DOI: 10.1083/jcb.147.3.619. Degraded Collagen Fragments Promote Rapid Disassembly of Smooth Muscle Focal Adhesions That Correlates with Cleavage of Pp125FAK, Paxillin, and Talin

Degraded Collagen Fragments Promote Rapid Disassembly of Smooth Muscle Focal Adhesions That Correlates with Cleavage of Pp125FAK, Paxillin, and Talin

10.1083/jcb.147.3.619

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Active matrix metalloproteinases and degraded collagen are observed in disease states, such as atherosclerosis. To examine whether degraded collagen fragments have distinct effects on vascular smooth muscle cells (SMC), collagenase-digested type I collagen was added to cultured human arterial SMC. After addition of collagen fragments, adherent SMC lose their focal adhesion structures and round up. Analysis of components of the focal adhesion complex demonstrates rapid cleavage of the focal adhesion kinase (pp125FAK), paxillin, and talin. Cleavage is suppressed by inhibitors of the proteolytic enzyme, calpain I. In vitro translated pp125FAK is a substrate for both calpain I– and II–mediated processing. Mapping of the proteolytic cleavage fragments of pp125FAK predicts a dissociation of the focal adhesion targeting (FAT) sequence and second proline-rich domain from the tyrosine kinase domain and integrin-binding sequence. Coimmunoprecipitation studies confirm that the ability of pp125FAK to associate with paxillin, vinculin, and p130cas is significantly reduced in SMC treated with degraded collagen fragments. Further, there is a significant reduction in the association of intact pp125FAK with the cytoskeletal fraction, while pp125FAK cleavage fragments appear in the cytoplasm in SMC treated with degraded collagen fragments. Integrin-blocking studies indicate that integrin-mediated signals are involved in degraded collagen induction of pp125FAK cleavage. Thus, collagen fragments induce distinct integrin signals that lead to initiation of calpain-mediated cleavage of pp125FAK, paxillin, and talin and dissolution of the focal adhesion complex.

Bibliography

Carragher, N. O., Levkau, B., Ross, R., & Raines, E. W. (1999). Degraded Collagen Fragments Promote Rapid Disassembly of Smooth Muscle Focal Adhesions That Correlates with Cleavage of Pp125FAK, Paxillin, and Talin. The Journal of Cell Biology, 147(3), 619â630.

Authors 4

Neil O. Carragher (first)
Bodo Levkau (additional)
Russell Ross (additional)
Elaine W. Raines (additional)

References 67 Referenced 200

10.1074/jbc.270.11.5872 / J. Biol. Chem. / Matrix metalloproteinase 2 is an interstitial collagenase by Aimes (1995)
10.1016/0167-4889(95)00176-X / Biochim. Biophys. Acta. / Association of phosphatidylinositol 3-kinase, via the SH2 domains of p85 with focal adhesion kinase in polyoma middle t-transformed fibroblasts by Bachelot (1996)
10.1016/S0174-173X(85)80048-0 / Collagen Rel. Res. / Collagens in atherosclerosis by Barnes (1985)
10.1016/0092-8674(87)90126-7 / Cell. / Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion by Beckerle (1987)
10.1161/01.RES.75.3.539 / Circ. Res. / Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat by Bendeck (1994)
10.1172/JCI117081 / J. Clin. Invest. / Insulin-like growth factor-I and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signaling pathways that are distinct from those of proliferation by Bornfeldt (1994)
10.1146/annurev.cellbio.12.1.463 / Annu. Rev. Cell Dev. Biol. / Focal adhesions, contractility, and cell signaling by Burridge (1996)
10.1146/annurev.cb.04.110188.002415 / Ann. Rev. Cell Biol. / Focal adhesionstransmembrane junctions between the extracellular matrix and the cytoskeleton by Burridge (1988)
10.1083/jcb.119.4.893 / J. Cell Biol. / Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrixa role in cytoskeleton assembly by Burridge (1992)
10.1074/jbc.270.28.16995 / J. Biol. Chem. / Interaction of focal adhesion kinase with cytoskeletal protein talin by Chen (1995)
10.1161/01.CIR.98.20.2195 / Circulation. / Adenovirus-mediated gene transfer of the human tissue inhibitor of metalloproteinase-2 blocks vascular smooth muscle invasiveness in vitro and modulates neointimal development in vivo by Cheng (1998)
10.1042/bj3180041 / Biochem. J. / Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain by Cooray (1996)
{'key': '2023072901110363000_Crouchetal1996', 'first-page': '2689', 'article-title': 'Targeted proteolysis of the focal adhesion kinase pp125FAK during c-Myc-induced apoptosis is suppressed by integrin signalling', 'volume': '12', 'author': 'Crouch', 'year': '1996', 'journal-title': 'Oncogene.'} / Oncogene. / Targeted proteolysis of the focal adhesion kinase pp125FAK during c-Myc-induced apoptosis is suppressed by integrin signalling by Crouch (1996)
