Shugoshin biases chromosomes for biorientation through condensin recruitment to the pericentromere

eLife

Volumn 2014, Issue 3, 2014, Pages

  Verzijlbergen, Kitty F ^a   Nerusheva, Olga O ^a   Kelly, David ^a   Kerr, Alastair ^a   Clift, Dean ^a,c   Alves, Flavia de Lima ^a   Rappsilber, Juri ^a,b   Marston, Adele L ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CONDENSIN; MICROTUBULE PROTEIN; SHUGOSHIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME; CHROMOSOME BIORIENTATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE AMPLIFICATION; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; KINETOCHORE MICROTUBULE; MASS SPECTROMETRY; MICROFLUIDICS; MICROTUBULE ASSEMBLY; MOLECULAR BIOLOGY; NONHUMAN; PERICENTROMERE; POLYMERASE CHAIN REACTION; QUANTITATIVE ASSAY; SEQUENCE ANALYSIS; WESTERN BLOTTING; CELL CYCLE; CENTROMERE; CHROMOSOME SEGREGATION; METABOLISM; PHYSIOLOGY; SACCHAROMYCETALES;

ADENOSINE TRIPHOSPHATASES; CELL CYCLE; CELL CYCLE PROTEINS; CENTROMERE; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; SACCHAROMYCETALES;

EID: 84898739128     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01374     Document Type: Article

References (65)

