Laminins promote the locomotion of skeletal myoblasts via the alpha 7 integrin receptor

Journal of Cell Science

Volumn 109, Issue 13, 1996, Pages 3139-3150

  Yao, Chung Chen ^a   Ziober, Barry L ^a   Sutherland, Ann E ^a,b   Mendrick, Donna L ^c   Kramer, Randall H ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c GLAXOSMITHKLINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

7 integrin; Adhesion; Laminin; Motility; Myoblast

Indexed keywords

FIBRONECTIN; INTEGRIN; KALININ; LAMININ; RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CHO CELL; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; RAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; CHO CELLS; CRICETINAE; CYTOPLASM; HUMANS; INTEGRIN ALPHA CHAINS; INTEGRIN ALPHA5; LAMININ; MICE; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; RATS; RECOMBINANT FUSION PROTEINS;

EID: 0030451425     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Alameddine, H. S., Hantai, D., Dehaupas, M. and Fardeau, M. (1991). Role of persisting basement membrane in the reorganization of myofibres originating from myogenic cell grafts in the rat. Neuromusc. Disord. 1. 143-152.
2. Bauer, J. S., Varner, J., Schreiner, C., Kornberg, L., Nicholas, R. and Juliano, R. L. (1993). Functional role of the cytoplasmic domain of the integrin alpha 5 subunit. J. Cell Biol. 122, 209-221.
3. Blau, H. M. and Hughes, S. M. (1990). Cell lineage in vertebrate development. Curr. Opin. Cell Biol. 2, 981-985.
4. Bronner-Fraser, M., Artinger, M., Muschler, J. and Horwitz, A. F. (1992). Developmentally regulated expression of alpha 6 integrin in avian embryos. Development 115, 197-211.
5. Campbell, J. S., Wenderoth, M. P., Hauschka, S. D. and Krebs, E. G. (1995). Differential activation of mitogen-activated protein kinase in response to basic fibroblast growth factor in skeletal muscle cells. Proc. Nat. Acad. Sci. USA 92, 870-874.
6. Chan, B. M., Kassner, P. D., Schiro, J. A., Byers, H. R., Kupper, T. S. and Hemler, M. E. (1992). Distinct cellular functions mediated by different VLA integrin alpha subunit cytoplasmic domains. Cell 68, 1051-1060.
7. Collo, G., Starr, L. and Quarante, V. (1993). A new isoform of the laminin receptor integrin alpha 7 beta 1 is developmentally regulated in skeletal muscle. J. Biol. Chem. 268, 19019-19024.
8. Cooper, H. M., Tamura, R. N. and Quaranta, V. (1991). The major laminin receptor of mouse embryonic stem cells is a novel isoform of the alpha 6 beta I integrin. J. Cell Biol. 115, 843-850.
9. Delwel, G. O., Hogervorst, F., Kuikman, I., Paulsson, M., Timpl, R. and Sonnenberg, A. (1993). Expression and function of the cytoplasmic variants of the integrin alpha 6 subunit in transfected K562 cells. Activation-dependent adhesion and interaction with isoforms of laminin. J. Biol. Chem. 268, 25865-25875.
10. Delwel, G. O., de Melker, A. A., Hogervorst, F., Jaspars, L. H., Fles, D. L. A., Kulkman, I., Lindblom, A., Paulsson, M., Timpl, R. and Sonnenberg, A. (1994). Distinct and overlapping ligand specificities of the alpha3Aß1 and alpha6Aß1 integrins: regulation of laminin isoforms. Mol. Biol. Cell 5, 203-215.
11. Delwel, G. O. and Sonnenberg, A. (1995). Laminin Isoforms and their integrin receptors. In Adhesion Receptors as Therapeutic Targets (ed. M. A. Horton), pp. 9-26. CRC Press, Boca Raton, FL.
12. Duband, J. L., Belkin, A. M., Syfrig, J., Thiery, J. P. and Koteliansky, V. E. (1992). Expression of alpha 1 integrin, a laminin-collagen receptor, during myogenesis and neurogenesis in the avian embryo. Development 116, 585-600.
