DOI: 10.1083/jcb.150.3.627. Restructuring of Focal Adhesion Plaques by Pi 3-Kinase

Restructuring of Focal Adhesion Plaques by Pi 3-Kinase

10.1083/jcb.150.3.627

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Focal adhesions are an elaborate network of interconnecting proteins linking actin stress fibers to the extracellular matrix substrate. Modulation of the focal adhesion plaque provides a mechanism for the regulation of cellular adhesive strength. Using interference reflection microscopy, we found that activation of phosphoinositide 3-kinase (PI 3-kinase) by PDGF induces the dissipation of focal adhesions. Loss of this close apposition between the cell membrane and the extracellular matrix coincided with a redistribution of α-actinin and vinculin from the focal adhesion complex to the Triton X-100–soluble fraction. In contrast, talin and paxillin remained localized to focal adhesions, suggesting that activation of PI 3-kinase induced a restructuring of the plaque rather than complete dispersion. Furthermore, phosphatidylinositol (3,4,5)-trisphosphate (PtdIns (3,4,5)-P3), a lipid product of PI 3-kinase, was sufficient to induce restructuring of the focal adhesion plaque. We also found that PtdIns (3,4,5)-P3 binds to α-actinin in PDGF-treated cells. Further evidence demonstrated that activation of PI 3-kinase by PDGF induced a decrease in the association of α-actinin with the integrin β subunit, and that PtdIns (3,4,5)-P3 could disrupt this interaction in vitro. Modification of focal adhesion structure by PI 3-kinase and its lipid product, PtdIns (3,4,5)-P3, has important implications for the regulation of cellular adhesive strength and motility.

Bibliography

Greenwood, J. A., Theibert, A. B., Prestwich, G. D., & Murphy-Ullrich, J. E. (2000). Restructuring of Focal Adhesion Plaques by Pi 3-Kinase. The Journal of Cell Biology, 150(3), 627â642.

Authors 4

Jeffrey A. Greenwood (first)
Anne B. Theibert (additional)
Glenn D. Prestwich (additional)
Joanne E. Murphy-Ullrich (additional)

References 73 Referenced 106

10.1091/mbc.10.3.581 / Mol. Biol. Cell. / GCS1, an arf guanosine triphosphate-activating protein in Saccharomyces cerevisiae, is required for normal actin cytoskeletal organization in vivo and stimulates actin polymerization in vitro by Blader (1999)
10.1007/BF01758424 / J. Muscle Res. Cell Motil / The structure and function of α-actinin by Blanchard (1989)
10.1126/science.282.5387.293 / Science. / Bifurcation of lipid and protein kinase signals of PI3Kγ to the protein kinases PKB and MAPK by Bondeva (1998)
10.1038/314469a0 / Nature. / Diacylglycerol in large α-actinin/actin complexes and in the cytoskeleton of activated platelets by Burn (1985)
10.1146/annurev.cellbio.12.1.463 / Annu. Rev. Cell Dev. Biol. / Focal adhesions, contractility, and signaling by Burridge (1996)
10.1016/0092-8674(91)90639-G / Cell. / Oncogenes and signal transduction by Cantley (1991)
10.1073/pnas.96.8.4240 / Proc. Natl. Acad. Sci. USA. / New insights into tumor suppressionPTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway by Cantley (1999)
10.1016/S0955-0674(96)80060-3 / Curr. Opin. Cell Biol. / Phosphoinositide kinases by Carpenter (1996)
{'key': '2023072902223409400_ChellaiahandHruska1996', 'first-page': '743', 'article-title': 'Osteopontin stimulates gelsolin-associated phosphoinositide levels and phosphatidylinositol triphosphate-hydroxyl kinase', 'volume': 'Cell. 7', 'author': 'Chellaiah', 'year': '1996', 'journal-title': 'Mol. Biol'} / Mol. Biol / Osteopontin stimulates gelsolin-associated phosphoinositide levels and phosphatidylinositol triphosphate-hydroxyl kinase by Chellaiah (1996)
10.1016/0092-8674(94)90259-3 / Cell. / The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells by Chong (1994)
10.1083/jcb.133.6.1403 / J. Cell Biol. / Rho-stimulated contractility drives the formation of stress fibers and focal adhesions by Chrzanowska-Wodnicka (1996)
10.1242/jcs.39.1.149 / J. Cell Sci. / The behaviour of fibroblasts migrating from chick heart explantschanges in adhesion, locomotion and growth, and in the distribution of actomyosin and fibronectin by Couchman (1979)
10.1002/(SICI)1097-4644(19960616)61:4<578::AID-JCB11>3.0.CO;2-C / J. Cell. Biochem. / Syndecans, signaling, and cell adhesion by Couchman (1996)
10.1016/S0955-0674(96)80051-2 / Curr. Opin. Cell Biol / Assembly of focal adhesionsprogress, paradigms, and portents by Craig (1996)
10.1074/jbc.272.10.6465 / J. Biol. Chem. / The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C by Derman (1997)
