Focal adhesions - The cytoskeletal connection

Current Opinion in Cell Biology

Volumn 12, Issue 1, 2000, Pages 133-139

  Critchley, David R ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CYTOSKELETON PROTEIN; FILAMIN; GUANOSINE TRIPHOSPHATASE; RHO FACTOR; TALIN; VINCULIN;

CELL ADHESION; CELL JUNCTION; CELL MOTILITY; CELL PROLIFERATION; CYTOSKELETON; EXTRACELLULAR MATRIX; MICROTUBULE; PRIORITY JOURNAL; REVIEW;

EID: 0033962672     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)00067-8     Document Type: Review

References (57)

1. Howe A., Aplin A.E., Alahari S.K., Juliano R.L. Integrin signalling and cell growth control. Curr Opin Cell Biol. 10:1998;220-231.
2. Schoenwaelder S.M., Burridge K. Bidirectional signalling between the cytoskeleton and integrins. Curr Opin Cell Biol. 11:1999;274-286.
3. Vuori K. Integrin signalling: tyrosine phosphorylation events in focal adhesions. J Membr Biol. 165:1998;191-199.
4. Pfaff M., Liu S., Erle D.J., Ginsberg M.H. Integrin β cytoplasmic domains differentially bind to cytoskeletal proteins. J Biol Chem. 273:1998;6104-6109. The authors demonstrate that dimerised β1 integrin cytoplasmic domains bind talin and filamin in vitro.
5. Sampath R., Gallagher P.J., Pavalko F.M. Cytoskeletal interactions with the leukocyte integrin β2 cytoplasmic tail. Activation-dependent regulation of associations with talin and α-actinin. J Biol Chem. 273:1998;33588-33594. β2 integrins are shown to coimmunoprecipitate with talin in resting but not activated polymorhonuclear leukocytes. In activated cells, talin was cleaved to the 220 kDa carboxy-terminal tail fragment, and β2-integrin was associated with α-actinin, not talin. Evidence is presented that the α-actinin-binding site in the integrin cytoplasmic domain (residues 736-746) is negatively regulated by residues 748-762.
6. 3 (GPIIB-IIIA) to talin. J Biol Chem. 271:1996;16416-16421.
7. Retta S.F., Balzac F., Ferraris P., Belkin A.M., Fassler R., Humphries M.J., De Leo G., Silengo L., Tarone G. β1-Integrin cytoplasmic subdomains involved in dominant negative function. Mol Biol Cell. 9:1998;715-731. Expression of the β1B integrin splice variant is shown to inhibit β1A- and β3/β5-mediated cell spreading, FA formation, FAK tyrosine phosphorylation and fibronectin matrix assembly.
8. Hemmings L., Rees D.J.G., Ohanian V., Bolton S.J., Gilmore A.P., Patel N., Priddle H., Trevithick J.E., Hynes R.O., Critchley D.R. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site. J Cell Sci. 109:1996;2715-2726.
9. McCann R.O., Craig S.W. The I/LWEQ module: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals. Proc Natl Acad Sci USA. 94:1997;5679-5684.
10. Kalchman M.A., Koide H.B., McCutcheon K., Graham R.K., Nichol K., Nishiyama K., KazemiEsfarjani P., Lynn F.C., Wellington C., Metzler M.et al. HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain. Nat Genet. 16:1997;44-53.
11. Schmidt J.M., Zhang J., Lee H-S., Stromer M.H., Robson R.M. Interaction of talin with actin: sensitive modulation of filament crosslinking activity. Arch Biochem Biophys. 366:1999;139-150.
12. Borowsky M.L., Hynes R.O. Layilin, a novel talin-binding transmembrane protein homologous with C-type lectins, is localized in membrane ruffles. J Cell Biol. 143:1998;429-442. The authors demonstrate that the integral membrane protein layilin binds to the talin head and colocalises with talin and F-actin in membrane ruffles. The FAK-binding site in talin was localised to the head domain.
13. Bass M.D., Smith B.J., Prigent S.A., Critchley D.R. Talin contains three similar vinculin-binding sites predicted to form an amphipathic helix. Biochem J. 341:1999;257-263. This paper describes the identification of three short talin peptides that bind vinculin using a yeast two-hybrid assay.
14. Horwitz A., Duggan K., Buck C., Beckerle M.C., Burridge K. Interaction of plasma-membrane fibronectin receptor with talin - a transmembrane linkage. Nature. 320:1986;531-533.