10.1073/pnas.77.11.6687 / Proc. Natl. Acad. Sci. USA / Altered distributions of the cytoskeletal proteins vinculin and α-actinin in cultured fibroblasts transformed by Rous sarcoma virus by David-Pfeuty (1980)
10.1016/0006-291X(92)91834-D / Biochem. Biophys. Res. Commun. / Affinity of integrins for damaged extracellular matrixαVβ3 binds to denatured collagen type I through RGD sites by Davis (1992)
10.1016/0076-6879(94)45011-0 / Methods Enzymol. / Receptors on platelets by Faull (1994)
{'key': '2023072901110363000_Finchametal1995', 'first-page': '2247', 'article-title': 'v-src-induced degradation of focal adhesion kinase during morphological transformation of chicken embryo fibroblasts', 'volume': '10', 'author': 'Fincham', 'year': '1995', 'journal-title': 'Oncogene.'} / Oncogene. / v-src-induced degradation of focal adhesion kinase during morphological transformation of chicken embryo fibroblasts by Fincham (1995)
10.1083/jcb.120.6.1501 / J. Cell Biol. / Evidence that activation of platelet calpain is induced as a consequence of binding of adhesive ligand to the integrin, glycoprotein IIb-IIIa by Fox (1993)
10.1172/JCI117619 / J. Clin. Invest. / Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques by Galis (1994)
10.1126/science.277.5323.225 / Science. / Induction of cell migration by matrix metalloproteinase-2 cleavage of laminin 5 by Gianelli (1997)
10.1016/S1357-2725(97)00051-4 / Int. J. Biochem. Cell. Biol. / Role of focal adhesion kinase in integrin signaling by Guan (1997)
10.1002/bies.950190208 / Bioessays. / Signaling through focal adhesion kinase by Hanks (1996)
10.1074/jbc.271.23.13649 / J. Biol. Chem. / p130Cas, a substrate associated with v-src and v-crk, localizes to focal adhesions and binds to focal adhesion kinase by Harte (1996)
10.1002/ajmg.1320340107 / Am. J. Med. Genet. / Extracellular matrix, cell skeletons, and embryonic development by Hay (1989)
10.1083/jcb.100.4.1031 / J. Cell Biol. / Platelet-derived growth factor induced alterations in vinculin and actin distribution in BALB/c 3T3 cells by Herman (1985)
10.1083/jcb.123.4.993 / J. Cell Biol. / Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions by Hildebrand (1993)
10.1091/mbc.6.6.637 / Mol. Biol. Cell. / Paxillin, a tyrosine phosphorylated focal adhesion-associated protein, binds to the carboxy terminal domain of focal adhesion kinase by Hildebrand (1995)
10.1016/0955-0674(95)80112-X / Curr. Opin. Cell Biol. / Adhesion in cell migration by Huttenlocher (1995)
10.1074/jbc.272.52.32719 / J. Biol. Chem. / Regulation of cell migration by the calcium-dependent protease calpain by Huttenlocher (1997)
10.1016/0092-8674(92)90115-S / Cell. / Integrinsversatility, modulation and signaling in cell adhesion by Hynes (1992)
10.1038/377539a0 / Nature. / Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice by Ilic (1995)
10.1006/abbi.1996.0152 / Arch. Biochem. Biophys. / Involvement of calpain in integrin-mediated signal transduction by Inomata (1996)
10.1016/S0021-9258(18)47130-X / J. Biol. Chem. / Adhesion receptor activation of phosphatidylinositol 3-kinase. von Willebrand factor stimulates the cytoskeletal association and activation of phosphatidylinositol 3-kinase and pp60c-src in human platelets by Jackson (1994)
10.1083/jcb.112.6.1249 / J. Cell Biol. / Multiple elevations of cytosolic free Ca2+ in human neutrophilsinitiation by adherence receptors of the integrin family by Jaconi (1991)
10.1083/jcb.139.1.279 / J. Cell Biol / Regulation of tenascin-C, a vascular smooth muscle cell survival factor that interacts with the αvβ3 integrin to promote epidermal growth factor receptor phosphorylation and growth by Jones (1997)
10.1016/S0092-8674(00)81801-2 / Cell. / Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of cdk2 inhibitors by Koyama (1996)
10.1084/jem.187.4.579 / J. Exp. Med. / Caspase-mediated cleavage of focal adhesion kinase pp125FAK and disassembly of focal adhesions in human endothelial cell apoptosis by Levkau (1998)
10.1242/jcs.111.8.1127 / J. Cell Sci / Effects of collagenase-cleavage of type I collagen on α2β1 integrin-mediated cell adhesion by Messent (1998)
10.1007/s002329900181 / J. Membrane Biol. / CalpainA cytosolic proteinase active at the membranes by Molanari (1997)
10.1073/pnas.91.19.8856 / Proc. Natl. Acad. Sci. USA / Integrin αvβ3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen by Montgomery (1994)
10.1016/0003-2697(86)90557-9 / Anal. Biochem. / Properties of radiolabelled type I, II and III collagens related to their use as substrates in collagenase assays by Mookhtiar (1986)
10.1016/S0021-9258(18)31431-5 / J. Biol. Chem. / pp60src is an endogenous substrate for calpain in human blood platelets by Oda (1993)
10.1161/01.RES.75.1.41 / Circ. Res. / Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation by Pauly (1994)
