Plakophilins 1a and 1b: Widespread nuclear proteins recruited in specific epithelial cells as desmosomal plaque components

Cell and Tissue Research

Volumn 290, Issue 3, 1997, Pages 481-499

  Schmidt, Ansgar ^a   Langbein, Lutz ^a   Rode, Michaela ^a   Prätzel, Silke ^a   Zimbelmann, Ralf ^a   Franke, Werner W ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Armadillo gene; Desmosomes; Nuclear proteins; Plakophilin

Indexed keywords

MESSENGER RNA; NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATTLE; CELL NUCLEUS; DESMOSOME; EPITHELIUM CELL; EXON; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA SPLICING; XENOPUS LAEVIS;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; BASE SEQUENCE; CATTLE; CELL LINE; CLONING, MOLECULAR; DESMOSOMES; DNA PRIMERS; DNA, COMPLEMENTARY; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PLAKOPHILINS; POLYMERASE CHAIN REACTION; PROTEINS; TRANSFECTION; XENOPUS LAEVIS;

ANIMALIA; ARMADILLO; BOS TAURUS; BOVINAE; XENOPUS LAEVIS;

EID: 0030856140     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050956     Document Type: Article

References (108)

1. Achtstätter T, Hatzfeld M, Quinlan RA, Parmelee DC, Franke WW (1986) Separation of cytokeratin polypeptides by gel electrophoretic and chromatographic techniques and their identification by immunoblotting. Methods Enzymol 134:355-371
2. Aghib DF, McCrea PE (1995) The E-cadherin complex contains the src substrate p120. Exp Cell Res 218:359-369
3. Ankenbauer T, Kleinschmidt JA, Walsh MJ, Weiner OH, Franke WW (1989) Identification of a widespread nuclear actin-binding protein. Nature 342:822-825
4. Behrens J, Kries JP von, Kühl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W (1996) Functional interaction of β-catenin with the transcription factor LEF-I. Nature 382:638-642
5. Bonner WM (1978) Protein migration and accumulation in nuclei. In: Busch H (ed) The cell nucleus, Vol VI, Chromatin, Part C. Academic Press, New York, pp 97-148
6. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-771
7. Bouteille M, Lavai M, Dupuy-Coin AM (1974) Localization of nuclear functions as revealed by ultrastructural autoradiography and cytochemistry. In: Busch H (ed) The cell nucleus. Vol I. Academic Press, New York London, pp 3-71
8. Butz S, Larue L (1995) Expression of catenins during mouse embryonic development and in adult tissues. Cell Adhes Commun 3:337-352
9. Capetanaki YG, Ngai J, Flytzanis CN, Lazarides E (1983) Tissue-specific expression of two mRNA species transcribed from single vimentin gene. Cell 35:411-420
10. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752
11. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acids from sources enriched in ribonuclease. Biochemistry 18:5294-5299
12. Chitaev NA, Leube RE, Troyanovsky RB, Eshkind LG, Franke WW, Troyanovsky SM (1996) The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J Cell Biol 133:359-369
13. Cordes VC, Reidenbach S, Franke WW (1995) High content of a nuclear pore complex protein in cytoplasmic annulate lamellae of Xenopus oocytes. Eur J Cell Biol 68:240-255
14. Cowin P (1994) Unraveling the cytoplasmic interactions of the cadherin superfamily. Proc Natl Acad Sci USA 91:10759-10761
15. Cowin P, Franke WW, Grund C, Kapprell H-P, Kartenbeck J (1985a) The desmosome-intermediate filament complex. In: Edelman GM, Thiery J-P (eds) The cell in contact. John Wiley & Sons, New York, pp 427-460
16. Cowin P, Kapprell H-P, Franke WW (1985b) The complement of desmosomal plaque proteins in different cell types. J Cell Biol 101:1442-1454
17. 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
18. Cox JV, Moon RT, Lazarides E (1985) Anion transporter: highly cell-type-specific expression of distinct polypeptides and transcripts in erythroid and nonerythroid cells. J Cell Biol 100:1548-1557
