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Journal Article
Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein
M.M. Mogensen, A. Malik, M. Piel, V. Bouckson-Castaing, M. Bornens
Journal of Cell Science 2000 113: 3013-3023;
M.M. Mogensen
Department of Anatomy and Physiology, MSI/WTB complex, Dow Street, University of Dundee, Dundee, DD1 5EH, UK.
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  • For correspondence: m.m.mogensen@dundee.ac.uk
A. Malik
Department of Anatomy and Physiology, MSI/WTB complex, Dow Street, University of Dundee, Dundee, DD1 5EH, UK.
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M. Piel
Department of Anatomy and Physiology, MSI/WTB complex, Dow Street, University of Dundee, Dundee, DD1 5EH, UK.
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V. Bouckson-Castaing
Department of Anatomy and Physiology, MSI/WTB complex, Dow Street, University of Dundee, Dundee, DD1 5EH, UK.
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M. Bornens
Department of Anatomy and Physiology, MSI/WTB complex, Dow Street, University of Dundee, Dundee, DD1 5EH, UK.
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Summary

The novel concept of a centrosomal anchoring complex, which is distinct from the gamma-tubulin nucleating complex, has previously been proposed following studies on cochlear epithelial cells. In this investigation we present evidence from two different cell systems which suggests that the centrosomal protein ninein is a strong candidate for the proposed anchoring complex. Ninein has recently been observed in cultured fibroblast cells to localise primarily to the post-mitotic mother centriole, which is the focus for a classic radial microtubule array. We show here by immunoelectron microscopical analyses of centrosomes from mouse L929 cells that ninein concentrates at the appendages surrounding the mother centriole and at the microtubule minus-ends. We further show that localisation of ninein in the cochlear supporting epithelial cells, where the vast majority of the microtubule minus-ends are associated with apical non-centrosomal sites, suggests that it is not directly involved in microtubule nucleation. Ninein seems to play an important role in the positioning and anchorage of the microtubule minus-ends in these epithelial cells. Evidence is presented which suggests that ninein is released from the centrosome, translocated with the microtubules, and is responsible for the anchorage of microtubule minus-ends to the apical sites. We propose that ninein is a non-nucleating microtubule minus-end associated protein which may have a dual role as a minus-end capping and anchoring protein.

  • © 2000 by Company of Biologists

REFERENCES

    1. Achler, C.,
    2. Filmer, D.,
    3. Merte, C. and
    4. Drenckhahn, D.
    (1989). Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium. J. Cell Biol 109, 179–189
    OpenUrlAbstract/FREE Full Text
    1. Baas, P. W. and
    2. Joshi, H. C.
    (1992). -Tubulin distribution in the neuron: Implications for the origin of neuritic microtubules. J. Cell Biol 119, 171–178
    OpenUrlAbstract/FREE Full Text
    1. Baas, P. W.
    (1998). The role of motor proteins in establishing the microtubule arrays of axons and dendrites. J. Chem. Neuroanat 14, 175–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Berns, M. W. and
    2. Richardson, S. M.
    (1977). Continuation of mitosis after selective laser microbeam destruction of the centriolar region. J. Cell Biol 75, 977–982
    OpenUrlAbstract/FREE Full Text
    1. Blomberg-Wirschell, M.,
    2. Young, A.,
    3. Zimmerman, W. and
    4. Doxsey, S. J.
    (1998). A novel centrosome protein localised to the subdistal appendages of the maternal centriole: possible role in microtubule binding at the centrosome. Mol. Biol. Cell 9, 9–.