10.1016/S0006-3495(91)82027-6 / Biophys. J. / Mathematical model for the effects of adhesion and mechanics on cell migration speed by DiMilla (1991)
10.1083/jcb.122.3.729 / J. Cell Biol. / Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength by DiMilla (1993)
10.1242/jcs.105.2.489 / J. Cell Sci. / Controlled induction of focal adhesion disassembly and migration in primary fibroblasts by Dunlevy (1993)
10.1242/jcs.92.1.67 / J. Cell Sci. / The distribution of distinct integrins in focal contacts is determined by the substratum composition by Fath (1989)
10.1126/science.275.5300.665 / Science. / Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate by Franke (1997)
10.1038/359150a0 / Nature. / Requirement of phosphatidylinositol 4,5-bisphosphate for α-actinin function by Fukami (1992)
10.1101/SQB.1992.057.01.069 / Cold Spring Harbor Symp. Quant. Biol. / Cytoplasmic control of cell adhesion by Geiger (1992)
10.1083/jcb.146.4.869 / J. Cell Biol. / Intracellular movement of green fluorescent protein-tagged phosphatidylinositol 3-kinase in response to growth factor receptor signaling by Gillham (1999)
{'key': '2023072902223409400_GilmoreandBurridge1996', 'first-page': '531', 'article-title': 'Regulation of vinculin binding to talin and actin by phosphatidylinositol-4,5-bisphosphate', 'volume': '381', 'author': 'Gilmore', 'year': '1996', 'journal-title': 'Science.'} / Science. / Regulation of vinculin binding to talin and actin by phosphatidylinositol-4,5-bisphosphate by Gilmore (1996)
10.1242/jcs.107.7.1773 / J. Cell Sci. / Modulation of α-actinin levels affects cell motility and confers tumorigenicity on 3T3 cells by Gluck (1994)
10.1002/(SICI)1097-0029(19981201)43:5<420::AID-JEMT8>3.0.CO;2-B / Microsc. Res. Tech / Signaling of de-adhesion in cellular regulation and motility by Greenwood (1998)
10.1074/jbc.273.3.1755 / J. Biol. Chem. / Thrombospondin signaling of focal adhesion disassembly requires activation of phosphoinositide 3-kinase by Greenwood (1998)
10.1016/S0092-8674(00)81279-9 / Cell. / Cell adhesionthe molecular basis of tissue architecture and morphogenesis by Gumbiner (1996)
10.1126/science.279.5350.509 / Science. / Rho GTPases and the actin cytoskeleton by Hall (1998)
10.1074/jbc.271.31.18859 / J. Biol. Chem. / Identification and cloning of centaurin-αa novel phosphatidylinositol 3,4,5-trisphosphate-binding protein from rat brain by Hammonds-Odie (1996)
10.1126/science.279.5350.558 / Science. / Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav by Han (1998)
10.1016/S0960-9822(95)00080-7 / Curr. Biol / PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase by Hawkins (1995)
{'key': '2023072902223409400_Heldinetal1998', 'first-page': 'F79', 'article-title': 'Signal transduction via platelet-derived growth factor receptors', 'volume': '1378', 'author': 'Heldin', 'year': '1998', 'journal-title': 'Biochim. Biophys. Acta.'} / Biochim. Biophys. Acta. / Signal transduction via platelet-derived growth factor receptors by Heldin (1998)
10.1074/jbc.273.28.17817 / J. Biol. Chem. / Lipid products of phosphoinositide 3-kinase and phosphatidylinositol 4′,5′-bisphosphate are both required for ADP-dependent platelet spreading by Heraud (1998)
10.1016/S0955-0674(98)80144-0 / Curr. Opin. Cell Biol. / Integrin signaling and cell growth control by Howe (1998)
10.1083/jcb.134.6.1551 / J. Cell Biol. / Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity by Huttenlocher (1996)
10.1242/jcs.21.1.129 / J. Cell Sci. / Cell-to-substrate contacts in living fibroblastsan interference reflexion study with an evaluation of the technique by Izzard (1976)
10.1146/annurev.ph.56.030194.001125 / Annu. Rev. Physiol / Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly by Janmey (1994)
10.1074/jbc.273.18.11017 / J. Biol. Chem. / Membrane-permeant esters of phosphatidylinositol 3,4,5-trisphosphate by Jiang (1998)
10.1006/bbrc.1995.1641 / Biochem. Biophys. Res. Commun / The carboxy-terminal tail domain of vinculin contains a cryptic binding site for acidic phospholipids by Johnson (1995)
10.1038/37656 / Nature. / Cdc42 and Rac 1 induce integrin-mediated cell motility and invasiveness through PI(3)K by Keely (1997)
10.1074/jbc.272.1.466 / J. Biol. Chem. / Selective recognition of phosphatidylinositol 3,4,5-trisphosphate by a synthetic peptide by Lu (1997)
10.1021/bi961878z / Biochemistry. / Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity by Lu (1996)
10.1016/S0962-8924(99)01519-6 / Trends Cell Biol / PTENa tumor suppressor that functions as a phospholipid phosphatase by Maehama (1999)
