Preimplantation mouse embryos depend on inhibitory phosphorylation of separase to prevent chromosome missegregation

Molecular and Cellular Biology

Volumn 29, Issue 6, 2009, Pages 1498-1505

  Huang, Xingxu ^a   Andreu Vieyra, Claudia V ^b   Wang, Meizhi ^a   Cooney, Austin J ^b   Matzuk, Martin M ^b   Zhang, Pumin ^b  

^a NANJING UNIVERSITY   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SECURIN; SEPARASE; SERINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; EMBRYO DEVELOPMENT; FEMALE; GENE MUTATION; GERM CELL; INFERTILITY; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; BLASTOCYST; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMATIDS; CHROMOSOME SEGREGATION; CHROMOSOMES, MAMMALIAN; ENDOPEPTIDASES; FEMALE; MICE; MUTATION; OOCYTES; PHOSPHORYLATION; PREGNANCY;

MUS; VERTEBRATA;

EID: 62849107373     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01778-08     Document Type: Article

References (38)

1. Cohen-Fix, O., J. M. Peters, M. W. Kirschner, and D. Koshland. 1996. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10:3081-3093.
2. Dej, K. J., and T. L. Orr-Weaver. 2000. Separation anxiety at the centromere. Trends Cell Biol. 10:392-399.
3. Fang, G., H. Yu, and M. W. Kirschner. 1999. Control of mitotic transitions by the anaphase-promoting complex. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 354:1583-1590.
4. Giménez-Abián, J. F., I. Sumara, T. Hirota, S. Hauf, D. Gerlich, C. de la Torre, J. Ellenberg, and J. M. Peters. 2004. Regulation of sister chromatid cohesion between chromosome arms. Curr. Biol. 14:1187-1193.
5. Gorr, I. H., D. Boos, and O. Stemmann. 2005. Mutual inhibition of separase and Cdk1 by two-step complex formation. Mol. Cell 19:135-141.
6. Hassold, T., H. Hall, and P. Hunt. 2007. The origin of human aneuploidy: where we have been, where we are going. Hum. Mol. Genet. 16:R203-R208.
7. Hassold, T., and P. Hunt. 2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2:280-291.
8. Hauf, S., E. Roitinger, B. Koch, C. M. Dittrich, K. Mechtler, and J. M. Peters. 2005. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3:e69.
9. Huang, X., C. V. Andreu-Vieyra, J. P. York, R. Hatcher, T. Lu, M. M. Matzuk, and P. Zhang. 2008. Inhibitory phosphorylation of separase is essential for genome stability and viability of murine embryonic germ cells. PLoS Biol. 6:e15.
10. Huang, X., R. Hatcher, J. P. York, and P. Zhang. 2005. Securin and separase phosphorylation act redundantly to maintain sister chromatid cohesion in mammalian cells. Mol. Biol. Cell 16:4725-4732.
11. Jallepalli, P. V., and C. Lengauer. 2001. Chromosome segregation and cancer: cutting through the mystery. Nat. Rev. Cancer 1:109-117.
12. Kim, K. R., B. H. Park, Y. O. Hong, H. C. Kwon, and S. J. Robboy. 17 October 2008, posting date. The villous stromal constituents of complete hydatidiform mole differ histologically in very early pregnancy from the normally developing placenta. Am. J. Surg. Pathol. [Epub ahead of print.]
13. Kitajima, T. S., T. Sakuno, K. Ishiguro, S. Iemura, T. Natsume, S. A. Kawashima, and Y. Watanabe. 2006. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46-52.
14. Kops, G. J., B. A. Weaver, and D. W. Cleveland. 2005. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5:773-785.
15. Koshland, D. E., and V. Guacci. 2000. Sister chromatid cohesion: the beginning of a long and beautiful relationship. Curr. Opin. Cell Biol. 12:297-301.