    OpenUrl
    1. Bouckson-Castaing, V.,
    2. Moudjou, M.,
    3. Ferguson, D. J. P.,
    4. Mucklow, Y. B. and
    5. Milon, G. C., P. R.
    (1996). Molecular characterisation of ninein, a new coiled-coil protein of the centrosome. J. Cell Sci 109, 179–190
    OpenUrlAbstract/FREE Full Text
    1. Bre, M.-H.,
    2. Kreis, T. E. and
    3. Karsenti, E.
    (1987). Control of microtubule nucleation and stability in Madin-Darby kidney cells: The occurrence of noncentrosomal, stable detyrosinated microtubules. J. Cell Biol 105, 1283–1296
    OpenUrlAbstract/FREE Full Text
    1. Bre, M.-H.,
    2. Pepperkok, R.,
    3. Hill, A. M.,
    4. Levilliers, N.,
    5. Ansorge, W.,
    6. Stelzer, E. H. K. and
    7. Karsenti, E.
    (1990). Regulation of microtubule dynamics and nucleation during polarization in MDCK II cells. J. Cell Biol 111, 3013–3021
    OpenUrlAbstract/FREE Full Text
    1. Brinkley, B. R.
    (1985). Microtubule organizing centres. Annu. Rev. Cell Biol 1, 145–172
    OpenUrlCrossRefWeb of Science
    1. De Brabander, M.
    (1982). A model for the microtubule organising activity of the centrosomes and kinetochores in mammalian cells. Biol. Int. Reports6.
    1. Dictenberg, J. B.,
    2. Zimmerman, W.,
    3. Sparks, C. A.,
    4. Young, A.,
    5. Vidair, C.,
    6. Zheng, Y.,
    7. Carrington, W.,
    8. Fay, F. S. and
    9. Doxsey, J.
    (1998). Pericentrinand -tubulin form a protein complex and are organised into a novel lattice at the centrosome. J. Cell Biol 141, 163–174
    OpenUrlAbstract/FREE Full Text
    1. Doxsey, S. J.,
    2. Stein, P.,
    3. Evans, L.,
    4. Calarco, P. D. and
    5. Kirschner, M.
    (1994). Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639–650
    OpenUrlCrossRefPubMedWeb of Science
    1. Gilbert, T.,
    2. Le Bivic, A.,
    3. Quaroni, A. and
    4. Rodriguez-Boulan, E.
    (1991). Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol 113, 275–288
    OpenUrlAbstract/FREE Full Text
    1. Gorgidze, L. A. and
    2. Vorobjev, I. A.
    (1995). Centrosome and microtubule behavior in the cytoplasts. J. Submicrosc. Cytol. Pathol 27, 381–389
    OpenUrlPubMed
    1. Gould, R. R. and
    2. Borisy, G. G.
    (1977). The pericentriolar material in Chinese hamster cells nucleates microtubule formation. J. Cell Biol 73, 601–615
    OpenUrlAbstract/FREE Full Text
    1. Henderson, C. G.,
    2. Tucker, J. B.,
    3. Chaplin, M. A.,
    4. Mackie, J. B.,
    5. Maidment, S. N.,
    6. Mogensen, M. M. and
    7. Paton, C. C.
    (1994). Reorganisation of the centrosome and associated microtubules during the morphogenesis of a mouse cochlear epithelial cell. J. Cell Sci 107, 589–600
    OpenUrlAbstract/FREE Full Text
    1. Horio, T.,
    2. Uzawa, S.,
    3. Jung, M. K.,
    4. Oakley, B. R.,
    5. Tanaka, K. and
    6. Yanagida, M.
    (1991). The fission yeast-tubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci 99, 693–700
    OpenUrlAbstract/FREE Full Text
    1. Ihrke, G.,
    2. Neufeld, E. B.,
    3. Meads, T.,
    4. Shanks, M. R.,
    5. Cassio, D.,
    6. Laurent, M.,
    7. Schroer, T. A.,
    8. Pagano, R. E. and
    9. Hubbard, A. L.
    (1993). WIF-B cells: An in vitro model for studies of hepatocyte polarity. J. Cell Biol 123, 1761–1775