10.1073/pnas.92.23.10678 / Proc. Natl. Acad. Sci. USA. / Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130cas by Polte (1995)
10.1074/jbc.272.9.5501 / J. Biol. Chem. / Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130(cas)) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. Requirements for Src kinase activity and FAK proline-rich motifs by Polte (1997)
10.1016/0076-6879(85)09128-5 / Methods Enzymol. / Purification of human platelet-derived growth factor by Raines (1985)
10.1038/380538a0 / Nature. / A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp125FAK by Richardson (1996)
10.1074/jbc.270.22.13548 / J. Biol. Chem. / Integrin α2β1 is a positive regulator of collagenase (MMP-1) and collagen α1(I) gene expression by Riikonen (1995)
10.1016/0955-0674(93)90031-K / Curr. Opin. Cell Biol. / Integrin cytoplasmic domainsmediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling by Sastry (1993)
10.1128/MCB.15.5.2635 / Mol. Cell Biol. / pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for crk by Schaller (1995)
10.1073/pnas.89.11.5192 / Proc. Natl. Acad. Sci. USA. / pp125FAK, a structurally unique protein tyrosine kinase associated with focal adhesions by Schaller (1992)
{'key': '2023072901110363000_Schalleretal1993', 'first-page': '785', 'article-title': 'Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK', 'volume': '13', 'author': 'Schaller', 'year': '1993', 'journal-title': 'Mol. Biol. Cell.'} / Mol. Biol. Cell. / Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK by Schaller (1993)
{'key': '2023072901110363000_Schalleretal1994', 'first-page': '1680', 'article-title': 'Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src', 'volume': '14', 'author': 'Schaller', 'year': '1994', 'journal-title': 'Mol. Cell Biol.'} / Mol. Cell Biol. / Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src by Schaller (1994)
10.1083/jcb.130.5.1181 / J. Cell Biol. / Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains by Schaller (1995)
10.1038/372786a0 / Nature. / Integrin-mediated signal transduction linked to the ras pathway by Grb2 binding to focal adhesion kinase by Schlaepfer (1994)
10.1074/jbc.272.3.1694 / J. Biol. Chem. / Calpain cleavage of focal adhesion proteins regulates the cytoskeletal attachment of integrin αIIbβ3 (platelet glycoprotein IIb/IIIa) and the cellular retraction of fibrin clots by Schoenwaelder (1997)
10.4049/jimmunol.156.9.3215 / J. Immunol. / Proteolytic cleavage of alpha-actinin by calpain in T cells stimulated with anti-CD3 monoclonal antibody by Selliah (1996)
10.1016/S0167-4889(96)00067-5 / Biochim. Biophys. Acta. / Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin by Senger (1996)
{'key': '2023072901110363000_Skinneretal1994', 'first-page': '1070', 'article-title': 'Dynamic expression of α1β1 and α2β1 integrin receptors by human vascular smooth muscle cellsα2β1 integrin is required for chemotaxis across type I collagen-coated membranes', 'volume': '145', 'author': 'Skinner', 'year': '1994', 'journal-title': 'Am. J. Pathol.'} / Am. J. Pathol. / Dynamic expression of α1β1 and α2β1 integrin receptors by human vascular smooth muscle cellsα2β1 integrin is required for chemotaxis across type I collagen-coated membranes by Skinner (1994)
10.1074/jbc.271.45.28485 / J. Biol. Chem / Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by α9β1 integrin by Smith (1996)
10.1074/jbc.272.35.22103 / J. Biol. Chem. / Induction and repression of collagenase-1 by keratinocytes is controlled by distinct components of different extracellular matrix compartments by Sudbeck (1997)
10.1161/01.ATV.10.6.966 / Arteriosclerosis. / Regulation of differentiated properties and proliferation of arterial smooth muscle cells by Thyberg (1990)
10.1074/jbc.272.41.26056 / J. Biol. Chem. / Cleavage of focal adhesion kinase by caspases during apoptosis by Wen (1997)
10.1242/jcs.108.6.2381 / J. Cell Sci. / pp125FAK tyrosine kinase activity is not required for the assembly of F-actin stress fibres and focal adhesions in cultured mouse aortic smooth muscle cells by Wilson (1995)
10.1016/0014-5793(94)01246-6 / FEBS. / Unphosphorylated and tyrosine-phosphorylated forms of a focal adhesion protein, paxillin, are substrates for calpain II in vitroimplications for the possible involvement of calpain II in mitosis-specific degradation of paxillin by Yamaguchi (1994)
10.1016/0014-5793(84)81324-1 / FEBS. / Degradation of actin and vimentin by calpain II, a Ca2+-dependent cysteine proteinase, in bovine lens by Yoshida (1984)
10.1016/0092-8674(92)90385-P / Cell / Focal adhesion kinase (p125FAK)a point of convergence in the action of neuropeptides, integrins, and oncogenes by Zachary (1992)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 9:12 p.m.)
