A minimal region on the integrin β4 subunit that is critical to its localization in hemidesmosomes regulates the distribution of HD1/plectin in COS-7 cells

Journal of Cell Science

Volumn 110, Issue 15, 1997, Pages 1705-1716

  Niessen, Carien M ^a   Hulsman, Esther H M ^a   Oomen, Lauran C J M ^a   Kuikman, I ^a   Sonnenberg, Arnoud ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

HD1 plectin; Hemidesmosome; Integrin 6 4; Laminin 5

Indexed keywords

COMPLEMENTARY DNA; FIBRONECTIN; INTEGRIN; KALININ; PROTEIN SUBUNIT; TYROSINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BLADDER CARCINOMA; CELL LINE; CONTROLLED STUDY; GENETIC TRANSFECTION; HEMIDESMOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; ANTIGENS, SURFACE; COS CELLS; DESMOSOMES; HUMANS; INTEGRIN ALPHA6BETA4; INTEGRIN BETA4; INTEGRINS; INTERMEDIATE FILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PLECTIN; RATS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; TRANSFECTION; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0030820604     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Aberdam, D., Galliano, M. F., Vailly, J., Pulkkinen, L., Bonifas, J., Christiano, A. M., Tryggvason, K., Uitto, J., Epstein Jr., E. H., Ortonne, J.-P. and Meneguzzi, G. (1994). Herlitz's junctional epidermolysis bullosa is linked to mutations in the gene (LAMC2) for the γ2 subunit of nicein/kalinin (laminin-5). Nature Genet. 6, 299-304.
2. Borradori, L. and Sonnenberg, A. (1996). Hemidesmosomes: roles in adhesion, signaling and human diseases. Curr. Opin. Cell Biol. 8, 647-656
3. Borradori, L., Koch, P. J., Niessen, C. M., Erkeland, S., van Leusden, M. R. and Sonnenberg, A. (1997). The localization of bullous pemphigoid antigen 180 (BP180) in hemidesmosomes is mediated by its cytoplasmic domain and seems to be regulated by the β4 integrin subunit. J. Cell Biol. (in press).
4. Brown, T. A., Gil, S. G., Sybert, V. P., Lestringant, G. G., Tadini, G., Caputo, R. and Carter, W. G. ( 1996). Defective integrin α6β4 expression in the skin of patients with junctional epidermolysis bullosa and pyloric atresia. J. Invest. Dermatol. 107, 384-391.
5. Campbell, I. D. and Spitzfaden, C. (1994). Building proteins with fibronectin type III modules. Structure 2, 333-337.
6. Carter, W. G., Ryan, M. C. and Gahr, P. J. (1991). Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell 65, 599-610.
7. Chavanas, S., Pulikkinen, L., Gache, Y., Smith, F. J. D., McLean, W. H. I., Uitto, J., Ortonne, J. P. and Meneguzzi, G. (1996). A homozygous nonsense mutation in the PLEC1 gene in patients with epidermolysis bullosa simplex with muscular dystrophy. J. Clin. Invest. 98, 2196-2200.
8. Clark, E. and Brugge, J. (1995). Integrins in signal transduction pathways: the road taken. Science 268, 233-239.
9. Defilippi, P., van Hinsbergh, V., Bertolotto, A., Rossino, P., Silengo, L. and Tarone, G. (1991). Differential distribution and modulation of expression of α1β1 integrin on human endothelial cells. J. Cell Biol. 111, 3141-3154.
10. Dipersio, C. M., Shah, S. and Hynes, R. O. (1995). α3Aβ1 integrin localizes to focal contacts in response to diverse extracellular matrix proteins. J. Cell Sci. 106, 2321-2336.
11. Dickinson, C. D., Veerapandian, B., Dai, X-P, Hamlin, R. C., Xuong, N., Ruoslahti, E. and Ely, K. R. (1994). Crystal structure of the tenth type III cell adhesion module of human fibronectin. J. Mol. Biol. 236, 1079-1092.
12. Dowling, J., Yu, Q.-C. and Fuchs, E. (1996). β4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol. 134, 559-572.