10.1210/edrv-17-3-207 / Endocr. Rev. / The regulation of growth and intracellular signaling by integrins by Meredith (1996)
10.1083/jcb.131.3.791 / J. Cell Biol. / Integrin functionmolecular hierarchies of cytoskeletal and signaling molecules by Miyamoto (1995)
10.1083/jcb.135.6.1633 / J. Cell Biol. / Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activationroles of integrin aggregation and occupancy of receptors by Miyamoto (1996)
10.4052/tigg.7.89 / Trends GlycoSci. Glycotechnol / Anti-adhesive proteins of the extracellular matrixthrombospondin, tenascin, and SPARC by Murphy-Ullrich (1995)
10.1083/jcb.109.3.1309 / J. Cell Biol. / Thrombospondin modulates focal adhesions in endothelial cells by Murphy-Ullrich (1989)
10.1083/jcb.115.4.1127 / J. Cell Biol. / Focal adhesion integrity is downregulated by the alternatively spliced domain of human tenascin by Murphy-Ullrich (1991)
10.1016/S0021-9258(19)74381-6 / J. Biol. Chem. / Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity by Murphy-Ullrich (1993)
10.1002/jcb.240570218 / J. Cell. Biochem / SPARC mediates focal adhesion disassembly in endothelial cells through a follistatin-like region and the Ca++-binding EF-hand by Murphy-Ullrich (1995)
10.1242/jcs.109.10.2499 / J. Cell Sci. / Cyclic GMP-dependent protein kinase is required for thrombospondin and tenascin mediated focal adhesion disassembly by Murphy-Ullrich (1996)
10.1016/S0021-9258(19)36909-1 / J. Biol. Chem. / Mapping of the α-actinin binding site with the β1 integrin cytoplasmic domain by Otey (1993)
10.1038/385537a0 / Nature. / Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness by Palecek (1997)
10.1042/bst0191065 / Biochem. Soc. Trans. / Alpha-actinina direct link between actin and integrins by Pavalko (1991)
10.1006/excr.1995.1119 / Exp. Cell Res. / Immunodetection of alpha-actinin in focal adhesions is limited by antibody inaccessibility by Pavalko (1995)
{'key': '2023072902223409400_Plopperetal1995', 'first-page': '1349', 'article-title': 'Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex', 'volume': 'Cell. 6', 'author': 'Plopper', 'year': '1995', 'journal-title': 'Mol. Biol'} / Mol. Biol / Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex by Plopper (1995)
10.1074/jbc.274.18.12361 / J. Biol. Chem. / Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration by Reiske (1999)
10.1074/jbc.274.2.1131 / J. Biol. Chem. / Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent Raf-1 translocation to the plasma membrane and the activation of the mitogen-activated protein kinase pathway by Rizzo (1999)
10.1002/cm.970220206 / Cell Motil. Cytoskeleton. / Overexpression of vinculin suppress cell motility in Balb/C 3T3 cells by Rodriguez Fernandez (1992)
10.1083/jcb.122.6.1285 / J. Cell Biol. / Suppression of vinculin expression by antisense transfection confers changes in cell morphology, motility, and anchorage-dependent growth of 3T3 cells by Rodriguez Fernandez (1993)
10.1016/S0092-8674(00)80226-3 / Cell. / Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras by Rodriguez-Viciana (1997)
10.1074/jbc.273.50.33588 / J. Biol. Chem. / Cytoskeletal interactions with the leukocyte integrin β2 cytoplasmic tail by Sampath (1998)
10.1016/S0092-8674(00)80486-9 / Cell. / Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion by Shaw (1997)
{'key': '2023072902223409400_Theibertetal1997'}
10.1038/42648 / Nature. / Signalling through the lipid products of phosphoinositide-3-OH kinase by Toker (1997)
10.1074/jbc.270.49.29525 / J. Biol. Chem. / Phosphorylation of the platelet p47 phosphoprotein is mediated by the lipid products of phosphoinositide 3-kinase by Toker (1995)
10.1242/jcs.75.1.279 / J. Cell Sci. / Interference reflection microscopy in cell biologymethodology and applications by Verschueren (1985)
10.1016/S0006-3495(93)81059-2 / Biophys. J. / Affinity of α-actinin for actin determines the structural and mechanical properties of actin filament gels by Wachsstock (1993)
10.1016/S0960-9822(00)00087-7 / Curr. Biol / Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling by Wennstrom (1994)
{'key': '2023072902223409400_Wennstrometal1994b', 'first-page': '651', 'article-title': 'Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase', 'volume': '9', 'author': 'Wennstrom', 'year': '1994', 'journal-title': 'Oncogene'} / Oncogene / Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase by Wennstrom (1994)
10.1242/jcs.101.2.277 / J. Cell Sci. / Protein kinase C involvement in focal adhesion formation by Woods (1992)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 10:24 p.m.)
Indexed	1 month, 1 week ago (July 19, 2025, 11:41 p.m.)
