Skip to main content
Log in

Cytoskeletons of retinal pigment epithelial cells: Interspecies differences of expression patterns indicate independence of cell function from the specific complement of cytoskeletal proteins

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

Summary

In vertebrate tissue development a given cell differentiation pathway is usually associated with a pattern of expression of a specific set of cytoskeletal proteins, including different intermediate filament (IF) and junctional proteins, which is identical in diverse species. The retinal pigment epithelium (RPE) is a layer of polar cells that have very similar morphological features and practically identical functions in different vertebrate species. However, in biochemical and immunolocalization studies of the cytoskeletal proteins of these cells we have noted remarkable interspecies differences. While chicken RPE cells contain only IFs of the vimentin type and do not possess desmosomes and desmosomal proteins RPE cells of diverse amphibian (Rana ridibunda, Xenopus laevis) and mammalian (rat, guinea pig, rabbit, cow, human) species express cytokeratins 8 and 18 either as their sole IF proteins, or together with vimentin IFs as in guinea pig and a certain subpopulation of bovine RPE cells. Plakoglobin, a plaque protein common to desmosomes and the zonula adhaerens exists in RPE cells of all species, whereas desmoplakin and desmoglein have been identified only in RPE desmosomes of frogs and cows, including bovine RPE cell cultures in which cytokeratins have disappeared and vimentin IFs are the only IFs present. These challenging findings show that neither cytokeratin IFs nor desmosomes are necessary for the establishment and function of a polar epithelial cell layer and that the same basic cellular architecture can be achieved by different programs of expression of cytoskeletal proteins. The differences in the composition of the RPE cytoskeleton further indicate that, at least in this tissue, a specific program of expression of IF and desmosomal proteins is not related to the functions of the RPE cell, which are very similar in the various species.

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

  • Achtstätter T, Hatzfeld M, Quinlan RA, Parmelee D, Franke WW (1986) Separation of cytokeratin polypeptides by gel electrophoretic and Chromatographic techniques and their identification by immunoblotting. Methods Enzymol 134:355–371

    Google Scholar 

  • Albert DM, Buyukmihci N (1979) Tissue culture of the retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 277–292

    Google Scholar 

  • Barritault D, Courtois Y, Paulin D (1980) Biochemical evidence that vimentin is the only in vivo constituent of the intermediate filaments in adult bovine epithelial lens cells. Biol Cell 39:335–338

    Google Scholar 

  • Blose SH, Meltzer DI (1981) Visualization of the 10 nm-filament vimentin rings in vascular endothelial cells in situ. Exp Cell Res 135:299–304

    Google Scholar 

  • Bok D, Young RW (1979) Phagocytic properties of the retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 148–174

    Google Scholar 

  • Bommeli W (1972) Die Ultrastruktur der Milchdrüsenalveole des Rindes, insbesondere Basalfalten des Epithels und der Mitochondrien-Desmosomen-Komplex. Zbl Vet Med C 1:299–325

    Google Scholar 

  • Burnside B, Adler R, O'Connor P (1983) Retinomotor pigment migration in the teleost retinal pigment epithelium. Invest Ophthalmol Vis Sci 24:1–25

    Google Scholar 

  • Chisholm JC, Houliston E (1987) Cytokeratin filament assembly in the preimplantation mouse embryo. Development 101:565–582

    Google Scholar 

  • Cohen SM, Gorbsky G, Steinberg MS (1983) Immunochemical characterization of related families of glycoproteins in desmosomes. J Biol Chem 258:2621–2627

    Google Scholar 

  • Connell ND, Rheinwald JG (1983) Regulation of the cytoskeleton in mesothelial cells: Reversible loss of keratin and increase in vimentin during rapid growth in culture. Cell 34:245–253

    Google Scholar 

  • Coulombre AJ (1979) Roles of the retinal pigment epithelium in the development of ocular tissues. In: Zinn KM, Marmor MF (eds) The Pigment Epithelium. Harvard University Press, Cambridge, pp 53–57

