Uncoupling integrin adhesion and signaling: The β(PS) cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo

Genes and Development

Volumn 13, Issue 6, 1999, Pages 729-739

  Martin Bermudo, Maria D ^a   Brown, Nicholas H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adhesion; Drosophila; Extracellular matrix; Integrin; Signal transduction

Indexed keywords

INTEGRIN;

ARTICLE; CELL SURFACE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

DROSOPHILA; HEXAPODA;

EID: 0033558941     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.6.729     Document Type: Article

References (58)

1. Adams, J. and F. Watt. 1993. Regulation of development and differentiation by the extracellular matrix. Development 117: 1183-1198.
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. Artavanis-Tsakonas, S., K. Matsuno, and M.E. Fortini. 1995. Notch signalling. Science 268: 225-232.
4. 1 integrin-deficient cells. Dev. Biol. 179: 184-196.
5. Brabant, M.C. and D.L. Brower. 1993. PS2 integrin requirements in Drosophila embryo and wing morphogenesis. Dev. Biol. 157: 49-59.
6. 1 integrin function: Confirmed, new and revised roles for a crucial family of cell adhesion molecules. J. Cell Sci. 110: 2895-2904.
7. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
8. PS1 integrin subunit. Development 121: 1311-1320.
9. Brown, N.H. 1993. Integrins hold Drosophila together. BioEssays 15: 383-390.
10. PS integrin subunit genes have distinct phenotypes. Development 120: 1221-1231.
11. Bunch, T.A., R. Salatino, M.C. Engelsgjerd, L. Mukai, R.F. West, and D.L. Brower. 1992. Characterization of mutant alleles of myospheroid, the gene encoding the β subunit of the Drosophila PS integrins. Genetics 132: 519-528.
12. 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.
13. Chen, Q., T.H. Lin, C.J. Der, and R.L. Juliano. 1996. Integrin-mediated activation of mitogen-activated protein (MAP) kinase or extracellular signal-related kinase (MEK) is independent of Ras. J. Biol. Chem. 271: 18122-18127.
14. Clark, E.A. and J.S. Brugge. 1995. Integrins and signal transduction pathways: The road taken. Science 268: 233-239.
15. De Arcangelis, A.P., R. Neuville, R. Boukamel, O. Lefebvre, M. Kedinger, and P. Simon-Assmann. 1996. Inhibition of laminin α1-chain expression leads to alteration of basement membrane assembly and cell differentiation. J. Cell. Biol. 133: 417-430.
16. Dickson, B., F. Sprenger, and E. Hafen. 1992. Prepattern in the developing Drosophila eye revealed by an activated torsosevenless chimeric protein. Genes & Dev. 6: 2327-2339.
17. Edwards, G.M., F.H. Wilford, X. Liu, L. Hennighausen, J. Djiane, and C.H. Streuli. 1998. Regulation of mammary differentiation by extracellular matrix involves protein-tyrosine phosphatases. J. Biol. Chem. 273: 9495-9500.
18. Gotwals, P.J., L.I. Fessler, M. Wehrli, and R.O. Hynes. 1994. Drosophila PS1 integrin is a laminin receptor and differs in ligand specificity from PS2. Proc. Natl. Acad. Sci. 91: 11447-11451.
19. Heldin, C.H. 1995. Dimerization of cell surface receptors in signal transduction. Cell 80: 213-223.
20. Hoppler, S. and M. Bienz. 1995. Two different thresholds of wingless signalling with distinct developmental consequences in the Drosophila midgut. EMBO J. 14: 5016-5026.
21. 1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J. Cell Biol. 129: 867-879.
22. Hynes, R.O. 1992. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
23. Immergluck, K., P.A. Lawrence, and M. Bienz. 1990. Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62: 261-268.
24. Juliano, R. 1996. Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. BioEssays 18: 911-917.
25. Juliano, R.L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120: 577-585.
26. Kreis, T. and R. Vale. 1993. Guidebook to the extracellular matrix and adhesion proteins. Oxford University Press, Oxford, UK.
27. Lawrence, P.A. and G. Struhl. 1996. Morphogens, compartments, and pattern-lessons from Drosophila. Cell 85: 591-961.
28. Lin, T.H., Q. Chen, A. Howe, and R.L. Juliano. 1997a. Cell anchorage permits efficient signal transduction between Ras and its downstream kinases. J. Biol. Chem. 272: 8849-8852.
29. Lin, T.H., A.E. Aplin, Y. Shen, Q.M. Chen, M. Schaller, L. Romer, I. Aukhil, and R.L. Juliano. 1997b. Integrin mediated activation of MAP kinase is independent of FAK: Evidence for dual integrin signaling pathways in fibroblasts. J. Cell Biol. 136: 1385-1395.
30. 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.
