Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Science Policy Alerts

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 23 February 2001:
Vol. 291. no. 5508, pp. 1550 - 1553
DOI: 10.1126/science.1057330

Reports

Centrosome-Dependent Exit of Cytokinesis in Animal Cells

Matthieu Piel,1 Joshua Nordberg,2 Ursula Euteneuer,3 Michel Bornens1*

As an organelle coupling nuclear and cytoplasmic divisions, the centrosome is essential to mitotic fidelity, and its inheritance could be critical to understanding cell transformation. Investigating the behavior of the centrosome in living mitotic cells, we documented a transient and remarkable postanaphase repositioning of this organelle, which apparently controls the release of central microtubules from the midbody and the completion of cell division. We also observed that the absence of the centrosome leads to defects in cytokinesis. Together with recent results in yeasts, our data point to a conserved centrosome-dependent pathway that integrates spatial controls into the decision of completing cell division, which requires the repositioning of the centrosome organelle.

1 Institut Curie, Section Recherche, UMR 144 du CNRS, 26 rue d'Ulm, 75248 Paris Cedex 05, France.
2 Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA.
3 Zellbiologie, Adolf-Butenandt-Institut, Ludwig-Maximilians-Universität, D-80336 München, Germany.
*   To whom correspondence should be addressed.


Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Prostate-specific membrane antigen associates with anaphase-promoting complex and induces chromosomal instability.
S. A. Rajasekaran, J. J. Christiansen, I. Schmid, E. Oshima, K. Sakamoto, J. Weinstein, N. P. Rao, and A. K. Rajasekaran (2008)
Mol. Cancer Ther. 7, 2142-2151
   Abstract »    Full Text »    PDF »
The Endocytic Adaptor Protein ARH Associates with Motor and Centrosomal Proteins and Is Involved in Centrosome Assembly and Cytokinesis.
S. Lehtonen, M. Shah, R. Nielsen, N. Iino, J. J. Ryan, H. Zhou, and M. G. Farquhar (2008)
Mol. Biol. Cell 19, 2949-2961
   Abstract »    Full Text »    PDF »
Abnormal Cytokinesis after X-Irradiation in Tumor Cells that Override the G2 DNA Damage Checkpoint.
H. Huang, L. Fletcher, N. Beeharry, R. Daniel, G. Kao, T. J. Yen, and R. J. Muschel (2008)
Cancer Res. 68, 3724-3732
   Abstract »    Full Text »    PDF »
Organellar dynamics during the cell cycle of Toxoplasma gondii.
M. Nishi, K. Hu, J. M. Murray, and D. S. Roos (2008)
J. Cell Sci. 121, 1559-1568
   Abstract »    Full Text »    PDF »
Downregulation of Protein 4.1R, a Mature Centriole Protein, Disrupts Centrosomes, Alters Cell Cycle Progression, and Perturbs Mitotic Spindles and Anaphase.
S. W. Krauss, J. R. Spence, S. Bahmanyar, A. I. M. Barth, M. M. Go, D. Czerwinski, and A. J. Meyer (2008)
Mol. Cell. Biol. 28, 2283-2294
   Abstract »    Full Text »    PDF »
Cofactor D Functions as a Centrosomal Protein and Is Required for the Recruitment of the {gamma}-Tubulin Ring Complex at Centrosomes and Organization of the Mitotic Spindle.
L. A. Cunningham and R. A. Kahn (2008)
J. Biol. Chem. 283, 7155-7165
   Abstract »    Full Text »    PDF »
Asymmetric centrosome behavior and the mechanisms of stem cell division.
Y. M. Yamashita and M. T. Fuller (2008)
J. Cell Biol. 180, 261-266
   Abstract »    Full Text »    PDF »
CDC25B Involvement in the Centrosome Duplication Cycle and in Microtubule Nucleation.
