DOI: 10.1242/jcs.108.3.1165. Stimulation of tyrosine phosphorylation of distinct proteins in response to antibody-mediated ligation and clustering of α3 and α6 integrins

Stimulation of tyrosine phosphorylation of distinct proteins in response to antibody-mediated ligation and clustering of α3 and α6 integrins

10.1242/jcs.108.3.1165

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT The interaction of cells with components of the extracellular matrix through their integrin receptors results in the stimulation of tyrosine phosphorylation of several proteins, suggesting that these receptors play a key role in signal transduction. Here we report that antibody-mediated ligation and clustering of α3β1 and α6β1/α6β4 integrins resulted in the stimulation of tyrosine phosphorylation of proteins that are specific for each heterodimer. Thus, ligation and clustering of the α3β1 integrin on human prostate carcinoma cells (PC-3) and human umbilical vein endothelial cells (HUVEC) with anti-α3 antibodies resulted in the stimulation of tyrosine phosphorylation of a 55 kDa protein. In contrast, ligation and clustering of the α6β1 integrin on these cells with anti-α6 antibody resulted in the dramatic stimulation of tyrosine phosphorylation of a 90 kDa protein in addition to a 52 kDa protein, and ligation and clustering of α5β1 on HUVEC did not result in the apparent stimulation of tyrosine phosphorylation of any proteins. Clustering with anti-β1 antibodies triggered the tyrosine phosphorylation of all of these proteins, whereas ligation and clustering of PC-3 cells with an anti-β4 antibody resulted in the tyrosine phosphorylation of a distinct 62 kDa protein. Since the PC-3 cells express both α6β1 and α6β4, these data suggest that these two receptors can transduce distinct signals. All of the phosphorylations could be inhibited by treating the cells with Genistein, a tyrosine kinase inhibitor. Antibody-mediated ligation and clustering of integrins on the two types of cells did not result in the stimulation of tyrosine phosphorylation of pp125 focal adhesion kinase, although this was observed upon cell attachment and spreading on fibronectin, laminin and anti-α3 monoclonal antibody. Collectively, these data demonstrate that cross-linking of different integrin het-erodimers can stimulate tyrosine kinase activities, leading to the phosphorylation of distinct proteins, which are also different from those observed when cells are allowed to spread on a matrix.

Bibliography

Jewell, K., Kapron-Bras, C., Jeevaratnam, P., & Dedhar, S. (1995). Stimulation of tyrosine phosphorylation of distinct proteins in response to antibody-mediated ligation and clustering of Î±3 and Î±6 integrins. Journal of Cell Science, 108(3), 1165â1174.

Authors 4

Kevin Jewell (first)
Carolyn Kapron-Bras (additional)
Premala Jeevaratnam (additional)
Shoukat Dedhar (additional)

