Advertisement
Journal Articles
Actin ‘purse string’ filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement
Y. Danjo, I.K. Gipson
Journal of Cell Science 1998 111: 3323-3332;

Summary

At the leading edge of healing embryonic epithelium, cables of actin filaments appear to extend from cell to cell, forming a ring around the wound circumference. It has been hypothesized that this actin filament cable functions as a contractile ‘purse string’ to facilitate wound closure. We have observed this cable in large, circular healing epithelial wounds in corneas of adult mice. To elucidate the role of the actin filament cable, we characterized the molecular components associated with the cell-cell junction where the actin filament cable inserts and with the actin filament cable itself, and we studied the effect of disruption of the cable using an E-cadherin function-blocking antibody, ECCD-1. Localization of E-cadherin and the direct association of catenins with actin filament cable at the cell-cell interface of the actin cable confirmed that the cell-cell junction associated with the actin filament cable is an adherens junction. The E-cadherin function-blocking antibody caused disruption of the actin filament cable and induction of prominent lamellipodial extensions on cells at the leading edge, leading to a ragged uneven epithelial wound margin. These data demonstrate that cell-to-cell associated E-cadherin molecules link the actin filament cable, forming a functional adherens junction, and that the actin filament cable plays a role in coordinating cell movement.

REFERENCES

    1. Adams C. L.,
    2. Nelson W. J. and
    3. Smith S. J.
    (1996). Quantitative analysis of cadherin-catenin-actin reorganization during development of cell-cell adhesion. J. Cell Biol 135, 1899–1911
    OpenUrlAbstract/FREE Full Text
    1. Angres B.,
    2. Barth A. and
    3. Nelson W. J.
    (1996). Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J. Cell Biol 134, 549–557
    OpenUrlAbstract/FREE Full Text
    1. Bement W. M.,
    2. Forscher P. and
    3. Mooseker M. S.
    (1993). A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol 121, 565–578
    OpenUrlAbstract/FREE Full Text
    1. Braga V. M.,
    2. Machesky L. M.,
    3. Hall A. and
    4. Hotchin N. A.
    (1997). The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol 137, 1421–1431
    OpenUrlAbstract/FREE Full Text
    1. Brock J.,
    2. Midwinter K.,
    3. Lewis J. and
    4. Martin P.
    (1996). Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement for Rho activation. J. Cell Biol 135, 1097–1107
    OpenUrlAbstract/FREE Full Text
    1. Buck R. C.
    (1979). Cell migration in repair of mouse corneal epithelium. Invest. Ophthalmol. Vis. Sci 18, 767–784
    OpenUrlAbstract/FREE Full Text
    1. Burridge K.,
    2. Fath K.,
    3. Kelly T.,
    4. Nuckolls G. and
    5. Turner C.
    (1988). Focal adhesions: Transmembrane junctions between the extracellular matrix and cytoskeleton. Annu. Rev. Cell Biol 4, 487–525
    OpenUrlCrossRefWeb of Science
    1. Condeelis J.
    (1993). Life at the leading edge: the formation of cell protrusions. Annu. Rev. Cell Biol 9, 411–444
    OpenUrlCrossRefWeb of Science
    1. Conrad P. A.,
    2. Nederlof M. A.,
    3. Herman I. M. and
    4. Taylor D. L.
    (1989). Correlated distribution of actin, myosin, and microtubules at the leading edge of migrating Swiss 3T3 fibroblasts. Cell Motil. Cytoskel 14, 527–543
    OpenUrlCrossRefPubMedWeb of Science
    1. Cowin P.,
    2. Kapprell H. P.,
    3. Franke W. W.,
    4. Tamkun J. and