    Google Scholar 

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

    Google Scholar 

  • Cowin P, Franke WW, Grund C, Kapprell H-P, Kartenbeck J (1985b) The desmosome-intermediate filament complex. In: Edelman G, Thiery JP (eds) The Cell in Contact. John Wiley and Sons, Inc., New York, pp 427–460

    Google Scholar 

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

    Google Scholar 

  • Crawford B (1980) Development of the junctional complex during differentiation of chick pigmented epithelial cells in clonal culture. Invest Ophthalmol Visual Sci 19:223–237

    Google Scholar 

  • Crawford B, Cloney RA, Cahn RD (1972) Cloned pigmented cells; the affects of cytochalasin B on ultrastructure and behavior. Z Zellforsch 130:135–151

    Google Scholar 

  • Dembitzer HM, Herz F, Schermer A, Wolley RC, Koss LG (1980) Desmosome development in an in vitro model. J Cell Biol 85:695–702

    Google Scholar 

  • Docherty RJ, Edwards JG, Garrod DR, Mattey DL (1984) Chick embryonic pigmented retina is one of the group of epithelioid tissues that lack cytokeratins and desmosomes and have intermediate filaments composed of vimentin. J Cell Sci 71:61–74

    Google Scholar 

  • Drenkhahn D, Wagner H-J (1985) Relation of retinomotor responses and contractile proteins in vertebrate retinas. Eur J Cell Biol 37:156–168

    Google Scholar 

  • Ducibella TD, Albertini F, Anderson E, Biggers JD (1975) The preimplantation mouse embryo: Characterization of intercellular junctions and their appearance during development. Dev Biol 45:231–250

    Google Scholar 

  • Franke WW, Lüder MR, Kartenbeck J, Zerban H, Keenan TW (1976) Involvement of vesicle coat material in casein secretion and surface regeneration. J Cell Biol 69:173–195

    Google Scholar 

  • Franke WW, Weber K, Osborn M, Schmid E, Freudenstein C (1978) Antibody to prekeratin. Decoration of tonofilament-like array in various cells of epithelial character. Exp Cell Res 116:429–445

    Google Scholar 

  • Franke WW, Appelhans B, Schmid E, Freudenstein C, Osborn M, Weber K (1979a) Identification and characterization of epithelial cells in mammalian tissues by immunofluorescence microscopy using antibodies to prekeratin. Differentiation 15:7–25

    Google Scholar 

  • Franke WW, Grund C, Schmid E (1979b) Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 19:269–275

    Google Scholar 

  • Franke WW, Schmid E, Osborn M, Weber K (1979c) Intermediate-sized filaments of human endothelial cells. J Cell Biol 81:570–580

    Google Scholar 

  • Franke WW, Schmid E, Winter S, Osborn M, Weber K (1979d) Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Exp Cell Res 123:25–46

    Google Scholar 

  • Franke WW, Denk H, Kalt R, Schmid E (1981a) Biochemical and immunological identification of cytokeratin proteins present in hepatocytes of mammalian liver tissue. Exp Cell Res 131:299–318

    Google Scholar 

  • Franke WW, Schmid E, Grund C, Müller H, Engelbrecht I, Moll R, Stadler J, Jarasch E-D (1981 b) Antibodies to high molecular weight polypeptides of desmosomes: specific localization of a class of junctional proteins in cells and tissues. Differentiation 20:217–241

    Google Scholar 

  • Franke WW, Moll R, Schiller DL, Schmid E, Kartenbeck J, Mueller H (1982a) Desmoplakins of epithelial and myocardial desmosomes are immunologically and biochemically related. Differentiation 23:115–127

    Google Scholar 

  • Franke WW, Schmid E, Grund C, Geiger B (1982b) Intermediate filament proteins and nonfilamentous structures: transient disintegration and inclusion of subunit proteins in granular aggregates. Cell 30:103–113

