Initiation of skin basement membrane formation at the epidermo-dermal interface involves assembly of laminins through binding to cell membrane receptors

Journal of Cell Science

Volumn 111, Issue 14, 1998, Pages 1929-1940

  Fleischmajer, Raul ^a   Utani, Atsushi ^b   MacDonald II, E Douglas ^a   Perlish, Jerome S ^a   Pan, Te Cheng ^c   Chu, Mon Li ^c   Nomizu, Motoyoshi ^b   Ninomiya, Yoshifumi ^d   Yamada, Yoshihiko ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Basement membrane; Integrin; Laminin

Indexed keywords

COLLAGEN TYPE 4; ENTACTIN; INTEGRIN; KALININ; LAMININ; MEMBRANE RECEPTOR;

ARTICLE; BASEMENT MEMBRANE; DERMOEPIDERMAL JUNCTION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; KERATINOCYTE; MEMBRANE FORMATION; MORPHOGENESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN CULTURE; SKIN FIBROBLAST;

AMINO ACID SEQUENCE; ANTIGENS, CD29; BASEMENT MEMBRANE; CELL COMMUNICATION; CELL MEMBRANE; CELLS, CULTURED; DESMOSOMES; EPIDERMIS; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; LAMININ; MALE; MICROFILAMENTS; MORPHOGENESIS; PEPTIDE FRAGMENTS; SKIN; SKIN PHYSIOLOGY;