References 38 Referenced 38

10.1038/340307a0 / Nature / Fibronectin inhibits the terminal differentiation of human keratinocytes by Adams (1989)
10.1016/S0021-9258(18)45614-1 / J. Biol. Chem / Genistein, a specific inhibitor of tyrosine-specific protein kinases by Akiyama (1987)
10.1083/jcb.119.4.893 / J. Cell Biol / Tyrosine phosphorylation of paxillin and pp125 FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly by Burridge (1992)
10.1016/0014-4827(89)90430-8 / Exp. Cell. Res / Signal transduction via the β1 integrins is a required intermediate in interleukin-1β induction of alkaline phosphatase activity in human osteosarcoma cells by Dedhar (1989)
10.1002/bies.950121205 / BioEssays / Integrins and tumor invasion by Dedhar (1990)
10.1016/S0021-9258(18)54715-3 / J. Biol. Chem / Induction of expression of the αvβ1 and αvβ3 integrin heterodimers during retionic acid-induced neuronal differentiation of murine embryonal carcinoma cells by Dedhar (1991)
10.1016/S0021-9258(19)37047-4 / J. Biol. Chem / The receptor for the basement membrane glycoprotein entactin is the integrin α3/β1 by Dedhar (1992)
{'key': '2023122401041881600_JOCES_108_3_1165C8', 'first-page': '1', 'article-title': 'Differential regulation of expression of specific integrin receptors by nerve growth factor and transforming growth factor β during differentiation of human neuroblastoma cells', 'volume': '1', 'author': 'Dedhar', 'year': '1993', 'journal-title': 'Mol. Cell Diff'} / Mol. Cell Diff / Differential regulation of expression of specific integrin receptors by nerve growth factor and transforming growth factor β during differentiation of human neuroblastoma cells by Dedhar (1993)
10.1007/BF00132982 / Clin. Exp. Metast / Specific alterations in the expression of α3β1 and α6β4 integrins in highly invasive and metastatic variants of human prostate carcinoma cells selected by in vitro invasion through reconstituted basement membrane by Dedhar (1993)
10.1073/pnas.85.18.6792 / Proc. Nat. Acad. Sci. USA / Cell adhesion induces expression of growth-associated genes in suspension-arrested fibroblasts by Dike (1988)
10.1038/363045a0 / Nature / Association of Sos ras exchange proteins with Grb2 is implicated in tyrosine kinase signal transduction and transformation by Egan (1993)
10.1091/mbc.2.11.951 / Cell Regul / Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120 kDa protein by Guan (1991)
10.1038/358690a0 / Nature / Regulation of focal adhesion associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation by Guan (1992)
10.1083/jcb.122.2.473 / J. Cell Biol / Adhesive ligand binding to integrin αIIbβ3 stimulates tyrosine phosphorylation of novel protein substrata before phosphorylation of pp125FAK by Huang (1993)
10.1016/0092-8674(92)90115-S / Cell / Integrins: versatility, modulation, and signaling in cell adhesion by Hynes (1992)
10.1083/jcb.120.3.577 / J. Cell Biol / Signal transduction from the extracellular matrix by Juliano (1993)
10.1016/S0021-9258(19)36834-6 / J. Biol. Chem / Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated α2β1 integrin activation in T-lymphoblastic cells by Kapron-Bras (1993)
10.1073/pnas.88.19.8392 / Proc. Nat. Acad. Sci. USA / Signal transduction by integrins: Increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins by Kornberg (1991)
10.1016/S0021-9258(18)35853-8 / J. Biol. Chem / Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion associated tyrosine kinase by Kornberg (1992)
10.1038/227680a0 / Nature / Cleavage of structural proteins during the assembly of the head of bacteriophage T4 by Laemmli (1970)
