Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells

doi:10.1083/jcb.130.1.105

This Article

	Full Text (PDF, 2435K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Balczon, R.
	Articles by Brinkley, B. R.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Balczon, R.
	Articles by Brinkley, B. R.


Social Bookmarking

	What's this?

ARTICLES

Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells

R Balczon, L Bao, WE Zimmer, K Brown, RP Zinkowski and BR Brinkley
Department of Structural and Cellular Biology, University of South Alabama, Mobile 36688, USA.

Relatively little is known about the mechanisms used by somatic cells to regulate the replication of the centrosome complex. Centrosome doubling was studied in CHO cells by electron microscopy and immunofluorescence microscopy using human autoimmune anticentrosome antiserum, and by Northern blotting using the cDNA encoding portion of the centrosome autoantigen pericentriolar material (PCM)-1. Centrosome doubling could be dissociated from cycles of DNA synthesis and mitotic division by arresting cells at the G1/S boundary of the cell cycle using either hydroxyurea or aphidicolin. Immunofluorescence micros-copy using SPJ human autoimmune anticentrosome antiserum demonstrated that arrested cells were able to undergo numerous rounds of centrosome replication in the absence of cycles of DNA synthesis and mitosis. Northern blot analysis demonstrated that the synthesis and degradation of the mRNA encoding PCM-1 occurred in a cell cycle-dependent fashion in CHO cells with peak levels of PCM-1 mRNA being present in G1 and S phase cells before mRNA amounts dropped to undetectable levels in G2 and M phases. Conversely, cells arrested at the G1/S boundary of the cell cycle maintained PCM-1 mRNA at artificially elevated levels, providing a possible molecular mechanism for explaining the multiple rounds of centrosome replication that occurred in CHO cells during prolonged hydroxyurea-induced arrest. The capacity to replicate centrosomes could be abolished in hydroxyurea-arrested CHO cells by culturing the cells in dialyzed serum. However, the ability to replicate centrosomes and to synthesize PCM-1 mRNA could be re- initiated by adding EGF to the dialyzed serum. This experimental system should be useful for investigating the positive and negative molecular mechanisms used by somatic cells to regulate the replication of centrosomes and for studying and the methods used by somatic cells for coordinating centrosome duplication with other cell cycle progression events.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Kuriyama, R., Bettencourt-Dias, M., Hoffmann, I., Arnold, M., Sandvig, L. (2009). {gamma}-Tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells. J. Cell Sci. 122: 2014-2023 [Abstract] [Full Text]
Prosser, S. L., Straatman, K. R., Fry, A. M. (2009). Molecular Dissection of the Centrosome Overduplication Pathway in S-Phase-Arrested Cells. Mol. Cell. Biol. 29: 1760-1773 [Abstract] [Full Text]
Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M., Rogers, S. L. (2009). The SCFSlimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. JCB 184: 225-239 [Abstract] [Full Text]