13. Fässler, R., Pfaff, M., Murphy, J., Noegel, A. A., Johansson, S., Timpl, R. and Albrecht, R. (1995). Lack of β1 integrin gene in embryonic stem cells affects morphology, adhesion and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol. 128, 979-988.
14. Feltri, M. L., Scherer, S. S., Nemni, R., Kamholz, J., Vogelbacker, H., Oronzi Scott, M., Canal, N., Quaranta, V. and Wrabetz, L. (1994). β4 integrin expression in myelinating Schwann cells is polarized. developmentally regulated and axonally dependent. Development 120, 1287-1301.
15. Foisner, R., Leichtfried, F. E., Herrmann, H., Small, J. V., Lawson, D. and Wiche, G. (1988). Cytoskeleton-associated plectin: in situ localization, in vitro reconstitution, and binding to immobilized intermediate filament proteins. J. Cell Biol. 106, 723-733.
16. Foisner, R., Feldman, B., Sander, L., Seifert, G., Artlieb, U. and Wiche, G. (1994). A panel of monoclonal antibodies to rat plectin: Distinction by epitope mapping and immunoreactivity with different tissues and cell lines. Acta Histochem. (Jena) 96, 421-438.
17. Foisner, R. and Wiche, G. (1991). Intermediate filament associated proteins. Curr. Opin. Cell Biol. 3, 75-81.
18. Gache, Y., Chavanas, S., Lacour, J. P., Wiche, G., Owaribe, K., Meneguzzi, G. and Ortonne, J. P. (1996). Defective expression of plectin/HD1 in epidermolysis bullosa simplex with muscular dystrophy. J. Clin. Invent. 97, 2289-2298.
19. Georges-Labouesse, E., Messaddeq, N., Yehia, G., Cadalbert, L., Dierich, A. and LeMeur, M. (1996). Absence of the α6 integrin leads to epidermolysis bullosa and neonatal death in mice. Nature Genet. 13, 370-373.
20. Giudice, G. J., Emery, D. J. and Diaz, L. A. (1992). Cloning and primary structure analysis of the bullous pemphigoid autoantigen BP180. J. Invest. Dermatol. 99, 243-250.
21. Green, K. J. and Jones, J. C. R. (1996). Desmosomes and hemidesmosomes: structure and function of molecular components. FASEB J. 10, 871-881.
22. Green, K. J., Virata, M. L., Elgart, G. W., Stanley, J. R. and Parry, D. A. D. (1992). Comparative structural analysis of desmoplakin, bullous pemphigoid antigen and plectin: members of a new gene family invoked in organization ot intermediate filaments. Int. J. Macrobiol. 14, 145-153.
23. Guo, L., Degenstein, L., Dowling, J., Yu, Q-C, Wollman, R., Perman, R. and Fuchs, E. (1995). Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell 81, 233-243.
24. Hessle, H., Sakai, L. Y., Hollister, D. W. and Engvall, E. (1984). Basement membrane diversity detected by monoclonal antibodies. Differentiation 26, 49-54.
25. Hieda, Y., Nishizawa, Y., Uematsu, J. and Owaribe, K. (1992). Identification of a new hemidesmosomal protein HD1: A major, high molecular mass component of isolated hemidesmosomes. J. Cell Biol. 116, 1497-1506.
26. Hogervorst, F., Kuikman, I., von dem Borne, A. E. G. Kr. and Sonnenberg, A. (1990). Cloning and sequence analysis of β4 cDNA: an integrin subunit that contains a unique 118 kD cytoplasmic domain. EMBO J. 9, 765-770.
27. Hogervorst, F., Admiraal., L. G., Niessen, C., Kuikman, I., Daanis, H., Janssen, H. and Sonnenberg, A. (1993). Biochemical characterization and tissue distribution of the A and B variants of the integrin α6 subunit. J. Cell Biol. 121, 179-191.
28. Hopkinson, S. B., Baker, S. E. and Jones, J. C. K. (1995). Molecular genetic studies of a human epidermal autoantigen (the 180-kD bullous pemphigoid antigen/BP180): Identification of functionally important sequences within the BP180 molecule and evidence for an interaction between BP180 and α6 integrin. J. Cell Biol. 130, 117-125.