{'key': '2023122401041881600_JOCES_108_3_1165C21', 'first-page': '5111', 'article-title': 'Inhibitory effects of the tyrosine kinase inhibitor Genistein on mammalian DNA topoisomerase II', 'volume': '49', 'author': 'Markovits', 'year': '1989', 'journal-title': 'Cancer Res'} / Cancer Res / Inhibitory effects of the tyrosine kinase inhibitor Genistein on mammalian DNA topoisomerase II by Markovits (1989)
10.1016/0092-8674(87)90009-2 / Cell / Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation by Menko (1987)
10.1084/jem.172.4.1185 / J. Exp. Med / VLA-4 mediates CD3-dependent CD4+ T-cells activation via the CSI alternatively spliced domain of fibronectin by Nojima (1990)
10.1084/jem.175.4.1045 / J. Exp. Med / Ligation of VLA-4 on T cells stimulates tyrosine phosphorylation of a 105-kD protein by Nojima (1992)
10.1016/0014-4827(90)90262-9 / Exp. Cell Res / Nerve growth factor induces increased expression of a laminin-binding integrin in rat pheochromocytoma PC12 cells by Rossino (1990)
10.1038/360689a0 / Nature / Association of the Shc and Grb2/sems SH2 containing proteins is implicated in activation of the Ras pathway by tyrosine kinases by Rozakis-Adcock (1992)
10.1126/science.2821619 / Science / New perspectives in cell adhesion: RGD and integrins by Ruoslahti (1987)
10.1073/pnas.89.11.5192 / Proc. Nat. Acad. Sci. USA / pp125FAK, as structurally distinctive protein-tyrosine kinase associated with focal adhesions by Schaller (1992)
10.1073/pnas.88.17.7849 / Proc. Nat. Acad. Sci. USA / Insoluble fibronectin activates the Na+/H+ antiporter by clustering and immobilizing integrin α5β1, independent of cell shape by Schwartz (1991)
10.4049/jimmunol.145.1.59 / J. Immunol / Costimulation of proliferative responses of resting CD4 and T cells by interaction of VLA4 and VLA5 with fibronectin or VLA6 with laminin by Shimizu (1990)
10.1038/346425a0 / Nature / Adhesion receptors of the immune system by Springer (1990)
10.1083/jcb.120.2.523 / J. Cell Biol / Interaction of integrins α3β1 and α2β1: potential role in keratinocyte intercellular adhesion by Symington (1993)
10.1073/pnas.76.9.4350 / Proc. Nat. Acad. Sci. USA / Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications by Towbin (1979)
10.1084/jem.174.4.901 / J. Exp. Med / Analysis of T cell stimulation by superantigen plus major histocompatibility complex class II molecules or by CD3 monoclonal antibody: costimulation by purified adhesion ligans VCAM-1, but not ELAM-1 by van Seventer (1991)
10.1016/0952-7915(91)90027-X / Curr. Opin. Immunol / Roles of multiple accessing molecules in T-cell activation by van Seventer (1991)
10.1083/jcb.109.2.877 / J. Cell Biol / Signal transduction through the fibronectin receptor induces collagenase and stromeysin gene expression by Werb (1989)
10.4049/jimmunol.146.1.53 / J. Immunol / Activation of human CD4-T lymphocytes: Interaction of fibronectin with VLA-5 receptor on CD4 cells induces the AP-1 transcription factor by Yamada (1991)
10.1073/pnas.89.19.9034 / Proc. Nat. Acad. Sci. USA / Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction by Yurochko (1992)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 12:15 p.m.)
Deposited	1 year, 8 months ago (Dec. 23, 2023, 8:04 p.m.)
Indexed	1 month, 2 weeks ago (July 12, 2025, 6:51 p.m.)
Issued	30 years, 6 months ago (March 1, 1995)
Published	30 years, 6 months ago (March 1, 1995)
Published Online	30 years, 6 months ago (March 1, 1995)
Published Print	30 years, 6 months ago (March 1, 1995)