19. Daniel JM, Reynolds AB (1995) The tyrosine kinase substrate p120cas binds directly to E-cadherin but not to the adenomatous polyposis coli protein or α-catenin. Mol Cell Biol 15:4819-4824
20. Demlehner MP, Schäfer S, Grund C, Franke WW (1995) Continual assembly of half-desmosomal structures in the absence of cell contacts and their frustrated endocytosis: a coordinated Sisyphus cycle. J Cell Biol 131:745-760
21. Dingwall C, Laskey RA (1991) Nuclear targeting sequences - a consensus? Trends Biochem Sci 16:478-481
22. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6-13
23. Fouquet B, Zimbelmann R, Franke WW (1992) Identification of plakoglobin in oocytes and early embryos of Xenopus laevis: maternal expression of a gene encoding a junctionul plaque protein. Differentiation 51:187-194
24. Fourney RM, Miyakoshi J, Day III RS, Paterson MC (1988) Northern blotting: efficient RNA staining and transfer. Focus 10:5-7
25. Franke WW, Schinko W (1969) Nuclear shape in muscle cells. J Cell Biol 42:326-331
26. Franke WW, Schmid E, Grund C, Müller H, Engelbrecht I, Moll R, Stadler J, Jarasch E-D (1981) Antibodies to high molecular weight polypeptides of desmosomes: specific localization of a class of junctional proteins in cells and tissues. Differentiation 20:217-241
27. Franke WW, Mueller H, Mittnacht S, Kapprell H-P, Jorcano JL (1983) Significance of two demosome plaque-associated polypeptides of molecular weights 75,000 and 83,000. EMBO J 2:2211-2215
28. Franke WW, Kapprell H-P, Cowin P (1987a) Immunolocalization of plakoglobin in endothelial junctions: identification as a special type of zonulae adhaerentes. Biol Cell 59:205-21
29. Franke WW, Kapprell H-P, Cowin P (1987b) Plakoglobin is a component of the filamentous subplasmalemmal coat of lens cells. Eur J Cell Biol 43:301-315
30. Franke WW, Goldschmidt MD, Zimbelmann R, Mueller HM, Schiller DL, Cowin P (1989) Molecular cloning and amino acid sequence of human plakoglobin, the common junctional plaque protein. Proc Natl Acad Sci USA 86:4027-4031
31. Funayama N, Fagotto F, McCrea P, Gumbiner BM (1995) Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling. J Cell Biol 128:959-968
32. Gabe M (1976) Histological techniques. Springer, New York, pp 180-181
33. Gallagher PG, Forget BG (1995) Structure, organization, and expression of the human band 72b gene, a candidate gene for hereditary hydrocytosis. J Biol Chem 270:26358-26363
34. Garrod DR (1993) Desmosomes and hemidesmosomes. Curr Opin Cell Biol 5:30-40
35. Görlich D, Kraft R, Kostka S, Vogel F, Hartmann E, Laskey RA, Mattaj IW, Izaurralde E (1996) Importin provides a link between nuclear protein import and U snRNA export. Cell 87:21-32
36. Gottardi CJ, Arpin M, Fanning AS, Louvard D (1996) The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc Natl Acad Sci USA 93:10779-10784
37. Green KJ, Jones JCR (1996) Desmosomes and hemidesmosomes: structure and function of molecular components. FASEB J 10:871-881
38. Gross-Bellard M, Oudet P, Chambon P (1972) Isolation of high-molecular-weight DNA from mammalian cells. Eur J Biochem 39:32-38
39. Gumbiner BM (1993) Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron 11:551-564
40. Hammerl P, Hartl A, Thalhammer J (1993) Particulate nitrocellulose as a solid phase for protein immobilization in immuno-affinity chromatography. J Immunol Methods 165:39-66
41. Hashimoto T, Amagai M, Parry DAD, Dixon TW, Tsukita S, Tsukita S, Miki K, Sakai K, Inokuchi Y, Kudoh J, Shimizu N, Nishikawa T (1993) Desmoyokin, a 680 kDa keratinocyte plasma membrane-associated protein, is homologous to the protein encoded by human gene AHNAK. J Cell Sci 105:275-286