    Google Scholar 

  • Franke WW, Winter S, Overbeck J von, Gudat F, Heitz PU, Stähli C (1987) Identification of the conserved conformation-dependent cytokeratin epitope recognized by monoclonal antibody (lu-5). Virchows Arch A 411:137–147

    Google Scholar 

  • Fujimoto T, Singer SJ (1986) Immunocytochemical studies of endothelial cells in vivo. I. The presence of desmin only, or of desmin plus vimentin, or vimentin only, in the endothelial cells of different capillaries of the adult chicken. J Cell Biol 103:2775–2786

    Google Scholar 

  • Gigi O, Geiger B, Eshhar Z, Moll R, Schmid E, Winter S, Schiller DL, Franke WW (1982) Detection of a cytokeratin determinant common to diverse epithelial cells by a broadly cross-reacting monoclonal antibody. EMBO J 1:1429–1437

    Google Scholar 

  • Giudice GJ, Cohen SM, Patel NH, Steinberg MS (1984) Immunological comparison of desmosomal components from several bovine tissue. 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 

  • Gordon SR, Essner E (1987) Investigation on circumferential microfilament bundles in rat retinal pigment epithelium. Eur J Cell Biol 44:97–104

    Google Scholar 

  • Granger BL, Lazarides E (1984) Expression of the intermediate-filament-associated protein synemin in chicken lens cells. Mol Cell Biol 4:1943–1950

    Google Scholar 

  • Guillouzo A, Guillouzo C, Boismard M (1978) Association of mitochondria with desmosomes in rat hepatocytes cultured in the presence of phenobarbital or in the presence of glucose at a high concentration. Biol Cell 31:315–318

    Google Scholar 

  • Hiscott PS, Grierson I, McLeod D (1984) Retinal pigment epithelial cells in epiretinal membranes: an immunohistochemical study. Br J Ophthalmol 68:708–715

    Google Scholar 

  • Hudspeth AJ, Yee AG (1973) The intercellular junctional complexes of retinal pigment epithelia. Invest Ophthalmol 12:354–365

    Google Scholar 

  • Jackson BW, Grund C, Schmid E, Bürki K, Franke WW, Illmensee K (1980) Formation of cytoskeletal elements during mouse embryogenesis. I. Intermediate filaments of the cytokeratin type and desmosomes in preimplantation embryos. Differentiation 17:161–179

    Google Scholar 

  • Jahn L, Fouquet B, Rohe K, Franke WW (1987) Cytokeratins in certain endothelial and smooth muscle cells of two taxonomically distant vertebrate species, Xenopus laevis and man. Differentiation 36:234–254

    Google Scholar 

  • Kartenbeck J, Schmid E, Franke WW, Geiger B (1982) Different modes of internalization of proteins associated with adherens junctions and desmosomes: experimental separation of lateral contacts induces endocytosis of desmosomal plaque material. EMBO J 1:725–732

    Google Scholar 

  • Kartenbeck J, Franke WW, Moser JG, Stoffels U (1983) Specific attachment of desmin filaments to desmosomal plaques in cardiac myocytes. EMBO J 2:735–742

    Google Scholar 

  • Kartenbeck J, Schwechheimer K, Moll R, Franke WW (1984) Attachment of vimentin filaments to desmosomal plaques in human meningiomal cells and arachnoidal tissue. J Cell Biol 98:1072–1081

    Google Scholar 

  • Kemler R, Brûlet P, Schnebelen M-T, Gaillard J, Jacob F (1981) Reactivity of monoclonal antibodies against intermediate filament proteins during embryonic development. J Embryol Exp Morphol 64:45–60

    Google Scholar 

  • Khyse-Anderson J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10:203–209