R. Boutros, V. Lobjois, and B. Ducommun (2007)
Cancer Res. 67, 11557-11564
   Abstract »    Full Text »    PDF »
Centrin1 Is Required for Organelle Segregation and Cytokinesis in Trypanosoma brucei.
A. Selvapandiyan, P. Kumar, J. C. Morris, J. L. Salisbury, C. C. Wang, and H. L. Nakhasi (2007)
Mol. Biol. Cell 18, 3290-3301
   Abstract »    Full Text »    PDF »
Centrosome replication in hydroxyurea-arrested CHO cells expressing GFP-tagged centrin2.
R. Kuriyama, Y. Terada, K. S. Lee, and C. L. C. Wang (2007)
J. Cell Sci. 120, 2444-2453
   Abstract »    Full Text »    PDF »
Structure and duplication of the centrosome.
J. Azimzadeh and M. Bornens (2007)
J. Cell Sci. 120, 2139-2142
   Full Text »    PDF »
LAPSER1 is a putative cytokinetic tumor suppressor that shows the same centrosome and midbody subcellular localization pattern as p80 katanin.
H. Sudo and Y. Maru (2007)
FASEB J 21, 2086-2100
   Abstract »    Full Text »    PDF »
Microtubule-induced cortical cell polarity.
S. E. Siegrist and C. Q. Doe (2007)
Genes & Dev. 21, 483-496
   Abstract »    Full Text »    PDF »
Dido disruption leads to centrosome amplification and mitotic checkpoint defects compromising chromosome stability.
V. Trachana, K. H. M. van Wely, A. A. Guerrero, A. Futterer, and C. Martinez-A (2007)
PNAS 104, 2691-2696
   Abstract »    Full Text »    PDF »
The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells.
A. Robert, G. Margall-Ducos, J.-E. Guidotti, O. Bregerie, C. Celati, C. Brechot, and C. Desdouets (2007)
J. Cell Sci. 120, 628-637
   Abstract »    Full Text »    PDF »
RalA-exocyst-dependent Recycling Endosome Trafficking Is Required for the Completion of Cytokinesis.
X.-W. Chen, M. Inoue, S. C. Hsu, and A. R. Saltiel (2006)
J. Biol. Chem. 281, 38609-38616
   Abstract »    Full Text »    PDF »
Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy.
G. M. Gaietta, B. N. G. Giepmans, T. J. Deerinck, W. B. Smith, L. Ngan, J. Llopis, S. R. Adams, R. Y. Tsien, and M. H. Ellisman (2006)
PNAS 103, 17777-17782
   Abstract »    Full Text »    PDF »
CP110 Cooperates with Two Calcium-binding Proteins to Regulate Cytokinesis and Genome Stability.
W. Y. Tsang, A. Spektor, D. J. Luciano, V. B. Indjeian, Z. Chen, J. L. Salisbury, I. Sanchez, and B. D. Dynlacht (2006)
Mol. Biol. Cell 17, 3423-3434
   Abstract »    Full Text »    PDF »
Motor protein KIFC5A interacts with Nubp1 and Nubp2, and is implicated in the regulation of centrosome duplication.
A. Christodoulou, C. W. Lederer, T. Surrey, I. Vernos, and N. Santama (2006)
J. Cell Sci. 119, 2035-2047
   Abstract »    Full Text »    PDF »
Arl2 and Arl3 Regulate Different Microtubule-dependent Processes.
C. Zhou, L. Cunningham, A. I. Marcus, Y. Li, and R. A. Kahn (2006)
Mol. Biol. Cell 17, 2476-2487
   Abstract »    Full Text »    PDF »
Characterization of Su48, a centrosome protein essential for cell division.
Q. Wang, X. Du, J. Meinkoth, Y. Hirohashi, H. Zhang, Q. Liu, M. Richter, and M. I. Greene (2006)
PNAS 103, 6512-6517
   Abstract »    Full Text »    PDF »
Spore number control and breeding in Saccharomyces cerevisiae: a key role for a self-organizing system.