42. Hatzfeld M, Nachtsheim C (1996) Cloning and characterization of a new armadillo family member, p0071, associated with the junctional plaque: evidence for a subfamily of closely related proteins. J Cell Sci 109:2767-2778
43. Hatzfeld M, Kristjansson GI, Plessmann U, Weber K (1994) Band 6 protein, a major constituent of desmosomes from stratified epithelia, is a novel member of the armadillo multigene family. J Cell Sci 107:2259-2270
44. Heid HW, Schmidt A, Zimbelmann R, Schäfer S, Winter-Simanowski S, Stumpp S, Keith M, Figge U, Schnölzer M, Franke WW (1994) Cell type-specific desmosomal plaque proteins of the plakoglobin family: plakophilin 1 (band 6 protein). Differentiation 58:113-131
45. Herrmann H, Hofmann I, Franke WW (1992) Identification of a nonapeptide motif in the vimentin head domain involved in intermediate filament assembly. J Mol Biol 223:637-650
46. Hinek L, Nelson WJ, Papkoff J (1994) Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing β-catenin binding to the cell adhesion protein cadherin. J Cell Biol 124:729-741
47. Horowitz SB, Miller DS (1984) Solvent properties of ground substance studied by cryomicrodissection and intracellular reference-phase techniques. J Cell Biol 99:172s-179s
48. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrman BG, Kemler R (1996) Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech Dev 59:3-10
49. Hülsken J, Behrens J, Birchmeier W (1994a) Tumor-suppressor gene products in cell contacts: the cadherin-APC-armadillo connection Curr Opin Cell Biol 6:711-716
50. Hülsken J, Birchmeier W, Behrens J (1994b) E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J Cell Biol 127:2061-2071
51. Joos TO, Whittaker CA, Meng F, DeSimone DW, Gnau V, Hausen P (1996) Integrin alpha 5 during early development of Xenopus laevis. Mech Dev 50:197-199
52. Kapprell H-P, Cowin P, Franke WW (1987) Biochemical characterization of the soluble form of the junctional plaque protein, plakoglobin, from different cell types. Eur J Biochem 166:505-517
53. r 75,000 as an accessory desmosomal plaque protein in stratified and complex epithelia. J Cell Biol 106:1679-1691
54. Kapprell H-P, Duden R, Owaribe K, Schmelz M, W W Kranke (1990) Subplasmalemmal plaques of intercellular junctions: common and distinguishing proteins. In: Edelman GM, Cunningham BA, Thiery JP (eds) Morphoregulatory molecules. John Wiley and Sons, New York, pp 285-314
55. Karnovsky A, Klymkowsky MW (1995) Anterior axis duplication in Xenopus induced by the over-expression of the cadherin-binding protein plakoglobin. Proc Natl Acad Sci USA 92: 4522-4526
56. Kemler R (1993) From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 9:317-321
57. Keon BH, Schäfer S, Kuhn C, Grund C, Franke WW (1996) Symplekin, a novel type of tight junction plaque protein. J Cell Biol 134:1003-1018
58. Koch PJ, Franke WW (1994) Desmosomal cadherins: another growing multigene family of adhesion molecules. Curr Opin Cell Biol 6:682-687
59. Köser J (1995) Charakterisierung von cytosolischem Plakophilin in epithelialen Gewebekulturzellen (Thesis), Faculty of Biology, University of Heidelberg, pp 1-70
60. Krohne G (1985) Immunological identification of the karyophilic, histone-binding proteins N1 and N2 in somatic cells and oocytes of diverse amphibia. Exp Cell Res 158:205-222
61. Krohne G, Franke WW (1980a) A major soluble acidic protein located in nuclei of diverse vertebrate species. Exp Cell Res 129:167-189
62. Krohne G, Franke WW (1980b) Immunological identification and localization of the predominant nuclear protein of the amphibian ooeyte nucleus. Proc Natl Acad Sci USA 77:1034-1038
63. Labidi B, Frackowiak S, Hernandez-Verdun D (1987) Identification and sorting of micronuclei containing individual chromosomes. Exp Cell Res 173:617-627
