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.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 14 July 2000:
Vol. 289. no. 5477, pp. 300 - 303
DOI: 10.1126/science.289.5477.300
Prev | Table of Contents | Next

Reports

Requirement of the Spindle Checkpoint for Proper Chromosome Segregation in Budding Yeast Meiosis

Marion A. Shonn, 1* Robert McCarroll, 2 Andrew W. Murray 13*dagger

The spindle checkpoint was characterized in meiosis of budding yeast. In the absence of the checkpoint, the frequency of meiosis I missegregation increased with increasing chromosome length, reaching 19% for the longest chromosome. Meiosis I nondisjunction in spindle checkpoint mutants could be prevented by delaying the onset of anaphase. In a recombination-defective mutant (spo11Delta ), the checkpoint delays the biochemical events of anaphase I, suggesting that chromosomes that are attached to microtubules but are not under tension can activate the spindle checkpoint. Spindle checkpoint mutants reduce the accuracy of chromosome segregation in meiosis I much more than that in meiosis II, suggesting that checkpoint defects may contribute to Down syndrome.

1 Department of Biochemistry and
3 Department of Physiology, University of California, San Francisco, CA 94143-0444, USA.
2 Cereon Genomics, LLC, 45 Sidney Street, Cambridge, MA 02139, USA.
*   Present address: Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.