Issued	25 years ago (Aug. 7, 2000)
Published	25 years ago (Aug. 7, 2000)
Published Online	25 years ago (Aug. 7, 2000)
Published Print	25 years ago (Aug. 7, 2000)

Funders 0

None

BibTeX

@article{Greenwood_2000, title={Restructuring of Focal Adhesion Plaques by Pi 3-Kinase}, volume={150}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.150.3.627}, DOI={10.1083/jcb.150.3.627}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Greenwood, Jeffrey A. and Theibert, Anne B. and Prestwich, Glenn D. and Murphy-Ullrich, Joanne E.}, year={2000}, month=aug, pages={627–642} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        20
      ]
    ],
    "date-time": "2025-07-20T03:41:38Z",
    "timestamp": 1752982898036
  },
  "reference-count": 73,
  "publisher": "Rockefeller University Press",
  "issue": "3",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        8,
        7
      ]
    ]
  },
  "abstract": "<jats:p>Focal adhesions are an elaborate network of interconnecting proteins linking actin stress fibers to the extracellular matrix substrate. Modulation of the focal adhesion plaque provides a mechanism for the regulation of cellular adhesive strength. Using interference reflection microscopy, we found that activation of phosphoinositide 3-kinase (PI 3-kinase) by PDGF induces the dissipation of focal adhesions. Loss of this close apposition between the cell membrane and the extracellular matrix coincided with a redistribution of \u03b1-actinin and vinculin from the focal adhesion complex to the Triton X-100\u2013soluble fraction. In contrast, talin and paxillin remained localized to focal adhesions, suggesting that activation of PI 3-kinase induced a restructuring of the plaque rather than complete dispersion. Furthermore, phosphatidylinositol (3,4,5)-trisphosphate (PtdIns (3,4,5)-P3), a lipid product of PI 3-kinase, was sufficient to induce restructuring of the focal adhesion plaque. We also found that PtdIns (3,4,5)-P3 binds to \u03b1-actinin in PDGF-treated cells. Further evidence demonstrated that activation of PI 3-kinase by PDGF induced a decrease in the association of \u03b1-actinin with the integrin \u03b2 subunit, and that PtdIns (3,4,5)-P3 could disrupt this interaction in vitro. Modification of focal adhesion structure by PI 3-kinase and its lipid product, PtdIns (3,4,5)-P3, has important implications for the regulation of cellular adhesive strength and motility.</jats:p>",
  "DOI": "10.1083/jcb.150.3.627",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:45:41Z",
    "timestamp": 1027701941000
  },
  "page": "627-642",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 106,
  "title": "Restructuring of Focal Adhesion Plaques by Pi 3-Kinase",
  "prefix": "10.1083",
  "volume": "150",
  "author": [
    {
      "given": "Jeffrey A.",
      "family": "Greenwood",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aDepartment of Pathology, Division of Molecular and Cellular Pathology,"
        }
      ]
    },
    {
      "given": "Anne B.",
      "family": "Theibert",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "bDepartment of Neurobiology, University of Alabama at Birmingham, Birmingham, Alabama 35294"
        }
      ]
    },
    {
      "given": "Glenn D.",
      "family": "Prestwich",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "cDepartment of Medicinal Chemistry, University of Utah, Salt Lake City, Utah 84112"
        }
      ]
    },
    {
      "given": "Joanne E.",
      "family": "Murphy-Ullrich",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Pathology, Division of Molecular and Cellular Pathology,"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2000,
        8,
        7
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072902223409400_Bladeretal1999",
      "doi-asserted-by": "crossref",
      "first-page": "581",
      "DOI": "10.1091/mbc.10.3.581",
      "article-title": "GCS1, an arf guanosine triphosphate-activating protein in Saccharomyces cerevisiae, is required for normal actin cytoskeletal organization in vivo and stimulates actin polymerization in vitro",
      "volume": "10",
      "author": "Blader",
      "year": "1999",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902223409400_Blanchardetal1989",
      "doi-asserted-by": "crossref",
      "first-page": "280",
      "DOI": "10.1007/BF01758424",
      "article-title": "The structure and function of \u03b1-actinin",
      "volume": "10",
      "author": "Blanchard",
      "year": "1989",
      "journal-title": "J. Muscle Res. Cell Motil"
    },
    {
      "key": "2023072902223409400_Bondevaetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "293",
      "DOI": "10.1126/science.282.5387.293",
      "article-title": "Bifurcation of lipid and protein kinase signals of PI3K\u03b3 to the protein kinases PKB and MAPK",
      "volume": "282",
      "author": "Bondeva",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072902223409400_Burnetal1985",
      "doi-asserted-by": "crossref",
      "first-page": "469",
      "DOI": "10.1038/314469a0",
      "article-title": "Diacylglycerol in large \u03b1-actinin/actin complexes and in the cytoskeleton of activated platelets",
      "volume": "314",
      "author": "Burn",
      "year": "1985",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902223409400_BurridgeandChrzanowska-Wodnicka1996",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1146/annurev.cellbio.12.1.463",
      "article-title": "Focal adhesions, contractility, and signaling",
      "volume": "12",
      "author": "Burridge",
      "year": "1996",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "2023072902223409400_Cantleyetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "281",
      "DOI": "10.1016/0092-8674(91)90639-G",
