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.

Published Online January 29, 2004
Science DOI: 10.1126/science.1094220

Reports

Submitted on December 1, 2003
Accepted on January 12, 2004

A Genome-Wide Screen Identifies Genes Required for Centromeric Cohesion

Adele L. Marston 1, Wai-Hong Tham 1, Hiral Shah 1, Angelika Amon 1*

1 Center for Cancer Research, Howard Hughes Medical Institute, Massachusetts Institute of Technology, E17-233, 40 Ames Street, Cambridge, MA 02139, USA.

* To whom correspondence should be addressed. E-mail: angelika{at}mit.edu.

During meiosis, two chromosome segregation phases follow a single round of DNA replication. We identified factors required to establish this specialized cell cycle by examining meiotic chromosome segregation in a collection of yeast strains lacking all non-essential genes. This analysis revealed Sgo1, Chl4 and Iml3 to be important for retaining centromeric cohesin until the onset of anaphase II. Consistent with this role, Sgo1 localizes to centromeric regions but dissociates at the onset of anaphase II. The screen described here provides a comprehensive analysis of the genes required for the meiotic cell cycle and identified three factors important for the stepwise loss of sister-chromatid cohesion.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Protein Phosphatase Type 1-Interacting Protein Ysw1 Is Involved in Proper Septin Organization and Prospore Membrane Formation during Sporulation.
M. Ishihara, Y. Suda, I. Inoue, T. Tanaka, T. Takahashi, X.-D. Gao, Y. Fukui, S. Ihara, A. M. Neiman, and H. Tachikawa (2009)
Eukaryot. Cell 8, 1027-1037
   Abstract »    Full Text »    PDF »
Shugoshin prevents cohesin cleavage by PP2ACdc55-dependent inhibition of separase.
D. Clift, F. Bizzari, and A. L. Marston (2009)
Genes & Dev. 23, 766-780
   Abstract »    Full Text »    PDF »
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 »
The cohesin complex and its roles in chromosome biology.
J.-M. Peters, A. Tedeschi, and J. Schmitz (2008)
Genes & Dev. 22, 3089-3114
   Abstract »    Full Text »    PDF »
LAB-1 antagonizes the Aurora B kinase in C. elegans.
C. E. de Carvalho, S. Zaaijer, S. Smolikov, Y. Gu, J. M. Schumacher, and M. P. Colaiacovo (2008)
Genes & Dev. 22, 2869-2885
   Abstract »    Full Text »    PDF »
Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice.
E. Llano, R. Gomez, C. Gutierrez-Caballero, Y. Herran, M. Sanchez-Martin, L. Vazquez-Quinones, T. Hernandez, E. de Alava, A. Cuadrado, J. L. Barbero, et al. (2008)
Genes & Dev. 22, 2400-2413
   Abstract »    Full Text »    PDF »
Regulators of Cellular Levels of Histone Acetylation in Saccharomyces cerevisiae.
W. Peng, C. Togawa, K. Zhang, and S. K. Kurdistani (2008)
Genetics 179, 277-289
   Abstract »    Full Text »    PDF »
Shugoshin Promotes Sister Kinetochore Biorientation in Saccharomyces cerevisiae.
B. M. Kiburz, A. Amon, and A. L. Marston (2008)
Mol. Biol. Cell 19, 1199-1209
   Abstract »    Full Text »    PDF »
Proteomic Analysis of a Nutritional Shift-up in Saccharomyces cerevisiae Identifies Gvp36 as a BAR-containing Protein Involved in Vesicular Traffic and Nutritional Adaptation.
L. Querin, R. Sanvito, F. Magni, S. Busti, A. Van Dorsselaer, L. Alberghina, and M. Vanoni (2008)
J. Biol. Chem. 283, 4730-4743
   Abstract »    Full Text »    PDF »
Minichromosome Analysis of Chromosome Pairing, Disjunction, and Sister Chromatid Cohesion in Maize.
F. Han, Z. Gao, W. Yu, and J. A. Birchler (2007)
PLANT CELL 19, 3853-3863
   Abstract »    Full Text »    PDF »
Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments.
H. Huang, J. Feng, J. Famulski, J. B. Rattner, S. T. Liu, G. D. Kao, R. Muschel, G. K.T. Chan, and T. J. Yen (2007)