Indexed	1 month, 1 week ago (July 25, 2025, 6:24 a.m.)
Issued	25 years, 10 months ago (Nov. 1, 1999)
Published	25 years, 10 months ago (Nov. 1, 1999)
Published Online	25 years, 10 months ago (Nov. 1, 1999)
Published Print	25 years, 10 months ago (Nov. 1, 1999)

Funders 0

None

BibTeX

@article{Carragher_1999, title={Degraded Collagen Fragments Promote Rapid Disassembly of Smooth Muscle Focal Adhesions That Correlates with Cleavage of Pp125FAK, Paxillin, and Talin}, volume={147}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.147.3.619}, DOI={10.1083/jcb.147.3.619}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Carragher, Neil O. and Levkau, Bodo and Ross, Russell and Raines, Elaine W.}, year={1999}, month=nov, pages={619–630} }

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      "key": "2023072901110363000_AimesandQuigley1995",
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      "first-page": "5872",
      "DOI": "10.1074/jbc.270.11.5872",
      "article-title": "Matrix metalloproteinase 2 is an interstitial collagenase",
      "volume": "270",
      "author": "Aimes",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
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    {
      "key": "2023072901110363000_Bachelotetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "45",
      "DOI": "10.1016/0167-4889(95)00176-X",
      "article-title": "Association of phosphatidylinositol 3-kinase, via the SH2 domains of p85 with focal adhesion kinase in polyoma middle t-transformed fibroblasts",
      "volume": "1311",
      "author": "Bachelot",
      "year": "1996",
      "journal-title": "Biochim. Biophys. Acta."
    },
    {
      "key": "2023072901110363000_Barnes1985",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1016/S0174-173X(85)80048-0",
      "article-title": "Collagens in atherosclerosis",
      "volume": "5",
      "author": "Barnes",
      "year": "1985",
      "journal-title": "Collagen Rel. Res."
    },
    {
      "key": "2023072901110363000_Beckerleetal1987",
      "doi-asserted-by": "crossref",
      "first-page": "569",
      "DOI": "10.1016/0092-8674(87)90126-7",
      "article-title": "Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion",
      "volume": "51",
      "author": "Beckerle",
      "year": "1987",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901110363000_Bendecketal1994",
      "doi-asserted-by": "crossref",
      "first-page": "539",
      "DOI": "10.1161/01.RES.75.3.539",
      "article-title": "Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat",
      "volume": "75",
      "author": "Bendeck",
      "year": "1994",
      "journal-title": "Circ. Res."
    },
    {
      "key": "2023072901110363000_Bornfeldtetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "1266",
      "DOI": "10.1172/JCI117081",
      "article-title": "Insulin-like growth factor-I and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signaling pathways that are distinct from those of proliferation",
      "volume": "93",
      "author": "Bornfeldt",
      "year": "1994",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "2023072901110363000_BurridgeandChrzanowska-Wodnicka1996",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1146/annurev.cellbio.12.1.463",
      "article-title": "Focal adhesions, contractility, and cell signaling",
      "volume": "2",
      "author": "Burridge",
      "year": "1996",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "2023072901110363000_Burridgeetal1988",
      "doi-asserted-by": "crossref",
      "first-page": "487",
      "DOI": "10.1146/annurev.cb.04.110188.002415",
      "article-title": "Focal adhesionstransmembrane junctions between the extracellular matrix and the cytoskeleton",
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      "year": "1988",
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      "volume": "119",
      "author": "Burridge",
      "year": "1992",
      "journal-title": "J. Cell Biol."
