the resting stage of the sloughing cycle. Cell Tissue Res. 215, 369-382.
47. Lane, N. J., 1981. Tight junctions in arthropod tissues. Int. Rev. Cytol. 73, 243-317.
48. Langbein, L., Grand, C., Kuhn, C., Praetzel, S., Kartenbeck, J., Brandner, J. M., Moll, I., Franke, W. W., 2002. Tight junctions and compositionally related junctional structures in mammalian stratified epithelia and cell cultures derived therefrom. Eur. J. Cell Biol. 81, 419-435.
49. Langbein, L., Pape, U.-F., Grund, C., Kuhn, C., Praetzel, S., Moll, I., Moll, R., Franke, W. W., 2003. Tight junction-related structures in the absence of a lumen: Occludin, claudins and tight junction plaque proteins in densely packed cell formations of stratified epithelia and squamous cell carcinomas. Eur. J. Cell Biol. 82, 385-400.
50. Lechaire, J.-P., 1988. Formation of desmosomes and other contact specializations in cultured skin of the frog (Rana esculenta . Cell Tissue Res. 252, 157-163.
51. Leloup, R., Laurent, L., Ronveaux, M.-F., Drohmans, P., Wanson, J.-C., 1979. Desmosomes and desmogenesis in the epidermis of calf muzzle. Biol. Cell. 34, 137-152.
52. Leube, R., Rustad, T. J., 1991. Squamous cell metaplasia in the human lung: Molecular characteristics of epithelial stratification. Virchows Arch. B Cell Pathol. 61, 227-253.
53. Madara, J. L., Dharmsathaphorn, K., 1985. Occluding junction structure-function relationships in a cultured epithelial monolayer. J. Cell Biol. 101, 2124-2133.
54. Madison, K. C., 2003. Barrier function of the skin: "La raison d'être" of the epidermis. J. Invest. Dermatol. 121, 231-241.
55. Malminen, M., Koivukangas, V., Peltonen, J., Karvonen, S.-L., Oikarinen, A., Peltonen, S., 2003. Immunohistological distribution of the tight junction components ZO-1 and occludin in regenerating human epidermis. Br. J. Dermatol. 149, 255-260.
56. Martinez-Palomo, A., 1970. Ultrastructural modifications of intercellular junctions in some epithelial tumors. Lab. Invest. 22, 605-614.
57. Martinez-Palomo, A., Erlij, D., Bracho, H., 1971. Localization of permeability barriers in frog skin epidermis. J. Cell Biol. 50, 277-287.
58. Martinez-Palomo, A., Meza, I., Beady, G., Cereijido, M., 1980. Experimental modulation of occluding junctions in a cultured transporting epithelium. J. Cell Biol. 87, 736-745.
59. Matter, K., Balda, M. S., 1999. Occludin and the functions of tight junctions. Int. Rev. Cytol. 186, 117-146.
60. McLaughlin, B. J., Caldwell, R. B., Sasaki, Y., Wood, T. O., 1985. Freeze-fracture quantitative comparison of rabbit corneal epithelial and endothelial membranes. Curr. Eye Res. 4, 951-961.
61. -+-dependent disassembly and reassembly of occluding junctions in guinea pig pancreatic acinar cells. J. Cell Biol. 79, 156-172.
62. Meyle, J., Gültig, K., Rascher, G., Wolburg, H., 1999. Transepithelial electrical resistance and tight junctions of human gingival keratinocytes. J. Periodont. Res. 34, 214-222.
63. Mittal, A. K., Whitear, M., 1979. Keratinizing of fish skin with special reference to the catfish Bagarius bagarius. Cell Tissue Res. 202, 213-230.
64. Montesano, R., Friend, D. S., Perrelet, A., Orci, L., 1975. In vivo assembly of tight junctions in fetal rat liver. J. Cell Biol. 67, 310-319.
65. Moor, H., Mühlethaler, K., 1963. Fine structure in frozen-etched yeast cells. J. Cell Biol. 17, 609-628.
66. Morita, K., Itoh, M., Saitou, M., Ando-Akatsuka, Y., Furuse, M., Yoneda, K., Imamura, S., Fujimoto, K., Tsukita, S., 1998. Subcellular distribution of tight junction-associated proteins (occludin, ZO-1, ZO-2) in rodent skin. J. Invest. Dermatol. 110, 862-866.
67. Morita, K., Tsukita, S., Miyachi, Y., 2004. Tight junction-associated proteins (occludin, ZO-1. claudin-1, claudin-4) in squamous cell carcinoma and Bowen's disease. Br. J. Dermatol. 151, 328-334.
68. Moulson, C. L., Martin, D. R., Lugus, J. J., Schaffer, J. E., Lind, A. C., Miner, J. H., 2003. Cloning of wrinkle-free, a previously uncharacterized mouse mutation, reveals crucial roles for fatty acid transport protein 4 in skin and hair development. Proc. Natl. Acad. Sci. USA 100, 5274-5279.
69. Nermuth, M. V., 1977. Freeze-drying for electron microscopy, in: M. A. Hayat (ed.). Principles and Techniques of Electron Microscopy. Van Nostrand Reinhold Company, New York. London, pp. 79-98.
70. Norlén, L., 2002. Molecular skin barrier models and some central problems for the understanding of skin barrier structure and function. Skin Pharmacol. Appl. Skin Physiol. 16, 203-211.
71. Orlando, R. C., Lacy, E. R., Tobey, N. A., Cowart, K., 1992. Barriers to paracellular permeability in rabbit esophageal epithelium. Gastroenterology 102, 910-923.
72. Orwin, D. F.G., Thomson, R. W., Flower, N. E., 1973. Plasma membrane differentiations of keratinizing cells of the wool follicle. III. Tight junctions. J. Ultrastruct. Res. 45, 30-40.
