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The intermediate filament system of the keratinizing mouse forestomach epithelium: Coexpression of keratins of internal squamous epithelia and of epidermal keratins in differentiating cells

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Summary

The internal epithelium of mouse forestomach represents a fully keratinized tissue that has many morphological aspects in common with the integumental epidermis. In the present study we have, therefore, analyzed keratin expression in the total epithelium, in subfractions of basal cells and in living and dead suprabasal cells that were obtained by Percoll density gradient centrifugation of trypsin-dissociated forestomach keratinocytes. The keratin analysis revealed that basal forestomach keratinocytes synthesize the same keratin types as basal epidermal cells (60 000, 52 000 and 47 000 daltons), whereas differentiating cells contain both the epidermal suprabasal keratin pair (67 000 and 59 000 daltons) and the suprabasal keratin pair characteristic for other internal squamous epithelia (57 000 and 47 000 daltons). Indirect immunofluorescence using an antibody recognizing the members of the epidermal-type suprabasal keratin pair and in-situ-hybridization experiments using specific cDNA probes for the members of the internal-type keratin pair showed that the two keratin pairs are uniformly coexpressed in living suprabasal forestomach keratinocytes. Furthermore, it could be shown that distinct cells in the basal cell layer acquire the ability to express both the 67 000/59 000 dalton and the 57 000/47 000 dalton keratin pair and that some basal cells apparently lose the ability to synthesize mRNAs for basal keratins.

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References

  • Achtstätter T, Moll R, Moore B, Franke WW (1985) Cytokeratin polypeptide patterns of different epithelia of the human male urogenital tract: immunofluorescence and gel electrophoretic studies. J Histochem Cytochem 33:415–426

    Google Scholar 

  • Adams D (1976) Keratinization of the oral epithelium. Ann R Coll Surg Engl 58:351–358

    Google Scholar 

  • Alvarez OF, Meyer I (1971) Variable features and regional differences in oral epithelium. In: Squier CA, Meyer I (eds) Current concepts of the histology of oral mucosa. Charles C Thomas, Illinois, pp 97–113

    Google Scholar 

  • Bowden PE, Quinlan RA, Breitkreutz D, Fusenig NE (1984) Proteolytic modification of acidic and basic keratins during terminal differentiation of mouse and human epidermis. Eur J Biochem 142:29–36

    Google Scholar 

  • Eichner R, Sun T-T, Aebi U (1986) The role of keratin subfamilies and keratin pairs in the formation of human epidermal intermediate filaments. J Cell Biol 102:1767–1777

    Google Scholar 

  • Franke WW, Schiller DL, Moll R, Winter S, Schmid E, Denk H, Krepier R, Platzer B (1981) Diversity of cytokeratins: Differentiation specific expression of cytokeratin polypeptides in epithelial cells and tissues. J Mol Biol 153:933–959

    Google Scholar 

  • Frankfurt OS (1967) Cell proliferation and differentiation in the squamous epithelium of the forestomach epithelium of the mouse. Exp Cell Res 46:603–606

    Google Scholar 

  • Fukamachi H, Mizuno T, Takayama S (1979) Epithelial-mesenchymal interactions in differentiation of stomach epithelium in fetal mice. Anat Embryol 157:151–160

    Google Scholar 

  • Fürstenberger G, Gross M, Schweizer J, Vogt J, Marks F (1986) Isolation, characterization and in vitro cultivation of subfractions of neonatal mouse keratinocytes: Effects of phorbol esters. Carcinogenesis 7:1745–1753

    Google Scholar 

  • Goerttler K, Loehrke H, Schweizer J, Hesse B (1979) Systemic two stage carcinogenesis in the epithelium of the forestomach of mice using DMBA as initiator and TPA as promoter. Cancer Res 39:1293–1297

    Google Scholar 

  • Hawkes R, Niday E, Gordon J (1982) A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem 119:142–147

    Google Scholar 

  • Higgins RC, Dahmus ME (1979) Rapid visualization of protein bands in preparative SDS-polyacrylamide gels. Anal Biochem 93:257–260

    Google Scholar 

  • Hummel KP, Richardson FL, Fekete E (1966) Skin and Derivatives: The Digestive System. In: Green EL (ed) Biology of the Laboratory Mouse. MacGraw Hill Book Company, New York Toronto Sydney London, pp 263–307