EID: 0031847121     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Adams, J. C. and Watt, F. M. (1990). Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes α5β1 integrin loss from the cell surface. Cell 63, 425-435.
2. Adams, J. C. and Watt, F. M. (1993). Regulation of development and differentiation by the extracellular matrix. Development 117, 1183-1198.
3. Asselineau, D., Bernard, B. A., Bailly, C. and Darmon, M. (1989) Retinoic acid improves epidermal morphogenesis. Dev. Biol. 133, 322-335.
4. Battaglia, C., Mayer, U., Aumailley, M. and Timpl, R. (1992). Basement membrane heparan sulfate proteoglycan binds to laminin by its heparan sulfate chains and to nidogen by sites in the protein core. Eur. J. Biochem. 208, 359-366.
5. Beck, K., Hunter, I. and Engel, J. (1990). Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4, 148-160.
6. Burgeson, R. K. (1996). Laminins in epidermal structures. In The Laminins (ed. P. E. Ekblom and R. Timpl). pp. 65-96. Harwood Academic. UK
7. Carter, W. G., Ryan, M. C. and Gahr, P. J. (1991). Epiligrin, a new cell adhesion ligand α3β1 in epithelial basement membranes. Cell 65, 599-610.
8. Champliaud, M. F., Lunstrum, G. P., Rousselle, P., Nishiyama, T., Keane, D. R. and Burgeson, R. E. (1996). Human amnion contains a novel laminin variant laminin 7. which like laminin 6 covalently associates with laminin 5 to promote epithelial-stromal attachment. J. Cell Biol. 132, 1189-1198.
9. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
10. Contard, P., Bartel, R. L., Jacobs, H., Perlish, J. S., MacDonald, E. D., Handler, H. L., Cone, D. and Fleischmajer, R. (1993) Culturing keratinocytes and fibroblasts in a 3-dimensional mesh results in epidermal differentiation and formation of a basal lamina-anchoring zone. J. Invest. Dermatol. 100, 35-39.
11. Davis, C. M., Papadopoulos, V., Sommers, C. L., Kleinman, H. K. and Dym, M. (1990). Differential expression of extracellular matrix components in rat sertoli cells. Biol. Reprod. 43, 860-869.
12. Dedhar, S., Jewel, K., Rosiani, M. and Gray, V. (1992). The receptor for the basement membrane glycoprotein entactin is the integrin α3β1 Biol. Chem. 267, 18908-18914.
13. DeLuca, M., Tamura, R. N., Kajiji, S., Bondanza, S., Rossino, P. C. and Quaranta, K. (1990). Polarized integrin mediates human keratinocyte adhesion to basal lamina. Proc. Nat. Acad. Sci. USA 87, 6888-6892
14. DiPersio, C. M., Hodivala-Dilke, K. M., Jaenisch, R., Kreidberg, J. A. and Hynes, R. O. (1997). α3β1 integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137, 729-742.
15. Engel, J. (1994). Concepts of self-assembly. In Biological Systems in Extracellular Matrix Assembly and Structure (ed. P. D. Yurchenco. D. E. Birk and P. Mechem). pp. 1-14. Academic Press. Inc., San Diego.
16. Fleischmajer, R., Mac-Donald, E. D., Contard, P. and Perlish. J. S. (1993) Immunochemistry of a keratinocyte-fibroblast co-culture model for reconstruction of human skin. J. Histochem. Cytochem. 41, 1359-1366.
17. Fleischmajer, R., Schechter, A., Bruns, H., Perlish, J. S., MacDonald, K. D., Timpl, R. and Chu, M.-L. (1995). Skin fibroblasts are the only source of nidogen during earls basal lamina formation in vitro. J. Invest. Dermal 105, 597-601.
18. Fleischmajer, R., Kühn K., Sato, Y., MacDonald. K. D., Perlish, J. S., Pan, T.-C. Chu, M.-L, Kishiro, Y., Oohashi, T., Besnier, S. M., Yamada, Y. and Ninomiya, Y. (1997). There is temporal and spatial expression of α1(IV). α2(IV). α5(IV). α6(IV) collagen chains and β1 inlegrins during the development of the basal lamina in an 'in vitro' skin model. J. Invent. Dermutol. 109, 527-533.
19. Gehlsen, K. R., Dickerson, K., Argraves, W. S., Engval, K. and Ruoslahti, K. (1989). Subunit structure of a laminin binding integin and localization of its binding site in laminin. J. Biol. Chem. 264, 19034-19038.
20. Guadagno, T. M. and Assoian, R. K. (1991). GIIS control of anchorage-dependent growth in the fibroblast cell cycle. J. Cell Biol. 115, 1419-1425.
21. Hertle, M. D., Adams, J. C. and Watt, F. M. (1991). Integrin expression during human epidermal development in vivo and in vitro. Development 112, 193-206.
22. Hulmes, D. J. S., Jesior, T.-C, Miller, A., Berthet-Colominos, C. and Wolff, C. (1981). Electron microscopy shows periodic structure in collagen fetal cross sections. Proc. Nat. Acad. Sci. USA 78, 3567-3571.