      "article-title": "Oncogenes and signal transduction",
      "volume": "64",
      "author": "Cantley",
      "year": "1991",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902223409400_CantleyandNeel1999",
      "doi-asserted-by": "crossref",
      "first-page": "4240",
      "DOI": "10.1073/pnas.96.8.4240",
      "article-title": "New insights into tumor suppressionPTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway",
      "volume": "96",
      "author": "Cantley",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072902223409400_CarpenterandCantley1996",
      "doi-asserted-by": "crossref",
      "first-page": "153",
      "DOI": "10.1016/S0955-0674(96)80060-3",
      "article-title": "Phosphoinositide kinases",
      "volume": "8",
      "author": "Carpenter",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072902223409400_ChellaiahandHruska1996",
      "first-page": "743",
      "article-title": "Osteopontin stimulates gelsolin-associated phosphoinositide levels and phosphatidylinositol triphosphate-hydroxyl kinase",
      "volume": "Cell. 7",
      "author": "Chellaiah",
      "year": "1996",
      "journal-title": "Mol. Biol"
    },
    {
      "key": "2023072902223409400_Chongetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1016/0092-8674(94)90259-3",
      "article-title": "The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells",
      "volume": "79",
      "author": "Chong",
      "year": "1994",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902223409400_Chrzanowska-WodnickaandBurridge1996",
      "doi-asserted-by": "crossref",
      "first-page": "1403",
      "DOI": "10.1083/jcb.133.6.1403",
      "article-title": "Rho-stimulated contractility drives the formation of stress fibers and focal adhesions",
      "volume": "133",
      "author": "Chrzanowska-Wodnicka",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_N0x3052130N0x37dc448",
      "doi-asserted-by": "crossref",
      "first-page": "149",
      "DOI": "10.1242/jcs.39.1.149",
      "article-title": "The behaviour of fibroblasts migrating from chick heart explantschanges in adhesion, locomotion and growth, and in the distribution of actomyosin and fibronectin",
      "volume": "39",
      "author": "Couchman",
      "year": "1979",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_CouchmanandWoods1996",
      "doi-asserted-by": "crossref",
      "first-page": "578",
      "DOI": "10.1002/(SICI)1097-4644(19960616)61:4<578::AID-JCB11>3.0.CO;2-C",
      "article-title": "Syndecans, signaling, and cell adhesion",
      "volume": "61",
      "author": "Couchman",
      "year": "1996",
      "journal-title": "J. Cell. Biochem."
    },
    {
      "key": "2023072902223409400_CraigandJohnson1996",
      "doi-asserted-by": "crossref",
      "first-page": "74",
      "DOI": "10.1016/S0955-0674(96)80051-2",
      "article-title": "Assembly of focal adhesionsprogress, paradigms, and portents",
      "volume": "8",
      "author": "Craig",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol"
    },
    {
      "key": "2023072902223409400_Dermanetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "6465",
      "DOI": "10.1074/jbc.272.10.6465",
      "article-title": "The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C",
      "volume": "272",
      "author": "Derman",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_DiMillaetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1016/S0006-3495(91)82027-6",
      "article-title": "Mathematical model for the effects of adhesion and mechanics on cell migration speed",
      "volume": "60",
      "author": "DiMilla",
      "year": "1991",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072902223409400_DiMillaetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "729",
      "DOI": "10.1083/jcb.122.3.729",
      "article-title": "Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength",
      "volume": "122",
      "author": "DiMilla",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_N0x3052130N0x1d0bc90",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1242/jcs.105.2.489",
      "article-title": "Controlled induction of focal adhesion disassembly and migration in primary fibroblasts",
      "volume": "105",
      "author": "Dunlevy",
      "year": "1993",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_Fathetal1989",
      "doi-asserted-by": "crossref",
      "first-page": "67",
      "DOI": "10.1242/jcs.92.1.67",
      "article-title": "The distribution of distinct integrins in focal contacts is determined by the substratum composition",
      "volume": "92",
      "author": "Fath",
      "year": "1989",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_Frankeetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "665",
      "DOI": "10.1126/science.275.5300.665",
      "article-title": "Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate",
      "volume": "275",
      "author": "Franke",
      "year": "1997",
      "journal-title": "Science."
    },
    {
      "key": "2023072902223409400_Fukamietal1992",
      "doi-asserted-by": "crossref",
      "first-page": "150",
      "DOI": "10.1038/359150a0",
      "article-title": "Requirement of phosphatidylinositol 4,5-bisphosphate for \u03b1-actinin function",
      "volume": "359",
      "author": "Fukami",
      "year": "1992",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902223409400_Geigeretal1992",
      "doi-asserted-by": "crossref",
      "first-page": "631",
      "DOI": "10.1101/SQB.1992.057.01.069",
      "article-title": "Cytoplasmic control of cell adhesion",
      "volume": "52",
      "author": "Geiger",
      "year": "1992",
      "journal-title": "Cold Spring Harbor Symp. Quant. Biol."
