DOI: 10.1091/mbc.12.10.3126. Cross Talk between β1and αVIntegrins: β1Affects β3mRNA Stability

Cross Talk between β1and αVIntegrins: β1Affects β3mRNA Stability

10.1091/mbc.12.10.3126

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

There is increasing evidence that a fine-tuned integrin cross talk can generate a high degree of specificity in cell adhesion, suggesting that spatially and temporally coordinated expression and activation of integrins are more important for regulated cell adhesive functions than the intrinsic specificity of individual receptors. However, little is known concerning the molecular mechanisms of integrin cross talk. With the use of β1-null GD25 cells ectopically expressing the β1A integrin subunit, we provide evidence for the existence of a cross talk between β1and αVintegrins that affects the ratio of αVβ3and αVβ5integrin cell surface levels. In particular, we demonstrate that a down-regulation of αVβ3and an up-regulation of αVβ5occur as a consequence of β1A expression. Moreover, with the use of GD25 cells expressing the integrin isoforms β1B and β1D, as well as two β1cytoplasmic domain deletion mutants lacking either the entire cytoplasmic domain (β1TR) or only its “variable” region (β1COM), we show that the effects of β1over αVintegrins take place irrespective of the type of β1isoform, but require the presence of the “common” region of the β1cytoplasmic domain. In an attempt to establish the regulatory mechanism(s) whereby β1integrins exert theirtrans-acting functions, we have found that the down-regulation of αVβ3is due to a decreased β3subunit mRNA stability, whereas the up-regulation of αVβ5is mainly due to translational or posttranslational events. These findings provide the first evidence for an integrin cross talk based on the regulation of mRNA stability.

Bibliography

Retta, S. F., CassarÃ , G., DâAmato, M., Alessandro, R., Pellegrino, M., Degani, S., De Leo, G., Silengo, L., & Tarone, G. (2001). Cross Talk between Î²1and Î±VIntegrins: Î²1Affects Î²3mRNA Stability. Molecular Biology of the Cell, 12(10), 3126â3138.

Authors 9

Saverio Francesco Retta (first)
Georgia Cassarà (additional)
Monica D'Amato (additional)
Riccardo Alessandro (additional)
Maurizio Pellegrino (additional)
Simona Degani (additional)
Giacomo De Leo (additional)
Lorenzo Silengo (additional)
Guido Tarone (additional)

