β1D integrin displaces the β1A isoform in striated muscles: Localization at junctional structures and signaling potential in nonmuscle cells

Journal of Cell Biology

Volumn 132, Issue 1-2, 1996, Pages 211-226

  Belkin, Alexey M ^a   Zhidkova, Natalia I ^b   Balzac, Fiorella ^c   Altruda, Fiorella ^c   Tomatis, Daniela ^c   Maier, Alfred ^b   Tarone, Guido ^c   Koteliansky, Victor E ^d   Burridge, Keith ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF TURIN   (Italy)

^d INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HEART MUSCLE CELL; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SARCOLEMMA; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALIA;

EID: 0029671374     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.1.211     Document Type: Article

References (79)

1. Adams M. E , M. H. Butler, T. M. Dwyer, M F. Peters, A. A. Murnane, and S. C Froehner. 1993 Two forms of mouse syntrophin, a 58 kD dystrophin-associated protein, differ in primary structure and tissue distribution. Neuron 11: 531-540.
2. Akiyama, S. K., S. S. Yamada, K. M. Yamada and S. E. LaFlamme. 1994. Transmembrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras. J Biol. Chem 269:15961-15964.
3. Altruda, F., P. Cervella, G. Tarone, C. Botta, F Balzac, O. Stefanuto, and L Silengo. 1990. A human integrin β1 subunit with a unique cytoplasmic domain generated by alternative mRNA processing. Gene (Amst). 95:261-266.
4. Argraves, W S , S Suzuki, H. Arai, K Thompson, M. D. Piersbacher, and E Ruoslahti. 1987 Amino acid sequence of the human fibronectin receptor J Cell Biol. 105:1183-1190.
5. Baker, L. P., D. F. Daggett, and H. B. Peng. 1994. Concentration of pp125 focal adhesion kinase (FAK) at the myotendinous junction. J. Cell Sci. 107:1485-1497.
6. Balzac, F , A. M. Belkin, V. E. Koteliansky, Y V Balabanov, F. Altruda L. Silengo, and G. Tarone. 1993. Expression and functional analysis of a cytoplasmic domain variant of the β1 integrin subunit. J. Cell Biol. 121.171-178
7. Balzac, F , S. F. Retta, A Albini, A Melchiorri, V. E. Koteliansky, M. Gcuna, L. Silengo, and G Tarone. 1994. Expression of β1B integrin isoform in CHO cells results in a dominant negative effect on cell adhesion and motility J Cell Biol. 127.557-565
8. Bao, Z Z., M. Lakomshok, S. Kaufman, and A. F Horwitz. 1993. α7β1 integrin is a component of the myotendinous junction on skeletal muscle. J. Cell Sci, 106:579-590.
9. Belkin, A. M., and K. Burridge. 1994. Expression and localization of the phosphoglucomutase-related cytoskeletal protein, aciculin, in skeletal muscle J Cell Sci. 107:1993-2003.
10. Belkin, A. M., and K. Burridge. 1995. Association of aciculin with dystrophin and utrophin. J. Biol. Chem. 270:6328-6337.
11. Bozyczko, D., C. Decker, J. Muschler, and A. F. Horwitz. 1989. Integrin on developing and adult skeletal muscle. Exp Cell Res 183:72-91.
12. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J Cell Biol. 119:893-903.
13. Chen, Q., M. S. Kinch, T. H. Lin, K. Burridge, and R L. Juliano. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol Chem. 269:26602-26605.
14. Chen, Y.-P., T. E. O'Toole, T. Shipley, J. Forsyth, S. E. LaFlamme, K. M. Yamada, S. J. Shatill, M. H Ginsberg. 1994. "Inside-out" signal transduction inhibited by isolated integrin cytoplasmic domains. J. Biol Chem. 269:18307-18310
15. Clark, E. A., and J S. Brugge. 1995. Integrins and signal transduction pathways: the road taken Science (Wash. DC). 268:233-239.
16. Cleves, A. E., T. P. McGee, E. A. Whitters, K. M. Champion, J. R. Aitken, W. Dowhan, M. Goebl, and V. A. Bankaitis. 1991. Mutations in the GDP-choline pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein. Cell. 64:789-800.