    OpenUrlAbstract/FREE Full Text
    1. Joshi, H. C.,
    2. Palacios, M. J.,
    3. McNamara, L. and
    4. Cleveland, D. W.
    (1992). -Tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356, 80–83
    OpenUrlCrossRefPubMedWeb of Science
    1. Keating, T. J.,
    2. Peloquin, J. G.,
    3. Rodionov, V. I.,
    4. Momcilovic, D. and
    5. Borisy, G. G.
    (1997). Microtubule release from the centrosome. Proc. Nat. Acad. Sci. USA 94, 5078–5083
    OpenUrlAbstract/FREE Full Text
    1. Kellogg, D. R.,
    2. Moritz, M. and
    3. Alberts, B. M.
    (1994). The centrosome and cellular organization. Annu. Rev. Biochem 63, 639–674
    OpenUrlCrossRefPubMedWeb of Science
    1. McIntosh, J. R. and
    2. Euteneuer, U.
    (1984). Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of dataon microtubule polarity in the mitotic spindle. J. Cell Biol 98, 525–533
    OpenUrlAbstract/FREE Full Text
    1. Meads, T. and
    2. Schroer, T. A.
    (1995). Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskel 32, 273–288
    OpenUrlCrossRefPubMedWeb of Science
    1. Mogensen, M. M.,
    2. Mackie, J. B.,
    3. Doxsey, S. J.,
    4. Stearns, T. and
    5. Tucker, J. B.
    (1997). Centrosomal deployment of-tubulin and pericentrin: Evidence for a microtubule-nucleating domain and a minus-end docking domain in certain mouse epithelial cells. Cell Motil. Cytoskel 36, 276–290
    OpenUrlCrossRefPubMedWeb of Science
    1. Mogensen, M. M.
    (1999). Microtubule release and capture in epithelial cells. Biol. Cell 91, 331–341
    OpenUrlCrossRefPubMed
    1. Moritz, M.,
    2. Braunfeld, M. B.,
    3. Sedat, J. W.,
    4. Albert, B. and
    5. Agard, D. A.
    (1995). Microtubule nucleation by-tubulin-containing rings in the centrosome. Nature 378, 638–640
    OpenUrlCrossRefPubMedWeb of Science
    1. Moritz, M.,
    2. Zheng, Y.,
    3. Alberts, B. M. and
    4. Oegema, K.
    (1998). Recruitment of the-tubulin ring complex to Drosophila salt-stripped centrosome scaffolds. J. Cell Biol 142, 775–786
    OpenUrlAbstract/FREE Full Text
    1. Moudjou, M.,
    2. Bordes, N.,
    3. Paintrand, M. and
    4. Bornens, M.
    (1996). -Tubulinin mammalian cells: the centrosomal and the cytosolic forms. J. Cell Sci 109, 875–887
    OpenUrlAbstract/FREE Full Text
    1. Nathke, I. S.,
    2. Adams, C. L.,
    3. Polakis, P.,
    4. Sellin, J. H. and
    5. Nelson, W. J.
    (1996). The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol 134, 165–179
    OpenUrlAbstract/FREE Full Text
    1. Oakley, C. E. and
    2. Oakley, B. R.
    (1989). Identification of-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662–664
    OpenUrlCrossRefPubMedWeb of Science
    1. Paintrand, M.,
    2. Moudjou, M.,
    3. Delacroix, H. and
    4. Bornens, M.
    (1992). Centrosome organisation and centriole architecture: Their sensitivity to divalent cations. J. Struct. Biol 108, 107–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Piel, M.,