References 69 Referenced 52

{'key': 'B1', 'first-page': '6757', 'volume': '50', 'author': 'Albelda S.M.', 'year': '1990', 'journal-title': 'Cancer Res.'} / Cancer Res. by Albelda S.M. (1990)
10.1016/S0092-8674(00)81618-9 / Cell by Bader B.L. (1998)
10.1083/jcb.127.2.557 / J. Cell Biol. by Balzac F. (1994)
10.1101/gad.12.8.1202 / Genes Dev. by Baudoin C. (1998)
10.1074/jbc.273.24.15234 / J. Biol. Chem. by Belkin A.M. (1998)
10.1083/jcb.139.6.1583 / J. Cell Biol. by Belkin A.M. (1997)
10.1172/JCI119582 / J. Clin. Invest. by Bilato C (1997)
10.1083/jcb.127.4.1129 / J. Cell Biol. by Blystone S.D. (1994)
10.1083/jcb.145.4.889 / J. Cell Biol. by Blystone S.D. (1999)
10.1242/jcs.110.23.2895 / J. Cell Sci. by Brakebusch C. (1997)
10.1126/science.7512751 / Science by Brooks P.C. (1994)
10.1016/S0171-9335(98)80053-8 / Eur. J. Cell Biol. by Calı̀ G (1998)
10.1016/0092-8674(95)90211-2 / Cell by Carroll J.M. (1995)
10.1111/j.1365-2133.1996.tb03606.x / Br. J. Dermatol. by Clark R.A. (1996)
{'key': 'B15', 'first-page': '1407', 'volume': '148', 'author': 'Clark R.A.', 'year': '1996', 'journal-title': 'Am. J. Pathol.'} / Am. J. Pathol. by Clark R.A. (1996)
10.1006/jsre.1998.5552 / J. Surg. Res. by Corbett S.A. (1999)
10.1016/S0955-0674(99)00067-8 / Curr. Opin. Cell Biol. by Critchley D.R. (2000)
10.1016/S0248-4900(00)88760-2 / Biol. Cell by Darribere T. (2000)
10.1006/excr.1995.1361 / Exp. Cell Res. by Defilippi P. (1995)
10.1016/S0021-9258(20)89495-2 / J. Biol. Chem. by Defilippi P. (1991)
10.1074/jbc.270.45.26794 / J. Biol. Chem. by Delcommenne M. (1995)
10.1016/S0955-0674(96)80105-0 / Curr. Opin. Cell Biol. by Fassler R. (1996)
10.1242/jcs.92.1.67 / J. Cell Sci. by Fath K.R. (1989)
10.1046/j.1523-1747.1999.00786.x / J. Invest. Dermatol. by Feng X. (1999)
10.1016/S0945-053X(97)90007-X / Matrix Biol. by Fornaro M. (1997)
10.1126/science.270.5241.1500 / Science by Friedlander M. (1995)
10.1016/S0955-0674(97)80123-8 / Curr. Opin. Cell Biol. by Giancotti F.G. (1997)
10.1038/71397 / Nat. Cell Biol. by Giancotti F.G. (2000)
10.1126/science.285.5430.1028 / Science by Giancotti F.G. (1999)
10.1006/jmcc.2000.1326 / J. Mol. Cell Cardiol. by Guan K. (2001)
10.1242/jcs.111.16.2397 / J. Cell Sci. by Hirsch E. (1998)
10.1172/JCI5487 / J. Clin. Invest. by Hodivala-Dilke K.M. (1999)
10.1016/0092-8674(92)90115-S / Cell by Hynes R.O. (1992)
10.1006/dbio.1996.0314 / Dev. Biol. by Hynes R.O. (1996)