Wu, J., Cho, H. P., Rhee, D. B., Johnson, D. K., Dunlap, J., Liu, Y., Wang, Y. (2008). Cdc14B depletion leads to centriole amplification, and its overexpression prevents unscheduled centriole duplication. JCB 181: 475-483 [Abstract] [Full Text]
Ferguson, R. L., Maller, J. L. (2008). Cyclin E-dependent localization of MCM5 regulates centrosome duplication. J. Cell Sci. 121: 3224-3232 [Abstract] [Full Text]
Simmons Kovacs, L. A., Nelson, C. L., Haase, S. B. (2008). Intrinsic and Cyclin-dependent Kinase-dependent Control of Spindle Pole Body Duplication in Budding Yeast. Mol. Biol. Cell 19: 3243-3253 [Abstract] [Full Text]
Wu, S., Chen, H., Alexeyev, M. F., King, J. A. C., Moore, T. M., Stevens, T., Balczon, R. D. (2007). Microtubule Motors Regulate ISOC Activation Necessary to Increase Endothelial Cell Permeability. J. Biol. Chem. 282: 34801-34808 [Abstract] [Full Text]
Chartier, N. T., Oddou, C. I., Laine, M. G., Ducarouge, B., Marie, C. A., Block, M. R., Jacquier-Sarlin, M. R. (2007). Cyclin-Dependent Kinase 2/Cyclin E Complex Is Involved in p120 Catenin (p120ctn) Dependent Cell Growth Control: A New Role for p120ctn in Cancer. Cancer Res. 67: 9781-9790 [Abstract] [Full Text]
Kuriyama, R., Terada, Y., Lee, K. S., Wang, C. L. C. (2007). Centrosome replication in hydroxyurea-arrested CHO cells expressing GFP-tagged centrin2. J. Cell Sci. 120: 2444-2453 [Abstract] [Full Text]
Lin, X., Liu, C.-C., Gao, Q., Zhang, X., Wu, G., Lee, W.-H. (2007). RINT-1 Serves as a Tumor Suppressor and Maintains Golgi Dynamics and Centrosome Integrity for Cell Survival. Mol. Cell. Biol. 27: 4905-4916 [Abstract] [Full Text]
Gill, M. B., Kutok, J. L., Fingeroth, J. D. (2007). Epstein-Barr Virus Thymidine Kinase Is a Centrosomal Resident Precisely Localized to the Periphery of Centrioles. J. Virol. 81: 6523-6535 [Abstract] [Full Text]
Kanai, M., Ma, Z., Izumi, H., Kim, S.-H., Mattison, C. P., Winey, M., Fukasawa, K. (2007). Physical and functional interaction between mortalin and Mps1 kinase. GENES CELLS 12: 797-810 [Abstract] [Full Text]
Dawe, H. R., Farr, H., Gull, K. (2007). Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J. Cell Sci. 120: 7-15 [Abstract] [Full Text]
Ma, Z., Kanai, M., Kawamura, K., Kaibuchi, K., Ye, K., Fukasawa, K. (2006). Interaction between ROCK II and Nucleophosmin/B23 in the Regulation of Centrosome Duplication. Mol. Cell. Biol. 26: 9016-9034 [Abstract] [Full Text]
Suizu, F., Ryo, A., Wulf, G., Lim, J., Lu, K. P. (2006). Pin1 Regulates Centrosome Duplication, and Its Overexpression Induces Centrosome Amplification, Chromosome Instability, and Oncogenesis. Mol. Cell. Biol. 26: 1463-1479 [Abstract] [Full Text]
Haren, L., Remy, M.-H., Bazin, I., Callebaut, I., Wright, M., Merdes, A. (2006). NEDD1-dependent recruitment of the {gamma}-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. JCB 172: 505-515 [Abstract] [Full Text]
Adams, L. D., Geary, R. L., Li, J., Rossini, A., Schwartz, S. M. (2006). Expression Profiling Identifies Smooth Muscle Cell Diversity Within Human Intima and Plaque Fibrous Cap: Loss of RGS5 Distinguishes the Cap. Arterioscler. Thromb. Vasc. Bio. 26: 319-325 [Abstract] [Full Text]
Guarguaglini, G., Duncan, P. I., Stierhof, Y. D., Holmstrom, T., Duensing, S., Nigg, E. A. (2005). The Forkhead-associated Domain Protein Cep170 Interacts with Polo-like Kinase 1 and Serves as a Marker for Mature Centrioles. Mol. Biol. Cell 16: 1095-1107 [Abstract] [Full Text]