29. Hynes, R. O. (1992). Integrins: versatility, modulation and signalling in cell adhesion. Cell 69, 11-25.
30. Izumi, K., Hirao, Y., Hopp, L. and Oyasu, R. (1981). In vitro induction of ornithine decarboxylase in urinary bladder carcinoma cells. Cancer Res. 4, 405-409.
31. Jones, J. C. R., Kurpakus, M. A., Cooper, H. M. and Quaranta, V. (1991). A function for the integrin α6β4 in the hemidesmosome. Cell Regul. 2, 427-438.
32. Jonkman, M. F., De Jong, M. C. J. M., Heeres, K., Pas, H. H., van der Meer, J. B., Owaribe, K., Martinez de Velasco, A. M., Niessen, C. M. and Sonnenberg, A. (1995). 180-kD bullous pemphigoid antigen (BP180) is deficient in generalized atrophic benign epidermolyxis bullosa. J. Clin. Invest. 95, 1345-1352.
33. Kemperman, H., Wijnands, Y., Wesseling, J., Niessen, C. M., Sonnenberg, A. and Roos, E. (1944). The mucin epiglycanin on TA3/HA carcinoma cells prevents α6β4-mediated adhesion to laminin and kalinin and E-cadherin-mediated cell-cell interaction. J. Cell Biol. 127, 2071-2080.
34. 4 in the integrin supertamily. J. Biol. Chem. 262, 15515-15521.
35. Kennel, S. J., Epler, R. G., Lankford, T. K., Foote, L. J., Dickas, V., Canamucio, M., Cavalierie, R., Cosimelli, M., Venturo, I., Falcioni, R. and Sacchi, A. (1990). Second generation monoclonal antibodies to the human integrin α6β4. Hybridoma 9, 243-255.
36. Kennel, S. J., Godfrey, V., Ch'ang, L. Y., Lankford, T. K., Foote, L. J. and Makkinje, A. (1992). The β4 subunit is displayed on a restricted subset of endothelium in mice. J. Cell Sci. 101, 145-150.
37. Kurpakus, M. A., Quaranta, V. and Jones, J. C. R. (1991). Surface relocation of α6β4 integrins and assembly of hemidesmosomes in an in vitro model of wound healing. J. Cell Biol. 115, 1737-1750.
38. Lee, E. C., Lotz, M. M., Steele Jr., G. D. and Mercurio, A. M. (1992). The integrin α6β4 is a laminin receptor. J. Cell Biol. 117, 671-678.
39. Main, A. L., Harvey, T. S., Baron, M., Boyd, J. and Campbell, I. D. (1992). The three-dimensional structure of the tenth type III module of fibronectin: An insight into RGD-mediated interactions. Cell 71, 671-678.
40. Mainiero, F., Pepe, A., Wary, K. K., Spinardi, L., Mohammadi, M., Schlessinger, J. and Giancotti, F. G. (1995). Signal transduction by the α6β4 integrin: distinct β4 subunit sites mediate recruitment of Shc/Grb2 and association with the cytoskeleton of hemidesmosomes. EMBO J. 14, 4470-4481.
41. McGrath, J. A., Gatalica, B., Christiano, A. M., Owaribe, K., McMillan, J. R., Eady, R. A. J. and Uitto, J. (1995). Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. Nature Genet. 11, 83-86.
42. McLean, W. H. I., Pulkkinen, L., Smith, F. J. D., Rugg, E. L., Lane, E. B., Bullrich, F., Burgeson, R. E., Amano, S., Hudson, D. L., Owaribe, K., McGrath, J. A., McMillan, J. R., Eady, R. A. J., Leigh, I. M., Christiano, A. M. and Uitto, J. (1996). Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organization. Genes Dev. 10, 1724-1735.
43. Niessen, C. M., Cremona, O., Daams, H., Ferraresi, S., Sonnenberg, A. and Marchisio, P. C. (1994a). Expression of the integrin α6β4 in peripheral nerves: localization in Schwann and perineural cells and different variants of the β4 subunit. J. Cell Sci. 107, 543-552.