C. Taxis, P. Keller, Z. Kavagiou, L. J. Jensen, J. Colombelli, P. Bork, E. H.K. Stelzer, and M. Knop (2005)
J. Cell Biol. 171, 627-640
   Abstract »    Full Text »    PDF »
Centrobin: a novel daughter centriole-associated protein that is required for centriole duplication.
C. Zou, J. Li, Y. Bai, W. T. Gunning, D. E. Wazer, V. Band, and Q. Gao (2005)
J. Cell Biol. 171, 437-445
   Abstract »    Full Text »    PDF »
Centrosomal Microtubule Nucleation Activity Is Inhibited by BRCA1-Dependent Ubiquitination.
S. Sankaran, L. M. Starita, A. C. Groen, M. J. Ko, and J. D. Parvin (2005)
Mol. Cell. Biol. 25, 8656-8668
   Abstract »    Full Text »    PDF »
Hsp70 Protects Mitotic Cells against Heat-induced Centrosome Damage and Division Abnormalities.
H. M.J. Hut, H. H. Kampinga, and O. C.M. Sibon (2005)
Mol. Biol. Cell 16, 3776-3785
   Abstract »    Full Text »    PDF »
Adhesion-dependent and Contractile Ring-independent Equatorial Furrowing during Cytokinesis in Mammalian Cells.
M. Kanada, A. Nagasaki, and T. Q.P. Uyeda (2005)
Mol. Biol. Cell 16, 3865-3872
   Abstract »    Full Text »    PDF »
The Dual-Specificity Phosphatase CDC14B Bundles and Stabilizes Microtubules.
H. P. Cho, Y. Liu, M. Gomez, J. Dunlap, M. Tyers, and Y. Wang (2005)
Mol. Cell. Biol. 25, 4541-4551
   Abstract »    Full Text »    PDF »
YB-1 Provokes Breast Cancer through the Induction of Chromosomal Instability That Emerges from Mitotic Failure and Centrosome Amplification.
S. Bergmann, B. Royer-Pokora, E. Fietze, K. Jurchott, B. Hildebrandt, D. Trost, F. Leenders, J.-C. Claude, F. Theuring, R. Bargou, et al. (2005)
Cancer Res. 65, 4078-4087
   Abstract »    Full Text »    PDF »
MKKS/BBS6, a divergent chaperonin-like protein linked to the obesity disorder Bardet-Biedl syndrome, is a novel centrosomal component required for cytokinesis.
J. C. Kim, Y. Y. Ou, J. L. Badano, M. A. Esmail, C. C. Leitch, E. Fiedrich, P. L. Beales, J. M. Archibald, N. Katsanis, J. B. Rattner, et al. (2005)
J. Cell Sci. 118, 1007-1020
   Abstract »    Full Text »    PDF »
The Forkhead-associated Domain Protein Cep170 Interacts with Polo-like Kinase 1 and Serves as a Marker for Mature Centrioles.
G. Guarguaglini, P. I. Duncan, Y. D. Stierhof, T. Holmstrom, S. Duensing, and E. A. Nigg (2005)
Mol. Biol. Cell 16, 1095-1107
   Abstract »    Full Text »    PDF »
Ablation of PRC1 by Small Interfering RNA Demonstrates that Cytokinetic Abscission Requires a Central Spindle Bundle in Mammalian Cells, whereas Completion of Furrowing Does Not.
C. Mollinari, J.-P. Kleman, Y. Saoudi, S. A. Jablonski, J. Perard, T. J. Yen, and R. L. Margolis (2005)
Mol. Biol. Cell 16, 1043-1055
   Abstract »    Full Text »    PDF »
The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation.
S. La Terra, C. N. English, P. Hergert, B. F. McEwen, G. Sluder, and A. Khodjakov (2005)
J. Cell Biol. 168, 713-722
   Abstract »    Full Text »    PDF »
Mitotic Infidelity and Centrosome Duplication Errors in Cells Overexpressing Tripeptidyl-Peptidase II.
