© The Rockefeller University Press,
0021-9525/1998//1575 $5.00
The Journal of Cell Biology, Volume 143, Number 6,
, 1998 1575-1589
Centriole Disassembly In Vivo and Its Effect on Centrosome Structure and Function in Vertebrate Cells
Y. Bobinnec*,
A. Khodjakov
,
L.M. Mir
,
C.L. Rieder
,
B. Eddé||, and
M. Bornens*
* Institut Curie, Section Recherche, UMR144 du Centre National de la Recherche Scientifque (CNRS), 75248 Paris Cedex 05, France;
Wadsworth Center, New York State Department of Health, Albany, New York 12201-0509;
UMR1772 du CNRS, Institut Gustave Roussy, 94805 Villejuif, France; and || Collège de France, UPR9065 du CNRS, Biochimie Cellulaire, 75005 Paris, France
Glutamylation is the major posttranslational modification of neuronal and axonemal tubulin and is restricted predominantly to centrioles in nonneuronal cells (Bobinnec, Y., M. Moudjou, J.P. Fouquet, E. Desbruyères, B. Eddé, and M. Bornens. 1998. Cell Motil. Cytoskel. 39:223–232). To investigate a possible relationship between the exceptional stability of centriole microtubules and the compartmentalization of glutamylated isoforms, we loaded HeLa cells with the monoclonal antibody GT335, which specifically reacts with polyglutamylated tubulin. The total disappearance of the centriole pair was observed after 12 h, as judged both by immunofluorescence labeling with specific antibodies and electron microscopic observation of cells after complete thick serial sectioning. Strikingly, we also observed a scattering of the pericentriolar material (PCM) within the cytoplasm and a parallel disappearance of the centrosome as a defined organelle. However, centriole disappearance was transient, as centrioles and discrete centrosomes ultimately reappeared in the cell population.
During the acentriolar period, a large proportion of monopolar half-spindles or of bipolar spindles with abnormal distribution of PCM and NuMA were observed. However, as judged by a quasinormal increase in cell number, these cells likely were not blocked in mitosis.
Our results suggest that a posttranslational modification of tubulin is critical for long-term stability of centriolar microtubules. They further demonstrate that in animal cells, centrioles are instrumental in organizing centrosomal components into a structurally stable organelle.
Key Words: centrosome centriole tubulin polyglutamylation mitosis mitotic spindle
Abbreviations used in this paper: IVEM, intermediate voltage electron microscopy; MAP, microtubule-associated protein; PCM, pericentriolar material.
Y. Bobinnec is the recipient of a fellowship from the Association pour la Recherche sur le Cancer. This work was supported in part by National Institutes of Health (NIH) GMS 40198 to C.L. Rieder, by NIH/NCRR P41-RR 01219 for the Wadsworth Center Biological Microscopy and Image Reconstruction Facility as a National Biotechnological Resource, and by Institut Curie, CNRS, and European Community grant CHRX-CT940642 to M. Bornens.

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-
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-
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-
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-
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-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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158: 1195-1206
[Full Text]
-
Meraldi, P., Nigg, E. A.
(2002). Centrosome cohesion is regulated by a balance of kinase and phosphatase activities. J. Cell Sci.
114: 3749-3757
[Abstract]
[Full Text]
-
Stein, P. A., Toret, C. P., Salic, A. N., Rolls, M. M., Rapoport, T. A.
(2002). A novel centrosome-associated protein with affinity for microtubules. J. Cell Sci.
115: 3389-3402
[Abstract]
[Full Text]
-
Ou, Y. Y., Mack, G. J., Zhang, M., Rattner, J. B.
(2002). CEP110 and ninein are located in a specific domain of the centrosome associated with centrosome maturation. J. Cell Sci.
115: 1825-1835
[Abstract]
[Full Text]
-
Buster, D., McNally, K., McNally, F. J.
(2002). Katanin inhibition prevents the redistribution of {gamma}-tubulin at mitosis. J. Cell Sci.
115: 1083-1092
[Abstract]
[Full Text]
-
Hinchcliffe, E. H., Sluder, G.
(2001). "It Takes Two to Tango": understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev.
15: 1167-1181
[Full Text]
-
Khodjakov, A., Rieder, C. L.