    },
    {
      "key": "2023072902223409400_Gillhametal1999",
      "doi-asserted-by": "crossref",
      "first-page": "869",
      "DOI": "10.1083/jcb.146.4.869",
      "article-title": "Intracellular movement of green fluorescent protein-tagged phosphatidylinositol 3-kinase in response to growth factor receptor signaling",
      "volume": "146",
      "author": "Gillham",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_GilmoreandBurridge1996",
      "first-page": "531",
      "article-title": "Regulation of vinculin binding to talin and actin by phosphatidylinositol-4,5-bisphosphate",
      "volume": "381",
      "author": "Gilmore",
      "year": "1996",
      "journal-title": "Science."
    },
    {
      "key": "2023072902223409400_GluckandBen-Zeev1994",
      "doi-asserted-by": "crossref",
      "first-page": "1773",
      "DOI": "10.1242/jcs.107.7.1773",
      "article-title": "Modulation of \u03b1-actinin levels affects cell motility and confers tumorigenicity on 3T3 cells",
      "volume": "107",
      "author": "Gluck",
      "year": "1994",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_GreenwoodandMurphy-Ullrich1998",
      "doi-asserted-by": "crossref",
      "first-page": "420",
      "DOI": "10.1002/(SICI)1097-0029(19981201)43:5<420::AID-JEMT8>3.0.CO;2-B",
      "article-title": "Signaling of de-adhesion in cellular regulation and motility",
      "volume": "43",
      "author": "Greenwood",
      "year": "1998",
      "journal-title": "Microsc. Res. Tech"
    },
    {
      "key": "2023072902223409400_Greenwoodetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1755",
      "DOI": "10.1074/jbc.273.3.1755",
      "article-title": "Thrombospondin signaling of focal adhesion disassembly requires activation of phosphoinositide 3-kinase",
      "volume": "273",
      "author": "Greenwood",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Gumbiner1996",
      "doi-asserted-by": "crossref",
      "first-page": "345",
      "DOI": "10.1016/S0092-8674(00)81279-9",
      "article-title": "Cell adhesionthe molecular basis of tissue architecture and morphogenesis",
      "volume": "84",
      "author": "Gumbiner",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902223409400_Hall1998",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1126/science.279.5350.509",
      "article-title": "Rho GTPases and the actin cytoskeleton",
      "volume": "279",
      "author": "Hall",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072902223409400_Hammonds-Odieetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "18859",
      "DOI": "10.1074/jbc.271.31.18859",
      "article-title": "Identification and cloning of centaurin-\u03b1a novel phosphatidylinositol 3,4,5-trisphosphate-binding protein from rat brain",
      "volume": "271",
      "author": "Hammonds-Odie",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Hanetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "558",
      "DOI": "10.1126/science.279.5350.558",
      "article-title": "Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav",
      "volume": "279",
      "author": "Han",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072902223409400_Hawkinsetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "393",
      "DOI": "10.1016/S0960-9822(95)00080-7",
      "article-title": "PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase",
      "volume": "5",
      "author": "Hawkins",
      "year": "1995",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072902223409400_Heldinetal1998",
      "first-page": "F79",
      "article-title": "Signal transduction via platelet-derived growth factor receptors",
      "volume": "1378",
      "author": "Heldin",
      "year": "1998",
      "journal-title": "Biochim. Biophys. Acta."
    },
    {
      "key": "2023072902223409400_Heraudetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "17817",
      "DOI": "10.1074/jbc.273.28.17817",
      "article-title": "Lipid products of phosphoinositide 3-kinase and phosphatidylinositol 4\u2032,5\u2032-bisphosphate are both required for ADP-dependent platelet spreading",
      "volume": "273",
      "author": "Heraud",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Howeetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "220",
      "DOI": "10.1016/S0955-0674(98)80144-0",
      "article-title": "Integrin signaling and cell growth control",
      "volume": "10",
      "author": "Howe",
      "year": "1998",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072902223409400_Huttenlocheretal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1551",
      "DOI": "10.1083/jcb.134.6.1551",
      "article-title": "Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity",
      "volume": "134",
      "author": "Huttenlocher",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_IzzardandLochner1976",
      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1242/jcs.21.1.129",
      "article-title": "Cell-to-substrate contacts in living fibroblastsan interference reflexion study with an evaluation of the technique",
      "volume": "21",
      "author": "Izzard",
      "year": "1976",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_Janmey1994",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1146/annurev.ph.56.030194.001125",
      "article-title": "Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly",
      "volume": "56",
      "author": "Janmey",
      "year": "1994",
      "journal-title": "Annu. Rev. Physiol"
    },
    {
      "key": "2023072902223409400_Jiangetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "11017",
      "DOI": "10.1074/jbc.273.18.11017",
      "article-title": "Membrane-permeant esters of phosphatidylinositol 3,4,5-trisphosphate",
      "volume": "273",
      "author": "Jiang",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_JohnsonandCraig1995",
      "doi-asserted-by": "crossref",
      "first-page": "159",
      "DOI": "10.1006/bbrc.1995.1641",
      "article-title": "The carboxy-terminal tail domain of vinculin contains a cryptic binding site for acidic phospholipids",
      "volume": "210",
      "author": "Johnson",
      "year": "1995",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "2023072902223409400_Keelyetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "632",
      "DOI": "10.1038/37656",
      "article-title": "Cdc42 and Rac 1 induce integrin-mediated cell motility and invasiveness through PI(3)K",
      "volume": "390",
      "author": "Keely",
      "year": "1997",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902223409400_LuandChen1997",
      "doi-asserted-by": "crossref",
      "first-page": "466",
      "DOI": "10.1074/jbc.272.1.466",
      "article-title": "Selective recognition of phosphatidylinositol 3,4,5-trisphosphate by a synthetic peptide",
      "volume": "272",
      "author": "Lu",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Luetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "14027",
      "DOI": "10.1021/bi961878z",
      "article-title": "Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity",
      "volume": "35",
      "author": "Lu",
      "year": "1996",
      "journal-title": "Biochemistry."