V. Stavropoulou, J. Xie, M. Henriksson, B. Tomkinson, S. Imreh, and M. G. Masucci (2005)
Cancer Res. 65, 1361-1368
   Abstract »    Full Text »    PDF »
Chromosomal Instability in Oral Cancer Cells.
S.C. Reshmi and S.M. Gollin (2005)
J. Dent. Res. 84, 107-117
   Abstract »    Full Text »    PDF »
BRCA1-Dependent Ubiquitination of {gamma}-Tubulin Regulates Centrosome Number.
L. M. Starita, Y. Machida, S. Sankaran, J. E. Elias, K. Griffin, B. P. Schlegel, S. P. Gygi, and J. D. Parvin (2004)
Mol. Cell. Biol. 24, 8457-8466
   Abstract »    Full Text »    PDF »
OFD1 Is a Centrosomal/Basal Body Protein Expressed during Mesenchymal-Epithelial Transition in Human Nephrogenesis.
L. Romio, A. M. Fry, P. J.D. Winyard, S. Malcolm, A. S. Woolf, and S. A. Feather (2004)
J. Am. Soc. Nephrol. 15, 2556-2568
   Abstract »    Full Text »    PDF »
G2 cell cycle arrest, down-regulation of cyclin B, and induction of mitotic catastrophe by the flavoprotein inhibitor diphenyleneiodonium.
R. M. Scaife (2004)
Mol. Cancer Ther. 3, 1229-1237
   Abstract »    Full Text »    PDF »
Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon.
A. Errico, P. Claudiani, M. D'Addio, and E. I. Rugarli (2004)
Hum. Mol. Genet. 13, 2121-2132
   Abstract »    Full Text »    PDF »
B23/Nucleophosmin Serine 4 Phosphorylation Mediates Mitotic Functions of Polo-like Kinase 1.
H. Zhang, X. Shi, H. Paddon, M. Hampong, W. Dai, and S. Pelech (2004)
J. Biol. Chem. 279, 35726-35734
   Abstract »    Full Text »    PDF »
Eukaryotic Cells and their Cell Bodies: Cell Theory Revised.
F. BALUSKA, D. VOLKMANN, and P. W. BARLOW (2004)
Ann. Bot. 94, 9-32
   Abstract »    Full Text »    PDF »
Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis.
A. Tomas, C. Futter, and S. E. Moss (2004)
J. Cell Biol. 165, 813-822
   Abstract »    Full Text »    PDF »
Centrin Gene Disruption Impairs Stage-specific Basal Body Duplication and Cell Cycle Progression in Leishmania.
A. Selvapandiyan, A. Debrabant, R. Duncan, J. Muller, P. Salotra, G. Sreenivas, J. L. Salisbury, and H. L. Nakhasi (2004)
J. Biol. Chem. 279, 25703-25710
   Abstract »    Full Text »    PDF »
Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a "tetraploidy checkpoint".
Y. Uetake and G. Sluder (2004)
J. Cell Biol. 165, 609-615
   Abstract »    Full Text »    PDF »
Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition.
S. Dutertre, M. Cazales, M. Quaranta, C. Froment, V. Trabut, C. Dozier, G. Mirey, J.-P. Bouche, N. Theis-Febvre, E. Schmitt, et al. (2004)
J. Cell Sci. 117, 2523-2531
   Abstract »    Full Text »    PDF »
Recruitment of NIMA kinase shows that maturation of the S. pombe spindle-pole body occurs over consecutive cell cycles and reveals a role for NIMA in modulating SIN activity.
A. Grallert, A. Krapp, S. Bagley, V. Simanis, and I. M. Hagan (2004)
Genes & Dev. 18, 1007-1021
   Abstract »    Full Text »    PDF »
Cleavage furrow positioning.
M. Glotzer (2004)
J. Cell Biol. 164, 347-351
   Abstract »    Full Text »    PDF »
Novel regulation of mitotic exit by the Cdc42 effectors Gic1 and Gic2.