1. Bachellier-Bassi S, Gadal O, Bourout G, Nehrbass U. 2008. Cell cycle-dependent kinetochore localization of condensin complex in Saccharomyces cerevisiae. Journal of Structural Biology 162:248-259. doi: 10.1016/j.jsb.2008.01.002.
2. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW. 1999. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes & Development 13:532-544. doi: 10.1101/gad.13.5.532.
3. Brito IL, Yu H-G, Amon A. 2010. Condensins promote coorientation of sister chromatids during meiosis I in budding yeast. Genetics 185:55-64. doi: 10.1534/genetics.110.115139.
4. Cho US, Harrison SC. 2012. Ndc10 is a platform for inner kinetochore assembly in budding yeast. Nature Structural & Molecular Biology 19:48-55. doi: 10.1038/nsmb.2178.
5. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K. 2000. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Molecular cell 5:243-254. doi: 10.1016/S1097-2765(00)80420-7.
6. Clift D, Bizzari F, Marston AL. 2009. Shugoshin prevents cohesin cleavage by PP2A(Cdc55)-dependent inhibition of separase. Genes & Development 23:766-780. doi: 10.1101/gad.507509.
7. Clift D, Marston AL. 2011. The role of shugoshin in meiotic chromosome segregation. Cytogenetic and Genome Research 133:234-242. doi: 10.1159/000323793.
8. Cuylen S, Haering CH. 2011. Deciphering condensin action during chromosome segregation. Trends in Cell Biology 21:552-559. doi: 10.1016/j.tcb.2011.06.003.
9. Cuylen S, Metz J, Haering CH. 2011. Condensin structures chromosomal DNA through topological links. Nature Structural & Molecular Biology 18:894-901. doi: 10.1038/nsmb.2087.
10. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F. 2008. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes & Development 22:2215-2227. doi: 10.1101/gad.1675708.
11. Fernius J, Hardwick KG. 2007. Bub1 kinase targets Sgo1 to ensure efficient chromsoome biorientation in budding yeast mitosis. PLOS Genetics 3:e213. doi: 10.1371/journal.pgen.0030213.
12. Fernius J, Marston AL. 2009. Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLOS Genetics 5:e1000629. doi: 10.1371/journal.pgen.1000629.
13. Fernius J, Nerusheva OO, Galander S, Alves Fde L, Rappsilber J, Marston AL. 2013. Cohesin-dependent association of scc2/4 with the centromere initiates pericentromeric cohesion establishment. Current Biology 23:599-606. doi: 10.1016/j.cub.2013.02.022.
14. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL. 2004. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLOS Biology 2:E259. doi: 10.1371/journal.pbio.0020259.
15. Gregan J, Riedel CG, Pidoux AL, Katou Y, Rumpf C, Schleiffer A, Kearsey SE, Shirahige K, Allshire RC, Nasmyth K. 2007. The kinetochore proteins pcs1 and mde4 and heterochromatin are required to prevent merotelic orientation. Current Biology 17:1190-1200. doi: 10.1016/j.cub.2007.06.044.
16. Gutiérrez-Caballero C, Cebollero LR, Pendás AM. 2012. Shugoshins: from protectors of cohesion to versatile adaptors at the centromere. Trends in Genetics 28:351-360. doi: 10.1016/j.tig.2012.03.003.
17. Hauf S, Watanabe Y. 2004. Kinetochore orientation in mitosis and meiosis. Cell 119:317-327. doi: 10.1016/j.cell.2004.10.014.
18. He X, Asthana S, Sorger PK. 2000. Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101:763-775. doi: 10.1016/S0092-8674(00)80888-0.
19. Hirano T. 2012. Condensins: universal organizers of chromosomes with diverse functions. Genes & Development 26:1659-1678. doi: 10.1101/gad.194746.112.
20. Huang H, Feng J, Famulski J, Rattner JB, Liu ST, Kao GD, Muschel R, Chan GK, Yen TJ. 2007. Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. Journal of Cell Biology 177:413-424. doi: 10.1083/jcb.200701122.
21. Huffaker TC, Thomas JH, Botstein D. 1988. Diverse effects of beta-tubulin mutations on microtubule formation and function. Journal of Cell Biology 106:1997-2010. doi: 10.1083/jcb.106.6.1997.
22. Indjeian VB, Murray AW. 2007. Budding yeast mitotic chromosomes have an intrinsic bias to biorient on the spindle. Current Biology 17:1837-1846. doi: 10.1016/j.cub.2007.09.056.
23. Indjeian VB, Stern BM, Murray AW. 2005. The centromeric protein Sgo1 is required to sense lack of tension on mitotic chromosomes. Science 307:130-133. doi: 10.1126/science.1101366.
24. Katis VL, Galova M, Rabitsch KP, Gregan J, Nasmyth K. 2004. Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332. Current Biology 14:560-572. doi: 10.1016/j.cub.2004.03.001.
25. Kawashima SA, Tsukahara T, Langegger M, Hauf S, Kitajima TS, Watanabe Y. 2007. Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes & Development 21:420-435. doi: 10.1101/gad.1497307.
26. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K-I, Watanabe Y. 2010. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172-177. doi: 10.1126/science.1180189.
27. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H. 2010. Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330:235-239. doi: 10.1126/science.1189505.
28. Kiburz BM, Amon A, Marston AL. 2008. Shugoshin promotes sister kinetochore biorientation in Saccharomyces cerevisiae. Molecular Biology of the Cell 19:1199-1209. doi: 10.1091/mbc.E07-06-0584.
29. Kiburz BM, Reynolds DB, Megee PC, Marston AL, Lee BH, Lee TI, Levine SS, Young RA, Amon A. 2005. The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes & Development 19:3017-3030. doi: 10.1101/gad.1373005.