dagger    To whom correspondence should be addressed. E-mail: amurray{at}mcb.harvard.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Multiple Roles of Cohesin in Meiotic Chromosome Morphogenesis and Pairing.
G. A. Brar, A. Hochwagen, L.-s. S. Ee, and A. Amon (2009)
Mol. Biol. Cell 20, 1030-1047
   Abstract »    Full Text »    PDF »
Pds1p Is Required for Meiotic Recombination and Prophase I Progression in Saccharomyces cerevisiae.
K. F. Cooper, M. J. Mallory, V. Guacci, K. Lowe, and R. Strich (2009)
Genetics 181, 65-79
   Abstract »    Full Text »    PDF »
Spindle checkpoint activation at meiosis I advances anaphase II onset via meiosis-specific APC/C regulation.
A. Yamamoto, K. Kitamura, D. Hihara, Y. Hirose, S. Katsuyama, and Y. Hiraoka (2008)
J. Cell Biol. 182, 277-288
   Abstract »    Full Text »    PDF »
Components of the Spindle Assembly Checkpoint Regulate the Anaphase-Promoting Complex During Meiosis in Caenorhabditis elegans.
K. K. Stein, E. S. Davis, T. Hays, and A. Golden (2007)
Genetics 175, 107-123
   Abstract »    Full Text »    PDF »
SSP2 and OSW1, Two Sporulation-Specific Genes Involved in Spore Morphogenesis in Saccharomyces cerevisiae.
J. Li, S. Agarwal, and G. S. Roeder (2007)
Genetics 175, 143-154
   Abstract »    Full Text »    PDF »
Dual Role of the Cdc7-regulatory Protein Dbf4 during Yeast Meiosis.
G. Valentin, E. Schwob, and F. D. Seta (2006)
J. Biol. Chem. 281, 2828-2834
   Abstract »    Full Text »    PDF »
Diverse Functions of Spindle Assembly Checkpoint Genes in Saccharomyces cerevisiae.
J. A. Daniel, B. E. Keyes, Y. P. Y. Ng, C. O. Freeman, and D. J. Burke (2006)
Genetics 172, 53-65
   Abstract »    Full Text »    PDF »
The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I.
B. M. Kiburz, D. B. Reynolds, P. C. Megee, A. L. Marston, B. H. Lee, T. I. Lee, S. S. Levine, R. A. Young, and A. Amon (2005)
Genes & Dev. 19, 3017-3030
   Abstract »    Full Text »    PDF »
Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes.
H. A Homer, A. McDougall, M. Levasseur, A. P Murdoch, and M. Herbert (2005)
Reproduction 130, 829-843
   Abstract »    Full Text »    PDF »
Novel Response to Microtubule Perturbation in Meiosis.
A. Hochwagen, G. Wrobel, M. Cartron, P. Demougin, C. Niederhauser-Wiederkehr, M. G. Boselli, M. Primig, and A. Amon (2005)
Mol. Cell. Biol. 25, 4767-4781
   Abstract »    Full Text »    PDF »
RNA interference in meiosis I human oocytes: towards an understanding of human aneuploidy.
H. A. Homer, A. McDougall, M. Levasseur, A. P. Murdoch, and M. Herbert (2005)
Mol. Hum. Reprod. 11, 397-404
   Abstract »    Full Text »    PDF »
From The Cover: Evaluating putative mechanisms of the mitotic spindle checkpoint.
A. Doncic, E. Ben-Jacob, and N. Barkai (2005)
PNAS 102, 6332-6337
   Abstract »    Full Text »    PDF »
Chromosomal instability and human cancer.
F. Michor (2005)
Phil Trans R Soc B 360, 631-635
   Abstract »    Full Text »    PDF »
Three-dimensional Ultrastructure of Saccharomyces cerevisiae Meiotic Spindles.
M. Winey, G. P. Morgan, P. D. Straight, T. H. Giddings Jr., and D. N. Mastronarde (2005)
Mol. Biol. Cell 16, 1178-1188
   Abstract »    Full Text »    PDF »
Reduced Expression of MAD2, BCL2, and MAP Kinase Activity in Pig Oocytes after In Vitro Aging Are Associated with Defects in Sister Chromatid Segregation During Meiosis II and Embryo Fragmentation After Activation.
W. Ma, D. Zhang, Y. Hou, Y.-H. Li, Q.-Y. Sun, X.-F. Sun, and W.-H. Wang (2005)
Biol Reprod 72, 373-383
   Abstract »    Full Text »    PDF »
Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes.
H. A. Homer, A. McDougall, M. Levasseur, K. Yallop, A. P. Murdoch, and M. Herbert (2005)
Genes & Dev. 19, 202-207
   Abstract »    Full Text »    PDF »
A role for centromere pairing in meiotic chromosome segregation.
B. Kemp, R. M. Boumil, M. N. Stewart, and D. S. Dawson (2004)
Genes & Dev. 18, 1946-1951
   Abstract »    Full Text »    PDF »
Cyclin B-Cdk Activity Stimulates Meiotic Rereplication in Budding Yeast.
R. Strich, M. J. Mallory, M. Jarnik, and K. F. Cooper (2004)
Genetics 167, 1621-1628
   Abstract »    Full Text »    PDF »
Germ cell aneuploidy in zebrafish with mutations in the mitotic checkpoint gene mps1.
K. D. Poss, A. Nechiporuk, K. F. Stringer, C. Lee, and M. T. Keating (2004)
Genes & Dev. 18, 1527-1532
   Abstract »    Full Text »    PDF »
The Signal from the Initiation of Meiotic Recombination to the First Division of Meiosis.
R. E. Malone, S. J. Haring, K. E. Foreman, M. L. Pansegrau, S. M. Smith, D. R. Houdek, L. Carpp, B. Shah, and K. E. Lee (2004)
Eukaryot. Cell 3, 598-609
   Abstract »    Full Text »    PDF »
Spindle checkpoint proteins and chromosome-microtubule attachment in budding yeast.
E. S. Gillett, C. W. Espelin, and P. K. Sorger (2004)