64. Madri JA, Pratt BM, Yannariello-Brown J (1988) Endothelial cell-extracellular matrix interactions. Matrix as a modulator of cell function. In: Simionescu N, Simionescu M (eds) Endothelial cell biology in health and disease. Plenum, New York, pp 167-188
65. Magee AI, Buxton RS (1991) Transmembrane molecular assemblies regulated by the greater cadherin family. Curr Opin Cell Biol 3:854-861
66. Makkerh JPS, Dingwall C, Laskey RA (1996) Comparative mutagenesis of nuclear localization signals reveals the importance of neutral and acidic amino acids. Curr Biol 6:1025-1027
67. Melan MA, Sluder G (1992) Redistribution and differential extraction of soluble proteins in permeabilized cultured cells. Implications for immunofluorescence microscopy. J Cell Sci 101:731-743
68. Mertens C, Kuhn C, Franke WW (1996) Plakophilins 2a and 2b: constitutive proteins of dual location in the karyoplasm and the desmosomal plaque. J Cell Biol 135:1009-1025
69. Miller JR, Moon RT (1996) Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev 10:2527-2539
70. Molenaar M, Wetering M van de, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destrée O, Clevers H (1996) XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86:391-399
71. Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459-472
72. Mueller 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
73. Nuber UA, Schäfer S, Stehr S, Rackwitz H-R, Franke WW (1996) Patterns of desmocollin synthesis in human epithelia: immunolocalization of desmocollins 1 and 3 in special epithelia and in cultured cells. Eur J Cell Biol 71:1-13
74. Orsulic S, Peifer M (1996) An in vivo structure-function study of armadillo, the β-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signalling. J Cell Biol 134:1283-1300
75. Ouyang P, Sugrue SP (1992) Identification of an epithelial protein related to the desmosome and intermediate filament network. J Cell Biol 118:1477-1488
76. Ozawa M, Hirokazu T, Pedraza C (1995) The fourth armadillo repeat of plakoglobin (γ-calenin) is required for its high affinity binding to the cytoplasmic domains of E-cadherin and desmosomal cadherin Dsg2, and tumor suppressor APC protein. J Biochem 118:1077-1082
77. Paine PL (1984) Diffusive and nondiffusive proteins in vivo. J Cell Biol 99:188s-195s
78. Paine PL, Austerberry CF, Desjarlais LJ, Horowitz SB (1983) Protein loss during nuclear isolation. J Cell Biol 97:1240-1242
79. Pasdar M, Li Z, Chlumecky V (1995) Plakoglobin: kinetics of synthesis, phosphorylation, stability, and interactions with desmoglein and E-cadherin. Cell Motil Cytoskeleton 32:258-272
80. Peifer M (1993) The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction. J Cell Sci 105:993-1000
81. Peifer M (1995) Cell adhesion and signal transduction: the armadillo connection. Trends Cell Biol 5:224-229
82. Peifer M, Wieschaus E (1990) The segment polarity gene armadillo encodes an evolutionarily conserved and functional modular protein that is the Drosophila homolog of human plakoglobin. Cell 63:1167-1178
83. Peifer M, McCrea P, Green KJ, Wieschaus E, Gumbiner B (1992) The vertrebrale adhesive junction proteins β-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J Cell Biol 118:681-691
84. Peifer M, Orsulic S, Sweeton D, Wieschaus E (1993) A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118:1191-1207
85. Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789-791
86. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G (1996) A novel receptor-mediated nuclear protein import pathway. Cell 86:985-994
87. cas associates with E-cadherin complexes. Mol Cell Biol 14:8333-8342
88. Rose O, Grund C, Reinhardt S, Starzinski-Powitz A, Franke WW (1995) Contactus adherens, a special type of plaque-bearing adhering junction containing M-cadherin, in the granule cell layer of the cerebellar glomerulus. Proc Natl Acad Sci USA 92:6022-6026