10.1016/S0962-8924(99)01667-0 / Trends Cell Biol. by Hynes R.O. (1999)
10.1002/jcp.1041510319 / J. Cell Physiol. by Janat M.F. (1992)
10.3181/00379727-214-44078 / Proc. Soc. Exp. Biol. Med. by Kim L.T. (1997)
10.1083/jcb.127.3.859 / J. Cell Biol. by Klemke R.L. (1994)
10.1016/0962-8924(94)90124-4 / Trends Cell Biol. by Kühn K. (1994)
10.1083/jcb.117.5.1101 / J. Cell Biol. by Leavesley D.I (1992)
10.1083/jcb.134.5.1323 / J. Cell Biol. by Lewis J.M. (1996)
10.1159/000024494 / Invasion Metastasis by Li X. (1998)
10.1242/jcs.113.20.3563 / J. Cell Sci. by Liu S. (2000)
10.1002/ijc.2910490621 / Int. J. Cancer by Marshall J.F. (1991)
10.1172/JCI8905 / J. Clin. Invest. by McHugh K.P. (2000)
10.1016/S0021-9258(18)54097-7 / J. Biol. Chem. by Medhora M.M. (1993)
10.1073/pnas.91.19.8856 / Proc. Natl. Acad. Sci. USA by Montgomery A.M. (1994)
10.1074/jbc.273.11.6104 / J. Biol. Chem. by Pfaff M. (1998)
10.1083/jcb.138.6.1437 / J. Cell Biol. by Porter J.C. (1997)
10.1091/mbc.9.4.715
10.1006/excr.1996.0376 / Exp. Cell Res. by Retta S.F. (1996)
{'key': 'B52', 'first-page': '119', 'volume': '96', 'author': 'Retta S.F.', 'year': '1999', 'journal-title': 'Methods Mol. Biol.'} / Methods Mol. Biol. by Retta S.F. (1999)
10.1016/0092-8674(93)80043-E / Cell. by Sachs A.B. (1993)
10.1083/jcb.133.1.169 / J. Cell Biol. by Sastry S.K. (1996)
10.1016/S0955-0674(99)80037-4 / Curr. Opin. Cell Biol. by Schoenwaelder S.M. (1999)
10.1111/1523-1747.ep12394617 / J. Invest. Dermatol. by Sepp N.T. (1994)
10.1074/jbc.272.46.29380 / J. Biol. Chem. by Simon K.O. (1997)
10.1111/1523-1747.ep12614207 / J. Invest. Dermatol. by Swerlick R.A. (1992)
{'key': 'B59', 'first-page': '725', 'volume': '44', 'author': 'Tarone G.', 'year': '2000', 'journal-title': 'Int. J. Dev. Biol.'} / Int. J. Dev. Biol. by Tarone G. (2000)
10.1006/excr.1998.4315 / Exp. Cell Res. by Tomatis D. (1999)
10.1016/S0955-0674(96)80115-3 / Curr. Opin. Cell Biol. by Varner J.A. (1996)
10.1083/jcb.113.4.919 / J. Cell Biol. by Wayner E.A. (1991)
10.1083/jcb.132.1.227 / J. Cell Biol. by Wennerberg K. (1996)
10.3109/15419069609014219 / Cell Adhes. Commun. by Wu C. (1996)
10.1083/jcb.132.1.239 / J. Cell Biol. by Xu J. (1996)
10.3109/15419069509081016 / Cell Adhes. Commun. by Yamada S. (1995)
10.1006/dbio.1999.9451 / Dev. Biol. by Yang J.T. (1999)
10.1091/mbc.7.11.1737
{'key': 'B69', 'first-page': '3103', 'volume': '56', 'author': 'Yun Z.', 'year': '1996', 'journal-title': 'Cancer Res.'} / Cancer Res. by Yun Z. (1996)