Nishimura, T., Takahashi, M., Kim, H.-S., Mukai, H., Ono, Y. (2005). Centrosome-targeting region of CG-NAP causes centrosome amplification by recruiting cyclin E-cdk2 complex. GENES CELLS 10: 75-86 [Abstract] [Full Text]
Uzawa, S., Li, F., Jin, Y., McDonald, K. L., Braunfeld, M. B., Agard, D. A., Cande, W. Z. (2004). Spindle Pole Body Duplication in Fission Yeast Occurs at the G1/S Boundary but Maturation Is Blocked until Exit from S by an Event Downstream of Cdc10+. Mol. Biol. Cell 15: 5219-5230 [Abstract] [Full Text]
Metge, B., Ofori-Acquah, S., Stevens, T., Balczon, R. (2004). Stat3 Activity Is Required for Centrosome Duplication in Chinese Hamster Ovary Cells. J. Biol. Chem. 279: 41801-41806 [Abstract] [Full Text]
van IJzendoorn, S. C.D., Theard, D., van der Wouden, J. M., Visser, W., Wojtal, K. A., Hoekstra, D. (2004). Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27Kip1-Regulated Cell Cycle Dynamics. Mol. Biol. Cell 15: 4105-4114 [Abstract] [Full Text]
Kawamura, K., Izumi, H., Ma, Z., Ikeda, R., Moriyama, M., Tanaka, T., Nojima, T., Levin, L. S., Fujikawa-Yamamoto, K., Suzuki, K., Fukasawa, K. (2004). Induction of Centrosome Amplification and Chromosome Instability in Human Bladder Cancer Cells by p53 Mutation and Cyclin E Overexpression. Cancer Res. 64: 4800-4809 [Abstract] [Full Text]
Delattre, M., Gonczy, P. (2004). The arithmetic of centrosome biogenesis. J. Cell Sci. 117: 1619-1630 [Abstract] [Full Text]
Di Fiore, B., Ciciarello, M., Mangiacasale, R., Palena, A., Tassin, A.-M., Cundari, E., Lavia, P. (2003). Mammalian RanBP1 regulates centrosome cohesion during mitosis. J. Cell Sci. 116: 3399-3411 [Abstract] [Full Text]
Keryer, G., Witczak, O., Delouvee, A., Kemmner, W. A., Rouillard, D., Tasken, K., Bornens, M. (2003). Dissociating the Centrosomal Matrix Protein AKAP450 from Centrioles Impairs Centriole Duplication and Cell Cycle Progression. Mol. Biol. Cell 14: 2436-2446 [Abstract] [Full Text]
Hut, H. M.J., Lemstra, W., Blaauw, E. H., van Cappellen, G. W.A., Kampinga, H. H., Sibon, O. C.M. (2003). Centrosomes Split in the Presence of Impaired DNA Integrity during Mitosis. Mol. Biol. Cell 14: 1993-2004 [Abstract] [Full Text]
Augustin, A., Spenlehauer, C., Dumond, H., Menissier-de Murcia, J., Piel, M., Schmit, A.-C., Apiou, F., Vonesch, J.-L., Kock, M., Bornens, M., de Murcia, G. (2003). PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression. J. Cell Sci. 116: 1551-1562 [Abstract] [Full Text]
Kanai, M., Tong, W.-M., Sugihara, E., Wang, Z.-Q., Fukasawa, K., Miwa, M. (2003). Involvement of Poly(ADP-Ribose) Polymerase 1 and Poly(ADP-Ribosyl)ation in Regulation of Centrosome Function. Mol. Cell. Biol. 23: 2451-2462 [Abstract] [Full Text]
Khodjakov, A., Rieder, C. L., Sluder, G., Cassels, G., Sibon, O., Wang, C.-L. (2002). De novo formation of centrosomes in vertebrate cells arrested during S phase. JCB 158: 1171-1181 [Abstract] [Full Text]
Borel, F., Lohez, O. D., Lacroix, F. B., Margolis, R. L. (2002). Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc. Natl. Acad. Sci. USA 99: 9819-9824 [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]
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]
