Advertisement
Journal Articles
Reorganization of the centrosome and associated microtubules during the morphogenesis of a mouse cochlear epithelial cell
C.G. Henderson, J.B. Tucker, M.A. Chaplin, J.B. Mackie, S.N. Maidment, M.M. Mogensen, C.C. Paton
Journal of Cell Science 1994 107: 589-600;

Summary

Reorganization of centrosomal microtubule-organizing centres and the minus ends of microtubules occurs as the centrosomal ends of large microtubule bundles are repositioned and anchored to cell junctions in certain epithelial cells called inner pillar cells in the mouse organ of Corti. The microtubule bundle that assembles in each cell consists of two distinct microtubule arrays that run closely alongside each other. Both arrays are attached to the cell surface at their upper and lower ends. One of the arrays spans the entire length of a cell but the other is confined to its lower portion. Initially, about 3,000 microtubules elongate downwards from an apically situated centrosome in each cell. Subsequently, the minus ends of these microtubules, and the centrosome and its two centrioles, migrate for about 12 microns to the tip of a laterally directed projection. Then, a meshwork of dense material accumulates to link microtubule minus ends and the centrosome to cell junctions at the tip of the projection. Pericentriolar satellite bodies, which form after the initial burst of microtubule nucleation, may represent a condensed and inactive concentration of microtubule-nucleating elements. Surprisingly, as a cell matures, about 2,000 microtubules are eliminated from the centrosomal end of the microtubule bundle. However, about 2,000 microtubules are added to the basal portion of each bundle at levels that are remote with respect to the location of the centrosome. Possibly, these microtubules have escaped from the centrosome. If this is the case, then both the plus and minus ends of most of the errant microtubules are captured by sites at the cell surface where the ends are finally anchored. Alternatively, each cell possesses at least one other major microtubule-nucleating site (which does not possess centrioles) in addition to its centrosome.