89. Sacco PA, McGranahan TM, Wheelock MJ, Johnson KR (1995) Identification of plakoglobin domains required for association with N-cadherin and α-catenin. J Biol Chem 270:20201-20206
90. Schäfer S, Troyanovsky SM, Heid HW, Eshkind LG, Koch PJ, Franke WW (1993) Cytoskeletal architecture and epithelial differentiation: Molecular determinants of cell interaction and cytoskeletal filament anchorage. C R Acad Sci Paris, Ser III 316:1316-1323
91. Schäfer S, Koch PJ, Franke WW (1994) Identification of the ubiquitous human desmoglein, Dsg2, and the expression catalogue of the desmoglein subfamily of desmosomal cadherins. Exp Cell Res 211:391-399
92. Schäfer S, Stumpp S, Franke WW (1996) Immunological identification and characterization of the desmosomal cadherin Dsg2 in coupled and uncoupled epithelial cells and in human tissues. Differentiation 60:99-108
93. r 165,000 (desmoglein) in epidermal and non-epidermal desmosomes. I. Biochemical identification of the polypeptide. Eur J Cell Biol 42:177-183
94. r 165,000 (desmoglein) in epidermal and non-epidermal desmosomes. II. Immunolocalization and microinjection studies. Eur J Cell Biol 42:184-199
95. Schmidt A, Heid HW, Schäfer S, Nuber UA, Zimbelmann R, Franke WW (1994) Desmosomes and cytoskeletal architecture in epithelial differentiation: cell type-specific plaque components and intermediate filament anchorage. Eur J Cell Biol 65:229-245
96. Schneider S, Steinbeisser H, Warga RM, Hausen P (1996) β-Catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev 57:191-198
97. Schwarz MA, Owaribe K, Kartenbeck J, Franke WW (1990) Desmosomes and hemidesmosomes: constitutive molecular components. Annu Rev Cell Biol 6:461-491
98. Shibamoto S, Hayakawa M, Takeuchi K, Hori T, Miyazawa K, Kitamura N, Johnson KR, Wheelock MJ, Matsuyoshi N, Takeichi M, Ito F (1995) Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes. J Cell Biol 128:949-957
99. Smalheiser NR (1996) Proteins in unexpected locations. Mol Biol Cell 7:1003-1014
100. Staddon JM, Smales C, Schulze C, Esch FS, Rubin LL (1995) p120, a p120-related protein (p100), and the cadherin/catenin complex. J Cell Biol 130:369-381
101. Takeichi M (1995) Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7:619-627
102. Troyanovsky SM, Eshkind LG, Troyanovsky RB, Leube RE, Franke WW (1993) Contributions of cytoplasmic domains of desmosomal cadherins to desmosome assembly and intermediate filament anchorage. Cell 72:561-574
103. Troyanovsky SM, Troyanovsky RB, Eshkind LG, Krutovskikh VA, Leube RE, Franke WW (1994a) Identification of the plakoglobin-binding domain in desmoglein and its role in plaque assembly and intermediate filament anchorage. J Cell Biol 127:151-160
104. Troyanovsky SM, Troyanovsky RB, Eshkind LG, Leube RE, Franke WW (1994b) Identification of amino acid sequence motifs in desmocollin, a desmosomal glycoprotein, that are required for plakoglobin binding and plaque formation. Proc Natl Acad Sei USA 91:10790-10794
105. Wahl JK, Sacco PA, McGranahan-Sadler TM, Sauppe LM, Wheelock MJ, Johnson KR (1996) Plakoglobin domains that define its association with the desmosomal cadherins and the classical cadherins: identification of unique and shared domains. J Cell Sei 109:1143-1154
106. Wessel EF, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141-143
107. Witcher LL, Collins R, Puttagunta S, Mechanic SE, Munson M, Gumbiner B, Cowin P (1996) Desmosomal cadherin binding domains of plakoglobin. J Biol Chem 271:10904-10909
108. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT (1996) The axis-inducing activity, stability, and subcellular distribution of β-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10:1443-1454