31. Martin-Bermudo, M.D., O.M. Dunin-Borkowski, and N.H. Brown. 1997. Specificity of PS integrin function during embryogenesis resides in the α subunit extracellular domain. EMBO J. 16: 4184-4193.
32. Miyamoto, S., S.K. Akiyama, and K.M. Yamada. 1995a. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267: 883-885.
33. Miyamoto, S., H. Teramoto, O.A. Coso, J.S. Gutkind, P.D. Burbelo, S.K. Akiyama, and K.M. Yamada. 1995b. Integrin function: Molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131: 791-805.
34. Murakami, R., A. Shigenaga, E. Kawano, A. Matsumoto, I. Yamaoka, and T. Tanimura. 1994. Novel tissue units of regional differentiation in the gut epithelium of Drosophila, as revealed by P-element-mediated detection of enhancer. Wilhelm Roux's Arch. Dev. Biol. 203: 243-249.
35. Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85: 357-368.
36. Panganiban, G.E.F., R. Reuter, M. Scott, and F.M. Hoffmann. 1990. A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110: 1041-1050.
37. Plopper, G.E., H.P. McNamee, L.E. Dike, K. Bojanowski, and D.E. Ingber. 1995. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6: 1349-1365.
38. Prokop, A., M.D. Martin-Bermudo, M. Bate, and N.H. Brown. 1998. In Drosophila embryos, the absence of the PS integrins or laminin A affects the extracellular adhesion of hemiadherens and neuromuscular junctions, but not their intracellular assembly. Dev. Biol. 196: 58-76.
39. Renshaw, M.W., D. Toksoz, and M.A. Schwartz. 1996. Involvement of the small GTPase Rho in integrin-mediated activation of mitogen-activated protein kinase. J. Biol. Chem. 27: 21691-21694.
40. Renshaw, M.W., X.D. Ren, and M.A. Schwartz. 1997. Growth factor activation of MAP kinase requires cell adhesion. EMBO J. 16: 5592-5599.
41. Reuter, R., B. Grunewald, and M. Leptin. 1993. A role for mesoderm in endodermal migration and morphogenesis in Drosophila. Development 119: 1135-1145.
42. Roskelley, C.D., A. Srebrow, and M.J. Bissell. 1995. A hierarchy of ECM-mediated signalling regulates tissue-specific gene-expression. Curr. Opin. Cell Biol. 7: 736-747.
43. Sastry, S.K. and A.F. Horwitz. 1996. Adhesion-growth factor interactions during differentiation: An integrated biological response. Dev. Biol. 180: 455-467.
44. Sastry, S.K., M. Lakonishok, D. Thomas, J. Muschler, and A. Horwitz. 1996. Integrin α subunit ratios, cytoplasmic domains, and growth factor synergy regulate muscle cell proliferation and differentiation. J. Cell Biol. 133: 169-184.
45. Schlaepfer, D.D. and T. Hunter. 1996. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell Biol. 16: 5623-5633.
46. _. 1998. Integrin signalling and tyrosine phosphorylation: Just the FAKs? Trends Cell Biol. 8: 151-157.
47. Schlaepfer, D.D., S.K. Hanks, T. Hunter, and P. van der Gecr. 1994. Integrin-mediated signal transduction linked to Ras pathway by Grb2 binding to the focal adhesion kinase. Nature 372: 786-791.
48. Shrivastava, A., C. Radiziejewski, E. Campbell, L. Kovac, M.P. Goldfarb, D.J. Glass, G. Lemke, and G.D. Yancopoulos. 1997. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1: 25-34.
49. Skavdis, G., I. Siden-Kiamos, H.M. Muller, A. Crisanti, and C. Louis. 1996. Conserved function of Anopheles gambiae midgut-specific promoters in the fruitfly. EMBO J. 15: 344-350.
50. Sprenger, F. and C. Nüsslein-Volhard. 1992. Torso receptor activity is regulated by a diffusible ligand produced at the extracellular terminal regions of the Drosophila egg. Cell 71: 987-1001.
51. Stark, K.A., G.H. Yee, C.E. Roote, E.L. Williams, S. Zusman, and R.O. Hynes. 1997. A novel α integrin subunit associates with βPS and functions in tissue morphogenesis and movement during Drosophila development. Development 124: 4583.
52. Taipale, J. and J. Keskioja. 1997. Growth factors in the extracellular matrix. FASEB J. 11: 51-59.
53. Vogel, W., G.D. Gish, F. Alves, and T. Pawson. 1997. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1: 13-25.
54. Wary, K.K., F. Mainiero, S.J. Isakoff, E.E. Marcantonio, and F.G. Giancotti. 1996. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87: 1733-743.
55. 6 integrin subunit. J. Biol. Chem. 273: 5903-5907.
56. γ, expressed in the midgut of Drosophila melanogaster. Development 118: 845-858.
57. Yurochko, A.D., Y.D. Liu, D. Eierman, and S. Haskill. 1992. Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction. Proc. Natl. Acad. Sci. 89: 9034-9038.
58. 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.