    5. Hynes R. O.
    (1986). Plakoglobin: a protein common to different kinds of intercellular adhering junctions. Cell 46, 1063–1073
    OpenUrlCrossRefPubMedWeb of Science
    1. Cramer L. P.,
    2. Mitchison T. J. and
    3. Theriot J. A.
    (1994). Actin-dependent motile forces and cell motility. Curr. Opin. Cell Biol 6, 82–86
    OpenUrlCrossRefPubMedWeb of Science
    1. Fey E. G.,
    2. Wan K. M. and
    3. Penman S.
    (1984). Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition. J. Cell Biol 98, 1973–1984
    OpenUrlAbstract/FREE Full Text
    1. Geiger B. and
    2. Ginsberg D.
    (1991). The cytoplasmic domain of adherens-type junctions. Cell. Motil. Cytoskel 20, 1–6
    OpenUrlCrossRefPubMedWeb of Science
    1. Geiger B. and
    2. Ayalon O.
    (1992). Cadherins. Annu. Rev. Cell. Biol 8, 307–332
    OpenUrlCrossRefWeb of Science
    1. Gipson I. K. and
    2. Anderson R. A.
    (1977). Actin filaments in normal and migrating corneal epithelial cells. Invest. Ophthalmol. Vis. Sci 16, 161–166
    OpenUrlAbstract
    1. Gipson I. K. and
    2. Keezer L.
    (1982). Effects of cytochalasins and colchicine on the ultrastructure of migrating corneal epithelium. Invest. Ophthalmol. Vis. Sci 22, 643–650
    OpenUrlAbstract/FREE Full Text
    1. Gipson I. K. and
    2. Kiorpes T. C.
    (1982). Epithelial sheet movement: protein and glycoprotein synthesis. Dev. Biol 92, 259–262
    OpenUrlCrossRefPubMedWeb of Science
    1. Gipson I. K.,
    2. Westcott M. J. and
    3. Brooksby N. G.
    (1982). Effects of cytochalasins B and D and colchicine on migration of the corneal epithelium. Invest. Ophthalmol. Vis. Sci 22, 633–642
    OpenUrlAbstract/FREE Full Text
    1. Hatta K.,
    2. Okada T. S. and
    3. Takeichi M.
    (1985). A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. Proc. Nat. Acad. Sci. USA 82, 2789–2793
    OpenUrlAbstract/FREE Full Text
    1. Hirai Y.,
    2. Nose A.,
    3. Kobayashi S. and
    4. Takeichi M.
    (1989). Expression and role of E-and P-cadherin adhesion molecules in embryonic histogenesis. I. Lung epithelial morphogenesis. Development 105, 263–270
    OpenUrlAbstract
    1. Hirai Y.,
    2. Nose A.,
    3. Kobayashi S. and
    4. Takeichi M.
    (1989). Expression and role of E-and P-cadherin adhesion molecules in embryonic histogenesis. II. Skin morphogenesis. Development 105, 271–277
    OpenUrlAbstract
    1. Itoh M.,
    2. Nagafuchi A.,
    3. Yonemura S.,
    4. Kitani-Yasuda T.,
    5. Tsukita S. and
    6. Tsukita S.
    (1993). The 220-kD protein colocalizing with cadherin in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J. Cell Biol 121, 491–502
    OpenUrlAbstract/FREE Full Text
    1. Itoh M.,
    2. Nagafuchi A.,
    3. Moroi S. and
    4. Tsukita S.
    (1997). Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to-catenin and actin filaments. J. Cell Biol 138, 181–192
    OpenUrlAbstract/FREE Full Text
    1. Jockusch B. M.,
    2. Bubeck P.,
    3. Giehl K.,
    4. Kroemker M.,
    5. Moschner J.,
    6. Rothkegel M.,
    7. Rudiger M.,
    8. Schluter K.,
    9. Stanke G. and
    10. Winkler J.
    (1995). The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol 11, 379–416
    OpenUrlCrossRefPubMedWeb of Science
    1. Kemler R.
    (1993). From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 9, 317–321
    OpenUrlCrossRefPubMedWeb of Science
    1. Kolega J.
    (1997). Asymmetry in the distribution of free versus cytoskeletal myosin II in locomoting microcapillary endothelial cells. Exp. Cell Res 231, 66–82
    OpenUrlCrossRefPubMedWeb of Science