    },
    {
      "key": "2023072902223409400_MaehamaandDixon1999",
      "doi-asserted-by": "crossref",
      "first-page": "125",
      "DOI": "10.1016/S0962-8924(99)01519-6",
      "article-title": "PTENa tumor suppressor that functions as a phospholipid phosphatase",
      "volume": "9",
      "author": "Maehama",
      "year": "1999",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2023072902223409400_Meredithetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "207",
      "DOI": "10.1210/edrv-17-3-207",
      "article-title": "The regulation of growth and intracellular signaling by integrins",
      "volume": "17",
      "author": "Meredith",
      "year": "1996",
      "journal-title": "Endocr. Rev."
    },
    {
      "key": "2023072902223409400_Miyamotoetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "791",
      "DOI": "10.1083/jcb.131.3.791",
      "article-title": "Integrin functionmolecular hierarchies of cytoskeletal and signaling molecules",
      "volume": "131",
      "author": "Miyamoto",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_Miyamotoetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1633",
      "DOI": "10.1083/jcb.135.6.1633",
      "article-title": "Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activationroles of integrin aggregation and occupancy of receptors",
      "volume": "135",
      "author": "Miyamoto",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_N0x3052130N0x3aeaa68",
      "doi-asserted-by": "crossref",
      "first-page": "89",
      "DOI": "10.4052/tigg.7.89",
      "article-title": "Anti-adhesive proteins of the extracellular matrixthrombospondin, tenascin, and SPARC",
      "volume": "7",
      "author": "Murphy-Ullrich",
      "year": "1995",
      "journal-title": "Trends GlycoSci. Glycotechnol"
    },
    {
      "key": "2023072902223409400_Murphy-UllrichandHook1989",
      "doi-asserted-by": "crossref",
      "first-page": "1309",
      "DOI": "10.1083/jcb.109.3.1309",
      "article-title": "Thrombospondin modulates focal adhesions in endothelial cells",
      "volume": "109",
      "author": "Murphy-Ullrich",
      "year": "1989",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_Murphy-Ullrichetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "1127",
      "DOI": "10.1083/jcb.115.4.1127",
      "article-title": "Focal adhesion integrity is downregulated by the alternatively spliced domain of human tenascin",
      "volume": "115",
      "author": "Murphy-Ullrich",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_Murphy-Ullrichetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "26784",
      "DOI": "10.1016/S0021-9258(19)74381-6",
      "article-title": "Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity",
      "volume": "268",
      "author": "Murphy-Ullrich",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Murphy-Ullrichetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "341",
      "DOI": "10.1002/jcb.240570218",
      "article-title": "SPARC mediates focal adhesion disassembly in endothelial cells through a follistatin-like region and the Ca++-binding EF-hand",
      "volume": "57",
      "author": "Murphy-Ullrich",
      "year": "1995",
      "journal-title": "J. Cell. Biochem"
    },
    {
      "key": "2023072902223409400_N0x3052130N0x38e3d40",
      "doi-asserted-by": "crossref",
      "first-page": "2499",
      "DOI": "10.1242/jcs.109.10.2499",
      "article-title": "Cyclic GMP-dependent protein kinase is required for thrombospondin and tenascin mediated focal adhesion disassembly",
      "volume": "109",
      "author": "Murphy-Ullrich",
      "year": "1996",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_Oteyetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "21193",
      "DOI": "10.1016/S0021-9258(19)36909-1",
      "article-title": "Mapping of the \u03b1-actinin binding site with the \u03b21 integrin cytoplasmic domain",
      "volume": "268",
      "author": "Otey",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Paleceketal1997",
      "doi-asserted-by": "crossref",
      "first-page": "537",
      "DOI": "10.1038/385537a0",
      "article-title": "Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness",
      "volume": "385",
      "author": "Palecek",
      "year": "1997",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902223409400_Pavalkoetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "1065",
      "DOI": "10.1042/bst0191065",
      "article-title": "Alpha-actinina direct link between actin and integrins",
      "volume": "19",
      "author": "Pavalko",
      "year": "1991",
      "journal-title": "Biochem. Soc. Trans."