17. Collo, G., L. Starr, and V. Quaranta. 1993. A new isoform of the laminin receptor integrin α7β1 is developmentally regulated in skeletal muscle. J. Biol Chem 268:19019-19023.
18. Defilippi, P., L. Silengo, and G. Tarone. 1992. α6β1 integrin (laminin receptor) is down-regulated by tumor necrosis factor β1 and interleukin-1β in human endothelial cells. J. Biol. Chem 267:18303-18307.
19. Ellis, L., E. Clauser, D. O Morgan, M. Edery, R. A. Roth, and W. J. Rutter. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromise insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell. 45:721-732.
20. Ervasti, J. M., and K. P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell. 66.1121-1131.
21. Ervasti, J. M., and K. P. Campbell. 1993. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol 122:809-823.
22. Path, K. R., C.-J. S. Edgell, and K. Burridge. 1989 The distribution of distinct integrins in focal contacts is determined by the substratum composition. J Cell Sci. 92:67-75.
23. r58000 (58K) protein concentrated at acetylcholine receptor-rich sites in Torpedo electroplaques and skeletal muscle. J. Cell Biol. 104: 1633-1646.
24. Fitzgerald, L. A., B. Steiner, S. C. Rall, Jr., S. Lo, and D. R. Phillips. 1987 Protein sequence of endothelial glycoprotein IIIA derived from a cDNA clone. J. Biol. Chem. 262.3936-3939.
25. Giancotti, F. G., and E Ruoslahti 1990. Elevated levels of the alphaS/beta1 fibronectin receptor suppress the transformed phenotype of chinese hamster ovary cells Cell 60:849-859.
26. Glukhova, M A , M. G Frid, and V. E. Kotekansky. 1990. Developmental changes in expression of contractile and cytoskeletal proteins in human aortic smooth muscle. J Biol. Chem 265:13042-13046.
27. Guan, J.-L., J. E Trevitnick, and R. O Hynes. 1991. Fibronectin-integrin interaction induces tyrosine phosphorylation of a 120 kDa protein. Cell Regul 2: 951-964.
28. Guan, J.-L., and D. Shalloway. 1992. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation Nature (Lond). 358:690-692
29. Hayashi, Y , B. Haimovich, A. Reszka, D. Boettiger, and A. F. Horwitz. 1990. Expression and function of chicken integral β1 subunit and its cytoplasmic domain mutants in mouse NIH 3T3 cells. J. Cell Biol 110:175-182.
30. Hemler, M E., J. B Weitzman, R Pasqualini, S. Kawaguchi, P. D. Kassner, and F. B. Berdichevsky. 1994 Structure, biochemical properties and biological functions of integrin cytoplasmic domains. In Integrin: The Biological Problem. Y Takada, editor. CRC Press Ann Arbor, MI. 1-35.
31. Hoffman, E. P., R. H. Brown, Jr., and L. M. Kunkel. 1987. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 51:919-928.
32. Holers, V. M., T G. Ruff, D. L. Parks, J. A. McDonald, L. L. Ballard, and E. J. Brown 1989 Molecular cloning of a murine fibronectin receptor and its expression during inflammation. J. Exp Med. 169:1569-1605.
33. Horwitz, R., E, Duggan, C. Buck, M. Beckerle, and K. Burridge. 1986. Interaction of plasma membrane fibronectin receptor with talin a transmembrane linkage. Nature (Lond.). 320:531-533.
34. Hynes, R O. 1992. Integrins: versatility, modulation and signalling in cell adhesion. Cell. 69:11-25
35. Ibraghirnov-Beskrovnaya, O., J. M. Ervasti, C J. Leveille, C. A. Slaughter, S. W. Sernett, and K. P. Campbell. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature (Lond.). 355.696-702.
36. Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
37. Kornberg, L , H S Earp, C. E. Turner, C. J. Prockop, and R. L. Juliano. 1991. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by integrin clustering. Proc Natl. Acad Sci. USA 88:8392-8396.