    1. Lauffenburger D. A. and
    2. Horwitz A. F.
    (1996). Cell migration: a physically integrated molecular process. Cell 84, 359–369
    OpenUrlCrossRefPubMedWeb of Science
    1. Lavker R. M.,
    2. Dong G.,
    3. Cheng S. Z.,
    4. Kudoh K.,
    5. Cotsarelis G. and
    6. Sun T. T.
    (1991). Relative proliferative rates of limbal and corneal epithelia. Implications of corneal epithelial migration, circadian rhythm, and suprabasally located DNA-synthesizing keratinocytes. Invest. Ophthalmol. Vis. Sci 32, 1864–1875
    OpenUrlAbstract/FREE Full Text
    1. Martin P. and
    2. Lewis J.
    (1992). Actin cables and epidermal movement in embryonic wound healing. Nature 360, 179–183
    OpenUrlCrossRefPubMed
    1. McNeill H.,
    2. Ozawa M.,
    3. Kemler R. and
    4. Nelson W. J.
    (1990). Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell 62, 309–316
    OpenUrlCrossRefPubMedWeb of Science
    1. McNeill H.,
    2. Ryan T. A.,
    3. Smith S. J. and
    4. Nelson W. J.
    (1993). Spatial and temporal dissection of immediate and early events following cadherin-mediated epithelial cell adhesion. J. Cell Biol 120, 1217–1226
    OpenUrlAbstract/FREE Full Text
    1. Mitchison T. J. and
    2. Cramer L. P.
    (1996). Actin-based cell motility and cell locomotion. Cell 84, 371–379
    OpenUrlCrossRefPubMedWeb of Science
    1. Nagafuchi A. and
    2. Takeichi M.
    (1988). Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J 7, 3679–3684
    OpenUrlPubMedWeb of Science
    1. Näthke I. S.,
    2. Hinck L.,
    3. Swedlow J. R.,
    4. Papkoff J. and
    5. Nelson W. J.
    (1994). Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol 125, 1341–1352
    OpenUrlAbstract/FREE Full Text
    1. Ogou S.,
    2. Yoshida-Noro C. and
    3. Takeichi M.
    (1983). Calcium-dependent cell-cell adhesion molecules common to hepatocytes and teratocarcinoma stem cells. J. Cell Biol 97, 944–948
    OpenUrlAbstract/FREE Full Text
    1. Overduin M.,
    2. Harvey T. S.,
    3. Bagby S.,
    4. Tong K. I.,
    5. Yau P.,
    6. Takeichi M. and
    7. Ikura M.
    (1995). Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 267, 386–389
    OpenUrlAbstract/FREE Full Text
    1. Ozawa M.,
    2. Baribault H. and
    3. Kemler R.
    (1989). The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO. J 8, 1711–1717
    OpenUrlPubMedWeb of Science
    1. Ozawa M.,
    2. Ringwald M. and
    3. Kemler R.
    (1990). Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Nat. Acad. Sci. USA 87, 4246–4250
    OpenUrlAbstract/FREE Full Text
    1. Rajasekaran A. K.,
    2. Hojo M.,
    3. Huima T. and
    4. Rodriguez-Boulan E.
    (1996). Catenins and Zonula Occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol 132, 451–463
    OpenUrlAbstract/FREE Full Text
    1. Richardson K. C.,
    2. Jarett L. and
    3. Finke E. H.
    (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35, 313–323
    OpenUrlPubMedWeb of Science
    1. Ridley A. J. and
    2. Hall A.
    (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389–399
    OpenUrlCrossRefPubMedWeb of Science
    1. Shimoyama Y.,
    2. Hirohashi S.,
    3. Hirano S.,
    4. Noguchi M.,
    5. Shimosato Y.,
    6. Takeichi M. and
    7. Abe O.
    (1989). Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res 49, 2128–2133
    OpenUrlAbstract/FREE Full Text
    1. Small J. V.
    (1994). Lamellipodia architecture: actin filament turnover and the lateral flow of actin filaments during motility. Semin. Cell Biol 5, 157–163
    OpenUrlCrossRefPubMed