44. Niessen, C. M., Hogervorst, F., Jaspars, L. H., De Melker, A. A., Delwel, G. O., Hulsman, E. H. M., Kuikman, I. and Sonnenberg, A. (1994b). The integrin α6β4 is a receptor for both laminin and kalinin. Exp. Cell Res. 211, 360-367.
45. Niessen, C. M., Van der Raaij-Helmer, L., Hulsman, E. H. M., van der Neut, R., Jonkman, M. F. and Sonnenberg, A. (1996). Deficiency of the integrin β4 subunit in junctional epidermolysis bullosa with pyloric atresia: consequences for hemidesmosome formation and adhesion properties. J. Cell Sci. 109, 1695-1706.
46. Niessen, C. M., Hulsman, E. H. M., Rots, E. S., Sánchez-Aparicio, P. and Sonnenberg, A. (1997). The integrin α6β4 forms a complex with the cytoskeletal protein HD1 and induces its redistribution in transfected COS-7 cells. Mol. Biol. Cell 8, 555-566.
47. Owaribe, K., Nishizawa, Y. and Franke, W. W. (1991). Isolation and characterization of hemidesmosomes from bovine corneal epithelial cells. Exp. Cell Res. 192, 622-630.
48. Pulkkinen, L., Christiano, A. M., Airenne, T., Haakana, H., Tryggvason, K. and Uitto, J. (1994). Mutations in the γ2 chain gene (LAMC2) of kalinin/laminin-5 in the junctional forms of epidermolysis bullosa. Nature Genet. 6, 293-298.
49. Riddelle, K. S., Green, K. J. and Jones, J. C. R. (1991). Formation of hemidesmosomes in vitro by a transformed rat bladder cell line. J. Cell Biol. 112, 159-168.
50. Rousselle, P., Lunstrum, G. P., Keene, D. R. and Burgeson, R. E. (1991). Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol. 114, 567-576.
51. Sánchez-Aparicio, P., Martínez de Velasco, A. M., Niessen, C. M., Borradori, L., Kuikman, I., Hulsman, E. H. M., Fässler, R., Owaribe, K. and Sonnenberg, A. (1997). The subcellular distribution of the high molecular weight prolein HD1 is determined by the cytoplasmic domain of the integrin β4 subunit. J. Cell Sci. 110, 169-178.
52. Sawamura, D., Li., K., Chu, M. L. and Uitto, J. (1991). Human bullous pemphigoid antigen (BPAG1). Amino acid sequences deduced from cloned cDNAs predict biologically important peptide segments and protein domains. J. Biol. Chem. 266, 17784-17790.
53. Sastry, S. K. and Horwitz, A. F. (1993). Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signalling. Curr. Opin. Cell Biol. 5, 819-831.
54. Schwartz, M., Schaller, M. and Ginsberg, M. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11, 549-599.
55. Seifert, G. J., Lawson, D. and Wiche, G. (1992). Immunolocalization of the filament-associated plectin at focal contacts and actin stress fibers. Eur. J. Cell Biol. 59, 138-147.
56. Skalli, O., Jones, J. C. R., Gagescu, R. and Goldman, R. D. (1994). IFAP300 is common to desmosomes and hemidesmosomes and is a possible linker of intermediate filaments to these junctions. J. Cell Biol. 125, 159-170.
57. Smith, F. J. D., Eady, R. A. J., Leigh, I. M., McMillan, J. R., Rugg, E. L., Kelsell, D. P., Bryant, S. P., Spurr, N. K., Geddes, J. F., Kirtschig, G. et al. (1996). Plectin deficiency: hereditary basis for muscular dystrophy with epidermolysis bullosa simplex. Nature Genet. 13, 450-457.
58. Sonnenberg, A., Daams, H., van der Valk, M., Hilkens, J. and Hilgers, J. (1986). Development of the mouse mammary gland: identification of stages in differentiation of luminal and myoepithelial cells using monoclonal antibodies and polyvalent antiserum against keratin. J. Histochem. Cytochem. 34, 1037-1046.
59. Sonnenberg, A., Linders, C. J. T., Daams, J. H. and Kennel, S. J. (1990). The α6β1 (VLA-6) and α6β4 protein complexes: tissue distribution and biochemical properties. J. Cell Sci. 96, 207-217.