38. Kornberg, L., H. S Earp, T. Parsons, M. Schaller, and R. L Juliano. 1992. Cell adhesion or integrin clustering increase phosphorylation of focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267:23439-23442.
39. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature (Lond.). 227:680-685.
40. LaFlamme, S. E., S. K. Akiyama, and K. M. Yamada. 1992. Regulation of fibronectin receptor distribution. J Cell Biol. 117:437-447.
41. LaFlamme, S. E., L. A. Thomas, S. S. Yamada, and K. M. Yamada. 1994. Single subunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration, and matrix assembly. J. Cell Biol 126:1287-1298.
42. Languino, L. R., and E. Ruoslahti. 1992. An alternative form of the integrin betal subunit with variant cytoplasmic domain. J Biol. Chem. 267:7116-7120.
43. Lanza, F., N. Kieffer, D. R. Phillips, and L. A. Fitzgerald. 1990. Characterization of the human platelet glycoprotein IIIa gene. J. Biol. Chem. 265:18098-18103
44. Lewis, J. M., and M. A. Schwartz. 1995. Mapping in vivo associations of cytoplasmic proteins with integrin β1 cytoplasmic domain mutants. Mol. Biol. Cell 6:151-160.
45. Lukashev, M. E., D. Sheppard, and R. Pytela 1994. Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed β1 integrin cytoplasmic domain. J. Biol Chem 269:18311-18314.
46. Marcantonio E. E., and R. Hynes. 1988. Antibodies to the conserved cytoplasmic domain of the integrin β1 subunit react with proteins in vertebrates, invertebrates and fungi. J Cell Biol. 106:1765-1772.
47. Marcantonio, E. E., J.-L. Guan, J. E. Trevitnick, and R. O. Hynes. 1990. Mapping of the functional determinants of the integrin β1 cytoplasmic domain by site-directed mutagenesis. Cell Regul. 1:597-604.
48. Martin-Padura, I., G. Bazzoni, A. Zanetti, S. Bernasconi, M. Elices, A. Mantovani, and E. Dejana. 1994. A novel mechanism of colon carcinoma cells adhesion to the endothelium triggered by β1 integrin chain. J. Biol. Chem. 269: 6124-6130
49. Menko, A. S., and D. Boettiger. 1987. Occupation of the extracellular matrix receptor, integrin, is a central point for myogenic differentiation. Cell 51:51-57.
50. Meredith, J., Jr , Y. Takada, M. Fornaro, L. R. Languino, and M. A. Schwartz. 1995. Inhibition of cell cycle progression by the alternatively spliced integrin β1C. Science (Wash. DC). 269:1570-1572.
51. Miyamoto, S., S K. Akiyama, and K M. Yamada, Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function Science (Wash. DC). 267 883-885.
52. Otey, C. A , F. M. Pavalko, and K. Burridge. 1990. An interaction between α-actinin and the β1 integrin subunit in vitro. J. Cell Biol 111:721-729.
53. Otey, C. A., G. B. Vasquez, K. Burridge and B. W. Erickson. 1993 Mapping of the α-actinin binding site within the β1 integrin cytoplasmic domain. J. Biol. Chem 268:21193-21197
54. O'Toole, T. E., Y. Katagiri, R. J. Faull, K. Peter, R. Tamura, V Quaranta, J. C. Loftus. S. J Shatill, and M. H. Ginsberg. 1994. Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124:1047-1059.
55. O'Toole, T E., J Ylanne, and B. M. Culley. 1995. Regulation of integrin affinity states through an NPXY motif in the β subunit cytoplasmic domain. J Biol. Chem. 270.8553-8558.
56. Pasqualini, R., and M. Hemler 1994. Contrasting roles for integrin β1 and β5 cytoplasmic domains in subcellular localization, cell proliferation and cell migration. J. Cell Biol. 125:447-460.
57. Porter, G. A., G. M. Dmytrenko, J. C Winkelmann, and R. J. Bloch. 1992. Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J. Cell Biol 117.997-1005