    Google Scholar 

  • Kim KH, Stellmach V, Javors J, Fuchs E (1987) Regulation of human mesothelial cell differentiation: opposing roles of retinoids and epidermal growth factor in the expression of intermediate filament proteins. J Cell Biol 105:3039–3051

    Google Scholar 

  • Kuwabara T (1979) Species differences in the rental pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 58–82

    Google Scholar 

  • Kuwabara T, Cogan DG (1983) The retina. In: Weiss L, Greep RO (eds) Histology. Fifth Edition. McGraw-Hill Book Company, New York, pp 1164–1172

    Google Scholar 

  • Lee CS, Morgan G, Wooding FBP (1979) Mitochondria and mitochondria tonofilament-desmosomal associations in the mammary gland secretory epithelium of lactating cows. J Cell Sci 38:125–135

    Google Scholar 

  • Lentz TL, Trinkaus JP (1971) Differentiation of the junctional complex of surface cells in the developing Fundulus blastoderm. J Cell Biol 48:455–472

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Moll R, Cowin P, Kapprell H-P, Franke WW (1986) Desmosomal proteins: New markers for identification and classification of tumors. Lab Invest 54:4–25

    Google Scholar 

  • Moll R, Achtstätter T, Becht E, Calcarova-Ständer J, Ittensohn M, Franke WW (1988) Cytokeratins in normal and malignant epithelium. Maintenance of expression of urothelial differentiation features in transitional cell carcinomas and bladder carcinoma cell culture lines. Am J Pathol 132:111–132

    Google Scholar 

  • Müller H, Franke WW (1983) Biochemical and immunological characterization of desmoplakins I and II, the major polypeptides of the desmosomal plaque. J Mol Biol 163:647–671

    Google Scholar 

  • Mund ML, Rodrigues MM (1979) Embryology of the human retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 45–52

    Google Scholar 

  • Opas M, Kalnins VI (1985) Spatial distribution of cortical proteins in cells of epithelial sheets. Cell Tissue Res 239:451–454

    Google Scholar 

  • Opas M, Turkson K, Kalnins VI (1985) Adhesiveness and distribution of vinculin and spectrin in retinal pigmented epithelial cells during growth and differentiation in vitro. Dev Biol 107:269–280

    Google Scholar 

  • Osborn M, Debus E, Weber K (1984) Monoclonal antibodies specific for vimentin. Eur J Cell Biol 34:137–143

    Google Scholar 

  • Oshima RG, Howe WE, Klier FG, Adamson ED, Shevinsky LH (1983) Intermediate filament protein synthesis in preimplantation murine embryos. Dev Biol 99:447–455

    Google Scholar 

  • Owaribe K, Eguchi G (1985) Increase in actin contents and elongation of apical projections in retinal pigmented epithelial cells during development of the chicken eye. J Cell Biol 101:590–596

    Google Scholar 

  • Owaribe K, Masuda H (1982) Isolation and characterization of circumferential microfilament bundles from retinal pigmented epithelial cells. J Cell Biol 95:310–315

    Google Scholar 

  • Owaribe K, Sugino H, Masuda H (1986) Characterization of intermediate filaments and their structural organization during epithelium formation in pigmented epithelial cells of the retina in vitro. Cell Tissue Res 244:87–93

    Google Scholar 

  • Paranko J, Kallajoki M, Pelliniemi LJ, Lehto V-P, Virtanen I (1986) Transient coexpression of cytokeratin and vimentin in differentiating rat Sertoli cells. Dev Biol 117:35–44

    Google Scholar 

  • Philp NJ, Nachmias VT (1985) Components of the cytoskeleton in the retinal pigmented epithelium of the chick. J Cell Biol 101:358–362

    Google Scholar 

  • Pruss RM, Mirsky R, Raff MC, Thorpe R, Dowding AJ, Anderton BH (1981) All classes of intermediate filaments share a common antigenic determinant defined by a monoclonal antibody. Cell 27:419–428