    Google Scholar 

  • Knapp B, Rentrop M, Schweizer J, Winter H (1986) Nonepidermal members of the keratin multigene family: cDNA sequences and in situ localization of the mRNAs. Nucleic Acids Res 14:751–763

    Google Scholar 

  • Knapp B, Rentrop M, Schweizer J, Winter H (1987) Three cDNA sequences of mouse type I keratins: Cellular localization of the mRNAs in normal and hyperproliferative tissues. J Biol Chem 262:938–945

    Google Scholar 

  • Kopan R, Traska G, Fuchs E (1987) Retinoids as important regulators of terminal differentiation: Examining keratin expression in individual epidermal cells at various stages of keratinization. J Cell Biol 105:427–440

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structure proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Laskin JD, Mufson RA, Piccinini L, Engelhardt DL, Weinstein IB (1981) Effects of the tumor promoter 12–0-tetradecanoylphorbol-13-acetate on newly synthesized proteins in mouse epidermis. Cell 25:441–449

    Google Scholar 

  • Mamrack MD, Klein-Szanto AJP, Reiners JJ, Slaga TJ (1984) Alterations in the distribution of the epidermal protein filaggrin during two-stage chemical carcinogenesis in SENCAR mouse skin. Cancer Res 44:2634–2641

    Google Scholar 

  • Moll R, Franke WW, Schiller DL, Geiger B, Krepler R (1982) The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells. Cell 31:11–24

    Google Scholar 

  • Molloy CJ, Gallo MA, Laskin JD (1987) Alterations in the expression of specific epidermal keratin markers in the hairless mouse by the topical application of the tumor promoters 2,3,7,8-tetrachlorobeno-p-dioxin and the phorbolester 12–0-tetradecanoylphorbol-13-acetate. Carcinogenesis 8:1193–1199

    Google Scholar 

  • O'Farrell PZ, Goodman HM, O'Farrell PH (1977) High resolution two dimensional electrophoresis of basic as well as acidic proteins. Cell 12:1133–1142

    Google Scholar 

  • Osmanski CP, Meyer J (1967) Differences in the fine structure of the mucosa of mouse cheek and palate. J Invest Dermatol 48:309–317

    Google Scholar 

  • Parakal PF (1967) An electron microscopic study of esophageal epithelium in the newborn and adult mouse. Am J Anat 121:175–196

    Google Scholar 

  • Regauer S, Franke WW, Virtanen J (1985) Intermediate filament cytoskeleton of amnion epithelium and cultured amnion epithelial cells: Expression of epidermal cytokeratins in cells of a simple epithelium. J Cell Biol 100:997–1009

    Google Scholar 

  • Rentrop M (1987) Lokalisierung differenzierungsabhängig exprimierter Keratin mRNAs in stratifizierten Epithelien der Maus. Ph. D. Thesis, Faculty of Biology, University of Kaiserslautern

  • Rentrop M, Knapp B, Winter H, Schweizer J (1986a) Differential localization of distinct keratin mRNA species in mouse tongue epithelium by in situ hybridization with specific cDNA probes. J Cell Biol 103:2583–2591

    Google Scholar 

  • Rentrop M, Knapp B, Winter H, Schweizer J (1986b) Aminoalkylsilane-treated glass slides as support for in situ hybridization of keratin cDNAs to frozen tissue sections under varying fixation and pretreatment conditions. Histochem J 18:271–276

    Google Scholar 

  • Roop DR, Cheng CK, Toftgard R, Stanley IR, Steinert PM, Yuspa SH (1985) The use of cDNA clones and monospecific antibodies as probes to monitor keratin gene expression. Ann NY Acad Sci 455:426–435

    Google Scholar 

  • Rowden G, Budd GC (1967) Macromolecular synthesis and secretion in the mouse alimentary tract: light and electron microscope autoradiographic studies. II Incorporation and turnover of tritiated glycine in esophageal and forestomach epithelia. J Invest Dermatol 48:571–587

    Google Scholar 

  • Schweizer J, Winter H (1982a) Changes in regional keratin polypeptide patterns during phorbol ester-mediated reversible and permanently sustained hyperplasia of mouse epidermis. Cancer Res 42:1517–1529