Dates

Type	When
Created	12 years, 2 months ago (July 2, 2013, 8:03 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:43 p.m.)
Indexed	2 months, 2 weeks ago (June 17, 2025, 11:30 a.m.)
Issued	23 years, 11 months ago (Oct. 1, 2001)
Published	23 years, 11 months ago (Oct. 1, 2001)
Published Print	23 years, 11 months ago (Oct. 1, 2001)

Funders 0

None

BibTeX

@article{Retta_2001, title={Cross Talk between β1and αVIntegrins: β1Affects β3mRNA Stability}, volume={12}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.12.10.3126}, DOI={10.1091/mbc.12.10.3126}, number={10}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Retta, Saverio Francesco and Cassarà, Georgia and D’Amato, Monica and Alessandro, Riccardo and Pellegrino, Maurizio and Degani, Simona and De Leo, Giacomo and Silengo, Lorenzo and Tarone, Guido}, editor={Hynes, Richard}, year={2001}, month=oct, pages={3126–3138} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        17
      ]
    ],
    "date-time": "2025-06-17T15:30:39Z",
    "timestamp": 1750174239010
  },
  "reference-count": 69,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "10",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        10
      ]
    ]
  },
  "abstract": "<jats:p>There is increasing evidence that a fine-tuned integrin cross talk can generate a high degree of specificity in cell adhesion, suggesting that spatially and temporally coordinated expression and activation of integrins are more important for regulated cell adhesive functions than the intrinsic specificity of individual receptors. However, little is known concerning the molecular mechanisms of integrin cross talk. With the use of \u03b2<jats:sub>1</jats:sub>-null GD25 cells ectopically expressing the \u03b2<jats:sub>1</jats:sub>A integrin subunit, we provide evidence for the existence of a cross talk between \u03b2<jats:sub>1</jats:sub>and \u03b1<jats:sub>V</jats:sub>integrins that affects the ratio of \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>3</jats:sub>and \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>5</jats:sub>integrin cell surface levels. In particular, we demonstrate that a down-regulation of \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>3</jats:sub>and an up-regulation of \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>5</jats:sub>occur as a consequence of \u03b2<jats:sub>1</jats:sub>A expression. Moreover, with the use of GD25 cells expressing the integrin isoforms \u03b2<jats:sub>1</jats:sub>B and \u03b2<jats:sub>1</jats:sub>D, as well as two \u03b2<jats:sub>1</jats:sub>cytoplasmic domain deletion mutants lacking either the entire cytoplasmic domain (\u03b2<jats:sub>1</jats:sub>TR) or only its \u201cvariable\u201d region (\u03b2<jats:sub>1</jats:sub>COM), we show that the effects of \u03b2<jats:sub>1</jats:sub>over \u03b1<jats:sub>V</jats:sub>integrins take place irrespective of the type of \u03b2<jats:sub>1</jats:sub>isoform, but require the presence of the \u201ccommon\u201d region of the \u03b2<jats:sub>1</jats:sub>cytoplasmic domain. In an attempt to establish the regulatory mechanism(s) whereby \u03b2<jats:sub>1</jats:sub>integrins exert theirtrans-acting functions, we have found that the down-regulation of \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>3</jats:sub>is due to a decreased \u03b2<jats:sub>3</jats:sub>subunit mRNA stability, whereas the up-regulation of \u03b1<jats:sub>V</jats:sub>\u03b2<jats:sub>5</jats:sub>is mainly due to translational or posttranslational events. These findings provide the first evidence for an integrin cross talk based on the regulation of mRNA stability.</jats:p>",
  "DOI": "10.1091/mbc.12.10.3126",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        7,
        3
      ]
    ],
    "date-time": "2013-07-03T00:03:26Z",
    "timestamp": 1372809806000
  },
  "page": "3126-3138",
  "source": "Crossref",
  "is-referenced-by-count": 52,
  "title": "Cross Talk between \u03b2<sub>1</sub>and \u03b1<sub>V</sub>Integrins: \u03b2<sub>1</sub>Affects \u03b2<sub>3</sub>mRNA Stability",
  "prefix": "10.1091",
  "volume": "12",
  "author": [
    {
      "given": "Saverio Francesco",
      "family": "Retta",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Genetics, Biology, and Biochemistry, University of Torino, 10126 Torino, Italy; and"
        }
      ]
    },
    {
      "given": "Georgia",
      "family": "Cassar\u00e0",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biopatologia e Metodologie Biomediche, University of Palermo, 90133 Palermo, Italy"
        }
      ]
    },
    {
      "given": "Monica",
      "family": "D'Amato",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biopatologia e Metodologie Biomediche, University of Palermo, 90133 Palermo, Italy"
        }
      ]
    },
    {
      "given": "Riccardo",