J. Cell Biol. 164, 535-546
   Abstract »    Full Text »    PDF »
Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization.
K. T. Jones (2004)
Mol. Hum. Reprod. 10, 1-5
   Abstract »    Full Text »    PDF »
Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division.
A. Storlazzi, S. Tesse, S. Gargano, F. James, N. Kleckner, and D. Zickler (2003)
Genes & Dev. 17, 2675-2687
   Abstract »    Full Text »    PDF »
Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis.
T. Voet, B. Liebe, C. Labaere, P. Marynen, and H. Scherthan (2003)
J. Cell Biol. 162, 795-808
   Abstract »    Full Text »    PDF »
Chromosome Choreography: The Meiotic Ballet.
S. L. Page and R. S. Hawley (2003)
Science 301, 785-789
   Abstract »    Full Text »    PDF »
Depletion of H2A-H2B Dimers in Saccharomyces cerevisiae Triggers Meiotic Arrest by Reducing IME1 Expression and Activating the BUB2-Dependent Branch of the Spindle Checkpoint.
S. E. Hanlon, D. N. Norris, and A. K. Vershon (2003)
Genetics 164, 1333-1344
   Abstract »    Full Text »    PDF »
Nonrandom Homolog Segregation at Meiosis I in Schizosaccharomyces pombe Mutants Lacking Recombination.
L. Davis and G. R. Smith (2003)
Genetics 163, 857-874
   Abstract »    Full Text »    PDF »
Attachment and tension in the spindle assembly checkpoint.
J. Zhou, J. Yao, and H. C. Joshi (2002)
J. Cell Sci. 115, 3547-3555
   Abstract »    Full Text »    PDF »
Spo13 protects meiotic cohesin at centromeres in meiosis I.
M. A. Shonn, R. McCarroll, and A. W. Murray (2002)
Genes & Dev. 16, 1659-1671
   Abstract »    Full Text »    PDF »
Fission Yeast Mad3p Is Required for Mad2p To Inhibit the Anaphase-Promoting Complex and Localizes to Kinetochores in a Bub1p-, Bub3p-, and Mph1p-Dependent Manner.
D. N. Millband and K. G. Hardwick (2002)
Mol. Cell. Biol. 22, 2728-2742
   Abstract »    Full Text »    PDF »
Saccharomycescerevisiae C-Type Cyclin Ume3p/Srb11p Is Required for Efficient Induction and Execution of Meiotic Development.
K. F. Cooper and R. Strich (2002)
Eukaryot. Cell 1, 66-74
   Abstract »    Full Text »    PDF »
Functional Interactions Between SPO11 and REC102 During Initiation of Meiotic Recombination in Saccharomyces cerevisiae.
K. Kee and S. Keeney (2002)
Genetics 160, 111-122
   Abstract »    Full Text »    PDF »
The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint.
S. Biggins and A. W. Murray (2001)
Genes & Dev. 15, 3118-3129
   Abstract »    Full Text »    PDF »
Interspecies conservation of gene order and intron-exon structure in a genomic locus of high gene density and complexity in Plasmodium.
L. H. M. van Lin, T. Pace, C. J. Janse, C. Birago, J. Ramesar, L. Picci, M. Ponzi, and A. P. Waters (2001)
Nucleic Acids Res. 29, 2059-2068
   Abstract »    Full Text »    PDF »
Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints.
D. A. Skoufias, P. R. Andreassen, F. B. Lacroix, L. Wilson, and R. L. Margolis (2001)
PNAS
   Abstract »    Full Text »
Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential.
R. B. Nicklas, J. C. Waters, E. D. Salmon, and S. C. Ward (2001)
J. Cell Sci. 114, 4173-4183
   Abstract »    Full Text »    PDF »
Live observation of fission yeast meiosis in recombination-deficient mutants: a study on achiasmate chromosome segregation.
M. Molnar, J. Bahler, J. Kohli, and Y. Hiraoka (2001)
J. Cell Sci. 114, 2843-2853
   Abstract »    Full Text »    PDF »
Association between spindle assembly checkpoint expression and maternal age in human oocytes.
N. Steuerwald, J. Cohen, R. J. Herrera, M. Sandalinas, and C. A. Brenner (2001)
Mol. Hum. Reprod. 7, 49-55
   Abstract »    Full Text »    PDF »
Metaphase to Anaphase (mat) Transition-defective Mutants in Caenorhabditis elegans.
A. Golden, P. L. Sadler, M. R. Wallenfang, J. M. Schumacher, D. R. Hamill, G. Bates, B. Bowerman, G. Seydoux, and D. C. Shakes (2000)
J. Cell Biol. 151, 1469-1482
   Abstract »    Full Text »    PDF »
Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast.
K. F. Cooper, M. J. Mallory, D. B. Egeland, M. Jarnik, and R. Strich (2000)
PNAS
   Abstract »    Full Text »
Mps1p Regulates Meiotic Spindle Pole Body Duplication in Addition to Having Novel Roles during Sporulation.
P. D. Straight, T. H. Giddings Jr., and M. Winey (2000)
Mol. Biol. Cell 11, 3525-3537
   Abstract »    Full Text »
Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints.
D. A. Skoufias, P. R. Andreassen, F. B. Lacroix, L. Wilson, and R. L. Margolis (2001)
PNAS 98, 4492-4497
   Abstract »    Full Text »    PDF »
Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast.
K. F. Cooper, M. J. Mallory, D. B. Egeland, M. Jarnik, and R. Strich (2000)
PNAS 97, 14548-14553
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

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