Plo1 phosphorylates Dam1 to promote chromosome bi-orientation in fission yeast

Journal of Cell Science

Volumn 125, Issue 7, 2012, Pages 1645-1651

  Buttrick, Graham J ^a   Lancaster, Theresa C ^a   Meadows, John C ^a   Millar, Jonathan B A ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Dam1; Kinetochore; Microtubule; Polo kinase

Indexed keywords

DAM1 PROTEIN; PLO1 PROTEIN; POLO LIKE KINASE; PROTEIN; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CENTROMERE; CHROMOSOME BI ORIENTATION; CONTROLLED STUDY; METAPHASE; MICROBIOLOGICAL PARAMETERS; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CHROMOSOMES; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES;

SACCHAROMYCETALES; SCHIZOSACCHAROMYCETACEAE;

EID: 84863085680     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.096826     Document Type: Article

References (47)

1. Ahonen, L. J., Kallio, M. J., Daum, J. R., Bolton, M., Manke, I. A., Yaffe, M. B., Stukenberg, P. T. and Gorbsky, G. J. (2005). Polo-like kinase 1 creates the tensionsensing 3F3/2 phosphoepitope and modulates the association of spindle-checkpoint proteins at kinetochores. Curr. Biol. 15, 1078-1089.
2. Akiyoshi, B., Sarangapani, K. K., Powers, A. F., Nelson, C. R., Reichow, S. L., Arellano-Santoyo, H., Gonen, T., Ranish, J. A., Asbury, C. L. and Biggins, S. (2010). Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468, 576-579.
3. Alvarez-Tabares, I., Grallert, A., Ortiz, J. M. and Hagan, I. M. (2007). Schizosaccharomyces pombe protein phosphatase 1 in mitosis, endocytosis and a partnership with Wsh3/Tea4 to control polarised growth. J. Cell Sci. 120, 3589-3601.
4. Bahler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P. and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
5. Burrack, L. S., Applen, S. E. and Berman, J. (2011). The requirement for the Dam1 complex is dependent upon the number of kinetochore proteins and microtubules. Curr. Biol. 21, 889-896.
6. Buttrick, G. J. and Millar, J. B. (2011). Ringing the changes: emerging roles for DASH at the kinetochore-microtubule Interface. Chromosome Res. 19, 393-407.
7. Buttrick, G. J., Meadows, J. C., Lancaster, T. C., Vanoosthuyse, V., Shepperd, L. A., Hoe, K. L., Kim, D. U., Park, H. O., Hardwick, K. G. and Millar, J. B. (2011). Nsk1 ensures accurate chromosome segregation by promoting association of kinetochores to spindle poles during anaphase B. Mol. Biol. Cell 22, 4486-4502.
8. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J., Yates, J. R., 3rd, Chan, C. S., Drubin, D. G. and Barnes, G. (2002). Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172.
9. Ding, R., McDonald, K. L. and McIntosh, J. R. (1993). Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120, 141-151.
10. Dou, Z., von Schubert, C., Korner, R., Santamaria, A., Elowe, S. and Nigg, E. A. (2011). Quantitative mass spectrometry analysis reveals similar substrate consensus motif for human mps1 kinase and plk1. PLoS ONE 6, e18793.
11. Elia, A. E., Cantley, L. C. and Yaffe, M. B. (2003a). Proteomic screen finds pSer/pThrbinding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231.
12. Elia, A. E., Rellos, P., Haire, L. F., Chao, J. W., Ivins, F. J., Hoepker, K., Mohammad, D., Cantley, L. C., Smerdon, S. J. and Yaffe, M. B. (2003b). The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115, 83-95.
13. Elowe, S., Hummer, S., Uldschmid, A., Li, X. and Nigg, E. A. (2007). Tensionsensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev. 21, 2205-2219.
14. Franco, A., Meadows, J. C. and Millar, J. B. (2007). The Dam1/DASH complex is required for the retrieval of unclustered kinetochores in fission yeast. J. Cell Sci. 120, 3345-3351.
15. Gachet, Y., Reyes, C., Courtheoux, T., Goldstone, S., Gay, G., Serrurier, C. and Tournier, S. (2008). Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2. Mol. Biol. Cell 19, 1646-1662.
16. Garcia, M. A., Koonrugsa, N. and Toda, T. (2002). Two kinesin-like Kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A. Curr. Biol. 12, 610-621.
17. Gould, K. L., Ren, L., Feoktistova, A. S., Jennings, J. L. and Link, A. J. (2004). Tandem affinity purification and identification of protein complex components. Methods 33, 239-244.
18. Griffiths, K., Masuda, H., Dhut, S. and Toda, T. (2008). Fission yeast dam1-A8 mutant is resistant to and rescued by an anti-microtubule agent. Biochem. Biophys. Res. Commun. 368, 670-676.
19. Grishchuk, E. L. and McIntosh, J. R. (2006). Microtubule depolymerization can drive poleward chromosome motion in fission yeast. EMBO J. 25, 4888-4896.
20. Hauf, S., Biswas, A., Langegger, M., Kawashima, S. A., Tsukahara, T. and Watanabe, Y. (2007). Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I. EMBO J. 26, 4475-4486.
21. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. and Pease, L. R. (1989). Sitedirected mutagenesis by overlap extension using the polymerase chain reaction. Gene [77,] 51-59.