Funders 0

None

BibTeX

@article{Jewell_1995, title={Stimulation of tyrosine phosphorylation of distinct proteins in response to antibody-mediated ligation and clustering of α3 and α6 integrins}, volume={108}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.108.3.1165}, DOI={10.1242/jcs.108.3.1165}, number={3}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Jewell, Kevin and Kapron-Bras, Carolyn and Jeevaratnam, Premala and Dedhar, Shoukat}, year={1995}, month=mar, pages={1165–1174} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        12
      ]
    ],
    "date-time": "2025-07-12T22:51:31Z",
    "timestamp": 1752360691321
  },
  "reference-count": 38,
  "publisher": "The Company of Biologists",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1995,
            3,
            1
          ]
        ],
        "date-time": "1995-03-01T00:00:00Z",
        "timestamp": 794016000000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1995,
        3,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>The interaction of cells with components of the extracellular matrix through their integrin receptors results in the stimulation of tyrosine phosphorylation of several proteins, suggesting that these receptors play a key role in signal transduction. Here we report that antibody-mediated ligation and clustering of \u03b13\u03b21 and \u03b16\u03b21/\u03b16\u03b24 integrins resulted in the stimulation of tyrosine phosphorylation of proteins that are specific for each heterodimer. Thus, ligation and clustering of the \u03b13\u03b21 integrin on human prostate carcinoma cells (PC-3) and human umbilical vein endothelial cells (HUVEC) with anti-\u03b13 antibodies resulted in the stimulation of tyrosine phosphorylation of a 55 kDa protein. In contrast, ligation and clustering of the \u03b16\u03b21 integrin on these cells with anti-\u03b16 antibody resulted in the dramatic stimulation of tyrosine phosphorylation of a 90 kDa protein in addition to a 52 kDa protein, and ligation and clustering of \u03b15\u03b21 on HUVEC did not result in the apparent stimulation of tyrosine phosphorylation of any proteins. Clustering with anti-\u03b21 antibodies triggered the tyrosine phosphorylation of all of these proteins, whereas ligation and clustering of PC-3 cells with an anti-\u03b24 antibody resulted in the tyrosine phosphorylation of a distinct 62 kDa protein. Since the PC-3 cells express both \u03b16\u03b21 and \u03b16\u03b24, these data suggest that these two receptors can transduce distinct signals. All of the phosphorylations could be inhibited by treating the cells with Genistein, a tyrosine kinase inhibitor. Antibody-mediated ligation and clustering of integrins on the two types of cells did not result in the stimulation of tyrosine phosphorylation of pp125 focal adhesion kinase, although this was observed upon cell attachment and spreading on fibronectin, laminin and anti-\u03b13 monoclonal antibody. Collectively, these data demonstrate that cross-linking of different integrin het-erodimers can stimulate tyrosine kinase activities, leading to the phosphorylation of distinct proteins, which are also different from those observed when cells are allowed to spread on a matrix.</jats:p>",
  "DOI": "10.1242/jcs.108.3.1165",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        25
      ]
    ],
    "date-time": "2021-04-25T16:15:05Z",
    "timestamp": 1619367305000
  },
  "page": "1165-1174",
  "source": "Crossref",
  "is-referenced-by-count": 38,
  "title": "Stimulation of tyrosine phosphorylation of distinct proteins in response to antibody-mediated ligation and clustering of \u03b13 and \u03b16 integrins",
  "prefix": "10.1242",
  "volume": "108",
  "author": [
    {
      "given": "Kevin",
      "family": "Jewell",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Cancer Research Program, Reichmann Research Building, S-218 Sunnybrook Health Science Centre, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5"
        }
      ]
    },
    {
      "given": "Carolyn",
      "family": "Kapron-Bras",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cancer Research Program, Reichmann Research Building, S-218 Sunnybrook Health Science Centre, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5"
        }
      ]
    },
    {
      "given": "Premala",
      "family": "Jeevaratnam",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cancer Research Program, Reichmann Research Building, S-218 Sunnybrook Health Science Centre, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5"
        }
      ]
    },
    {
      "given": "Shoukat",
      "family": "Dedhar",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cancer Research Program, Reichmann Research Building, S-218 Sunnybrook Health Science Centre, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1995,
        3,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023122401041881600_JOCES_108_3_1165C1",
      "doi-asserted-by": "publisher",