T. Hofken and E. Schiebel (2004)
J. Cell Biol. 164, 219-231
   Abstract »    Full Text »    PDF »
Mammalian RanBP1 regulates centrosome cohesion during mitosis.
B. Di Fiore, M. Ciciarello, R. Mangiacasale, A. Palena, A.-M. Tassin, E. Cundari, and P. Lavia (2003)
J. Cell Sci. 116, 3399-3411
   Abstract »    Full Text »    PDF »
Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage.
G. B. Alsop and D. Zhang (2003)
J. Cell Biol. 162, 383-390
   Abstract »    Full Text »    PDF »
Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles.
A. J. Faragher and A. M. Fry (2003)
Mol. Biol. Cell 14, 2876-2889
   Abstract »    Full Text »    PDF »
Physical and functional interactions between polo kinase and the spindle pole component Cut12 regulate mitotic commitment in S. pombe.
F. H. MacIver, K. Tanaka, A. M. Robertson, and I. M. Hagan (2003)
Genes & Dev. 17, 1507-1523
   Abstract »    Full Text »    PDF »
Dissociating the Centrosomal Matrix Protein AKAP450 from Centrioles Impairs Centriole Duplication and Cell Cycle Progression.
G. Keryer, O. Witczak, A. Delouvee, W. A. Kemmner, D. Rouillard, K. Tasken, and M. Bornens (2003)
Mol. Biol. Cell 14, 2436-2446
   Abstract »    Full Text »    PDF »
A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase.
A. Gromley, A. Jurczyk, J. Sillibourne, E. Halilovic, M. Mogensen, I. Groisman, M. Blomberg, and S. Doxsey (2003)
J. Cell Biol. 161, 535-545
   Abstract »    Full Text »    PDF »
Centrosomes Split in the Presence of Impaired DNA Integrity during Mitosis.
H. M.J. Hut, W. Lemstra, E. H. Blaauw, G. W.A. van Cappellen, H. H. Kampinga, and O. C.M. Sibon (2003)
Mol. Biol. Cell 14, 1993-2004
   Abstract »    Full Text »    PDF »
Centrosome Abnormalities and Chromosome Instability Occur Together in Pre-invasive Carcinomas.
G. A. Pihan, J. Wallace, Y. Zhou, and S. J. Doxsey (2003)
Cancer Res. 63, 1398-1404
   Abstract »    Full Text »    PDF »
E1A Deregulates the Centrosome Cycle in a Ran GTPase-dependent Manner.
A. De Luca, R. Mangiacasale, A. Severino, L. Malquori, A. Baldi, A. Palena, A. M. Mileo, P. Lavia, and M. G. Paggi (2003)
Cancer Res. 63, 1430-1437
   Abstract »    Full Text »    PDF »
Citron Kinase Is a Cell Cycle-dependent, Nuclear Protein Required for G2/M Transition of Hepatocytes.
H. Liu, F. Di Cunto, S. Imarisio, and L. M. Reid (2003)
J. Biol. Chem. 278, 2541-2548
   Abstract »    Full Text »    PDF »
The centrosomal kinase Aurora-A/STK15 interacts with a putative tumor suppressor NM23-H1.
J. Du and G. J. Hannon (2002)
Nucleic Acids Res. 30, 5465-5475
   Abstract »    Full Text »    PDF »
epsilon -Tubulin Is an Essential Component of the Centriole.
S. K. Dutcher, N. S. Morrissette, A. M. Preble, C. Rackley, and J. Stanga (2002)
Mol. Biol. Cell 13, 3859-3869
   Abstract »    Full Text »    PDF »
Distinct cell cycle-dependent roles for dynactin and dynein at centrosomes.
N. J. Quintyne and T. A. Schroer (2002)
J. Cell Biol. 159, 245-254
   Abstract »    Full Text »    PDF »
The Mammalian Septin MSF Localizes with Microtubules and Is Required for Completion of Cytokinesis.