13. Echtermeyer, F., Schober, S., Poschl, E., von der Mark, H. and von der Mark, K. (1996). Specific induction of cell motility on laminin by alpha7 integrin. J. Biol. Chem. 271, 2071-2075.
14. Engvall, E., Earwicker, D., Jaaparanta, T., Touslahti, E. and Sane, J. R. (1990). Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul. 1, 731-740.
15. Enomoto, M. I., Boettiger, D. and Menko, A. S. (1993). Alpha 5 integrin is a critical component of adhesion plaques in myogenesis. Dev. Biol. 155, 180-197.
16. Ervasti, J. M. and Campbell, K. P. (1993). A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823.
17. Foster, R., Thompson, J. and Kaufman, S. (1987). A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using anti-desmin and anti-BrdU monoclonal antibodies. Dev. Biol. 122, 11-20.
18. George-Weinstein, M., Foster, R. F., Gerhart, J. V. and Kaufman, S. J. (1993). In vitro and in vivo expression of alpha 7 integrin and desmin define the primary and secondary myogenic lineages. Dev. Biol. 156, 209-229.
19. Giancotti, F. G. and Ruoslahti, E. (1990). Elevated levels of the alpha 5 beta I fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell 60, 849-859.
20. Goodman, S. L., Risse, G. and von der Mark, K. (1989). The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix. J. Cell Biol. 109, 799-809.
21. Gu, M., Wang, W., Song, W. K., Cooper, D. N. and Kaufman, S. J. (1994). Selective modulation of the interaction of alpha 7 beta 1 integrin with fibronectin and laminin by L-14 lectin during skeletal muscle differentiation. J. Cell Sci. 107, 175-181.
22. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
23. Hirsch, E., Gullberg, D., Balzac, F., Altruda, F., Silengo, L. and Tarone, G. (1994). Alpha v integrin subunit is predominantly located in nervous tissue and skeletal muscle during mouse development. Dev. Dynam. 201, 108-120.
24. Hogervorst, F., Kuikman, I., van Kessel, A. G. and Sonnenberg, A. (1991). Molecular cloning of the human alpha 6 integrin subunit. Alternative splicing of alpha 6 mRNA and chromosomal localization of the alpha 6 and beta 4 genes. Eur. J. Biochem. 199, 425-433.
25. Hogervorst, F., Admiraal, L. G., Niessen, C., Kuikman, I., Janssen, H., Daams, H. and Sonnenberg, A. (1993a). Biochemical characterization and tissue distribution of the A and B variants of the integrin alpha 6 subunit. J. Cell Biol. 121, 179-191.
26. Hogervorst, F., Kuikman, L, Noteboom, E. and Sonnenberg, A. (1993b). The role of phosphorylation in activation of the alpha6Aβ1 laminin receptor. J. Biol. Chem. 268, 18427-18430.
27. Hughes, S. M. and Blau, H. M. (1990). Migration of myoblasts across basal lamina during skeletal muscle development. Nature 345, 350-353.
28. Klietsch, R., Ervasti, J. M., Arnold, W., Campbell, K. P. and Jorgensen, A. O. (1993). Dystrophin-glycoprotein complex and laminin colocalize to the sarcolemma and transverse tubules of cardiac muscle. Circul. Res. 72, 349-360.
29. Kramer, R. H., McDonald, K. A. and Vu, M. P. (1989). Human melanoma cells express a novel integrin receptor for laminin [published erratum appears in J. Biol. Chem. (1989) 264, 21432], J. Biol. Chem. 264, 15642-15649.
30. Kramer, R. H., Vu, M. P., Cheng, Y. F., Kamos, D. M., Timpl, R. and Waleh, N. (1991). Laminin-binding integrin alpha 7 beta 1: functional characterization and expression in normal and malignant melanocytes. Cell Regul. 2, 805-817.
31. Lakonishok, M., Muschler, J. and Horwitz, A. F. (1992). The alpha 5 beta 1 integrin associates with a dystrophin-containing lattice during muscle development. Dev. Biol. 152, 209-220.