      "family": "Alessandro",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biopatologia e Metodologie Biomediche, University of Palermo, 90133 Palermo, Italy"
        }
      ]
    },
    {
      "given": "Maurizio",
      "family": "Pellegrino",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Genetics, Biology, and Biochemistry, University of Torino, 10126 Torino, Italy; and"
        }
      ]
    },
    {
      "given": "Simona",
      "family": "Degani",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Genetics, Biology, and Biochemistry, University of Torino, 10126 Torino, Italy; and"
        }
      ]
    },
    {
      "given": "Giacomo",
      "family": "De Leo",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biopatologia e Metodologie Biomediche, University of Palermo, 90133 Palermo, Italy"
        }
      ]
    },
    {
      "given": "Lorenzo",
      "family": "Silengo",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Genetics, Biology, and Biochemistry, University of Torino, 10126 Torino, Italy; and"
        }
      ]
    },
    {
      "given": "Guido",
      "family": "Tarone",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Genetics, Biology, and Biochemistry, University of Torino, 10126 Torino, Italy; and"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "first-page": "6757",
      "volume": "50",
      "author": "Albelda S.M.",
      "year": "1990",
      "journal-title": "Cancer Res."
    },
    {
      "key": "B2",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1016/S0092-8674(00)81618-9",
      "volume": "95",
      "author": "Bader B.L.",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "557",
      "DOI": "10.1083/jcb.127.2.557",
      "volume": "127",
      "author": "Balzac F.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "1202",
      "DOI": "10.1101/gad.12.8.1202",
      "volume": "12",
      "author": "Baudoin C.",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "15234",
      "DOI": "10.1074/jbc.273.24.15234",
      "volume": "273",
      "author": "Belkin A.M.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "1583",
      "DOI": "10.1083/jcb.139.6.1583",
      "volume": "139",
      "author": "Belkin A.M.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "693",
      "DOI": "10.1172/JCI119582",
      "volume": "100",
      "author": "Bilato C",
      "year": "1997",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "1129",
      "DOI": "10.1083/jcb.127.4.1129",
      "volume": "127",
      "author": "Blystone S.D.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "889",
      "DOI": "10.1083/jcb.145.4.889",
      "volume": "145",
      "author": "Blystone S.D.",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "2895",
      "DOI": "10.1242/jcs.110.23.2895",
      "volume": "110",
      "author": "Brakebusch C.",
      "year": "1997",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "569",
      "DOI": "10.1126/science.7512751",
      "volume": "264",
      "author": "Brooks P.C.",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "107",
      "DOI": "10.1016/S0171-9335(98)80053-8",
      "volume": "75",
      "author": "Cal\u0131\u0300 G",
      "year": "1998",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "957",
      "DOI": "10.1016/0092-8674(95)90211-2",
      "volume": "83",
      "author": "Carroll J.M.",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "46",
      "DOI": "10.1111/j.1365-2133.1996.tb03606.x",
      "volume": "135",
      "author": "Clark R.A.",
      "year": "1996",
      "journal-title": "Br. J. Dermatol."
    },
    {
      "key": "B15",
      "first-page": "1407",
      "volume": "148",
      "author": "Clark R.A.",
      "year": "1996",
      "journal-title": "Am. J. Pathol."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "27",
      "DOI": "10.1006/jsre.1998.5552",
      "volume": "83",
      "author": "Corbett S.A.",
      "year": "1999",
      "journal-title": "J. Surg. Res."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "133",
      "DOI": "10.1016/S0955-0674(99)00067-8",
      "volume": "12",
      "author": "Critchley D.R.",
      "year": "2000",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1016/S0248-4900(00)88760-2",
      "volume": "92",
      "author": "Darribere T.",
      "year": "2000",
      "journal-title": "Biol. Cell"
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1006/excr.1995.1361",
      "volume": "221",
      "author": "Defilippi P.",
      "year": "1995",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "7638",
      "DOI": "10.1016/S0021-9258(20)89495-2",
      "volume": "266",
      "author": "Defilippi P.",
      "year": "1991",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "26794",
      "DOI": "10.1074/jbc.270.45.26794",
      "volume": "270",
      "author": "Delcommenne M.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "641",
      "DOI": "10.1016/S0955-0674(96)80105-0",
