Regulation of sororin by cdk1-mediated phosphorylation

Journal of Cell Science

Volumn 124, Issue 17, 2011, Pages 2976-2987

  Dreier, Megan R ^a   Bekier, Michael E ^a   Taylor, William R ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

Aneuploid; Cell cycle; Cohesion; Sister chromatids; Spindle assembly checkpoint

Indexed keywords

AURORA A KINASE; COHESIN; CYCLIN DEPENDENT KINASE 1; N [4 [6 METHOXY 7 (3 MORPHOLINOPROPOXY) 4 QUINAZOLINYLAMINO]PHENYL]BENZAMIDE; PROTEIN; PROTEIN SORORIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CHROMATIN; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOSIS; MITOSIS SPINDLE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SISTER CHROMATID;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; HELA CELLS; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; MITOSIS; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; SISTER CHROMATID EXCHANGE; TRANSFECTION;

EID: 80053954585     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.085431     Document Type: Article

References (41)

1. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J. and Gygi, S. P. (2006). A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292.
2. Cantin, G. T., Yi, W., Lu, B., Park, S. K., Xu, T., Lee, J. D. and Yates, J. R., 3rd (2008). Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 7, 1346-1351.
3. Chen, R. Q., Yang, Q. K., Lu, B. W., Yi, W., Cantin, G., Chen, Y. L., Fearns, C., Yates, J. R., 3rd and Lee, J. D. (2009). CDC25B mediates rapamycin-induced oncogenic responses in cancer cells. Cancer Res. 69, 2663-2668.
4. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J. and Gygi, S. P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
5. Diaz-Martinez, L. A., Gimenez-Abian, J. F. and Clarke, D. J. (2007). Regulation of centromeric cohesion by sororin independently of the APC/C. Cell Cycle 6, 714-724.
6. Dreier, M. R., Grabovich, A. Z., Katusin, J. D. and Taylor, W. R. (2009). Short and long-term tumor cell responses to Aurora kinase inhibitors. Exp. Cell Res. 315, 1085-1099.
7. Gandhi, R., Gillespie, P. J. and Hirano, T. (2006). Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr. Biol. 16, 2406-2417.
8. Gnad, F., Ren, S., Cox, J., Olsen, J. V., Macek, B., Oroshi, M. and Mann, M. (2007). PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol. 8, R250.
9. Guacci, V., Koshland, D. and Strunnikov, A. (1997). A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91, 47-57.
10. Haering, C. H., Lowe, J., Hochwagen, A. and Nasmyth, K. (2002). Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773-788.
11. Haering, C. H., Farcas, A. M., Arumugam, P., Metson, J. and Nasmyth, K. (2008). The cohesin ring concatenates sister DNA molecules. Nature 454, 297-301.
12. Hauf, S., Roitinger, E., Koch, B., Dittrich, C. M., Mechtler, K. and Peters, J. M. (2005). Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3, e69.
13. Huang, H. C., Shi, J., Orth, J. D. and Mitchison, T. J. (2009). Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell 16, 347-358.
14. Jin, P., Hardy, S. and Morgan, D. O. (1998). Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J. Cell Biol. 141, 875-885.
15. Kaur, H., Bekier, M. E. and Taylor, W. R. (2010). Regulation of Borealin by phosphorylation at serine 219. J. Cell. Biochem. 111, 1291-1298.
16. Kitajima, T. S., Sakuno, T., Ishiguro, K., Iemura, S., Natsume, T., Kawashima, S. A. and Watanabe, Y. (2006). Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441, 46-52.
17. Klein, U. R., Nigg, E. A. and Gruneberg, U. (2006). Centromere targeting of the chromosomal passenger complex requires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol. Biol. Cell 17, 2547-2558.
18. Lafont, A. L., Song, J. and Rankin, S. (2010). Sororin cooperates with the acetyltransferase Eco2 to ensure DNA replication-dependent sister chromatid cohesion. Proc. Natl. Acad. Sci. USA 107, 20364-20369.