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      "volume": "98",
      "author": "Cheng",
      "year": "1998",
      "journal-title": "Circulation."
    },
    {
      "key": "2023072901110363000_Coorayetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1042/bj3180041",
      "article-title": "Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain",
      "volume": "318",
      "author": "Cooray",
      "year": "1996",
      "journal-title": "Biochem. J."
    },
    {
      "key": "2023072901110363000_Crouchetal1996",
      "first-page": "2689",
      "article-title": "Targeted proteolysis of the focal adhesion kinase pp125FAK during c-Myc-induced apoptosis is suppressed by integrin signalling",
      "volume": "12",
      "author": "Crouch",
      "year": "1996",
      "journal-title": "Oncogene."
    },
    {
      "key": "2023072901110363000_David-PfeutyandSinger1980",
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      "first-page": "6687",
      "DOI": "10.1073/pnas.77.11.6687",
      "article-title": "Altered distributions of the cytoskeletal proteins vinculin and \u03b1-actinin in cultured fibroblasts transformed by Rous sarcoma virus",
      "volume": "77",
      "author": "David-Pfeuty",
      "year": "1980",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023072901110363000_Davis1992",
      "doi-asserted-by": "crossref",
      "first-page": "1025",
      "DOI": "10.1016/0006-291X(92)91834-D",
      "article-title": "Affinity of integrins for damaged extracellular matrix\u03b1V\u03b23 binds to denatured collagen type I through RGD sites",
      "volume": "182",
      "author": "Davis",
      "year": "1992",
      "journal-title": "Biochem. Biophys. Res. Commun."
    },
    {
      "key": "2023072901110363000_Faulletal1994",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1016/0076-6879(94)45011-0",
      "article-title": "Receptors on platelets",
      "volume": "245",
      "author": "Faull",
      "year": "1994",
      "journal-title": "Methods Enzymol."
    },
    {
      "key": "2023072901110363000_Finchametal1995",
      "first-page": "2247",
      "article-title": "v-src-induced degradation of focal adhesion kinase during morphological transformation of chicken embryo fibroblasts",
      "volume": "10",
      "author": "Fincham",
      "year": "1995",
      "journal-title": "Oncogene."
    },
    {
      "key": "2023072901110363000_Foxetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "1501",
      "DOI": "10.1083/jcb.120.6.1501",
      "article-title": "Evidence that activation of platelet calpain is induced as a consequence of binding of adhesive ligand to the integrin, glycoprotein IIb-IIIa",
      "volume": "120",
      "author": "Fox",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901110363000_Galisetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "2493",
      "DOI": "10.1172/JCI117619",
      "article-title": "Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques",
      "volume": "94",
      "author": "Galis",
      "year": "1994",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "2023072901110363000_Gianellietal1997",
      "doi-asserted-by": "crossref",
      "first-page": "225",
      "DOI": "10.1126/science.277.5323.225",
      "article-title": "Induction of cell migration by matrix metalloproteinase-2 cleavage of laminin 5",
      "volume": "277",
      "author": "Gianelli",
      "year": "1997",
      "journal-title": "Science."
    },
    {
      "key": "2023072901110363000_Guan1997",
      "doi-asserted-by": "crossref",
      "first-page": "1085",
      "DOI": "10.1016/S1357-2725(97)00051-4",
      "article-title": "Role of focal adhesion kinase in integrin signaling",
      "volume": "29",
      "author": "Guan",
      "year": "1997",
      "journal-title": "Int. J. Biochem. Cell. Biol."
    },
    {
      "key": "2023072901110363000_HanksandPolte1996",
      "doi-asserted-by": "crossref",
      "first-page": "137",
      "DOI": "10.1002/bies.950190208",
      "article-title": "Signaling through focal adhesion kinase",
      "volume": "19",
      "author": "Hanks",
      "year": "1996",
      "journal-title": "Bioessays."
    },
    {
      "key": "2023072901110363000_Harteetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "13649",
      "DOI": "10.1074/jbc.271.23.13649",
      "article-title": "p130Cas, a substrate associated with v-src and v-crk, localizes to focal adhesions and binds to focal adhesion kinase",
      "volume": "271",
      "author": "Harte",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Hay1989",
      "doi-asserted-by": "crossref",
      "first-page": "14",
      "DOI": "10.1002/ajmg.1320340107",
      "article-title": "Extracellular matrix, cell skeletons, and embryonic development",
      "volume": "1",
      "author": "Hay",
      "year": "1989",
      "journal-title": "Am. J. Med. Genet."