      "first-page": "307",
      "DOI": "10.1038/340307a0",
      "article-title": "Fibronectin inhibits the terminal differentiation of human keratinocytes",
      "volume": "340",
      "author": "Adams",
      "year": "1989",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C2",
      "doi-asserted-by": "publisher",
      "first-page": "5592",
      "DOI": "10.1016/S0021-9258(18)45614-1",
      "article-title": "Genistein, a specific inhibitor of tyrosine-specific protein kinases",
      "volume": "262",
      "author": "Akiyama",
      "year": "1987",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C3",
      "doi-asserted-by": "publisher",
      "first-page": "893",
      "DOI": "10.1083/jcb.119.4.893",
      "article-title": "Tyrosine phosphorylation of paxillin and pp125 FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly",
      "volume": "119",
      "author": "Burridge",
      "year": "1992",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C4",
      "doi-asserted-by": "publisher",
      "first-page": "207",
      "DOI": "10.1016/0014-4827(89)90430-8",
      "article-title": "Signal transduction via the \u03b21 integrins is a required intermediate in interleukin-1\u03b2 induction of alkaline phosphatase activity in human osteosarcoma cells",
      "volume": "183",
      "author": "Dedhar",
      "year": "1989",
      "journal-title": "Exp. Cell. Res"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C5",
      "doi-asserted-by": "publisher",
      "first-page": "583",
      "DOI": "10.1002/bies.950121205",
      "article-title": "Integrins and tumor invasion",
      "volume": "12",
      "author": "Dedhar",
      "year": "1990",
      "journal-title": "BioEssays"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C6",
      "doi-asserted-by": "publisher",
      "first-page": "21846",
      "DOI": "10.1016/S0021-9258(18)54715-3",
      "article-title": "Induction of expression of the \u03b1v\u03b21 and \u03b1v\u03b23 integrin heterodimers during retionic acid-induced neuronal differentiation of murine embryonal carcinoma cells",
      "volume": "266",
      "author": "Dedhar",
      "year": "1991",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C7",
      "doi-asserted-by": "publisher",
      "first-page": "18908",
      "DOI": "10.1016/S0021-9258(19)37047-4",
      "article-title": "The receptor for the basement membrane glycoprotein entactin is the integrin \u03b13/\u03b21",
      "volume": "267",
      "author": "Dedhar",
      "year": "1992",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C8",
      "first-page": "1",
      "article-title": "Differential regulation of expression of specific integrin receptors by nerve growth factor and transforming growth factor \u03b2 during differentiation of human neuroblastoma cells",
      "volume": "1",
      "author": "Dedhar",
      "year": "1993",
      "journal-title": "Mol. Cell Diff"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C9",
      "doi-asserted-by": "publisher",
      "first-page": "391",
      "DOI": "10.1007/BF00132982",
      "article-title": "Specific alterations in the expression of \u03b13\u03b21 and \u03b16\u03b24 integrins in highly invasive and metastatic variants of human prostate carcinoma cells selected by in vitro invasion through reconstituted basement membrane",
      "volume": "11",
      "author": "Dedhar",
      "year": "1993",
      "journal-title": "Clin. Exp. Metast"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C10",
      "doi-asserted-by": "publisher",
      "first-page": "6792",
      "DOI": "10.1073/pnas.85.18.6792",
      "article-title": "Cell adhesion induces expression of growth-associated genes in suspension-arrested fibroblasts",
      "volume": "85",
      "author": "Dike",
      "year": "1988",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C11",
      "doi-asserted-by": "publisher",
      "first-page": "45",
      "DOI": "10.1038/363045a0",
      "article-title": "Association of Sos ras exchange proteins with Grb2 is implicated in tyrosine kinase signal transduction and transformation",
      "volume": "363",
      "author": "Egan",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C12",
      "doi-asserted-by": "publisher",
      "first-page": "951",
      "DOI": "10.1091/mbc.2.11.951",
      "article-title": "Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120 kDa protein",
      "volume": "2",
      "author": "Guan",
      "year": "1991",
      "journal-title": "Cell Regul"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C13",
      "doi-asserted-by": "publisher",
      "first-page": "390",
      "DOI": "10.1038/358690a0",
      "article-title": "Regulation of focal adhesion associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation",
      "volume": "358",
      "author": "Guan",
      "year": "1992",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C14",
      "doi-asserted-by": "publisher",
      "first-page": "473",
      "DOI": "10.1083/jcb.122.2.473",