23. Kalb, K. and Engel, J. (1991). Binding and calcium-induced aggregation of laminin onto lipid bilayers. J. Biol. Chem. 266, 19046-19052.
24. Kern, A., Eble, J., Golbik, R. and Kühn, K. (1993). Interaction of type IV collagen with the isolated integrins α1β1 and α2β1. Eur. J. Biochem. 215, 151-159.
25. Kim, J. P., Zhang, K., Kramer, R. H., Schall, T. J. and Woodley, D. T. (1992). Integrin receptors and ROD sequences in human keratinocyte migration: unique antimigratory function of α3βepilignn receptor. J Invest. Dermatol. 98, 764-770.
26. Kim, W. H., Nomize, M., Song, S.-Y, Tanaka, K., Kuratomi, Y., Kleinman, H. K. and Yamada, Y. (1998). Laminin-α1 chain sequence Leu-Glu-ValGlu-Leu-Ser-Ile-Arg (LQVQLSIR) enhances murine melanoma cell metastasis. Int. J. Cancer Res. (in press).
27. Kirchhofer, D., Languino, L. R., Ruoslahti, E. and Pierschbacher, M. (1990). α2β1 integrins from different cell types show different binding specificities. J. Biol. Chem. 265, 615-618.
28. Kreidberg, J. A., Donovan, M. J., Goldstein, S. L., Rennke, H., Shepherd, K., Jones, R. C. and Jaenisch, R. (1996). α3β1 integrin has a crucial role in kidney and lung organogenesis. Development 122, 3537-3547.
29. 3 Mr polypeptidc during adhesion complex formation J. Cell Sci. 96, 651-660.
30. 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.
31. Langhofer, M., Hopkinson, S. B. and Jones, J. C. R. (1993). The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J. Cell Sci. 105, 753-764.
32. Larvaja, H., Salo, T., Haapasaimi, K., Kramer, R. H. and Heino, J. (1993). Expression of integrins and basement membrane components by wound keratinocytes. J. Clin. Invest. 92, 1425-1435.
33. Lightner, V. A., Gumkowski, F., Bigner, D. D. and Erickson, H. P. (1989). Tenascin/hexabrachion in human skin. Biochemical identification and localization by light and electron microscopy. J. Cell Biol. 108, 2483-2493.
34. Mann, K., Deutzmann, R. and Timpl, R. (1988). Characterization of proteolytic fragments of the laminin-nidogen complex and their activity in ligand-binding assays. Eur. J. Biochem. 178, 71-80.
35. Marinkovich, M. P., Lundstrum, G. P. and Burgeson, R. E. (1992a). The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J. Biol. Chem 267. 17900-17906.
36. Marinkovich, M. P., Lundstrum, C. P., Keene, D. R. and Burgeson, R. E. (1992b). The dermal-epidermal junction of human skin contains a novel laminin variant. J. Cell Biol. 119, 695-703
37. Marinkovich, M. P., Keene, D. R., Rimberg, C. S. and Burgeson, R. E. (1993). Cellular origin of the dermal-epidermal basement membrane Dev. Dynam. 197, 255-267.
38. Mallei, M. G., Well, U., Pribula-Conway, D., Bernar, M. P., Passage, E., Van, N. C., Timpl, R. and Chu, M.-L. (1988). cDNA cloning expression and mapping of human laminin B2 gene to chromosome Iq31. Hum. Genet 79, 235-241.
39. Mayer, U., Nischt, R., Poschl, E., Mann, K., Fukuda, K., Gerl, M., Yamada, Y. and Timpl, R. (1993). A single EGF-like motif of laminin is resposible for high affinity nidogen hinding. EMBO J 12, 877-889.
40. Montell, D. J. and Goodman, C. S. (1989). Drosophila laminin: Sequence of B2 suhunit and expression of all three subunits during embryogenesis. J. Cell Biol. 109, 2441-2453.
41. Naughton, G. K., Jacob, L., and Naughton, B. A. (1989). A polydonal skin model for in vitro toxicity studies. In Alternative Methods in Toxicity (ed. A. M. Goldberg). pp. 183-189. Mary Ann Liebert, New York
42. Niessen, C. M., Hogervorst, F., Jaspars, F., DeMelker, L. H., Delwel, A. A., Hulsman, G. O., Kuikman, E. H. M. and Sonnenberg, A. (1994). The α6β4 integrin is a receptor for both laminin and kalinin. Exp. Cell Res. 211, 360-367.
43. Ninomiya, Y., Kagawa, M., Ken-Ichi, K., Naito, I., Kishiro, Y., Seyer, J. M., Sugimoto, M., Oohashi, T. and Sado, Y. (1995). Differential expression of two basement membrane collagen genes COL4A6 and COL4A5 demonstrated immunofluorescence staining using peptide specific monoclonal antibodies. J. Celt Biol. 130, 1219-1229.
44. Nomizu, M., Kim, W. H., Yamanura, K., Utani, A., Song, S. -Y, Otaka, A., Roller, P. P., Kleinman, H. K. and Yamada, Y. (1995). Identification of cell binding sites in the laminin α1 chain carboxyl-terminal globular domain by systematic screening of synthetic peptides. J. Biol. Chem. 270, 20583-20590.