58. Reszka, A. A., Y. Hayashi, and A. F. Horwitz. 1992. Identification of amino acid sequences in the integrin β1 cytoplasmic domain implicated in cytoskeletal association J Cell Biol. 117:1321-1330.
59. Sastry, S. K., and A. F. Horwitz. 1993 Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signalling. Curr. Opin. Cell Biol. 5:819-831.
60. FAK, a structurally unique protein kinase associated with focal adhesions. Proc. Natl Acad. Sci , USA. 89:5192-5196
61. Schlaepfer, D. D , S K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature (Lond) 372:786-790
62. Schwartz, M. A. 1992 Transmembrane signaling by integrins. Trends Cell Biol. 2.304-308.
63. Sealock, R., M. H. Butler, N. R. Kramarcy, K.-X. Gao, A. A. Murnane, K Douville, and S. C Froehner. 1991. Localization of dystrophin relative to acetylcholine receptor domains in electric tissue and adult and cultured skeletal muscle. J Cell Biol. 113:1133-1144.
64. Smilenov L., R. Bitesewitz, and E E. Marcantonio. 1994. Integrin β1 cytoplasmic domain dominant negative effects revealed by lysophosphatidic acid treatment. Mol Biol Cell 5:1215-1223
65. Song, W. K., W Wang, R F. Foster, D. A Bielser, and S. J. Kaufman. 1992 H36-α7 is a novel integrin alpha chain that is developmentally regulated during skeletal myogenesis J Cell Biol. 117:643-657.
66. Southern, P J., and P. W. Berg 1982. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J. Mol Appl. Genet. 1:327-341.
67. Straub, V., R. E. Bittner, J. J. Leger, and T. Voit. 1992. Direct visualization of the dystrophin network on skeletal muscle fiber membrane. J. Cell Biol. 119: 1183-1191.
68. Swasdison, S., and R. Mayne 1989. Location of the integral complex and extracellular matrix molecules at the chicken myotendinous junction. Cell Tissue Res. 257:537-543.
69. Tamkun, J. W., D. W. DeSimone, D. Fonda, R. S. Patel, C. Buck, A. F. Horwitz, and R. O. Hynes. 1986. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell. 46:271-282.
70. v-src. Oncogene. 4:325-333.
71. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from acrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl. Acad Sci. USA. 76:4350-4354.
72. van der Flier, A., I. Kuikman, C. Baudoin, R. van der Neut, and A. Sonnenberg. 1995. A novel β1 integrin isoform produced by alternative splicing: unique expression in cardiac and skeletal muscle. FEBS (Fed. Eur. Biochem. Soc.) Lett. 369:340-344.
73. van Kuppevelt, T. H., L. R. Languino, J. O. Gailit, S. Suzuki, and E. Ruoslahti. 1989. An alternative cytoplasmic domain of the integral β3 subunit. Proc. Natl Acad. Sci. USA. 86:5415-5418.
74. Volk, T., L. I. Fessler, and J. H. Fessier. 1990. A role for integrin in the formation of sarcomeric cytoarchitecture. Cell. 63:525-536.
75. Watkins, S. C., E. P. Hoffman, H. S. Slayter, and L M. Kunkel. 1988. Immunoelectron microscopic localization of dystrophin in myofibres. Nature (Lond.). 333:863-866
76. Yang, B., O. Ibraghimov-Beskrovnaya, C. R. Moonaw, C. A. Slaughter, and K. P. Campbell. 1994. Heterogeneity of the 59-kDa dystrophin-associated protein revealed by cDNA cloning and expression. J. Biol. Chem. 269:6040-6044.
77. Ylanne, J., Y. Chen, T. E. O'Toole, J. C. Loftus, Y Takada, and M. H. Ginsberg. 1993. Distinct roles of integrin α and β subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J. Cell Biol. 122:223-233.
78. Zhidkova, N. I., A. M. Belkin, and R. Mayne. 1995. Novel isoform of β1 integrin expressed in skeletal and cardiac muscle. Biochem. Biophys. Res Commun. 214:279-285.
79. Zhu, X., and R. K. Assoian. 1995. Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation. Mol. Biol. Cell. 6:273-282.