Advertisement
Journal Articles
Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells
S. Yonemura, M. Itoh, A. Nagafuchi, S. Tsukita
Journal of Cell Science 1995 108: 127-142;

Summary

Cadherin has an intimate spatial relationship with actin filaments (AF) in various types of cells, forming the cell-to-cell adherens junction (AJ). We compared the AJ/AF relationship between non-polarized fibroblasts (NRK cells) and polarized epithelial cells (MTD-1A cells). E/P-cadherin, alpha-catenin, ZO-1 and vinculin were localized with reference to AF in these cells using laser scan microscopy as well as conventional light and electron microscopy. NRK cells adhered to each other at the tips of thin cellular processes, where spot-like AJ were formed, where P-cadherin, alpha-catenin, ZO-1 and vinculin were concentrated. Some stress-fiber-like AF bundles ran axially in these processes and terminated at spot-like AJ on their tips. At the electron microscopic level these spot-like AJ were seen as aggregates of small ‘units’ of AJ, where AF were densely and perpendicularly associated with the plasma membrane. In MTD-1A cells, the AJ/AF relationship was investigated during the cell polarization process after replating or wounding. At the early stage, the AJ/AF relationship was quite similar to that in NRK cells. As polarization proceeded, the spot-like AJs were gradually fused side by side with the concomitant shortening of the associated stress-fiber-like AF bundles. Finally, the belt-like AJ was established, which was lined with circumferential AF bundles. The similarities and differences in the AJ/AF relationship between non-polarized fibroblasts and polarized epithelial cells are discussed.