16. Kumada, K., R. Yao, T. Kawaguchi, M. Karasawa, Y. Hoshikawa, K. Ichikawa, Y. Sugitani, I. Imoto, J. Inazawa, M. Sugawara, M. Yanagida, and T. Noda. 2006. The selective continued linkage of centromeres from mitosis to interphase in the absence of mammalian separase. J. Cell Biol. 172:835-846.
17. Lan, Z. J., X. Xu, and A. J. Cooney. 2004. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol. Reprod. 71:1469-1474.
18. Li, M., J. P. York, and P. Zhang. 2007. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell. Biol. 27:3481-3488.
19. Losada, A., M. Hirano, and T. Hirano. 2002. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev. 16:3004-3016.
20. Losada, A., M. Hirano, and T. Hirano. 1998. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 12:1986-1997.
21. McGuinness, B. E., T. Hirota, N. R. Kudo, J. M. Peters, and K. Nasmyth. 2005. Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. PLoS Biol. 3:e86.
22. Mei, J., X. Huang, and P. Zhang. 2001. Securin is not required for cellular viability, but is required for normal growth of mouse embryonic fibroblasts. Curr. Biol. 11:1197-1201.
23. Nasmyth, K. 2002. Segregating sister genomes: the molecular biology of chromosome separation. Science 297:559-565.
24. Nasmyth, K., and C. H. Haering. 2005. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 74:595-648.
25. Nasmyth, K., J. M. Peters, and F. Uhlmann. 2000. Splitting the chromosome: cutting the ties that bind sister chromatids. Science 288:1379-1385.
26. Pellestor, F., B. Andreo, F. Arnal, C. Humeau, and J. Demaille. 2002. Mechanisms of non-disjunction in human female meiosis: the co-existence of two modes of malsegregation evidenced by the karyotyping of 1397 in-vitro unfertilized oocytes. Hum. Reprod. 17:2134-2145.
27. Peters, J. M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9:931-943.
28. Riedel, C. G., V. L. Katis, Y. Katou, S. Mori, T. Itoh, W. Helmhart, M. Galova, M. Petronczki, J. Gregan, B. Cetin, I. Mudrak, E. Ogris, K. Mechtler, L. Pelletier, F. Buchholz, K. Shirahige, and K. Nasmyth. 2006. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53-61.
29. Salic, A., J. C. Waters, and T. J. Mitchison. 2004. Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118:567-578.
30. Stemmann, O., H. Zou, S. A. Gerber, S. P. Gygi, and M. W. Kirschner. 2001. Dual inhibition of sister chromatid separation at metaphase. Cell 107:715-726.
31. Sumara, I., E. Vorlaufer, P. T. Stukenberg, O. Kelm, N. Redemann, E. A. Nigg, and J. M. Peters. 2002. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell 9:515-525.
32. Tang, Z., H. Shu, W. Qi, N. A. Mahmood, M. C. Mumby, and H. Yu. 2006. PP2A is required for centromeric localization of SgoI and proper chromosome segregation. Dev. Cell 10:575-585.
33. Uhlmann, F., F. Lottspeich, and K. Nasmyth. 1999. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400:37-42.
34. Uhlmann, F., D. Wernic, M. A. Poupart, E. V. Koonin, and K. Nasmyth. 2000. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103:375-386.
35. Waizenegger, I. C., S. Hauf, A. Meinke, and J. M. Peters. 2000. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399-410.
36. Wirth, K. G., G. Wutz, N. R. Kudo, C. Desdouets, A. Zetterberg, S. Taghybeeglu, J. Seznec, G. M. Ducos, R. Ricci, N. Firnberg, J. M. Peters, and K. Nasmyth. 2006. Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J. Cell Biol. 172:847-860.
37. Wolstenholme, J., and R. R. Angell. 2000. Maternal age and trisomy - a unifying mechanism of formation. Chromosoma 109:435-438.
38. Zhivotovsky, B., and G. Kroemer. 2004. Apoptosis and genomic instability. Nat. Rev. Mol. Cell Biol. 5:752-762.