32. Linkhart, T. A., Clegg, C. H. and Hauschka, S. D. (1981) Myogenic differentiation in permanent clonal mouse myoblast cell lines: regulation by macromolecular growth factors in the culture medium. Dev. Biol. 86, 19-30.
33. Martin, P. T., Kaufman, S. J., Kramer, R. H. and Sanes, J. R. (1996). Synaptic integrins: selective association of alpha I. alpha7A and alpha7B integrins with the neuromuscular junction. Dev. Biol. 174, 125-139.
34. Matsumoto, K., Matsumoto, K., Nakamura, T. and Kramer, R. H. (1994). Hepatocyte growth factor/scatter factor induces tyrosine phosphorylation of focal adhesion kinase (p125FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269, 31807-31813.
35. McDonald, K. A., Lakonishok, M. and Horwitz, A. F. (1995). Alpha v and alpha 3 integrin subunits are associated with myofibrils during myofibrillogenesis. J. Cell Sci. 108, 975-983.
36. Mehul, B., Doyennette-Moyne, M. A., Aubery, M., Mannherz, H. G. and Codogno, P. (1990). 5′-Nucleotidase is involved in chick embryo myoblast spreading on laminin. Cell Biol. Int. Rep. 14, 155-164.
37. Mehul, B., Doyennette-Moyne, M. A., Aubery, M., Codogno, P. and Mannherz, H. G. (1992). Enzymatic activity and in vivo distribution of 5′-nucleotidase, an extracellular matrix binding glycoprotein, during the development of chicken striated muscle. Exp. Cell Res. 203, 62-71.
38. Mendrick, D. L., Kelly, D. M., duMont, S. S. and Sandstrom, D. J. (1995). Glomerular epithelial and mesangial cells differentially modulate the binding specificities of VLA-1 and VLA-2. Lab. Invest. 72, 367-375.
39. Natali, P. G., Nicotra, M. R., Bigotti, A. and De Martino, C. (1992). Localization of the α6 and β4 integrin subunits in normal human non-lymphoid tissues. J. Cell Sci. 103, 1243-1247.
40. O'Toole, T. E., Katagiri, Y., Faull, R. J., Peter, K., Tamura, R., Quaranta, V., Loftus, J. C., Shattil, S. J. and Ginsberg, M. H. (1994). Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124, 1047-1059.
41. Ocalan, M., Goodman, S., Kuhl, U., Hauschka, S. and von der Mark, K. (1988). Laminin alters cell shape and stimulates mobility and proliferation of murine skeletal myoblasts. Dev. Biol. 125, 158-167.
42. Pavlath, G. K., Rich, K., Webster, S. G. and Blau, H. M. (1989). Localization of muscle gene products in nuclear domains. Nature 337, 570-573.
43. Sanes, J. R., Engvall, E., Butkowski, R. and Hunter, D. D. (1990). Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J. Cell Biol. 111, 1685-1699.
44. Sastry, S. K., Lakonishok, M., Thomas, D. A., Muschler, J. and Horwitz, A. F. (1996). Integrin alpha subunit ratios, cytoplasmic domains and growth factor synergy regulate muscle proliferation and differentiation. J. Cell Biol. 133, 169-184.
45. Schreiner, C., Fisher, M., Hussein, S. and Juliano, R. L. (1991). Increased tumorigenicity of fibronectin receptor deficient Chinese hamster ovary cell variants. Cancer Res. 51, 1738-1740.
46. Schultz, E. and McCormick, K. M. (1994). Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol. 123, 213-257.
47. Shaw, L. M., Lotz, M. M. and Mercurio, A. M. (1993). Inside-out integrin signaling in macrophages. Analysis of the role of the alpha 6A beta I and alpha 6B beta 1 integrin variants in laminin adhesion by cDNA expression in an alpha 6 integrin-deficient macrophage cell line. J. Biol. Chem. 268, 11401-11408.
48. Shaw, L. M. and Mercurio, A. M. (1994). Regulation of cellular interactions with laminin by integrin cytoplasmic domains: the A and B structural variants of the alpha 6 beta I integrin differentially modulate the adhesive strength, morphology, and migration of macrophages. Mol. Biol. Cell 5, 679-690.