    2. Meyer, P.,
    3. Khodjakov, A.,
    4. Rieder, C. L. and
    5. Bornens, M.
    (2000). The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol 149, 317–329
    OpenUrlFREE Full Text
    1. Purohit, A.,
    2. Tynan, S. A.,
    3. Vallee, R. and
    4. Doxsey, S. J.
    (1999). Direct interaction of pericentrin with cytoplasmic dynein light intermediate chain contributes to mitotic spindle organisation. J. Cell Biol 147, 481–491
    OpenUrlAbstract/FREE Full Text
    1. Rizzolo, L. J. and
    2. Joshi, H. C.
    (1993). Apical orientation of the microtubule organizing center and associated-tubulin during the polarization of the retinal pigment epithelium in vivo. Dev. Biol 157, 147–156
    OpenUrlCrossRefPubMed
    1. Shu, H. B. and
    2. Joshi, H. C.
    (1995). -Tubulin can both nucleate microtubule assembly and self-assemble into novel tubular structures in mammalian cells. J. Cell Biol 130, 1137–1147
    OpenUrlAbstract/FREE Full Text
    1. Stearns, T.,
    2. Evans, L. and
    3. Kirschner, M.
    (1991). -Tubulin is a highly conserved component of the centrosome. Cell 65, 825–836
    OpenUrlCrossRefPubMedWeb of Science
    1. Stearns, T. and
    2. Kirschner, M.
    (1994). In vitro reconstitution of centrosome assembly and function: the central role of-tubulin. Cell 76, 623–637
    OpenUrlCrossRefPubMedWeb of Science
    1. Sunkel, C. E.,
    2. Gomes, R.,
    3. Sampaio, P.,
    4. Perdigao, J. and
    5. Gonzalez, C.
    (1995). -Tubulin is required for the structure and function of the microtubule organizing centre in Drosophila neuroblasts. EMBO J 14, 28–36
    OpenUrlPubMedWeb of Science
    1. Tassin, A.-M. and
    2. Bornens, M.
    (1999). Centrosome structure and microtubule nucleation in animal cells. Biol. Cell 91, 343–354
    OpenUrlCrossRefPubMedWeb of Science
    1. Troutt, L. L. and
    2. Burnside, B.
    (1988). The unusual microtubule polarity in teleost retinal pigment epithelial cells. J. Cell Biol 107, 1461–1464
    OpenUrlAbstract/FREE Full Text
    1. Tucker, J. B.,
    2. Paton, C. C.,
    3. Richardson, G. P.,
    4. Mogensen, M. M. and
    5. Russell, I. J.
    (1992). A cell surface-associated centrosomal layer of microtubule-organizing material in the inner pillar cell of the mouse cochlea. J. Cell Sci 102, 215–226
    OpenUrlAbstract/FREE Full Text
    1. Tucker, J. B.,
    2. Mogensen, M. M.,
    3. Paton, C. C.,
    4. Mackie, J. B.,
    5. Henderson, C. G. and
    6. Leckie, L. M.
    (1995). Formation of two microtubule-nucleating sites which perform differently during centrosomal reorganization in a mouse cochlear epithelial cell. J. Cell Sci 108, 1333–1345
    OpenUrlAbstract/FREE Full Text
    1. Vogel, J. M.,
    2. Stearns, T.,
    3. Rieder, C. L. and
    4. Palazzo, R. E.
    (1997). Centrosomes isolated from Spisula solidissima oocytes contain rings and an unusual stoichiometric ratio of/ tubulin. J. Cell Biol 137, 193–202
    OpenUrlAbstract/FREE Full Text
    1. Zheng, Y.,
    2. Wong, M. L.,
    3. Alberts, B. and
    4. Mitchison, T.
    (1995). Nucleation of microtubule assembly by a-tubulin-containing ring complex. Nature 378, 578–583
    OpenUrlCrossRefPubMedWeb of Science
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Journal Article
Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein
M.M. Mogensen, A. Malik, M. Piel, V. Bouckson-Castaing, M. Bornens
Journal of Cell Science 2000 113: 3013-3023;
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Journal Article
Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein
M.M. Mogensen, A. Malik, M. Piel, V. Bouckson-Castaing, M. Bornens
Journal of Cell Science 2000 113: 3013-3023;

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