M. C. Surka, C. W. Tsang, and W. S. Trimble (2002)
Mol. Biol. Cell 13, 3532-3545
   Abstract »    Full Text »    PDF »
Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells.
F. Borel, O. D. Lohez, F. B. Lacroix, and R. L. Margolis (2002)
PNAS 99, 9819-9824
   Abstract »    Full Text »    PDF »
Cyclin G2 Associates with Protein Phosphatase 2A Catalytic and Regulatory B' Subunits in Active Complexes and Induces Nuclear Aberrations and a G1/S Phase Cell Cycle Arrest.
D. A. Bennin, A. S. A. Don, T. Brake, J. L. McKenzie, H. Rosenbaum, L. Ortiz, A. A. DePaoli-Roach, and M. C. Horne (2002)
J. Biol. Chem. 277, 27449-27467
   Abstract »    Full Text »    PDF »
Disruption of Centrosome Structure, Chromosome Segregation, and Cytokinesis by Misexpression of Human Cdc14A Phosphatase.
B. K. Kaiser, Z. A. Zimmerman, H. Charbonneau, and P. K. Jackson (2002)
Mol. Biol. Cell 13, 2289-2300
   Abstract »    Full Text »    PDF »
Cytokinesis in Eukaryotes.
D. A. Guertin, S. Trautmann, and D. McCollum (2002)
Microbiol. Mol. Biol. Rev. 66, 155-178
   Abstract »    Full Text »    PDF »
Centrosome Reorientation in Wound-Edge Cells Is Cell Type Specific.
A.-M. C. Yvon, J. W. Walker, B. Danowski, C. Fagerstrom, A. Khodjakov, and P. Wadsworth (2002)
Mol. Biol. Cell 13, 1871-1880
   Abstract »    Full Text »    PDF »
The Rho-associated protein kinase p160ROCK is required for centrosome positioning.
V. Chevrier, M. Piel, N. Collomb, Y. Saoudi, R. Frank, M. Paintrand, S. Narumiya, M. Bornens, and D. Job (2002)
J. Cell Biol. 157, 807-817
   Abstract »    Full Text »    PDF »
Centrosome cohesion is regulated by a balance of kinase and phosphatase activities.
P. Meraldi and E. A. Nigg (2002)
J. Cell Sci. 114, 3749-3757
   Abstract »    Full Text »    PDF »
CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis.
R. Kuriyama, C. Gustus, Y. Terada, Y. Uetake, and J. Matuliene (2002)
J. Cell Biol. 156, 783-790
   Abstract »    Full Text »    PDF »
The centrosome is a dynamic structure that ejects PCM flares.
T. L. Megraw, S. Kilaru, F. R. Turner, and T. C. Kaufman (2002)
J. Cell Sci. 115, 4707-4718
   Abstract »    Full Text »    PDF »
"It Takes Two to Tango": understanding how centrosome duplication is regulated throughout the cell cycle.
E. H. Hinchcliffe and G. Sluder (2001)
Genes & Dev. 15, 1167-1181
   Full Text »
Requirement of a Centrosomal Activity for Cell Cycle Progression Through G1 into S Phase.
E. H. Hinchcliffe, F. J. Miller, M. Cham, A. Khodjakov, and G. Sluder (2001)
Science 291, 1547-1550
   Abstract »    Full Text »    PDF »
beta III Spectrin Binds to the Arp1 Subunit of Dynactin.
E. A. Holleran, L. A. Ligon, M. Tokito, M. C. Stankewich, J. S. Morrow, and E. L. F. Holzbaur (2001)
J. Biol. Chem. 276, 36598-36605
   Abstract »    Full Text »    PDF »
CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis.
R. Kuriyama, C. Gustus, Y. Terada, Y. Uetake, and J. Matuliene (2002)
J. Cell Biol. 156, 783-790
   Abstract »    Full Text »    PDF »



ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)