    },
    {
      "key": "2023072901110363000_HermanandPledger1985",
      "doi-asserted-by": "crossref",
      "first-page": "1031",
      "DOI": "10.1083/jcb.100.4.1031",
      "article-title": "Platelet-derived growth factor induced alterations in vinculin and actin distribution in BALB/c 3T3 cells",
      "volume": "100",
      "author": "Herman",
      "year": "1985",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901110363000_Hildebrandetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "993",
      "DOI": "10.1083/jcb.123.4.993",
      "article-title": "Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions",
      "volume": "123",
      "author": "Hildebrand",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901110363000_Hildebrandetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "637",
      "DOI": "10.1091/mbc.6.6.637",
      "article-title": "Paxillin, a tyrosine phosphorylated focal adhesion-associated protein, binds to the carboxy terminal domain of focal adhesion kinase",
      "volume": "6",
      "author": "Hildebrand",
      "year": "1995",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072901110363000_Huttenlocheretal1995",
      "doi-asserted-by": "crossref",
      "first-page": "697",
      "DOI": "10.1016/0955-0674(95)80112-X",
      "article-title": "Adhesion in cell migration",
      "volume": "7",
      "author": "Huttenlocher",
      "year": "1995",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072901110363000_Huttenlocheretal1997",
      "doi-asserted-by": "crossref",
      "first-page": "32719",
      "DOI": "10.1074/jbc.272.52.32719",
      "article-title": "Regulation of cell migration by the calcium-dependent protease calpain",
      "volume": "272",
      "author": "Huttenlocher",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Hynes1992",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1016/0092-8674(92)90115-S",
      "article-title": "Integrinsversatility, modulation and signaling in cell adhesion",
      "volume": "69",
      "author": "Hynes",
      "year": "1992",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901110363000_Ilicetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "539",
      "DOI": "10.1038/377539a0",
      "article-title": "Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice",
      "volume": "377",
      "author": "Ilic",
      "year": "1995",
      "journal-title": "Nature."
    },
    {
      "key": "2023072901110363000_Inomataetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1006/abbi.1996.0152",
      "article-title": "Involvement of calpain in integrin-mediated signal transduction",
      "volume": "328",
      "author": "Inomata",
      "year": "1996",
      "journal-title": "Arch. Biochem. Biophys."
    },
    {
      "key": "2023072901110363000_Jacksonetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "27093",
      "DOI": "10.1016/S0021-9258(18)47130-X",
      "article-title": "Adhesion receptor activation of phosphatidylinositol 3-kinase. von Willebrand factor stimulates the cytoskeletal association and activation of phosphatidylinositol 3-kinase and pp60c-src in human platelets",
      "volume": "269",
      "author": "Jackson",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Jaconietal1991",
      "doi-asserted-by": "crossref",
      "first-page": "1249",
      "DOI": "10.1083/jcb.112.6.1249",
      "article-title": "Multiple elevations of cytosolic free Ca2+ in human neutrophilsinitiation by adherence receptors of the integrin family",
      "volume": "112",
      "author": "Jaconi",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901110363000_Jonesetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "279",
      "DOI": "10.1083/jcb.139.1.279",
      "article-title": "Regulation of tenascin-C, a vascular smooth muscle cell survival factor that interacts with the \u03b1v\u03b23 integrin to promote epidermal growth factor receptor phosphorylation and growth",
      "volume": "139",
      "author": "Jones",
      "year": "1997",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901110363000_Koyamaetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1069",
      "DOI": "10.1016/S0092-8674(00)81801-2",
      "article-title": "Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of cdk2 inhibitors",
      "volume": "87",
      "author": "Koyama",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901110363000_Levkauetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1084/jem.187.4.579",
      "article-title": "Caspase-mediated cleavage of focal adhesion kinase pp125FAK and disassembly of focal adhesions in human endothelial cell apoptosis",
      "volume": "187",
      "author": "Levkau",
      "year": "1998",
      "journal-title": "J. Exp. Med."
    },
    {
      "key": "2023072901110363000_Messentetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1127",
      "DOI": "10.1242/jcs.111.8.1127",
      "article-title": "Effects of collagenase-cleavage of type I collagen on \u03b12\u03b21 integrin-mediated cell adhesion",
      "volume": "111",
      "author": "Messent",
      "year": "1998",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2023072901110363000_MolanariandCarafoli1997",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1007/s002329900181",
      "article-title": "CalpainA cytosolic proteinase active at the membranes",
      "volume": "156",
      "author": "Molanari",
      "year": "1997",
      "journal-title": "J. Membrane Biol."