15. Nuckolls G.H., Turner C.E., Burridge K. Functional studies of the domains of talin. J Cell Biol. 110:1990;1635-1644.
16. Calderwood D.A., Zent R., Grant R., Rees D.J.G., Hynes R.O., Ginsburg M.H. The talin head domain binds to integrin β subunit cytoplasmic tails and regulates integrin activation. J Biol Chem. 274:1999;28071-28074. This paper contains compelling evidence that β1A, β1D and β3-integrin cytoplasmic domains bind specifically to both the talin head and rod domain in vitro. In addition it includes data that suggest that this interaction negatively regulates integrin activation.
17. Priddle H., Hemmings L., Monkley S., Woods A., Patel B., Sutton D., Dunn G.A., Zicha D., Critchley D.R. Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated ES cells. J Cell Biol. 142:1998;1121-1133. The authors demonstrate that talin, but not vinculin, is essential for FA formation in undifferentiated mouse embryonic stem cells, and that talin(-/-) cells have reduced motility and polarity compared with vinculin(-/-) cells.
18. Zamir E., Katz B-Z., Aota S., Yamada K.M., Geiger B., Kam Z. Molecular diversity of cell-matrix adhesions. J Cell Sci. 112:1999;1655-1669. Using fluorescence ratio imaging, the authors found that cell-matrix junctions in REF-52 cells are heterogeneous. Some of the junctions were rich in vinculin, paxillin and phosphotyrosine, whereas others were rich in tensin and contained little phosphotyrosine.
19. Tsujioka M., Machesky L.M., Cole S.L., Yahata K., Inouye K. A unique talin homologue with a villin headpiece-like domain is required for multicellular morphogenesis in Dictyostelium. Curr Biol. 9:1999;389-392. Studying Dictyostelium, the authors report that unlike talA mutants, which show defects in cell movement, aggregation and cytokinesis, talB mutants show no apparent defect at the cellular level, but fail to differentiate into slugs.
20. 2. Interestingly, a talin-related peptide is shown to displace the vinculin head-tail interaction, unmasking the actin-binding site.
21. Gilmore A.P., Burridge K. Regulation of vinculin binding to talin and actin by phosphatidylinositol-4-5-bisphosphate. Nature. 381:1996;531-535.
22. Weekes J., Barry S.T., Critchley D.R. Acidic phospholipids inhibit the intramolecular association between the N- and C-terminal regions of vinculin, exposing actin-binding and protein kinase C phosphorylation sites. Biochem J. 314:1996;827-832.
23. Huttelmaier S., Mayboroda O., Harbeck B., Jarchau T., Jockusch B.M., Rudiger M. The interaction of the cell-contact proteins VASP and vinculin is regulated by phosphatidylinositol-4,5-bisphosphate. Curr Biol. 8:1998;479-488.
24. Johnson R.P., Niggli V., Durrer P., Craig S.W. A conserved motif in the tail domain of vinculin mediates association with and insertion into acidic phospholipid bilayers. Biochemistry. 37:1998;10211-10222. Residues 916-970 in the vinculin tail are shown to insert into acidic phospholipid vesicles. This site of activity is masked in intact vinculin but is revealed by cycles of freeze thawing or in low-salt buffers.
25. Bakolitsa C., de-Pereda J.M., Bagshaw C.R., Critchley D.R., Liddington R.C. Crystal structure of the viriculin tail suggests a pathway for activation. Cell. 99:1999;603-613.
26. Huttelmaier S., Bubeck P., Rudiger M., Jockusch B.M. Characterisation of two F-actin-binding and oligomerisation sites in the cell-contact protein vinculin. Eur J Biochem. 247:1997;1136-1142.
27. Winkler J., Lunsdorf H., Jockusch B.M. The ultrastructure of chicken gizzard vinculin as visualised by high-resolution electron microscopy. J Struct Biol. 116:1996;270-277.
28. Isenberg G., Goldmann W.H. Peptide-specific antibodies localise the major lipid binding sites of talin dimers to oppositely arranged N-terminal 47 kDa subdomains. FEBS Lett. 426:1998;165-170.
29. Goldmann W.H., Niggli V., Kaufmann S., Isenberg G. Probing actin and liposome interaction of talin and talin vinculin complexes - a kinetic, thermodynamic and lipid labeling study. Biochemistry. 31:1992;7665-7671.