    Google Scholar 

  • Schweizer J, Winter H (1982b) Keratin polpeptide analysis in fetal and in terminally differentiating newborn mouse epidermis. Differentiation 22:19–24

    Google Scholar 

  • Schweizer, J, Winter H (1983) Keratin biosynthesis in normal mouse epithelia and in squamous cell carcinomas. mRNA-dependent alterations of the primary structure of distinct keratin subunits in tumors. J Biol Chem 258:13268–13272

    Google Scholar 

  • Schweizer J, Kinjo M, Fürstenberger G, Winter H (1984a) Sequential expression of mRNA-encoded keratin sets in neonatal mouse epidermis: Basal cells with properties of terminally differentiating cells. Cell 37:159–170

    Google Scholar 

  • Schweizer J, Winter H, Hill MW, Mackenzie IC (1984b) The keratin polypeptide patterns in heterotypically recombined epithelia of skin and mucosa of adult mouse. Differentiation 26:144–153

    Google Scholar 

  • Silverman S (1971) Nonkeratinization and keratinization: The extremes of the human range. In: Squier CA, Meyer J (eds) Current concepts of the histology of oral mucosa. Charles C Thomas, Illinois, pp 80–96

    Google Scholar 

  • Steinert PM, Steven AC, Roop DR (1985) The molecular biology of intermediate filaments. Cell 42:411–419

    Google Scholar 

  • Sun T-T, Eichner R, Nelson WG, Tseng SCG, Weiss RA, Jarvinen M, Woodcock-Mitchell J (1983) Keratin classes: Molecular markers for different types of epithelial differentiation. J Invest Dermatol 81:109s-115s

    Google Scholar 

  • Sun T-T, Eichner R, Schermer A, Cooper D, Nelson WG, Weiss AR (1984) Classification, expression and possible mechanisms of evolution of mammalian epithelial keratins: a unifying model. In: A Levine, W Topp, G Vande Woude and JD Watson (eds) Cancer Cells. Vol I. The transformed phenotype. Cold Spring Harbor Laboratory, Cold Spring Harbor NY, pp 169–176

    Google Scholar 

  • 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

    Google Scholar 

  • Weinmann JP, Meyer J, Medak H (1960) Correlated differences in granular and keratinous layers in the oral mucosa of the mouse. J Invest Dermatol 34:423–431

    Google Scholar 

  • Weiss LW, Zelickson AS (1975) Embryology of the epidermis: ultrastructural aspects. II Period of differentiation in the mouse with mammalian comparisons. Acta Derm Venereol (Stockh) 55:321–329

    Google Scholar 

  • Winter H, Schweizer J, Goerttler K (1980) Keratins as markers of malignancy in mouse epidermal tumors. Carcinogenesis 1:391–398

    Google Scholar 

  • Woodcock-Mitchell J, Eichner R, Nelson WG, Sun T-T (1982) Immunolocalization of keratin polypeptides in human epidermis using monoclonal antibodies. J Cell Biol 95:580–588

    Google Scholar 

  • Yuspa SH, Harris CC (1974) Altered differentiation of mouse epidermal cells treated with retinyl acetate in vitro. Exp Cell Res 86:95–105

    Google Scholar 

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Author notes

  1. Mitsuru Kinjo

    Present address: Division of Clinical Pathology, Sahshin-kai Hara Hospital, 1-8 Taihaku-cho Hakata-ku, 812, Fukuoka, Japan

Authors and Affiliations

  1. Institute of Experimental Pathology, German Cancer Research Center, Heidelberg, Germany

    Jürgen Schweizer, Martin Rentrop, Roswitha Nischt, Mitsuru Kinjo & Hermelita Winter

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  1. Jürgen Schweizer
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  2. Martin Rentrop
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  3. Roswitha Nischt
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  4. Mitsuru Kinjo
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  5. Hermelita Winter
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Schweizer, J., Rentrop, M., Nischt, R. et al. The intermediate filament system of the keratinizing mouse forestomach epithelium: Coexpression of keratins of internal squamous epithelia and of epidermal keratins in differentiating cells. Cell Tissue Res. 253, 221–229 (1988). https://doi.org/10.1007/BF00221757

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