      "article-title": "Adhesive ligand binding to integrin \u03b1IIb\u03b23 stimulates tyrosine phosphorylation of novel protein substrata before phosphorylation of pp125FAK",
      "volume": "122",
      "author": "Huang",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C15",
      "doi-asserted-by": "publisher",
      "first-page": "11",
      "DOI": "10.1016/0092-8674(92)90115-S",
      "article-title": "Integrins: versatility, modulation, and signaling in cell adhesion",
      "volume": "69",
      "author": "Hynes",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C16",
      "doi-asserted-by": "publisher",
      "first-page": "577",
      "DOI": "10.1083/jcb.120.3.577",
      "article-title": "Signal transduction from the extracellular matrix",
      "volume": "120",
      "author": "Juliano",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C17",
      "doi-asserted-by": "publisher",
      "first-page": "20701",
      "DOI": "10.1016/S0021-9258(19)36834-6",
      "article-title": "Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated \u03b12\u03b21 integrin activation in T-lymphoblastic cells",
      "volume": "268",
      "author": "Kapron-Bras",
      "year": "1993",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C18",
      "doi-asserted-by": "publisher",
      "first-page": "8392",
      "DOI": "10.1073/pnas.88.19.8392",
      "article-title": "Signal transduction by integrins: Increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins",
      "volume": "88",
      "author": "Kornberg",
      "year": "1991",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C19",
      "doi-asserted-by": "publisher",
      "first-page": "23439",
      "DOI": "10.1016/S0021-9258(18)35853-8",
      "article-title": "Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion associated tyrosine kinase",
      "volume": "267",
      "author": "Kornberg",
      "year": "1992",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C20",
      "doi-asserted-by": "publisher",
      "first-page": "680",
      "DOI": "10.1038/227680a0",
      "article-title": "Cleavage of structural proteins during the assembly of the head of bacteriophage T4",
      "volume": "227",
      "author": "Laemmli",
      "year": "1970",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C21",
      "first-page": "5111",
      "article-title": "Inhibitory effects of the tyrosine kinase inhibitor Genistein on mammalian DNA topoisomerase II",
      "volume": "49",
      "author": "Markovits",
      "year": "1989",
      "journal-title": "Cancer Res"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C22",
      "doi-asserted-by": "publisher",
      "first-page": "51",
      "DOI": "10.1016/0092-8674(87)90009-2",
      "article-title": "Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation",
      "volume": "51",
      "author": "Menko",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C23",
      "doi-asserted-by": "publisher",
      "first-page": "1185",
      "DOI": "10.1084/jem.172.4.1185",
      "article-title": "VLA-4 mediates CD3-dependent CD4+ T-cells activation via the CSI alternatively spliced domain of fibronectin",
      "volume": "172",
      "author": "Nojima",
      "year": "1990",
      "journal-title": "J. Exp. Med"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C24",
      "doi-asserted-by": "publisher",
      "first-page": "1045",
      "DOI": "10.1084/jem.175.4.1045",
      "article-title": "Ligation of VLA-4 on T cells stimulates tyrosine phosphorylation of a 105-kD protein",
      "volume": "175",
      "author": "Nojima",
      "year": "1992",
      "journal-title": "J. Exp. Med"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C25",
      "doi-asserted-by": "publisher",
      "first-page": "100",
      "DOI": "10.1016/0014-4827(90)90262-9",
      "article-title": "Nerve growth factor induces increased expression of a laminin-binding integrin in rat pheochromocytoma PC12 cells",
      "volume": "189",
      "author": "Rossino",
      "year": "1990",
      "journal-title": "Exp. Cell Res"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C26",
      "doi-asserted-by": "publisher",
      "first-page": "689",
      "DOI": "10.1038/360689a0",
      "article-title": "Association of the Shc and Grb2/sems SH2 containing proteins is implicated in activation of the Ras pathway by tyrosine kinases",
      "volume": "360",
      "author": "Rozakis-Adcock",
      "year": "1992",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C27",
      "doi-asserted-by": "publisher",
      "first-page": "491",
      "DOI": "10.1126/science.2821619",
      "article-title": "New perspectives in cell adhesion: RGD and integrins",
      "volume": "238",
      "author": "Ruoslahti",
      "year": "1987",
      "journal-title": "Science"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C28",
      "doi-asserted-by": "publisher",
      "first-page": "5192",
      "DOI": "10.1073/pnas.89.11.5192",