49. Song, W. K., Wang, W., Sato, H., Bielser, D. A. and Kaufman, S. J. (1993). Expression of alpha 7 integrin cytoplasmic domains during skeletal muscle development: alternate forms, conformational change, and homologies with serine/threonine kinases and tyrosine phosphatases. J. Cell Sci. 106, 1139-1152.
50. 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.
51. Spinardi, L., Einheber, S., Cullen, T., Milner. T. A. and Giancotti, F. G. (1995). A recombinant tail-less integrin beta 4 subunit disrupts hemidesmosomes, but does not suppress alpha 6 beta 4-mediated cell adhesion to laminins. J. Cell Biol. 129, 473-487.
52. Steffensen, B., Magnuson, V. L., Potempa, C. L., Chen, D. and Klebe, R. J. (1992). Alpha 5 integrin subunit expression changes during myogenesis. Biochem. Biophys. Acta 1137, 95-100.
53. Tamura, R. N., Rozzo, C., Starr, L., Chambers, J., Reichardt, L. F., Cooper, H. M. and Quaranta, V. (1990). Epithelial integrin alpha 6 beta 4: complete primary structure of alpha 6 and variant forms of beta 4. J. Cell Biol. 111, 1593-1604.
54. Timpl, R. and Brown, J. C. (1994). The laminins. Matrix Biol. 14, 275-281.
55. Topp, W. C. (1981). Normal rat cell lines deficient in nuclear thymidine kinase. Virology 113, 408-411.
56. Vachon, P. H., Loechel, F., Xu, H., Wewer, U. M. and Engvall, E. (1996). Merosin and laminin in myogenesis; specific requirement for merosin in myotube stability and survival. J. Cell Biol. 134, 1483-1497.
57. van der Flier, A., Kuikman, I., Baudoin, C., van der Neut, R. and Sonnenberg, A. (1995). A novel beta 1 integrin isoform produced by alternative splicing: unique expression in cardiac and skeletal muscle. FEBS Lett. 369, 340-344.
58. Van Swearingen, J. and Lance-Jones, C. (1995). Slow and fast muscle fibers are preferentially derived from myoblasts migrating into the chick limb bud at different developmental times. Dev. Biol. 170, 321-337.
59. von der Mark, H., Durr, J., Sonnenberg, A., von der Mark, K., Deutzmann, R. and Goodman, S. L. (1991). Skeletal myoblasts utilize a novel beta 1-series integrin and not alpha 6 beta I for binding to the E8 and T8 fragments of laminin. J. Biol. Chem. 266, 23593-23601.
60. von der Mark, K. and Ocalan, M. (1989). Antagonistic effects of laminin and fibronectin on the expression of the myogenic phenotype. Differentiation 40, 150-157.
61. Wu, C., Fields, A. J., Kapteijn, B. A. and McDonald, J. A. (1995). The role of alpha 4 beta 1 integrin in cell motility and fibronectin matrix assembly. J. Cell Sci. 108, 821-829.
62. Yaffe, D. and Saxel, O. (1977). Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727.
63. Yao, C-C, Ziober, B. L., Squillace, R. M. and Kramer, R. H. (1996). Alpha7 integrin mediates cell motility and migration on specific laminin isoforms. J. Biol. Chem. 291, 25598-25603.
64. Zhidkova, N. I., Belkin, A. M. and Mayne, R. (1995). Novel isoform of beta I integrin expressed in skeletal and cardiac muscle. Biochem. Biophys. Res. Commun. 214, 279-285.
65. Ziober, B. L., Vu, M. P., Waleh, N., Crawford, J., Lin, C. and Kramer, R. H. (1993). Alternative extracellular and cytoplasmic domains of the integrin alpha7 subunit are differentially expressed during development. J. Biol. Chem. 268, 26773-26783.
66. Ziober, B. L. and Kramer, R. H. (1996). Identification and characterization of the cell type-specific and developmentally regulated alpha7 integrin gene promoter. J. Biol. Chem. 271, 22915-22922.