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Science 26 July 2002:
Vol. 297. no. 5581, pp. 559 - 565
DOI: 10.1126/science.1074757
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Review

Segregating Sister Genomes: The Molecular Biology of Chromosome Separation

Kim Nasmyth

During cell division, each daughter cell inherits one copy of every chromosome. Accurate transmission of chromosomes requires that the sister DNA molecules created during DNA replication are disentangled and then pulled to opposite poles of the cell before division. Defects in chromosome segregation produce cells that are aneuploid (containing an abnormal number of chromosomes)--a situation that can have dire consequences. Aneuploidy is a leading cause of spontaneous miscarriages in humans and is also a hallmark of many human cancer cells. Recent work with yeast, Xenopus, and other model systems has provided new information about the proteins that control chromosome segregation during cell division and how the activities of these proteins are coordinated with the cell cycle.

IMP, Dr. Bohr-Gasse 7, A-1030 Vienna, Austria.

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S. V. Holt, M. A. S. Vergnolle, D. Hussein, M. J. Wozniak, V. J. Allan, and S. S. Taylor (2005)
J. Cell Sci. 118, 4889-4900
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J. Cell Sci. 118, 4621-4632
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Rad50 depletion impacts upon ATR-dependent DNA damage responses.
H. Zhong, A. Bryson, M. Eckersdorff, and D. O. Ferguson (2005)
Hum. Mol. Genet. 14, 2685-2693
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Post-ovulatory aging of mouse oocytes leads to decreased MAD2 transcripts and increased frequencies of premature centromere separation and anaphase.
N. M. Steuerwald, M. D. Steuerwald, and J. B. Mailhes (2005)
Mol. Hum. Reprod. 11, 623-630
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Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog.
S. Heeger, O. Leismann, R. Schittenhelm, O. Schraidt, S. Heidmann, and C. F. Lehner (2005)
Genes & Dev. 19, 2041-2053
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Human MMS21/NSE2 Is a SUMO Ligase Required for DNA Repair.
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Mol. Cell. Biol. 25, 7021-7032
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Tension-dependent Regulation of Microtubule Dynamics at Kinetochores Can Explain Metaphase Congression in Yeast.
M. K. Gardner, C. G. Pearson, B. L. Sprague, T. R. Zarzar, K. Bloom, E. D. Salmon, and D. J. Odde (2005)
Mol. Biol. Cell 16, 3764-3775
   Abstract »    Full Text »    PDF »
Membrane Type-1 Matrix Metalloproteinase (MT1-MMP) Exhibits an Important Intracellular Cleavage Function and Causes Chromosome Instability.
V. S. Golubkov, S. Boyd, A. Y. Savinov, A. V. Chekanov, A. L. Osterman, A. Remacle, D. V. Rozanov, S. J. Doxsey, and A. Y. Strongin (2005)
J. Biol. Chem. 280, 25079-25086
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Chromosome bi-orientation on the mitotic spindle.
T. U Tanaka (2005)
Phil Trans R Soc B 360, 581-589
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Chromosomal instability and human cancer.
F. Michor (2005)
Phil Trans R Soc B 360, 631-635
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Explaining the oligomerization properties of the spindle assembly checkpoint protein Mad2.
A. DeAntoni, V. Sala, and A. Musacchio (2005)
Phil Trans R Soc B 360, 637-648
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Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome.
M. B. Mann, C. A. Hodges, E. Barnes, H. Vogel, T. J. Hassold, and G. Luo (2005)
Hum. Mol. Genet. 14, 813-825
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The Centromeric Protein Sgo1 Is Required to Sense Lack of Tension on Mitotic Chromosomes.
V. B. Indjeian, B. M. Stern, and A. W. Murray (2005)
Science 307, 130-133
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HTLV-I Tax directly binds the Cdc20-associated anaphase-promoting complex and activates it ahead of schedule.
B. Liu, S. Hong, Z. Tang, H. Yu, and C.-Z. Giam (2005)
PNAS 102, 63-68
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Primary Flagellar Abnormality Is Associated With an Increased Rate of Spermatozoa Aneuploidy.
N. Rives, N. Mousset-Simeon, S. Mazurier, and B. Mace (2005)
J Androl 26, 61-69
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Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis.
Z. Tang, Y. Sun, S. E. Harley, H. Zou, and H. Yu (2004)
PNAS 101, 18012-18017