Vidwans, S. J., Wong, M. L., O'Farrell, P. H. (1999). Mitotic Regulators Govern Progress through Steps in the Centrosome Duplication Cycle. JCB 147: 1371-1378 [Abstract] [Full Text]
Lingle, W. L., Salisbury, J. L. (1999). Altered Centrosome Structure Is Associated with Abnormal Mitoses in Human Breast Tumors. Am. J. Pathol. 155: 1941-1951 [Abstract] [Full Text]
Kubo, A., Sasaki, H., Yuba-Kubo, A., Tsukita, S., Shiina, N. (1999). Centriolar Satellites: Molecular Characterization, Atp-Dependent Movement toward Centrioles and Possible Involvement in Ciliogenesis. JCB 147: 969-980 [Abstract] [Full Text]
Quintyne, N.J., Gill, S.R., Eckley, D.M., Crego, C.L., Compton, D.A., Schroer, T.A. (1999). Dynactin Is Required for Microtubule Anchoring at Centrosomes. JCB 147: 321-334 [Abstract] [Full Text]
Freed, E., Lacey, K. R., Huie, P., Lyapina, S. A., Deshaies, R. J., Stearns, T., Jackson, P. K. (1999). Components of an SCF ubiquitin ligase localize to the centrosome and regulate the centrosome duplication cycle. Genes Dev. 13: 2242-2257 [Abstract] [Full Text]
Giet, R., Uzbekov, R., Cubizolles, F., Le Guellec, K., Prigent, C. (1999). The Xenopus laevis Aurora-related Protein Kinase pEg2 Associates with and Phosphorylates the Kinesin-related Protein XlEg5. J. Biol. Chem. 274: 15005-15013 [Abstract] [Full Text]
Lacey, K. R., Jackson, P. K., Stearns, T. (1999). Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. USA 96: 2817-2822 [Abstract] [Full Text]
Hinchcliffe, E. H., Li, C., Thompson, E. A., Maller, J. L., Sluder, G. (1999). Requirement of Cdk2-Cyclin E Activity for Repeated Centrosome Reproduction in Xenopus Egg Extracts. Science 283: 851-854 [Abstract] [Full Text]
Hinchcliffe, E. H., Cassels, G. O., Rieder, C. L., Sluder, G. (1998). The Coordination of Centrosome Reproduction with Nuclear Events of the Cell Cycle in the Sea Urchin Zygote. JCB 140: 1417-1426 [Abstract] [Full Text]
Jerka-Dziadosz, M, Ruiz, F, Beisson, F (1998). Uncoupling of basal body duplication and cell division in crochu, a mutant of Paramecium hypersensitive to nocodazole. Development 125: 1305-1314 [Abstract]
Roghi, C, Giet, R, Uzbekov, R, Morin, N, Chartrain, I, Le Guellec, R, Couturier, A, Doree, M, Philippe, M, Prigent, C (1998). The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J. Cell Sci. 111: 557-572 [Abstract]
Hinchcliffe, E., Linck, R. (1998). Two proteins isolated from sea urchin sperm flagella: structural components common to the stable microtubules of axonemes and centrioles. J. Cell Sci. 111: 585-595 [Abstract]
Meng, Y. X., Wilson, G. W., Avery, M. C., Varden, C. H., Balczon, R. (1997). Suppression of the Expression of a Pancreatic {beta}-Cell Form of the Kinesin Heavy Chain by Antisense Oligonucleotides Inhibits Insulin Secretion from Primary Cultures of Mouse {beta}-Cells. Endocrinology 138: 1979-1987 [Abstract] [Full Text]
Li, X, Nicklas, R. (1997). Tension-sensitive kinetochore phosphorylation and the chromosome distribution checkpoint in praying mantid spermatocytes. J. Cell Sci. 110: 537-545 [Abstract]
Tokuyama, Y., Horn, H. F., Kawamura, K., Tarapore, P., Fukasawa, K. (2001). Specific Phosphorylation of Nucleophosmin on Thr199 by Cyclin- dependent Kinase 2-Cyclin E and Its Role in Centrosome Duplication. J. Biol. Chem. 276: 21529-21537 [Abstract] [Full Text]