      "article-title": "pp125FAK, as structurally distinctive protein-tyrosine kinase associated with focal adhesions",
      "volume": "89",
      "author": "Schaller",
      "year": "1992",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C29",
      "doi-asserted-by": "publisher",
      "first-page": "7849",
      "DOI": "10.1073/pnas.88.17.7849",
      "article-title": "Insoluble fibronectin activates the Na+/H+ antiporter by clustering and immobilizing integrin \u03b15\u03b21, independent of cell shape",
      "volume": "88",
      "author": "Schwartz",
      "year": "1991",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C30",
      "doi-asserted-by": "publisher",
      "first-page": "59",
      "DOI": "10.4049/jimmunol.145.1.59",
      "article-title": "Costimulation of proliferative responses of resting CD4 and T cells by interaction of VLA4 and VLA5 with fibronectin or VLA6 with laminin",
      "volume": "145",
      "author": "Shimizu",
      "year": "1990",
      "journal-title": "J. Immunol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C31",
      "doi-asserted-by": "publisher",
      "first-page": "425",
      "DOI": "10.1038/346425a0",
      "article-title": "Adhesion receptors of the immune system",
      "volume": "346",
      "author": "Springer",
      "year": "1990",
      "journal-title": "Nature"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C32",
      "doi-asserted-by": "publisher",
      "first-page": "523",
      "DOI": "10.1083/jcb.120.2.523",
      "article-title": "Interaction of integrins \u03b13\u03b21 and \u03b12\u03b21: potential role in keratinocyte intercellular adhesion",
      "volume": "120",
      "author": "Symington",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C33",
      "doi-asserted-by": "publisher",
      "first-page": "4350",
      "DOI": "10.1073/pnas.76.9.4350",
      "article-title": "Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications",
      "volume": "76",
      "author": "Towbin",
      "year": "1979",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C34",
      "doi-asserted-by": "publisher",
      "first-page": "901",
      "DOI": "10.1084/jem.174.4.901",
      "article-title": "Analysis of T cell stimulation by superantigen plus major histocompatibility complex class II molecules or by CD3 monoclonal antibody: costimulation by purified adhesion ligans VCAM-1, but not ELAM-1",
      "volume": "174",
      "author": "van Seventer",
      "year": "1991",
      "journal-title": "J. Exp. Med"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C35",
      "doi-asserted-by": "publisher",
      "first-page": "294",
      "DOI": "10.1016/0952-7915(91)90027-X",
      "article-title": "Roles of multiple accessing molecules in T-cell activation",
      "volume": "3",
      "author": "van Seventer",
      "year": "1991",
      "journal-title": "Curr. Opin. Immunol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C36",
      "doi-asserted-by": "publisher",
      "first-page": "877",
      "DOI": "10.1083/jcb.109.2.877",
      "article-title": "Signal transduction through the fibronectin receptor induces collagenase and stromeysin gene expression",
      "volume": "109",
      "author": "Werb",
      "year": "1989",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C37",
      "doi-asserted-by": "publisher",
      "first-page": "53",
      "DOI": "10.4049/jimmunol.146.1.53",
      "article-title": "Activation of human CD4-T lymphocytes: Interaction of fibronectin with VLA-5 receptor on CD4 cells induces the AP-1 transcription factor",
      "volume": "146",
      "author": "Yamada",
      "year": "1991",
      "journal-title": "J. Immunol"
    },
    {
      "key": "2023122401041881600_JOCES_108_3_1165C38",
      "doi-asserted-by": "publisher",
      "first-page": "9034",
      "DOI": "10.1073/pnas.89.19.9034",
      "article-title": "Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction",
      "volume": "89",
      "author": "Yurochko",
      "year": "1992",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    }
  ],
  "container-title": "Journal of Cell Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/108/3/1165/3324748/joces_108_3_1165.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/108/3/1165/3324748/joces_108_3_1165.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        12,
        24
      ]
    ],
    "date-time": "2023-12-24T01:04:32Z",
    "timestamp": 1703379872000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/jcs/article/108/3/1165/24464/Stimulation-of-tyrosine-phosphorylation-of"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1995,
        3,
        1
      ]
    ]
  },
  "references-count": 38,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1995,
          3,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/jcs.108.3.1165",
  "relation": {},
  "ISSN": [
    "0021-9533",
    "1477-9137"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1995,
        3,
        1
      ]
    ]
  }
}