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Construction, Characterization, and Complementation of a Conditional-Lethal DNA Topoisomerase II{alpha} Mutant Human Cell Line.
A. J. Carpenter and A. C.G. Porter (2004)
Mol. Biol. Cell 15, 5700-5711
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Condensin restructures chromosomes in preparation for meiotic divisions.
R. C. Chan, A. F. Severson, and B. J. Meyer (2004)
J. Cell Biol. 167, 613-625
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At the interface between signaling and executing anaphase--Cdc14 and the FEAR network.
D. D'Amours and A. Amon (2004)
Genes & Dev. 18, 2581-2595
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The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly.
J.-C. Labbe, E. K. McCarthy, and B. Goldstein (2004)
J. Cell Biol. 167, 245-256
   Abstract »    Full Text »    PDF »
Mutations in the Drosophila Condensin Subunit dCAP-G: Defining the Role of Condensin for Chromosome Condensation in Mitosis and Gene Expression in Interphase.
K. J. Dej, C. Ahn, and T. L. Orr-Weaver (2004)
Genetics 168, 895-906
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Hormone-Induced Chromosomal Instability in p53-Null Mammary Epithelium.
D. Pati, B. R. Haddad, A. Haegele, H. Thompson, F. S. Kittrell, A. Shepard, C. Montagna, N. Zhang, G. Ge, S. K. Otta, et al. (2004)
Cancer Res. 64, 5608-5616
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Modifying sister chromatid cohesion for meiosis.
Y. Watanabe (2004)
J. Cell Sci. 117, 4017-4023
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Evolutionary dynamics of tumor suppressor gene inactivation.
M. A. Nowak, F. Michor, N. L. Komarova, and Y. Iwasa (2004)
PNAS 101, 10635-10638
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Bipolar orientation of chromosomes in Saccharomyces cerevisiae is monitored by Mad1 and Mad2, but not by Mad3.
M. S. Lee and F. A. Spencer (2004)
PNAS 101, 10655-10660
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Spatial and Temporal Regulation of Condensins I and II in Mitotic Chromosome Assembly in Human Cells.
T. Ono, Y. Fang, D. L. Spector, and T. Hirano (2004)
Mol. Biol. Cell 15, 3296-3308
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J. Virol. 78, 6621-6635
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Spindle checkpoint regulates Cdc20p stability in Saccharomyces cerevisiae.
J. Pan and R.-H. Chen (2004)
Genes & Dev. 18, 1439-1451
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The cell cycle and how it is steered by Kaposi's sarcoma-associated herpesvirus cyclin.
E. W. Verschuren, N. Jones, and G. I. Evan (2004)
J. Gen. Virol. 85, 1347-1361
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The Origin Recognition Complex Links Replication, Sister Chromatid Cohesion and Transcriptional Silencing in Saccharomyces cerevisiae.
B. Suter, A. Tong, M. Chang, L. Yu, G. W. Brown, C. Boone, and J. Rine (2004)
Genetics 167, 579-591
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Isolation and characterization of a novel DNA methyltransferase complex linking DNMT3B with components of the mitotic chromosome condensation machinery.
T. M. Geiman, U. T. Sankpal, A. K. Robertson, Y. Chen, M. Mazumdar, J. T. Heale, J. A. Schmiesing, W. Kim, K. Yokomori, Y. Zhao, et al. (2004)
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Molecular characterization of OsRAD21-1, a rice homologue of yeast RAD21 essential for mitotic chromosome cohesion.
L.-R. Zhang, J.-Y. Tao, and T. Wang (2004)
J. Exp. Bot. 55, 1149-1152
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Drosophila Nipped-B Protein Supports Sister Chromatid Cohesion and Opposes the Stromalin/Scc3 Cohesion Factor To Facilitate Long-Range Activation of the cut Gene.
R. A. Rollins, M. Korom, N. Aulner, A. Martens, and D. Dorsett (2004)
Mol. Cell. Biol. 24, 3100-3111
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Sister chromatid separation at human telomeric regions.
M. Yalon, S. Gal, Y. Segev, S. Selig, and K. L. Skorecki (2004)
J. Cell Sci. 117, 1961-1970
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Securin Is a Target of the UV Response Pathway in Mammalian Cells.
F. Romero, A. M. Gil-Bernabe, C. Saez, M. A. Japon, J. A. Pintor-Toro, and M. Tortolero (2004)
Mol. Cell. Biol. 24, 2720-2733
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Genetic Interaction of an Origin Recognition Complex Subunit and the Polycomb Group Gene MEDEA during Seed Development.
M. A. Collinge, C. Spillane, C. Kohler, J. Gheyselinck, and U. Grossniklaus (2004)
PLANT CELL 16, 1035-1046