22. Keating, P., Rachidi, N., Tanaka, T. U. and Stark, M. J. (2009). Ipl1-dependent phosphorylation of Dam1 is reduced by tension applied on kinetochores. J. Cell Sci. [122,] 4375-4382.
23. Kinoshita, N., Yamano, H., Niwa, H., Yoshida, T. and Yanagida, M. (1993). Negative regulation of mitosis by the fission yeast protein phosphatase ppa2. Genes Dev. 7, 1059-1071.
24. Lampert, F., Hornung, P. and Westermann, S. (2010). The Dam1 complex confers microtubule plus end-tracking activity to the Ndc80 kinetochore complex. J. Cell Biol. 189, 641-649.
25. Li, Y. and Elledge, S. J. (2003). The DASH complex component Ask1 is a cell cycleregulated Cdk substrate in Saccharomyces cerevisiae. Cell Cycle 2, 143-148.
26. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. and Lens, S. M. (2009). Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353.
27. Liu, X., McLeod, I., Anderson, S., Yates, J. R., 3rd and He, X. (2005). Molecular analysis of kinetochore architecture in fission yeast. EMBO J. 24, 2919-2930.
28. Meadows, J. C., Shepperd, L. A., Vanoosthuyse, V., Lancaster, T. C., Sochaj, A. M., Buttrick, G. J., Hardwick, K. G. and Millar, J. B. (2011). Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev. Cell 20, 739-750.
29. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
30. Nakajima, H., Toyoshima-Morimoto, F., Taniguchi, E. and Nishida, E. (2003). Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J. Biol. Chem. 278, 25277-25280.
31. Ohkura, H., Kinoshita, N., Miyatani, S., Toda, T. and Yanagida, M. (1989). The fission yeast dis2+ gene required for chromosome disjoining encodes one of two putative type 1 protein phosphatases. Cell 57, 997-1007.
32. Papadopoulou, K., Ng, S. S., Ohkura, H., Geymonat, M., Sedgwick, S. G. and McInerny, C. J. (2008). Regulation of gene expression during M-G1-phase in fission yeast through Plo1p and forkhead transcription factors. J. Cell Sci. 121, 38-47.
33. Pinsky, B. A., Kotwaliwale, C. V., Tatsutani, S. Y., Breed, C. A. and Biggins, S. (2006). Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol. Cell. Biol. 26, 2648-2660.
34. Ramey, V. H., Wong, A., Fang, J., Howes, S., Barnes, G. and Nogales, E. (2011). Subunit organization in the Dam1 kinetochore complex and its ring around microtubules. Mol. Biol. Cell 22, 4332-4342.
35. Sanchez-Perez, I., Renwick, S. J., Crawley, K., Karig, I., Buck, V., Meadows, J. C., Franco-Sanchez, A., Fleig, U., Toda, T. and Millar, J. B. (2005). The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J. 24, 2931-2943.
36. Shimogawa, M. M., Graczyk, B., Gardner, M. K., Francis, S. E., White, E. A., Ess, M., Molk, J. N., Ruse, C., Niessen, S., Yates, J. R., 3rd et al. (2006). Mps1 phosphorylation of Dam1 couples kinetochores to microtubule plus ends at metaphase. Curr. Biol. 16, 1489-1501.
37. Thakur, J. and Sanyal, K. (2011). The essentiality of the fungal specific Dam1 complex is correlated with one kinetochore one microtubule interaction present throughout the cell cycle, independent of the nature of a centromere. Eukaryot. Cell [10,] 1295-1305.
38. Tien, J. F., Umbreit, N. T., Gestaut, D. R., Franck, A. D., Cooper, J., Wordeman, L., Gonen, T., Asbury, C. L. and Davis, T. N. (2010). Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J. Cell Biol. 189, 713-723.
39. Vanoosthuyse, V. and Hardwick, K. G. (2009). A novel protein phosphatase 1- dependent spindle checkpoint silencing mechanism. Curr. Biol. 19, 1176-1181.
40. Vanoosthuyse, V., Prykhozhij, S. and Hardwick, K. G. (2007). Shugoshin 2 regulates localization of the chromosomal passenger proteins in fission yeast mitosis. Mol. Biol. Cell 18, 1657-1669.
41. Welburn, J. P., Vleugel, M., Liu, D., Yates, J. R., 3rd, Lampson, M. A., Fukagawa, T. and Cheeseman, I. M. (2010). Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell 38, 383-392
42. West, R. R., Malmstrom, T., Troxell, C. L. and McIntosh, J. R. (2001). Two related kinesins, klp5+ and klp6+, foster microtubule disassembly and are required for meiosis in fission yeast. Mol. Biol. Cell 12, 3919-3932.
43. Westermann, S., Avila-Sakar, A., Wang, H. W., Niederstrasser, H., Wong, J., Drubin, D. G., Nogales, E. and Barnes, G. (2005). Formation of a dynamic kinetochore- microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17, 277-290.
44. Wilson-Grady, J. T., Villen, J. and Gygi, S. P. (2008). Phosphoproteome analysis of fission yeast. J. Proteome Res. 7, 1088-1097.
45. Wong, O. K. and Fang, G. (2006). Loading of the 3F3/2 antigen onto kinetochores is dependent on the ordered assembly of the spindle checkpoint proteins. Mol. Biol. Cell [17,] 4390-4399.
46. Wong, O. K. and Fang, G. (2007). Cdk1 phosphorylation of BubR1 controls spindle checkpoint arrest and Plk1-mediated formation of the 3F3/2 epitope. J. Cell Biol. 179, 611-617.
47. Wurzenberger, C. and Gerlich, D. W. (2011). Phosphatases: providing safe passage through mitotic exit. Nat. Rev. Mol. Cell Biol. 12, 469-482.