19. Maresca, T. J. and Salmon, E. D. (2010). Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J. Cell Sci. 123, 825-835.
20. Michaelis, C., Ciosk, R. and Nasmyth, K. (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
21. Nakajima, M., Kumada, K., Hatakeyama, K., Noda, T., Peters, J. M. and Hirota, T. (2007). The complete removal of cohesin from chromosome arms depends on separase. J. Cell Sci. 120, 4188-4196.
22. Nezi, L. and Musacchio, A. (2009). Sister chromatid tension and the spindle assembly checkpoint. Curr. Opin. Cell Biol. 21, 785-795.
23. Nishiyama, T., Ladurner, R., Schmitz, J., Kreidl, E., Schleiffer, A., Bhaskara, V., Bando, M., Shirahige, K., Hyman, A. A., Mechtler, K. et al. (2010). Sororin mediates sister chromatid cohesion by antagonizing wapl. Cell 143, 737-749.
24. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006). Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648.
25. Onn, I., Heidinger-Pauli, J. M., Guacci, V., Unal, E. and Koshland, D. E. (2008). Sister chromatid cohesion: a simple concept with a complex reality. Annu. Rev. Cell Dev. Biol. 24, 105-129.
26. Panizza, S., Tanaka, T., Hochwagen, A., Eisenhaber, F. and Nasmyth, K. (2000). Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr. Biol. 10, 1557-1564.
27. Rankin, S., Ayad, N. G. and Kirschner, M. W. (2005). Sororin, a substrate of the anaphase-promoting complex, is required for sister chromatid cohesion in vertebrates. Mol. Cell 18, 185-200.
28. Schmitz, J., Watrin, E., Lenart, P., Mechtler, K. and Peters, J. M. (2007). Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr. Biol. 17, 630-636.
29. Schvartzman, J. M., Sotillo, R. and Benezra, R. (2010). Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat. Rev. Cancer 10, 102-115.
30. Shintomi, K. and Hirano, T. (2009). Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev. 23, 2224-2236.
31. Skibbens, R. V. (2009). Establishment of sister chromatid cohesion. Curr. Biol. 19, R1126-R1132.
32. Sonoda, E., Matsusaka, T., Morrison, C., Vagnarelli, P., Hoshi, O., Ushiki, T., Nojima, K., Fukagawa, T., Waizenegger, I. C., Peters, J. M. et al. (2001). Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev. Cell 1, 759-770.
33. Sumara, I., Vorlaufer, E., Gieffers, C., Peters, B. H. and Peters, J. M. (2000). Characterization of vertebrate cohesin complexes and their regulation in prophase. J. Cell Biol. 151, 749-762.
34. Sumara, I., Vorlaufer, E., Stukenberg, P. T., Kelm, O., Redemann, N., Nigg, E. A. and Peters, J. M. (2002). The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell 9, 515-525.
35. Taylor, W. R., DePrimo, S. E., Agarwal, A., Agarwal, M. L., Schonthal, A. H., Katula, K. S. and Stark, G. R. (1999). Mechanisms of G2 arrest in response to overexpression of p53. Mol. Biol. Cell 10, 3607-3622.
36. Tiwari, R. K., Kusari, J. and Sen, G. C. (1987). Functional equivalents of interferon-mediated signals needed for induction of an mRNA can be generated by double-stranded RNA and growth factors. EMBO J. 6, 3373-3378.
37. Ubersax, J. A., Woodbury, E. L., Quang, P. N., Paraz, M., Blethrow, J. D., Shah, K., Shokat, K. M. and Morgan, D. O. (2003). Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864.
38. Uhlmann, F. (2004). The mechanism of sister chromatid cohesion. Exp. Cell Res. 296, 80-85.
39. Van Hoof, D., Munoz, J., Braam, S. R., Pinkse, M. W., Linding, R., Heck, A. J., Mummery, C. L. and Krijgsveld, J. (2009). Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5, 214-226.
40. Waizenegger, I. C., Hauf, S., Meinke, A. and Peters, J. M. (2000). Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103, 399-410.
41. Wang, L. H., Mayer, B., Stemmann, O. and Nigg, E. A. (2010). Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J. Cell Sci. 123, 806-813.