73. Palekar, M. S., Sirsat, S. M., 1975. Lanthanum staining of cell surface and junctional complexes in normal and malignant human oral mucosa. J. Pathol. 4, 231-243.
74. Pfeiffer, S., Vielhaber, G., Vietzke, J. P., Wittern, K. P., Hintze, U., Wepf, R., 2000. High-pressure freezing provides new information on human epidermis: simultaneous protein antigen and lamellar lipid structure preservation. Study on human epidermis by cryoimmobilization. J. Invest. Dermatol. 114, 1030-1038.
75. Polak-Charcon, S., Shoham, J., Ben-Shaul, Y., 1980. Tight junctions in epithelial cells of human fetal hindgm, normal colon, and colon adenocarcinoma. J. Natl. Cancer Inst. 65, 53-62.
76. Posalaky, Z., McGinley, D., Cutler, B., Katz, H. I., 1979. Intercellular junctional specializations in human basal cell carcinoma. Virchows Arch. A Path. Anat. Histol. 384, 53-63.
77. Pummi, K., Malminen, M., Aho, H., Karvonen, S.-L., Peltonen, J., Peltonen, S., 2001. Epidermal tight junctions: ZO-1 and occludin are expressed in mature, developing, and affected skin and in vitro differentiating keratinocytes. J. Invest. Dermatol. 117, 1050-1058.
78. Richter, T., Peuckert, C., Sattler, M., König, K., Riemann, I., Hintze, U., Wittern, K.-P., Wiesendanger, R., Wepf, R., 2004. Dead but highly dynamic - the stratum corneum is divided into three hydration zones. Skin Pharmacol. Physiol. 17, 246-257.
79. Ritter, M., Henry, D., Wiesner, S., Pfeiffer, S., Wepf, R., 1999. A versatile high-vacuum cryo-transfer for Cryo-FESEM, cryo-SPM and other imaging techniques. Microsc. Microanal. 5 (Supp. 2), 424-425.
80. Schneeberger, E. E., Lynch, R. D., 2004. The tight junction: a multifunctional complex. Am. J. Physiol. Cell. Physiol. 286, C1213-C1228.
81. Schroeder, H. E., Theilade, J., 1966. Electron microscopy of normal human gingival epithelium. J. Periodont. Res. 1, 95-119.
82. Shimono, M., Clementi, F., 1976. Intercellular junctions of oral epithelium. Studies with freeze-fracture and tracing methods. J. Ultrastruct. Res. 56, 121-136.
83. Simon, S. A., Holland, V. F., Benos, D. J., Zampighi, G., 1993. Transcellular and paracellular pathways in lingual epithelia and their influence in taste transduction. Microsc. Res. Tech. 26, 196-208.
84. Squier, C. A., 1973. The permeability of keratinized and nonkeratinized oral epithelium to horseradish peroxidase. J. Ultrastruct. Res. 43, 160-177.
85. Stachelin, L. A., 1974. Structure and function of intercellular junctions. Int. Rev. Cytol. 39, 191-283.
86. Stevenson, B. R., Keon, B. H., 1998. The tight junction: morphology to molecules. Annu. Rev. Cell Dev. Biol. 14, 89-109.
87. Tebbe, B., Mankerts, J., Schwarz, C., Amasheh, S., Fromm, M., Assaf, C., Schultz-Ehrenburg, U., Sánchez Ruderisch, H., Schulzke, J.-D., Orfanos, C. E., 2002. Tight junction proteins: a novel class of integral membrane proteins. Expression in human epidermis and in HaCaT keratinocytes. Arch. Dermatol. Res. 294, 14-18.
88. Tepass, U., 2003. Claudin complexities at the apical junctional complex. Nat. Cell Biol. 5, 595-597.
89. Thilander, H., Bloom, G. D., 1968. Cell contacts in oral epithelia. J. Periodont. Res. 3, 96-110.
90. Tsukita, S., Furuse, M., Itoh, M., 2001. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293.
91. Vasioukhin, V., Fuchs, E., 2001. Actin dynamics and cell-cell adhesion in epithelia. Curr. Opin. Cell Biol. 13, 76-84.
92. Walther, P., Müller, M., 1997. Double-layer coating for field-emission cryo-scanning electron microscopy - present state and applications. Scanning 19, 343-348.
93. Walther, P., Hentschel, J., Herter, P., Müller, T., Zierold, K., 1990. Imaging of intramembranous particles in frozen-hydrated cells by high resolution cryo-SEM. Scanning 12, 300-307.
94. Wang, Y., Chen, M., Wolosin, J. M., 1993. ZO-1 in corneal epithelium; stratal distribution and synthesis induction by outer cell removal. Exp. Eye Res. 57, 283-292.
95. Whitear, M., 1986. The skin of fishes including cyclostomes: epidermis, in: J. Bereiter-Hahn, A. G. Matoltsy, K. S. Richards (eds.). Biology of the Integument. 2. Vertebrates. Springer-Verlag, Berlin, pp. 8-38.
96. Wolosin, J. M., 1988. Regeneration of resistance and ion transport in rabbit corneal epithelium after induced surface cell exfoliation. J. Membr. Biol. 104, 45-55.
97. Yap, A. S., Mullin, J. M., Stevenson, B. R., 1998. Molecular analyses of tight junction physiology: insights and paradoxes. J. Membrane Biol. 163, 159-167.
98. Yoshida, Y., Morita, K., Mizoguchi, A., Ide, C., Miyachi, Y., 2001. Altered expression of occludin and tight junction formation in psoriasis. Arch. Dermatol. Res. 293, 239-244.