(2001). Centrosomes Enhance the Fidelity of Cytokinesis in Vertebrates and Are Required for Cell Cycle Progression. JCB
153: 237-242
[Abstract]
[Full Text]
-
Piel, M., Nordberg, J., Euteneuer, U., Bornens, M.
(2001). Centrosome-Dependent Exit of Cytokinesis in Animal Cells. Science
291: 1550-1553
[Abstract]
[Full Text]
-
McKean, P. G., Vaughan, S., Gull, K.
(2001). The extended tubulin superfamily. J. Cell Sci.
114: 2723-2733
[Abstract]
[Full Text]
-
Li, Q, Hansen, D, Killilea, A, Joshi, H., Palazzo, R., Balczon, R
(2001). Kendrin/pericentrin-B, a centrosome protein with homology to pericentrin that complexes with PCM-1. J. Cell Sci.
114: 797-809
[Abstract]
-
Preble, A. M., Giddings, T. H. , Jr., Dutcher, S. K.
(2001). Extragenic Bypass Suppressors of Mutations in the Essential Gene BLD2 Promote Assembly of Basal Bodies With Abnormal Microtubules in Chlamydomonas reinhardtii. Genetics
157: 163-181
[Abstract]
[Full Text]
-
Young, A., Dictenberg, J. B., Purohit, A., Tuft, R., Doxsey, S. J.
(2000). Cytoplasmic Dynein-mediated Assembly of Pericentrin and gamma Tubulin onto Centrosomes. Mol. Biol. Cell
11: 2047-2056
[Abstract]
[Full Text]
-
Xia, L., Hai, B., Gao, Y., Burnette, D., Thazhath, R., Duan, J., Bre, M.-H., Levilliers, N., Gorovsky, M. A., Gaertig, J.
(2000). Polyglycylation of Tubulin Is Essential and Affects Cell Motility and Division in Tetrahymena thermophila. JCB
149: 1097-1106
[Abstract]
[Full Text]
-
Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L., Bornens, M.
(2000). The Respective Contributions of the Mother and Daughter Centrioles to Centrosome Activity and Behavior in Vertebrate Cells. JCB
149: 317-330
[Full Text]
-
Bobinnec, Y, Fukuda, M, Nishida, E
(2000). Identification and characterization of Caenorhabditis elegans gamma-tubulin in dividing cells and differentiated tissues. J. Cell Sci.
113: 3747-3759
[Abstract]
-
Regnard, C, Desbruyeres, E, Denoulet, P, Edde, B
(1999). Tubulin polyglutamylase: isozymic variants and regulation during the cell cycle in HeLa cells. J. Cell Sci.
112: 4281-4289
[Abstract]
-
Million, K, Larcher, J, Laoukili, J, Bourguignon, D, Marano, F, Tournier, F
(1999). Polyglutamylation and polyglycylation of alpha- and beta-tubulins during in vitro ciliated cell differentiation of human respiratory epithelial cells. J. Cell Sci.
112: 4357-4366
[Abstract]
-
Regnard, C., Desbruyeres, E., Huet, J.-C., Beauvallet, C., Pernollet, J.-C., Edde, B.
(2000). Polyglutamylation of Nucleosome Assembly Proteins. J. Biol. Chem.
275: 15969-15976
[Abstract]
[Full Text]
-
Barthelmes, H. U., Grue, P., Feineis, S., Straub, T., Boege, F.
(2000). Active DNA Topoisomerase IIalpha Is a Component of the Salt-stable Centrosome Core. J. Biol. Chem.
275: 38823-38830
[Abstract]
[Full Text]
-
Ciciarello, M., Mangiacasale, R., Casenghi, M., Zaira Limongi, M., D'Angelo, M., Soddu, S., Lavia, P., Cundari, E.
(2001). p53 Displacement from Centrosomes and p53-mediated G1 Arrest following Transient Inhibition of the Mitotic Spindle. J. Biol. Chem.
276: 19205-19213
[Abstract]
[Full Text]
-
Bonnet, C., Boucher, D., Lazereg, S., Pedrotti, B., Islam, K., Denoulet, P., Larcher, J. C.
(2001). Differential Binding Regulation of Microtubule-associated Proteins MAP1A, MAP1B, and MAP2 by Tubulin Polyglutamylation. J. Biol. Chem.
276: 12839-12848
[Abstract]
[Full Text]