30. Machesky L.M., Insall R.H. Signalling to actin dynamics. J Cell Biol. 146:1999;267-272. This article reviews the role of Cdc42, ARP2/3, WASP, VASP and gelsolin in actin dynamics.
31. Volberg T., Geiger B., Kam Z., Pankov R., Simcha I., Sabanay H., Coll J-L., Adamson E., Ben-Ze'ev A. Focal adhesion formation by F9 embryonal carcinoma cells after vinculin gene disruption. J Cell Sci. 108:1995;2253-2260.
32. Rodriguez Fernanedez J.L., Geiger B., Salomon D., Ben-Ze'ev A. Overexpression of vinculin suppresses cell motility in Balb/c 3T3 cells. Cell Motil Cytoskeleton. 22:1992;127-134.
33. Rodriguez Fernandez J.L., Geiger B., Salomon D., Ben-Ze'ev A. Suppression of vinculin expression by antisense transfection confers changes in cell morphology, motility, and anchorage-dependent growth of 3T3-cells. J Cell Biol. 122:1993;1285-1294.
34. Xu W., Baribault H., Adamson E.D. Vinculin knockout results in heart and brain defects during embryonic development. Development. 125:1998;327-337. This paper describes the detailed characterisation of the effects of vinculin knockout on mouse embryonic development.
35. Fassler R., Meyer M. Consequences of lack of β-1 integrin gene-expression in mice. Genes Dev. 9:1995;1896-1908.
36. Illc D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T., Alzawa S. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 377:1995;539-544.
37. Loo D.T., Kanner S.B., Aruffo A. Filamin binds to the cytoplasmic domain of the β1-integrin. J Biol Chem. 273:1998;23304-23312. Filamin was pulled out of a yeast two-hybrid screen of an activated T-cell cDNA library using the β1-integrin cytoplasmic domain as bait; the interaction was confirmed by co-immunoprecipitation, and the binding sites in integrin and filamin were mapped.
38. Fox J.W., Lamperti E.D., Eksioglu Y.Z., Hong S.E., Feng Y., Graham D.A., Scheffer I.E., Dobyns W.B., Hirsch B.A., Radtke R.A.et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron. 21:1998;1315-1325. Filamin 1 (FLN-1) is identified as the gene mutated in the X-linked dominant human disorder periventricular heterotopia. Mutations are embryonic lethal in males; in females, they are characterised by defects in the migration of cerebral cortical neurons and vascular abnormalities.
39. Cunningham C.C., Gorlin J.B., Kwiatkowski D.J., Janmey P.A., Byers H.R., Stossel T.P. Actin-binding protein requirement for cortical stability and efficient locomotion. Science. 255:1992;325-327.
40. Critchley D.R. Talin. Kreis T., Vale R. Guidebook to the Cytoskeletal and Motor Proteins, edn 2. 1999;141-144 Oxford University Press, Oxford. A concise review of talin structure and function.
41. Hock R.S. Filamin. Kreis T., Vale R. Guidebook to the Cytoskeletal and Motor Proteins, edn 2. 1999;94-97 Oxford University Press, Oxford. A concise review of filamin structure and function.
42. Critchley D.R., Flood G. α-Actinins. Kreis T., Vale R. Guidebook to the Cytoskeletal and Motor Proteins, edn 2. 1999;24-27 Oxford University Press, Oxford.
43. Hobert O., Schilling J.W., Beckerle M.C., Ullrich A., Jallal B. SH3 domain-dependent interaction of the proto-oncogene product Vav with the focal contact protein zyxin. Oncogene. 12:1996;1577-1581.
44. Fischer K.D., Kong Y.Y., Nishina H., Tedford K., Marengere L.E.M., Kozieradzki I., Sasaki T., Starr M., Chan G., Gardener S.et al. Vav is a regulator of cytoskeletal reorganization mediated by the T-cell receptor. Curr Biol. 8:1998;554-562. The guanine nucleotide exchange factor Vav is shown to coimmunoprecipitate with talin and vinculin in T-cells.
45. Yron I., Deckert M., Reff M.E., Munshi A., Schwartz M.A., Altman A. Integrin-dependent tyrosine phosphorylation and growth regulation by Vav. Cell Adhes Commun. 7:1999;1-11.
46. Mukai H., Toshimori M., Shibata H., Takanaga H., Kitagawa M., Miyahara M., Shimakawa M., Ono Y. Interaction of PKN with α-actinin. J Biol Chem. 272:1997;4740-4746.
47. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-mediated cell migration. J Cell Sci. 112:1999;2677-2691. FAK null cells were used to study focal adhesion kinase activity by expressing a variety of FAK mutants. Evidence is presented in this paper that FAK activity, the Tyr397-SH2 domain binding site, and the first proline-rich SH3 binding site are all required to promote maximal cell migration, whereas paxillin binding is not required.
48. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., Stossel T.P. The Ras related small GTPases Rac, Rho, Cdc42, and RalA bind filamin. Proc Natl Acad Sci USA. 96:1999;2122-2128. Ral1A is reported to bind filamin in a GTP-dependent manner and to act downstream of Cdc42 in filopod formation.
49. Glogauer M., Arora P., Chou D., Janmey P.A., Downey G.P., McCulloch C.A.G. The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J Biol Chem. 273:1998;1689-1698.
50. Kioka N., Sakata S., Kawauchi T., Amachi T., Akiyama S.K., Okazaki K., Yaen C., Yamada K.M., Aota S. Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organisation. J Cell Biol. 144:1999;59-69. Vinexin was identified in a yeast two-hybrid screen using the proline-rich region of chicken vinculin as bait. Two splice variants (82 kDa and 37 kDa) with variable amino-terminal domains were identified, both of which localise to FAs when expressed in NIH 3T3 fibroblast cells, increase the size of FAs and actin stress fibres, and enhance cell spreading on fibronectin.
51. Mandai K., Nakanishi H., Satoh A., Takahashi K., Satoh K., Nishioka H., Mizoguchi A., Takai Y. Ponsin/SH3P12: an 1-afadin- and vinculin-binding protein localized at cell-cell and cell-matrix adherens junctions. J Cell Biol. 144:1999;1001-1017. Ponsin (also known as SH3P12 and CAP) contains three SH3 domains in the carboxy-terminal half of the protein and has limited sequence homology to vinexin. There are numerous splice variants, two of which have variable amino-terminal regions. Ponsin has been localised to both cell-cell and cell-matrix junctions, and it binds to vinculin via the first two SH3 domains.
52. Ribon V., Herrera R., Kay B.K., Saltiel A.R. A role for CAP, a novel multifunctional src homology 3 domain-containing protein in formation of actin stress fibers and focal adhesions. J Biol Chem. 273:1998;4073-4080. CAP (ponsin/SH3P12) is shown to bind FAK via the middle SH3 domain (this interaction would be expected to be competitive with vinculin), and to c-Cbl and Sos via the carboxy-terminal SH3 domain.
53. Norman J.C., Jones D., Barry S.T., Holt M.R., Cockcroft S., Critchley D.R. ARF1 mediates paxillin recruitment to focal adhesions and potentiates rho-stimulated stress fibre formation in intact and permeabilised Swiss 3T3 cells. J Cell Biol. 143:1998;1981-1995. Identifies a novel role for the ARF-1 GTPase in targeting paxillin from a perinuclear compartment in serum-starved Swiss 3T3 cells to FA-like structures.
54. Brown M.C., Perotta J.A., Turner C.E. Serine and threonine phosphorylation of the paxillin LIM domains regulates paxillin focal adhesion localisation and cell adhesion to fibronectin. Mol Biol Cell. 9:1998;1803-1816. Phosphorylation of serine residues 457 and 481 in the LIM3 domain is shown to be required for efficient targeting of paxillin to Fas. LIM3 kinase activity is also demonstrated to be adhesion dependent.
55. Turner C.E., Brown M.C., Perotta J.A., Riedy M.C., Nikolopoulos S.N., McDonald A.R., Bagrodia S., Thomas S., Leventhal P.S. Paxillin LD4 motif binds PAK and Pix through a novel 95-kDa ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodelling. J Cell Biol. 145:1999;851-863. The paxillin LD4 motif is shown to bind FAK and to a protein complex containing PAK, Nck and Pix. Binding of the complex is mediated by a novel 95 kDa protein that is localised to FAs.
56. Shen Y., Schneider G., Cloutier J-F., Veilette A., Schaller M.D. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J Biol Chem. 273:1998;6474-6481. The carboxy-terminal region of FAK is shown to bind indirectly to PTP-PEST via paxillin.
57. CAS and FAK.