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Identification of Two Novel Components of the Human NDC80 Kinetochore Complex.
R. Bharadwaj, W. Qi, and H. Yu (2004)
J. Biol. Chem. 279, 13076-13085
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Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I.
M. T. Parra, A. Viera, R. Gomez, J. Page, R. Benavente, J. L. Santos, J. S. Rufas, and J. A. Suja (2004)
J. Cell Sci. 117, 1221-1234
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Evidence of a Transcriptional Co-activator Function of Cohesin STAG/SA/Scc3.
E. Lara-Pezzi, N. Pezzi, I. Prieto, I. Barthelemy, C. Carreiro, A. Martinez, A. Maldonado-Rodriguez, M. Lopez-Cabrera, and J. L. Barbero (2004)
J. Biol. Chem. 279, 6553-6559
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A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis.
J. Fan and K. A. Beck (2004)
J. Cell Sci. 117, 619-629
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In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding.
B. D. Lavoie, E. Hogan, and D. Koshland (2004)
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Mitotic partitioning and selective reorganization of tissue-specific transcription factors in progeny cells.
S. K. Zaidi, D. W. Young, S. M. Pockwinse, A. Javed, J. B. Lian, J. L. Stein, A. J. van Wijnen, and G. S. Stein (2003)
PNAS 100, 14852-14857
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Inactivating Mutations Targeting the chfr Mitotic Checkpoint Gene in Human Lung Cancer.
G. Mariatos, J. Bothos, P. Zacharatos, M. K. Summers, D. M. Scolnick, C. Kittas, T. D. Halazonetis, and V. G. Gorgoulis (2003)
Cancer Res. 63, 7185-7189
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Events at the end of mitosis in the budding and fission yeasts.
V. Simanis (2003)
J. Cell Sci. 116, 4263-4275
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Overexpressed Pituitary Tumor-Transforming Gene Causes Aneuploidy in Live Human Cells.
R. Yu, W. Lu, J. Chen, C. J. McCabe, and S. Melmed (2003)
Endocrinology 144, 4991-4998
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Hyperproliferation and p53 Status of Lens Epithelial Cells Derived from {alpha}B-crystallin Knockout Mice.
F. Bai, J. H. Xi, E. F. Wawrousek, T. P. Fleming, and U. P. Andley (2003)
J. Biol. Chem. 278, 36876-36886
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Histone Hyperacetylation in Mitosis Prevents Sister Chromatid Separation and Produces Chromosome Segregation Defects.
D. Cimini, M. Mattiuzzo, L. Torosantucci, and F. Degrassi (2003)
Mol. Biol. Cell 14, 3821-3833
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Bacterial Chromosome Dynamics.
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Human T-Lymphotropic Virus Type 1 Oncoprotein Tax Promotes Unscheduled Degradation of Pds1p/Securin and Clb2p/Cyclin B1 and Causes Chromosomal Instability.
B. Liu, M.-H. Liang, Y.-l. Kuo, W. Liao, I. Boros, T. Kleinberger, J. Blancato, and C.-Z. Giam (2003)
Mol. Cell. Biol. 23, 5269-5281
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Expression and Functional Dynamics of the XCAP-D2 Condensin Subunit in Xenopus laevis Oocytes.
E. Watrin, F. Cubizolles, H. B. Osborne, K. Le Guellec, and V. Legagneux (2003)
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   Abstract »    Full Text »    PDF »
Drosophila securin destruction involves a D-box and a KEN-box and promotes anaphase in parallel with Cyclin A degradation.
O. Leismann and C. F. Lehner (2003)
J. Cell Sci. 116, 2453-2460
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Cohesins Determine the Attachment Manner of Kinetochores to Spindle Microtubules at Meiosis I in Fission Yeast.
S. Yokobayashi, M. Yamamoto, and Y. Watanabe (2003)
Mol. Cell. Biol. 23, 3965-3973
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Essential Role of Fkbp6 in Male Fertility and Homologous Chromosome Pairing in Meiosis.
M. A. Crackower, N. K. Kolas, J. Noguchi, R. Sarao, K. Kikuchi, H. Kaneko, E. Kobayashi, Y. Kawai, I. Kozieradzki, R. Landers, et al. (2003)
Science 300, 1291-1295
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The Yeast RSC Chromatin-Remodeling Complex Is Required for Kinetochore Function in Chromosome Segregation.
J.-m. Hsu, J. Huang, P. B. Meluh, and B. C. Laurent (2003)
Mol. Cell. Biol. 23, 3202-3215
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Synergistic inhibition of APC/C by glucose and activated Ras proteins can be mediated by each of the Tpk1-3 proteins in Saccharomyces cerevisiae.
M. Bolte, P. Dieckhoff, C. Krause, G. H. Braus, and S. Irniger (2003)
Microbiology 149, 1205-1216
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