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. 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. Baas P. W. and
    2. Joshi H. C.
    (1992). -Tubulin distribution in the neuron: implications for the origins of neuritic microtubules. J. Cell Biol 119, 171–178
    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 canine kidney cells: the occurrence of non-centrosomal, stable detyrosinated microtubules. J. Cell Biol 105, 1283–1296
    OpenUrlAbstract/FREE Full Text
    1. Brinkley B. R.
    (1985). Microtubule organizing centers. Annu. Rev. Cell Biol 1, 145–172
    OpenUrlCrossRefWeb of Science
    1. Flock Å.,
    2. Bretscher A. and
    3. Weber K.
    (1982). Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hearing Res 6, 7–89
    OpenUrlCrossRefPubMed
    1. Gulley R. L. and
    2. Reese T. S.
    (1976). Intercellular junctions in the reticular lamina of the organ of Corti. J. Neurocytol 5, 479–507
    OpenUrlCrossRefPubMed
    1. Hudspeth A. J.
    (1989). How the ear's works work. Nature 341, 397–404
    OpenUrlCrossRefPubMed
    1. Kimura R. S.
    (1975). The ultrastructure of the organ of Corti. Int. Rev. Cytol 42, 173–222
    OpenUrlPubMedWeb of Science
    1. Kimble M. and
    2. Kuriyama R.
    (1992). Functional components of microtubule-organizing centers. Int. Rev. Cytol 136, 1–50
    OpenUrlPubMedWeb of Science
    1. Kronebusch P. J. and
    2. Singer S. J.
    (1987). The microtubule-organizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphasic cardiac myocytes. J. Cell Sci 88, 25–34
    OpenUrlAbstract/FREE Full Text
    1. Kuijpers W.,
    2. Tonnaer E. L. G. M.,
    3. Peters T. A. and
    4. Ramaekers F. C. S.
    (1991). Expression of intermediate filament proteins in the mature inner ear of the rat and guinea pig. Hearing Res 52, 133–146
    OpenUrlCrossRefPubMedWeb of Science
    1. Mazia D.
    (1987). The chromosome cycle and the centrosome cycle in the mitotic cycle. Int. Rev. Cytol 100, 49–92
    OpenUrlPubMedWeb of Science
    1. McBeath E. and
    2. Fujiwara K.
    (1990). Microtubule detachment from the microtubule-organizing center as a key event in the complete turnover of microtubules in cells. Eur. J. Cell Biol 52, 1–16
    OpenUrlPubMedWeb of Science
    1. Mogensen M. M.,
    2. Tucker J. B. and
    3. Stebbings H.
    (1989). Microtubule polarities indicate that nucleation and capture of microtubules occurs at cell surfaces in Drosophila. J. Cell Biol 108, 1445–1452
    OpenUrlAbstract/FREE Full Text
    1. Mogensen M. M.,
    2. Tucker J. B. and
    3. Baggalay T. B.
    (1993). Multiple plasma membrane-associated MTOC systems in the acentrosomal cone cells of Drosophila ommatidia. Eur J. Cell Biol 60, 67–75
    OpenUrlPubMed
    1. Rieder C. L. and
    2. Borisy G. G.
    (1982). The centrosome cycle in PtK2cells:asymmetric distribution and structural changes in the pericentriolar material. Biol. Cell 44, 117–132
    OpenUrl
    1. Slepecky N. B. and
    2. Chamberlain S. C.
    (1983). Distribution and polarity of actin in inner ear supporting cells. Hearing Res 10, 359–370
    OpenUrlCrossRefPubMed
    1. Slepecky N. B. and
    2. Ulfendahl M.
    (1992). Actin-binding and microtubule-associated proteins in the organ of Corti. Hearing Res 57, 201–215
    OpenUrlCrossRefPubMed
    1. Steyger P. S.,
    2. Furness D. N.,
    3. Hackney C. M. and
    4. Richardson G. P.
    (1989). Tubulin and microtubules in cochlear hair cells: comparative immunocytochemistry and ultrastructure. Hearing Res 42, 1–16
    OpenUrlCrossRefPubMedWeb of Science
    1. Tassin A.-M.,
    2. Maro B. and
    3. Bornens M.
    (1985). Fate of microtubule-organizing centers during myogenesis in vitro. J. Cell Biol 100, 35–46
    OpenUrlAbstract/FREE Full Text
    1. Tucker J. B.
    (1981). Cytoskeletal coordination and intercellular signalling during metazoan embryogenesis. J. Embryol. Exp. Morph 65, 1–25
    OpenUrlPubMedWeb of Science
    1. Tucker J. B.
    (1984). Spatial organization of microtubule-organizing centres and microtubules. J. Cell Biol 99, 55–.
    OpenUrl
    1. Tucker J. B.
    (1992). The microtubule-organizing centre. BioEssays 14, 861–867
    OpenUrlCrossRefPubMed
    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 ofmicrotubule-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. Paton C. C.,
    3. Henderson C. G. and
    4. Mogensen M. M.
    (1993). Microtubule rearrangement and bending during assembly of large curved microtubule bundles in mouse cochlear epithelial cells. Cell Motil. Cytoskeleton 25, 49–58
    OpenUrlCrossRefPubMed
    1. Vorobjev I. A. and
    2. Chentsov Y. S.
    (1983). The dynamics of reconstitution of microtubules around the cell center after cooling. Eur. J. Cell Biol 30, 149–153
    OpenUrlPubMedWeb of Science
    1. Vorobjev I. A. and
    2. Nadezhdina E. S.
    (1987). The centrosome and its role in the organization of microtubules. Int. Rev. Cytol 106, 227–293
    OpenUrlPubMedWeb of Science
    1. Yu W.,
    2. Centonze V. E.,
    3. Ahmad F. J. and
    4. Baas P. W.
    (1993). Microtubule nucleation and release from the neuronal centrosome. J. Cell Biol 122, 349–359
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Articles
Reorganization of the centrosome and associated microtubules during the morphogenesis of a mouse cochlear epithelial cell
C.G. Henderson, J.B. Tucker, M.A. Chaplin, J.B. Mackie, S.N. Maidment, M.M. Mogensen, C.C. Paton
Journal of Cell Science 1994 107: 589-600;
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.