      "volume": "8",
      "author": "Fassler R.",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "67",
      "DOI": "10.1242/jcs.92.1.67",
      "volume": "92",
      "author": "Fath K.R.",
      "year": "1989",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "913",
      "DOI": "10.1046/j.1523-1747.1999.00786.x",
      "volume": "113",
      "author": "Feng X.",
      "year": "1999",
      "journal-title": "J. Invest. Dermatol."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "185",
      "DOI": "10.1016/S0945-053X(97)90007-X",
      "volume": "16",
      "author": "Fornaro M.",
      "year": "1997",
      "journal-title": "Matrix Biol."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "1500",
      "DOI": "10.1126/science.270.5241.1500",
      "volume": "270",
      "author": "Friedlander M.",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "691",
      "DOI": "10.1016/S0955-0674(97)80123-8",
      "volume": "9",
      "author": "Giancotti F.G.",
      "year": "1997",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "E13",
      "DOI": "10.1038/71397",
      "volume": "2",
      "author": "Giancotti F.G.",
      "year": "2000",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "1028",
      "DOI": "10.1126/science.285.5430.1028",
      "volume": "285",
      "author": "Giancotti F.G.",
      "year": "1999",
      "journal-title": "Science"
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "521",
      "DOI": "10.1006/jmcc.2000.1326",
      "volume": "33",
      "author": "Guan K.",
      "year": "2001",
      "journal-title": "J. Mol. Cell Cardiol."
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "2397",
      "DOI": "10.1242/jcs.111.16.2397",
      "volume": "111",
      "author": "Hirsch E.",
      "year": "1998",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1172/JCI5487",
      "volume": "103",
      "author": "Hodivala-Dilke K.M.",
      "year": "1999",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1016/0092-8674(92)90115-S",
      "volume": "69",
      "author": "Hynes R.O.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "402",
      "DOI": "10.1006/dbio.1996.0314",
      "volume": "180",
      "author": "Hynes R.O.",
      "year": "1996",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "33",
      "DOI": "10.1016/S0962-8924(99)01667-0",
      "volume": "9",
      "author": "Hynes R.O.",
      "year": "1999",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "588",
      "DOI": "10.1002/jcp.1041510319",
      "volume": "151",
      "author": "Janat M.F.",
      "year": "1992",
      "journal-title": "J. Cell Physiol."
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "123",
      "DOI": "10.3181/00379727-214-44078",
      "volume": "214",
      "author": "Kim L.T.",
      "year": "1997",
      "journal-title": "Proc. Soc. Exp. Biol. Med."
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "859",
      "DOI": "10.1083/jcb.127.3.859",
      "volume": "127",
      "author": "Klemke R.L.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "256",
      "DOI": "10.1016/0962-8924(94)90124-4",
      "volume": "4",
      "author": "K\u00fchn K.",
      "year": "1994",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "1101",
      "DOI": "10.1083/jcb.117.5.1101",
      "volume": "117",
      "author": "Leavesley D.I",
      "year": "1992",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "1323",
      "DOI": "10.1083/jcb.134.5.1323",
      "volume": "134",
      "author": "Lewis J.M.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1159/000024494",
      "volume": "18",
      "author": "Li X.",
      "year": "1998",
      "journal-title": "Invasion Metastasis"
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "3563",
      "DOI": "10.1242/jcs.113.20.3563",
      "volume": "113",
      "author": "Liu S.",
      "year": "2000",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "924",
      "DOI": "10.1002/ijc.2910490621",
      "volume": "49",
      "author": "Marshall J.F.",
      "year": "1991",
      "journal-title": "Int. J. Cancer"
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1172/JCI8905",
      "volume": "105",
      "author": "McHugh K.P.",
      "year": "2000",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "1456",
      "DOI": "10.1016/S0021-9258(18)54097-7",
      "volume": "268",
      "author": "Medhora M.M.",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B47",
      "doi-asserted-by": "crossref",
      "first-page": "8856",
      "DOI": "10.1073/pnas.91.19.8856",
      "volume": "91",
      "author": "Montgomery A.M.",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "6104",
      "DOI": "10.1074/jbc.273.11.6104",
      "volume": "273",
      "author": "Pfaff M.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "1437",
      "DOI": "10.1083/jcb.138.6.1437",