J. Cell Biol. 177, 413-424
   Abstract »    Full Text »    PDF »
Shugoshin 2 Regulates Localization of the Chromosomal Passenger Proteins in Fission Yeast Mitosis.
V. Vanoosthuyse, S. Prykhozhij, and K. G. Hardwick (2007)
Mol. Biol. Cell 18, 1657-1669
   Abstract »    Full Text »    PDF »
Erv14 family cargo receptors are necessary for ER exit during sporulation in Saccharomyces cerevisiae.
H. Nakanishi, Y. Suda, and A. M. Neiman (2007)
J. Cell Sci. 120, 908-916
   Abstract »    Full Text »    PDF »
Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres.
S. A. Kawashima, T. Tsukahara, M. Langegger, S. Hauf, T. S. Kitajima, and Y. Watanabe (2007)
Genes & Dev. 21, 420-435
   Abstract »    Full Text »    PDF »
Genetic interaction screens advance in reverse.
S. Komili and F. P. Roth (2007)
Genes & Dev. 21, 137-142
   Full Text »    PDF »
Reconstruction of the Kinetochore during Meiosis in Fission Yeast Schizosaccharomyces pombe.
A. Hayashi, H. Asakawa, T. Haraguchi, and Y. Hiraoka (2006)
Mol. Biol. Cell 17, 5173-5184
   Abstract »    Full Text »    PDF »
Genomewide Screen Reveals a Wide Regulatory Network for Di/Tripeptide Utilization in Saccharomyces cerevisiae.
H. Cai, S. Kauffman, F. Naider, and J. M. Becker (2006)
Genetics 172, 1459-1476
   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 »
A genome-wide visual screen reveals a role for sphingolipids and ergosterol in cell surface delivery in yeast.
T. J. Proszynski, R. W. Klemm, M. Gravert, P. P. Hsu, Y. Gloor, J. Wagner, K. Kozak, H. Grabner, K. Walzer, M. Bagnat, et al. (2005)
PNAS 102, 17981-17986
   Abstract »    Full Text »    PDF »
Ascospore Formation in the Yeast Saccharomyces cerevisiae.
A. M. Neiman (2005)
Microbiol. Mol. Biol. Rev. 69, 565-584
   Abstract »    Full Text »    PDF »
Silencing Cenp-F weakens centromeric cohesion, prevents chromosome alignment and activates the spindle checkpoint.
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
   Abstract »    Full Text »    PDF »
AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis.
L. Chelysheva, S. Diallo, D. Vezon, G. Gendrot, N. Vrielynck, K. Belcram, N. Rocques, A. Marquez-Lema, A. M. Bhatt, C. Horlow, et al. (2005)
J. Cell Sci. 118, 4621-4632
   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 »
Dynamic molecular linkers of the genome: the first decade of SMC proteins.
A. Losada and T. Hirano (2005)
Genes & Dev. 19, 1269-1287
   Abstract »    Full Text »    PDF »
Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses.
T. Panavas, E. Serviene, J. Brasher, and P. D. Nagy (2005)
PNAS 102, 7326-7331
   Abstract »    Full Text »    PDF »
How might cohesin hold sister chromatids together?.
K. Nasmyth (2005)
Phil Trans R Soc B 360, 483-496
   Abstract »    Full Text »    PDF »
Shugoshin protects cohesin complexes at centromeres.
Y. Watanabe and T. S Kitajima (2005)
Phil Trans R Soc B 360, 515-521
   Abstract »    Full Text »    PDF »
Roles and regulation of the Drosophila centromere cohesion protein MEI-S332 family.
J. Y Lee, A. Hayashi-Hagihara, and T. L Orr-Weaver (2005)
Phil Trans R Soc B 360, 543-552
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Modifying sister chromatid cohesion for meiosis.
Y. Watanabe (2004)
J. Cell Sci. 117, 4017-4023
   Abstract »    Full Text »    PDF »
Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-{alpha}-associated protein Ctf4 is essential for chromatid disjunction during meiosis II.
M. Petronczki, B. Chwalla, M. F. Siomos, S. Yokobayashi, W. Helmhart, A. M. Deutschbauer, R. W. Davis, Y. Watanabe, and K. Nasmyth (2004)
J. Cell Sci. 117, 3547-3559
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

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