    Google Scholar 

  • Ramaekers FCS, Osborn M, Schmid E, Weber K, Bloemendal H, Franke WW (1980) Identification of the cytoskeletal proteins in lens-forming cells, a special epithelioid cell type. Exp Cell Res 127:309–327

    Google Scholar 

  • Regauer S, Franke WW, Virtanen I (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 

  • Rungger-Brändle E, Achtstätter T, Franke WW (1988) Glial elements in amphibian optic nerve formed by cells containing cytokeratin filaments and desmosomes (submitted)

  • Schliwa M (1982) Action of cytochalasin D on cytoskeletal networks. J Cell Biol 92:79–91

    Google Scholar 

  • Schmelz M, Duden R, Cowin P, Franke WW (1986) A constitutive transmembrane glycoprotein of Mr 165000 (desmoglein) in epidermal and non-epidermal desmosomes. II. Immunolocalization and microinjection. Eur J Cell Biol 42:184–199

    Google Scholar 

  • Schmid E, Tapscott S, Bennett GS, Groop J, Fellini SA, Holtzer H, Franke WW (1979) Differential location of different types of intermediate-sized filaments in various tissues of the chick embryo. Differentiation 15:27–40

    Google Scholar 

  • Schmid E, Schiller DL, Grund C, Stadler J, Franke WW (1983) Tissue type specific expression of intermediate filament proteins in a cultured epithelial cell line from bovine mammary gland. J Cell Biol 96:37–50

    Google Scholar 

  • Shaw G, Weber K (1984) The intermediate filament complement of retina: a comparison between different mammalian species. Eur J Cell Biol 33:95–104

    Google Scholar 

  • Steinberg RH, Wood I (1979) The relationship of the retinal pigment epithelium to photoreceptor outer segments in human retina. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 32–44

    Google Scholar 

  • Sternlieb I (1969) Mitochondrion — desmosome complexes in human heptocytes. Z Zellforsch 93:249–253

    Google Scholar 

  • Sun T-T, Shih C, Green H (1979) Keratin cytoskeletons in epithelial cells of internal organs. Proc Natl Acad Sci USA 76:2813–2817

    Google Scholar 

  • Turksen K, Kalnins VI (1987) The cytoskeleton of chick retinal pigment epithelial cells in situ. Cell Tissue Res 248:95–101

    Google Scholar 

  • Van Vorstenbosch CJAHV, Colenbrander B, Wensing CJG, Ramaekers FCS, Vooijs GP (1984) Cytoplasmic filaments in fetal and neonatal pig testis. Eur J Cell Biol 34:292–299

    Google Scholar 

  • Venetianer A, Schiller DL, Magin T, Franke WW (1983) Cessation of cytokeratin expression in a rat hepatoma cell line lacking differentiated functions. Nature 305:730–733

    Google Scholar 

  • Virtanen I, Lehto V-P, Lehtonen E, Vartio T, Stenman S, Kurki P, Wager O, Small JV, Dahl D, Badley RA (1981) Expression of intermediate filaments in cultured cells. J Cell Sci 50:45–63

    Google Scholar 

  • Volberg T, Geiger B, Kartenbeck J, Franke WW (1986) Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ -ions. J Cell Biol 102:1832–1842

    Google Scholar 

  • Young RW, Bok D (1979) Metabolism of the retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 103–123

    Google Scholar 

  • Zinn KM, Benjamin-Henkind JV (1979) Anatomy of the human retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The Retinal Pigment Epithelium. Harvard University Press, Cambridge, pp 3–52

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Owaribe, K., Kartenbeck, J., Rungger-Brändle, E. et al. Cytoskeletons of retinal pigment epithelial cells: Interspecies differences of expression patterns indicate independence of cell function from the specific complement of cytoskeletal proteins. Cell Tissue Res. 254, 301–315 (1988). https://doi.org/10.1007/BF00225803

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00225803

Key words

Navigation