      "volume": "138",
      "author": "Porter J.C.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.9.4.715"
    },
    {
      "key": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "307",
      "DOI": "10.1006/excr.1996.0376",
      "volume": "229",
      "author": "Retta S.F.",
      "year": "1996",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B52",
      "first-page": "119",
      "volume": "96",
      "author": "Retta S.F.",
      "year": "1999",
      "journal-title": "Methods Mol. Biol."
    },
    {
      "key": "B53",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1016/0092-8674(93)80043-E",
      "volume": "74",
      "author": "Sachs A.B.",
      "year": "1993",
      "journal-title": "Cell."
    },
    {
      "key": "B54",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1083/jcb.133.1.169",
      "volume": "133",
      "author": "Sastry S.K.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B55",
      "doi-asserted-by": "crossref",
      "first-page": "274",
      "DOI": "10.1016/S0955-0674(99)80037-4",
      "volume": "11",
      "author": "Schoenwaelder S.M.",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B56",
      "doi-asserted-by": "crossref",
      "first-page": "295",
      "DOI": "10.1111/1523-1747.ep12394617",
      "volume": "103",
      "author": "Sepp N.T.",
      "year": "1994",
      "journal-title": "J. Invest. Dermatol."
    },
    {
      "key": "B57",
      "doi-asserted-by": "crossref",
      "first-page": "29380",
      "DOI": "10.1074/jbc.272.46.29380",
      "volume": "272",
      "author": "Simon K.O.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B58",
      "doi-asserted-by": "crossref",
      "first-page": "715",
      "DOI": "10.1111/1523-1747.ep12614207",
      "volume": "99",
      "author": "Swerlick R.A.",
      "year": "1992",
      "journal-title": "J. Invest. Dermatol."
    },
    {
      "key": "B59",
      "first-page": "725",
      "volume": "44",
      "author": "Tarone G.",
      "year": "2000",
      "journal-title": "Int. J. Dev. Biol."
    },
    {
      "key": "B60",
      "doi-asserted-by": "crossref",
      "first-page": "421",
      "DOI": "10.1006/excr.1998.4315",
      "volume": "246",
      "author": "Tomatis D.",
      "year": "1999",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B61",
      "doi-asserted-by": "crossref",
      "first-page": "724",
      "DOI": "10.1016/S0955-0674(96)80115-3",
      "volume": "8",
      "author": "Varner J.A.",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B62",
      "doi-asserted-by": "crossref",
      "first-page": "919",
      "DOI": "10.1083/jcb.113.4.919",
      "volume": "113",
      "author": "Wayner E.A.",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B63",
      "doi-asserted-by": "crossref",
      "first-page": "227",
      "DOI": "10.1083/jcb.132.1.227",
      "volume": "132",
      "author": "Wennerberg K.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B64",
      "doi-asserted-by": "crossref",
      "first-page": "149",
      "DOI": "10.3109/15419069609014219",
      "volume": "4",
      "author": "Wu C.",
      "year": "1996",
      "journal-title": "Cell Adhes. Commun."
    },
    {
      "key": "B65",
      "doi-asserted-by": "crossref",
      "first-page": "239",
      "DOI": "10.1083/jcb.132.1.239",
      "volume": "132",
      "author": "Xu J.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B66",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.3109/15419069509081016",
      "volume": "3",
      "author": "Yamada S.",
      "year": "1995",
      "journal-title": "Cell Adhes. Commun."
    },
    {
      "key": "B67",
      "doi-asserted-by": "crossref",
      "first-page": "264",
      "DOI": "10.1006/dbio.1999.9451",
      "volume": "215",
      "author": "Yang J.T.",
      "year": "1999",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "B68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.7.11.1737"
    },
    {
      "key": "B69",
      "first-page": "3103",
      "volume": "56",
      "author": "Yun Z.",
      "year": "1996",
      "journal-title": "Cancer Res."
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        27
      ]
    ],
    "date-time": "2022-02-27T02:43:49Z",
    "timestamp": 1645929829000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.12.10.3126"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Richard",
      "family": "Hynes",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        10
      ]
    ]
  },
  "references-count": 69,
  "journal-issue": {
    "issue": "10",
    "published-print": {
      "date-parts": [
        [
          2001,
          10
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.12.10.3126"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.12.10.3126",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2001,
        10
      ]
    ]
  }
}