    },
    {
      "key": "2023072902223409400_Pavalkoetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "534",
      "DOI": "10.1006/excr.1995.1119",
      "article-title": "Immunodetection of alpha-actinin in focal adhesions is limited by antibody inaccessibility",
      "volume": "217",
      "author": "Pavalko",
      "year": "1995",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902223409400_Plopperetal1995",
      "first-page": "1349",
      "article-title": "Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex",
      "volume": "Cell. 6",
      "author": "Plopper",
      "year": "1995",
      "journal-title": "Mol. Biol"
    },
    {
      "key": "2023072902223409400_Reiskeetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "12361",
      "DOI": "10.1074/jbc.274.18.12361",
      "article-title": "Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration",
      "volume": "274",
      "author": "Reiske",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Rizzoetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "1131",
      "DOI": "10.1074/jbc.274.2.1131",
      "article-title": "Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent Raf-1 translocation to the plasma membrane and the activation of the mitogen-activated protein kinase pathway",
      "volume": "274",
      "author": "Rizzo",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_RodriguezFernandezetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1002/cm.970220206",
      "article-title": "Overexpression of vinculin suppress cell motility in Balb/C 3T3 cells",
      "volume": "22",
      "author": "Rodriguez Fernandez",
      "year": "1992",
      "journal-title": "Cell Motil. Cytoskeleton."
    },
    {
      "key": "2023072902223409400_RodriguezFernandezetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "1285",
      "DOI": "10.1083/jcb.122.6.1285",
      "article-title": "Suppression of vinculin expression by antisense transfection confers changes in cell morphology, motility, and anchorage-dependent growth of 3T3 cells",
      "volume": "122",
      "author": "Rodriguez Fernandez",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902223409400_Rodriguez-Vicianaetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "457",
      "DOI": "10.1016/S0092-8674(00)80226-3",
      "article-title": "Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras",
      "volume": "89",
      "author": "Rodriguez-Viciana",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902223409400_Sampathetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "33588",
      "DOI": "10.1074/jbc.273.50.33588",
      "article-title": "Cytoskeletal interactions with the leukocyte integrin \u03b22 cytoplasmic tail",
      "volume": "273",
      "author": "Sampath",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Shawetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "949",
      "DOI": "10.1016/S0092-8674(00)80486-9",
      "article-title": "Activation of phosphoinositide 3-OH kinase by the \u03b16\u03b24 integrin promotes carcinoma invasion",
      "volume": "91",
      "author": "Shaw",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902223409400_Theibertetal1997"
    },
    {
      "key": "2023072902223409400_TokerandCantley1997",
      "doi-asserted-by": "crossref",
      "first-page": "673",
      "DOI": "10.1038/42648",
      "article-title": "Signalling through the lipid products of phosphoinositide-3-OH kinase",
      "volume": "387",
      "author": "Toker",
      "year": "1997",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902223409400_Tokeretal1995",
      "doi-asserted-by": "crossref",
      "first-page": "29525",
      "DOI": "10.1074/jbc.270.49.29525",
      "article-title": "Phosphorylation of the platelet p47 phosphoprotein is mediated by the lipid products of phosphoinositide 3-kinase",
      "volume": "270",
      "author": "Toker",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902223409400_Verschueren1985",
      "doi-asserted-by": "crossref",
      "first-page": "279",
      "DOI": "10.1242/jcs.75.1.279",
      "article-title": "Interference reflection microscopy in cell biologymethodology and applications",
      "volume": "75",
      "author": "Verschueren",
      "year": "1985",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902223409400_Wachsstocketal1993",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1016/S0006-3495(93)81059-2",
      "article-title": "Affinity of \u03b1-actinin for actin determines the structural and mechanical properties of actin filament gels",
      "volume": "65",
      "author": "Wachsstock",
      "year": "1993",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072902223409400_Wennstrometal1994a",
      "doi-asserted-by": "crossref",
      "first-page": "385",
      "DOI": "10.1016/S0960-9822(00)00087-7",
      "article-title": "Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling",
      "volume": "4",
      "author": "Wennstrom",
      "year": "1994",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072902223409400_Wennstrometal1994b",
      "first-page": "651",
      "article-title": "Membrane ruffling and chemotaxis transduced by the PDGF \u03b2-receptor require the binding site for phosphatidylinositol 3\u2032 kinase",
      "volume": "9",
      "author": "Wennstrom",
      "year": "1994",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023072902223409400_WoodsandCouchman1992",
      "doi-asserted-by": "crossref",
      "first-page": "277",
      "DOI": "10.1242/jcs.101.2.277",
      "article-title": "Protein kinase C involvement in focal adhesion formation",
      "volume": "101",
      "author": "Woods",
      "year": "1992",
      "journal-title": "J. Cell Sci."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/150/3/627/1859255/9909138.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/150/3/627/1859255/9909138.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T02:24:25Z",
    "timestamp": 1690597465000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/150/3/627/54036/Restructuring-of-Focal-Adhesion-Plaques-by-Pi-3"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        8,
        7
      ]
    ]
  },
  "references-count": 73,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          2000,
          8,
          7
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.150.3.627",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2000,
        8,
        7
      ]
    ]
  }
}