    1. Spurr-Michaud S. J.,
    2. Barza M. and
    3. Gipson I. K.
    (1988). An organ culture system for study of adherence of pseudomonas aeruginosa to normal and wounded corneas. Invest. Ophthalmol. Vis. Sci 29, 379–386
    OpenUrlAbstract/FREE Full Text
    1. Stevenson B. R.,
    2. Siliciano J. D.,
    3. Mooseker M. S. and
    4. Goodenough D. A.
    (1986). Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol 103, 755–766
    OpenUrlAbstract/FREE Full Text
    1. Stossel T. P.
    (1993). On the crawling of animal cells. Science 260, 1086–1094
    OpenUrlAbstract/FREE Full Text
    1. Svitkina T. M.,
    2. Verkhovsky A. B.,
    3. McQuade K. M. and
    4. Borisy G. G.
    (1997). Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol 139, 397–415
    OpenUrlAbstract/FREE Full Text
    1. Takaishi K.,
    2. Sasaki T.,
    3. Kotani H.,
    4. Nishioka H. and
    5. Takai Y.
    (1997). Regulation of cell-cell adhesion by rac and rho small G proteins in MDCK cells. J. Cell Biol 139, 1047–1059
    OpenUrlAbstract/FREE Full Text
    1. Takeichi M.
    (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451–1455
    OpenUrlAbstract/FREE Full Text
    1. Tsukita S.,
    2. Tsukita S.,
    3. Nagafuchi A. and
    4. Yonemura S.
    (1992). Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol 4, 834–839
    OpenUrlCrossRefPubMed
    1. Yap A. S.,
    2. Brieher W. M. and
    3. Gumbiner B. M.
    (1997). Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol 13, 119–146
    OpenUrlCrossRefPubMedWeb of Science
    1. Yonemura S.,
    2. Itoh M.,
    3. Nagafuchi A. and
    4. Tsukita S.
    (1995). Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J. Cell Sci 108, 127–142
    OpenUrlAbstract/FREE Full Text
    1. Yoshida-Noro C.,
    2. Suzuki N. and
    3. Takeichi M.
    (1984). Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev. Biol 101, 19–27
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
Journal Articles
Actin ‘purse string’ filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement
Y. Danjo, I.K. Gipson
Journal of Cell Science 1998 111: 3323-3332;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

2020 at The Company of Biologists

Despite the challenges of 2020, we were able to bring a number of long-term projects and new ventures to fruition. While we look forward to a new year, join us as we reflect on the triumphs of the last 12 months.

Mole – The Corona Files

"This is not going to go away, 'like a miracle.' We have to do magic. And I know we can."

Mole continues to offer his wise words to researchers on how to manage during the COVID-19 pandemic.

Cell scientist to watch – Christine Faulkner

In an interview, Christine Faulkner talks about where her interest in plant science began, how she found the transition between Australia and the UK, and shares her thoughts on virtual conferences.

Read & Publish participation extends worldwide

“The clear advantages are rapid and efficient exposure and easy access to my article around the world. I believe it is great to have this publishing option in fast-growing fields in biomedical research.”

Dr Jaceques Behmoaras (Imperial College London) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 60 institutions in 12 countries taking part – find out more and view our full list of participating institutions.

JCS and COVID-19

For more information on measures Journal of Cell Science is taking to support the community during the COVID-19 pandemic, please see here.

If you have any questions or concerns, please do not hestiate to contact the Editorial Office.