    },
    {
      "key": "2023072901110363000_Montgomeryetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "8856",
      "DOI": "10.1073/pnas.91.19.8856",
      "article-title": "Integrin \u03b1v\u03b23 rescues melanoma cells from apoptosis in three-dimensional dermal collagen",
      "volume": "91",
      "author": "Montgomery",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023072901110363000_Mookhtiaretal1986",
      "doi-asserted-by": "crossref",
      "first-page": "322",
      "DOI": "10.1016/0003-2697(86)90557-9",
      "article-title": "Properties of radiolabelled type I, II and III collagens related to their use as substrates in collagenase assays",
      "volume": "158",
      "author": "Mookhtiar",
      "year": "1986",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "2023072901110363000_Odaetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "12603",
      "DOI": "10.1016/S0021-9258(18)31431-5",
      "article-title": "pp60src is an endogenous substrate for calpain in human blood platelets",
      "volume": "268",
      "author": "Oda",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Paulyetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1161/01.RES.75.1.41",
      "article-title": "Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation",
      "volume": "75",
      "author": "Pauly",
      "year": "1994",
      "journal-title": "Circ. Res."
    },
    {
      "key": "2023072901110363000_PolteandHanks1995",
      "doi-asserted-by": "crossref",
      "first-page": "10678",
      "DOI": "10.1073/pnas.92.23.10678",
      "article-title": "Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130cas",
      "volume": "92",
      "author": "Polte",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072901110363000_PolteandHanks1997",
      "doi-asserted-by": "crossref",
      "first-page": "5501",
      "DOI": "10.1074/jbc.272.9.5501",
      "article-title": "Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130(cas)) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. Requirements for Src kinase activity and FAK proline-rich motifs",
      "volume": "272",
      "author": "Polte",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_RainesandRoss1985",
      "doi-asserted-by": "crossref",
      "first-page": "749",
      "DOI": "10.1016/0076-6879(85)09128-5",
      "article-title": "Purification of human platelet-derived growth factor",
      "volume": "109",
      "author": "Raines",
      "year": "1985",
      "journal-title": "Methods Enzymol."
    },
    {
      "key": "2023072901110363000_RichardsonandParsons1996",
      "doi-asserted-by": "crossref",
      "first-page": "538",
      "DOI": "10.1038/380538a0",
      "article-title": "A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp125FAK",
      "volume": "380",
      "author": "Richardson",
      "year": "1996",
      "journal-title": "Nature."
    },
    {
      "key": "2023072901110363000_Riikonenetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "13548",
      "DOI": "10.1074/jbc.270.22.13548",
      "article-title": "Integrin \u03b12\u03b21 is a positive regulator of collagenase (MMP-1) and collagen \u03b11(I) gene expression",
      "volume": "270",
      "author": "Riikonen",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_SastryandHorwitz1993",
      "doi-asserted-by": "crossref",
      "first-page": "819",
      "DOI": "10.1016/0955-0674(93)90031-K",
      "article-title": "Integrin cytoplasmic domainsmediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling",
      "volume": "5",
      "author": "Sastry",
      "year": "1993",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072901110363000_SchallerandParsons1995",
      "doi-asserted-by": "crossref",
      "first-page": "2635",
      "DOI": "10.1128/MCB.15.5.2635",
      "article-title": "pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for crk",
      "volume": "15",
      "author": "Schaller",
      "year": "1995",
      "journal-title": "Mol. Cell Biol."
    },
    {
      "key": "2023072901110363000_Schalleretal1992",
      "doi-asserted-by": "crossref",
      "first-page": "5192",
      "DOI": "10.1073/pnas.89.11.5192",
      "article-title": "pp125FAK, a structurally unique protein tyrosine kinase associated with focal adhesions",
      "volume": "89",
      "author": "Schaller",
      "year": "1992",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072901110363000_Schalleretal1993",
      "first-page": "785",
      "article-title": "Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK",
      "volume": "13",
      "author": "Schaller",
      "year": "1993",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072901110363000_Schalleretal1994",
      "first-page": "1680",
      "article-title": "Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src",
      "volume": "14",
      "author": "Schaller",
      "year": "1994",
      "journal-title": "Mol. Cell Biol."
    },
    {
      "key": "2023072901110363000_Schalleretal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1181",
      "DOI": "10.1083/jcb.130.5.1181",
      "article-title": "Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains",
      "volume": "130",
      "author": "Schaller",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901110363000_Schlaepferetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "786",
      "DOI": "10.1038/372786a0",
      "article-title": "Integrin-mediated signal transduction linked to the ras pathway by Grb2 binding to focal adhesion kinase",
      "volume": "372",
      "author": "Schlaepfer",
      "year": "1994",
      "journal-title": "Nature."