45. Paulsson, M. (1994). Biosynthesis, tissue distribution and isolation of laminins. In The Laminins (ed. P. Ekblo, and R. Timpl). pp. 1-26, Academic Pub. Amsterdam, The Netherlands.
46. Rhode, H., Wick, G. and Timpl. R. (1979). Immunochemical characterization of the basement membrane glycoprotein laminin. Eur. J. Biochem. 102, 195-201.
47. 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.
48. Rousselle, P. and Aumailley, M. (1994). Kalinin is more efficient than laminin in promoting adhesion of primary keratinocytes and some other epithelial cells and has a different requirement for integrin receptors. J. Cell Biol. 125, 205-214.
49. Ryynanen, J., Jaakkola, A. S., Engvall, K., Peltonen, J. and Uitto, J. (1991). Expression of β4 integrins in human skin: comparison of epidermal distribution with β1-integrin epitopes and modulation by calcium and vitamin D3, in cultured keratinocytes. J. Invest. Dermal. 97, 562-567.
50. Senior, P. V., Critchley, D. R., Beck, F., Walker, R. A. and Varley, J. M. (1988). The localization of laminin mRNA and protein in the postimplantation embryo and placenta ot the mouse: An in situ hyhridization immunocytochemical study. Development 104, 431-446.
51. Simo, P., Bouziges, E. Lissitsky, L. C., Sorokin, L., Kedinger, M. and Simon-Assnian, P. (1992). Dual and asynchtonous deposition of laminin chains at the epithelial-mesenchymal interface in the gut. Gastroenterology 102, 1835-1845.
52. Slivka, S. R., Landeen, L. K., Zeigler, F., Zimber, M. P and Bartel, R. L. (1993). Characterization barrier function and drug metabolism of an in vitro skin model. J. Invest. Dermal. 100, 40-46.
53. Sollberg, S., Peltonen, J. and Uitto, J. (1992). Differential expression of laminin isoforms and β4 integrin epitopes in the basement membrane zone of normal human skin and basal cell carcinomas. J. Invest. Dermal. 98, 864-870.
54. Song, S.-Y. Nomizu M., Yamada, Y. and Kleinman, H. K. (1997). Liver metastasis termination by laminin-1 peptide (LQVQLSIR) -adhesion selected BIG-FIO melanoma cells. Int. J. Cancer 71, 436-441.
55. Sung, U., O'Rear, J. J. and Yurchenco, P. D. (1993). Cell and heparin binding in the distal long arm of laminin: identification of active and cryptic sites with recominant and hybrid glycoprotems. J. Cell Bid 123, 1255-1268.
56. Tanaka, T., Korman, N. J., Shimizu, H., Eady, R. A. J., Kovtun, V, K., Cehrs, K. and Stanley, J. R. (1990). Production of rabbit antibodies against carboxy-terminal epitopes encoded by Bullous Pemphigoid cDNA. J. Invest. Dermatol. 94, 617-623.
57. Thomas, T. and Dziadek, M. (1993). Genes coding for basement membrane glycoproteins laminin. nidogen, and collagen IV are differentially expressed in the nervous system and by epithelial, endothelial. and mesenchymal cells of the mouse embryo. Exp. Cell Res. 208, 54-67.
58. Timpl, R., Rohde. H., Robey, G., Rennard, P., Foidart, S. L. and Martin. G. R. (1979). Laminin. a glycoprotein from basement membranes. J. Biol. Chem. 254, 9933-9937.
59. Timpl, R. (1996). Macromolecular organisation of basement membranes. Curr. Opin. Cell Biol. 8, 618-624.
60. Vanderberg, P., Kern, A., Ries. A., Luckenbill-Edds, L., Mann, K. and Kühn, K. (1991). Characterization of a type IV collagen major cell binding site with affinity to the (α1β1 and the α2β1 integrins. J. Cell Biol. 113, 1475-1483.
61. Varner, J. A. and Cheresh, D. A. (1996). Integrins and cancer. Curr. Opin. Cell Biol. 8, 724-730.
62. Wayner, K. A. and Carter, W. G. (1987). Identilication of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J, Cell Biol. 105, 1873-1884
63. Werb, Z., Tremble, O., Behrendtsen, O., Crowley, E. and Damsky, C. H. (1989). Signal transduction through the fibronectin receptor induces collagenase and slromelysin gene expression. J. Cell Biol. 109, 877-889.
64. Yurchenco, P. and Furthmayr, H. (1984). Self-assembly of basement membrane collagen. Binchemistry 23, 1839-1850.
65. Yurchenco, P. D. and Ruben, G. C. (1987) Basement membrane structure in situ: evidence for lateral associations in the Type IV collagen network. J. Cell Biol. 105. 2559-2568.
66. Yurchenco, P. D)., Cheng, Y.-S and Colognato. H. (1992). Laminin forms an independent network in basement membranes. J Cell Biol. 117, 1119-1133.