REFERENCES

    1. Albrecht-Buchler G.
    (1979). Group locomotion of PtK1 cells. Exp. Cell Res 122, 402–407
    OpenUrlCrossRefPubMedWeb of Science
    1. Anderson J. M.,
    2. Stevenson B. R.,
    3. Jesaitis L. A.,
    4. Goodenough D. A. and
    5. Mooseker. M. S.
    (1988). Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J. Cell Biol 106, 1141–1149
    OpenUrlAbstract/FREE Full Text
    1. Bacallao R.,
    2. Antony C.,
    3. Dotti C.,
    4. Karsenti E.,
    5. Stelzer E. H. K. and
    6. Simons K.
    (1989). The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol 109, 2817–2832
    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. Boller K.,
    2. Vestweber D. and
    3. Kemler R.
    (1985). Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epitheilal cells. J. Cell Biol 100, 327–332
    OpenUrlAbstract/FREE Full Text
    1. De Larco J. E. and
    2. Todaro G. J.
    (1978). Epithelioid and fibroblastic rat kidney cell clones: Epidermal growth factor (EGF) receptors and virus transformation. J. Cell. Physiol 94, 335–342
    OpenUrlCrossRefPubMedWeb of Science
    1. Enami J.,
    2. Enami S. and
    3. Koga M.
    (1984). Isolation of an insulin-responsive preadipose cell line and a mammary tumor-producing, dome-forming epithelial cell line from a mouse mammary tumor. Dev. Growth Differ 26, 223–234
    OpenUrlCrossRef
    1. Farquhar M. G. and
    2. Palade G. E.
    (1963). Junctional complexes in various epithelia. J. Cell Biol 17, 375–412
    OpenUrlAbstract/FREE Full Text
    1. Geiger B.,
    2. Tokuyasu K. T.,
    3. Dutton A. H. and
    4. Singer S. J.
    (1980). Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc. Nat. Acad. Sci. USA 77, 4127–4131
    OpenUrlAbstract/FREE Full Text
    1. Geiger B.,
    2. Volk T. and
    3. Volberg T.
    (1985). Molecular heterogeneity of adherens junctions. J. Cell Biol 101, 1523–1531
    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. Green K. J. B.,
    2. Geiger B.,
    3. Jones J. C. R.,
    4. Talian J. C. and
    5. Goldman R. D.
    (1987). The relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes. J. Cell Biol 104, 1389–1402
    OpenUrlAbstract/FREE Full Text
    1. Gumbiner B. and
    2. Simons K.
    (1986). A functional assay for proteins involved in establishing an epithelial occluding barrier: Identification of a uvomorulin-like polypeptide. J. Cell Biol 102, 457–468
    OpenUrlAbstract/FREE Full Text
    1. Gumbiner B.,
    2. Stevenson B. and
    3. Grimaldi A.
    (1988). The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol 107, 1575–1587
    OpenUrlAbstract/FREE Full Text
    1. Heaysman J. E. M. and
    2. Pegrum S. M.
    (1973). Early contacts between fibroblasts. Exp. Cell Res 78, 71–78
    OpenUrlCrossRefPubMedWeb of Science
    1. Hirano S.,
    2. Nose A.,
    3. Hatta K.,
    4. Kawakami A. and
    5. Takeichi M.
    (1987). Calcium-dependent cell-cell adhesion molecules (cadherins): Subclass specificities and possible involvement of actin bundles. J. Cell Biol 105, 2501–2510
    OpenUrlAbstract/FREE Full Text
    1. Hormia M.,
    2. Badley R. A.,
    3. Lehto V.-P. and
    4. Virtanen I.
    (1985). Actomyosin organization in stationary and migrating sheets of cultured human endothelial cells. Exp. Cell Res 157, 116–126
    OpenUrlCrossRefPubMed
    1. Itoh M.,
    2. Yonemura S.,
    3. Nagafuchi A.,
    4. Tsukita Sa. and
    5. Tsukita Sh
    (1991). A 220-kD undercoat-constitutive protein: Its specific localization at cadherin-based cell-cell adhesion sites. J. Cell Biol 115, 1449–1462
    OpenUrlAbstract/FREE Full Text
    1. Itoh M.,
    2. Nagafuchi A.,
    3. Yonemura S.,
    4. Kitani-Yasuda T.,
    5. Tsukita Sa. and
    6. Tsukita Sh
    (1993). The 220-kD protein colocalizing with cadherins 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. Jainchill J. L.,
    2. Aaronson S. A. and
    3. Todaro G. J.
    (1969). Murine sarcoma and leukemia viruses: assay using clonal lines of contact-inhibited mouse cells. J. Virol 4, 549–553
    OpenUrlAbstract/FREE Full Text
    1. Jensen F. C.,
    2. Girardi A. J.,
    3. Gilden R. V. and
    4. Koprowski H.
    (1964). Infection of human and simian tissue cultures with rous sarcoma virus. Microbiology 52, 53–59
    OpenUrl
    1. Kimura G.,
    2. Itagaki A. and
    3. Summers J.
    (1975). Rat cell line 3Y1 and its virogenic polyoma-and SV40-transformed derivatives. Int. J. Cancer 15, 694–706
    OpenUrlPubMedWeb of Science
    1. Kodama R.,
    2. Eguchi G. and
    3. Kelly. R. O.
    (1991). Ultrastructural and immunocytochemical analysis of the circumferential microfilament bundle in avian retinal pigmented epithelial cells in vitro. Cell Tiss. Res 263, 29–40
    OpenUrlCrossRefPubMed
    1. Kolodney M. S. and
    2. Wysolmerski R. B.