    },
    {
      "key": "2023072901110363000_Schoenwaelderetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1694",
      "DOI": "10.1074/jbc.272.3.1694",
      "article-title": "Calpain cleavage of focal adhesion proteins regulates the cytoskeletal attachment of integrin \u03b1IIb\u03b23 (platelet glycoprotein IIb/IIIa) and the cellular retraction of fibrin clots",
      "volume": "272",
      "author": "Schoenwaelder",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Selliahetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "3215",
      "DOI": "10.4049/jimmunol.156.9.3215",
      "article-title": "Proteolytic cleavage of alpha-actinin by calpain in T cells stimulated with anti-CD3 monoclonal antibody",
      "volume": "159",
      "author": "Selliah",
      "year": "1996",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023072901110363000_SengerandPerruzzi1996",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1016/S0167-4889(96)00067-5",
      "article-title": "Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin",
      "volume": "1314",
      "author": "Senger",
      "year": "1996",
      "journal-title": "Biochim. Biophys. Acta."
    },
    {
      "key": "2023072901110363000_Skinneretal1994",
      "first-page": "1070",
      "article-title": "Dynamic expression of \u03b11\u03b21 and \u03b12\u03b21 integrin receptors by human vascular smooth muscle cells\u03b12\u03b21 integrin is required for chemotaxis across type I collagen-coated membranes",
      "volume": "145",
      "author": "Skinner",
      "year": "1994",
      "journal-title": "Am. J. Pathol."
    },
    {
      "key": "2023072901110363000_Smithetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "28485",
      "DOI": "10.1074/jbc.271.45.28485",
      "article-title": "Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by \u03b19\u03b21 integrin",
      "volume": "271",
      "author": "Smith",
      "year": "1996",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901110363000_Sudbecketal1997",
      "doi-asserted-by": "crossref",
      "first-page": "22103",
      "DOI": "10.1074/jbc.272.35.22103",
      "article-title": "Induction and repression of collagenase-1 by keratinocytes is controlled by distinct components of different extracellular matrix compartments",
      "volume": "272",
      "author": "Sudbeck",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Thybergetal1990",
      "doi-asserted-by": "crossref",
      "first-page": "966",
      "DOI": "10.1161/01.ATV.10.6.966",
      "article-title": "Regulation of differentiated properties and proliferation of arterial smooth muscle cells",
      "volume": "10",
      "author": "Thyberg",
      "year": "1990",
      "journal-title": "Arteriosclerosis."
    },
    {
      "key": "2023072901110363000_Wenetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "56",
      "DOI": "10.1074/jbc.272.41.26056",
      "article-title": "Cleavage of focal adhesion kinase by caspases during apoptosis",
      "volume": "272",
      "author": "Wen",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072901110363000_Wilsonetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "2381",
      "DOI": "10.1242/jcs.108.6.2381",
      "article-title": "pp125FAK tyrosine kinase activity is not required for the assembly of F-actin stress fibres and focal adhesions in cultured mouse aortic smooth muscle cells",
      "volume": "108",
      "author": "Wilson",
      "year": "1995",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072901110363000_Yamaguchietal1994",
      "doi-asserted-by": "crossref",
      "first-page": "114",
      "DOI": "10.1016/0014-5793(94)01246-6",
      "article-title": "Unphosphorylated and tyrosine-phosphorylated forms of a focal adhesion protein, paxillin, are substrates for calpain II in vitroimplications for the possible involvement of calpain II in mitosis-specific degradation of paxillin",
      "volume": "356",
      "author": "Yamaguchi",
      "year": "1994",
      "journal-title": "FEBS."
    },
    {
      "key": "2023072901110363000_Yoshidaetal1984",
      "doi-asserted-by": "crossref",
      "first-page": "259",
      "DOI": "10.1016/0014-5793(84)81324-1",
      "article-title": "Degradation of actin and vimentin by calpain II, a Ca2+-dependent cysteine proteinase, in bovine lens",
      "volume": "170",
      "author": "Yoshida",
      "year": "1984",
      "journal-title": "FEBS."
    },
    {
      "key": "2023072901110363000_ZacharyandRozengurt1992",
      "doi-asserted-by": "crossref",
      "first-page": "891",
      "DOI": "10.1016/0092-8674(92)90385-P",
      "article-title": "Focal adhesion kinase (p125FAK)a point of convergence in the action of neuropeptides, integrins, and oncogenes",
      "volume": "71",
      "author": "Zachary",
      "year": "1992",
      "journal-title": "Cell"
    }
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