60. Sonnenberg, A., Calafat, J., Janssen, H., Daams, H., Van der Raaij-Helmer, L. M. H., Falcioni, R., Kennel, S. J., Aplin, J. D., Baker, J., Loizidou, M. and Garrod, D. (1991). Integrin α6β4 is located in hemidesmosomes, suggesting a major role in epidermal-basement membrane adhesion. J. Cell Biol. 113, 907-917.
61. Sonnenberg, A., De Melker, A. A., Martinez de Velasco, A. M., Janssen, H., Calafat, J. and Niessen, C. M. (1993). Formation of hemidesmosomes in cells of a transformed murine mammary tumor cell line and mechanisms involved in adherence of these cells to laminin and kalinin. J. Cell Sci. 106, 1083-1102.
62. Spinardi, L., Ren, Y-L., Sanders, R. and Giancotti, F. G. (1993). The β4 subunit cytoplasmic domain mediates the interaction of α6β4 integrin with the cytoskeleton of hemidesmosomes. Mol. Biol. Cell 4, 871-884.
63. Stepp, M. A., Spurr-Michaud, S., Tisdale, A., Elwell, J. and Gipson, I. K. (1990). α6β4 integrin heterodimer is a component of hemidesmosomes. Proc. Natl. Acad. Sci. USA 87, 8970-8974.
64. Suzuki, S. and Naitoh, Y. (1990). Amino acid sequence of a novel integrin β4 subunit and primary expression of the mRNA in epithelial cells. EMBO J. 9, 757-763.
65. Tamura, R. N., Rozzo, C., Starr, L., Chambers, J., Reichardt, L. F., Cooper, H. M. and Quaranta, V. (1990). Epithelial integrin α6β4: complete primary structure of α6 and variant forms of β4. J. Cell Biol. 111, 1593-1604.
66. Tanaka, T., Parry, D. A., Klaus-Kovtun, V., Steinert, P. M. and Stanley, J. R. (1991). Comparison of molecularly cloned bullous pemphigoid antigen to desmoplakin I confirms that they define a new family of cell adhesion junction plaque proteins. J. Biol. Chem. 266, 12555-12559.
67. Uematsu, J., Nishizawa, Y., Sonnenberg, A. and Owaribe, K. (1994). Demonstration of type II hemidesmosomes in a mammary gland epithelial cell line. BMGE-H. J. Biochem. 115, 469-476.
68. Van der Neut, R., Krimpenfort, P., Calafat, J., Niessen, C. M. and Sonnenberg, A. (1996). Epithelial detachment due to absence of hemidesmosomes in integrin β4 null mice. Nature Genet. 13, 366-369
69. Vidal, F., Aberdam, D., Miquel, C., Christiano, A. M., Pulkkinen, L., Uitto, J., Ortonne, J-P. and Meneguzzi, G. (1995). Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nature Genet. 10, 229-234.
70. Wadsworth, S., Halvorson, M. J. and Coligan, J. E. (1992). Developmentally regulated expression of the β4 integrin on immature mouse thymocytes. J. Immunol. 149, 421-428.
71. Wiche, G., Krepler, R.m Artlieb, U., Pytela, R. and Aberer, W. (1984). Identification of plectin in different human cell types and immunolocalization of epithelial basal cell surface membranes. Exp. Cell Res. 155, 43-49.
72. Wiche, G. (1989). Plectin: a general overview and appraisal of its potential role as a subunit protein of the cytomatrix. Crit. Rev. Biochem. Mol. Biol. 24, 41-67.
73. Wiche, G. Becker, B., Luber, K., Weitzer, G., Castañon, M. J., Hauptmann, R. Stratowa, C. and Stewart, M. (1991). Cloning and sequencing of rat plectin indicates a 446-kD polypeptide chain with a three-domain structure based on a alpha-helical coiled coil. J. Cell Biol. 114, 83-99.
74. Yamada, K. and Miyamoto, S. (1995). Integrin transmembrane signaling and cytoskeletal control. Curr. Opin. Cell Biol. 7, 681-689.
75. Yang, Y., Dowling, J., Yu, Q.-C., Kouklis, P., Cleveland, D. W. and Fuchs, E. (1996). An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 86, 665-665.