    (1992). Isometric contraction by fibroblasts and endothelial cells in tissue culture: A quantitative study. J. Cell Biol 117, 73–82
    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. 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. Miettinen A.,
    2. Virtanen I. and
    3. Linder E.
    (1978). Cellular actin and junction formation during reaggregation of adult rat hepatocytes into epithelial cell sheets. J. Cell Sci 31, 341–353
    OpenUrlAbstract/FREE Full Text
    1. Nagafuchi A. and
    2. Tsukita Sh
    (1994). The loss of the expression ofcatenin, the 102 kD cadherin associated protein, in central nervous tissues during development. Dev. Growth Differ 36, 59–71
    OpenUrlCrossRef
    1. Nelson W. J. and
    2. Veshnock P. J.
    (1986). Dynamics of membrane-skeleton (fodrin) organization during development of polarity in Madin-Darby canine kidney epithelial cells. J. Cell Biol 103, 1751–1765
    OpenUrlAbstract/FREE Full Text
    1. Nelson W. J.,
    2. Shore E. M.,
    3. Wang A. Z. and
    4. Hammerton R. W.
    (1990). Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells. J. Cell Biol 110, 349–357
    OpenUrlAbstract/FREE Full Text
    1. Nose A.,
    2. Tsuji K. and
    3. Takeichi M.
    (1987). Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 61, 147–155
    OpenUrl
    1. Salmon D.,
    2. Ayalon O.,
    3. Patel-King R.,
    4. Hynes R. O. and
    5. Geiger B.
    (1992). Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci 102, 7–17
    OpenUrlAbstract/FREE Full Text
    1. Sanger J. M. and
    2. Sanger J. W.
    (1980). Banding and polarity of actin filaments in interphase and cleaving cells. J. Cell Biol 86, 568–575
    OpenUrlAbstract/FREE Full Text
    1. Shirayoshi Y.,
    2. Nose A.,
    3. Iwasaki K. and
    4. Takeichi M.
    (1986). N-linked oligosaccharides are not involved in the function of a cell-cell binding glycoprotein E-cadherin. Cell Struct. Funct 11, 245–252
    OpenUrlPubMedWeb of Science
    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. Takeichi M.
    (1988). The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102, 639–655
    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 Sh. and
    2. Tsukita Sa
    (1989). Isolation of cell-to-cell adherens junctions from rat liver. J. Cell Biol 108, 31–41
    OpenUrlAbstract/FREE Full Text
    1. Tsukita Sh.,
    2. Tsukita Sa.,
    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. Volk T. and
    2. Geiger B.
    (1984). A 135-kd membrane protein of intercellular adherens junctions. EMBO J 3, 2249–2260
    OpenUrlPubMedWeb of Science
    1. Volk T. and
    2. Geiger B.
    (1986). A-CAM: A 135-kD receptor of intercellular adherens junctions. II. Antibody-mediated modulation of junctional formation. J. Cell Biol 103, 1451–1464
    OpenUrlAbstract/FREE Full Text
    1. Wang A. Z.,
    2. Ojakian G. K. and
    3. Nelson W. J.
    (1990). Steps in the morphogenesis of a polarized epithelium I. Uncoupling the roles of cell-celland cell-substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci 95, 137–151
    OpenUrlAbstract/FREE Full Text
    1. Zahraoui A.,
    2. Joberty G.,
    3. Arpin M.,
    4. Fontaine J. J.,
    5. Hellio R.,
    6. Tavitian A. and
    7. Louvard D.
    (1994). A small rab GTPase is distributed in cytoplasmicvesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J. Cell Biol 124, 101–115
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Articles
Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells
S. Yonemura, M. Itoh, A. Nagafuchi, S. Tsukita
Journal of Cell Science 1995 108: 127-142;
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

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

We are pleased to welcome Esperanza to the Journal of Cell Science team. The new Community Manager for FocalPlane, Esperanza is joining us from the Microscopy Core at Mount Sinai School of Medicine. Find out more about Esperanza in her introductory post over on FocalPlane.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

"Alongside pre-printing for early documentation of work, such mechanisms are particularly helpful for early-career researchers like me.”

Dr Chris MacDonald (University of York) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Cell scientist to watch: Romain Levayer

In an interview, Romain Levayer talks about starting his own lab, his love for preprints and his experience of balancing parenting with his research goals.

Live lactating mammary tissue

In a stunning video, Stewart et al. demonstrate warping of the alveolar unit due to basal cell-generated force as part of their recent work investigating roles for mechanically activated ion channels in lactation and involution.

Visit our YouTube channel to watch more videos from JCS, our sister journals and the Company.

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.