30. Kitajima TS, Kawashima SA, Watanabe Y. 2004. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510-517. doi: 10.1038/nature02312.
31. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y. 2006. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46-52. doi: 10.1038/nature04663.
32. Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963-972. doi: 10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W.
33. Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F. 2004. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430:573-578. doi: 10.1038/nature02742.
34. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589-595. doi: 10.1093/bioinformatics/btp698.
35. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 genome project data processing subgroup. 2009. The Sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. doi: 10.1093/bioinformatics/btp352.
36. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U.
37. Marston AL, Tham WH, Shah H, Amon A. 2004. A genome-wide screen identifies genes required for centromeric cohesion. Science 303:1367-1370. doi: 10.1126/science.1094220.
38. Michaelis C, Ciosk R, Nasmyth K. 1997. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35-45. doi: 10.1016/S0092-8674(01)80007-6.
39. Natsume T, Müller CA, Katou Y, Retkute R, GierliDski M, Araki H, Blow JJ, Shirahige K, Nieduszynski CA, Tanaka TU. 2013. Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. Molecular Cell 50:661-674. doi: 10.1016/j.molcel.2013.05.011.
40. Ng TM, Waples WG, Lavoie BD, Biggins S. 2009. Pericentromeric sister chromatid cohesion promotes kinetochore biorientation. Molecular Biology of the Cell 20:3818-3827. doi: 10.1091/mbc.E09-04-0330.
41. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. 2009. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nature Methods 6:917-922. doi: 10.1038/nmeth.1401.
42. Pinsky BA, Kung C, Shokat KM, Biggins S. 2006. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nature Cell Biology 8:78-83. doi: 10.1038/ncb1341.
43. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. doi: 10.1093/bioinformatics/btq033.
44. Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K. 2004. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Current Biology 14:287-301. doi: 10.1016/j.cub.2004.01.051.
45. Rattani A, Wolna M, Ploquin M, Helmhart W, Morrone S, Mayer B, Godwin J, Xu W, Stemmann O, Pendas A, Nasmyth K. 2013. Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. eLife 2:e01133. doi: 10.7554/eLife.01133.
46. Ribeiro SA, Gatlin JC, Dong Y, Joglekar A, Cameron L, Hudson DF, Farr CJ, McEwen BF, Salmon ED, Earnshaw WC, Vagnarelli P. 2009. Condensin regulates the stiffness of vertebrate centromeres. Molecular Biology of the Cell 20:2371-2380. doi: 10.1091/mbc.E08-11-1127.
47. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K. 2006. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53-61. doi: 10.1038/nature04664.
48. Rivera T, Ghenoiu C, Rodríguez-Corsino M, Mochida S, Funabiki H, Losada A. 2012. Xenopus Shugoshin 2 regulates the spindle assembly pathway mediated by the chromosomal passenger complex. The EMBO Journal 31:1467-1479. doi: 10.1038/emboj.2012.4.
49. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nature Biotechnology 29:24-26. doi: 10.1038/nbt.1754.
50. Sakuno T, Tada K, Watanabe Y. 2009. Kinetochore geometry defined by cohesion within the centromere. Nature 458:852-858. doi: 10.1038/nature07876.
51. Stephens AD, Haase J, Vicci L, Taylor RM, Bloom K. 2011. Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring. Journal of Cell Biology 193:1167-1180. doi: 10.1083/jcb.201103138.
52. Tada K, Susumu H, Sakuno T, Watanabe Y. 2011. Condensin association with histone H2A shapes mitotic chromosomes. Nature 474:477-483. doi: 10.1038/nature10179.
53. Tanaka TU. 2010. Kinetochore-microtubule interactions: steps towards bi-orientation. The EMBO Journal 29:4070-4082. doi: 10.1038/emboj.2010.294.
54. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K. 2002. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108:317-329. doi: 10.1016/S0092-8674(02)00633-5.
55. Tang Z, Shu H, Qi W, Mahmood NA, Mumby MC, Yu H. 2006. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Developmental Cell 10:575-585. doi: 10.1016/j.devcel.2006.03.010.
56. Tsukahara T, Tanno Y, Watanabe Y. 2010. Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 467:719-723. doi: 10.1038/nature09390.
57. Vanoosthuyse V, Prykhozhij S, Hardwick KG. 2007. Shugoshin 2 regulates localization of the chromosomal passenger proteins in fission yeast mitosis. Molecular Biology of the Cell 18:1657-1669. doi: 10.1091/mbc.E06-10-0890.
58. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT, Gorbsky GJ, Higgins JMG. 2010. Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330:231-235. doi: 10.1126/science.1189435.
59. Weber SA, Gerton JL, Polancic JE, DeRisi JL, Koshland D, Megee PC. 2004. The kinetochore is an enhancer of pericentric cohesin binding. PLOS Biology 2:E260. doi: 10.1371/journal.pbio.0020260.
60. Winey M, Mammay CL, O'Toole ET, Mastronarde DN, Giddings TH Jnr, McDonald KL, McIntosh JR. 1995. Three-dimensional ultrastrutural analysis of the Saccharomyces cerevisiae mitotic spindle. Journal of Cell Biology 129:1601-1615. doi: 10.1083/jcb.129.6.1601.
61. Xu Z, Cetin B, Anger M, Cho US, Helmhart W, Nasmyth K, Xu W. 2009. Structure and function of the PP2A-shugoshin interaction. Molecular Cell 35:426-441. doi: 10.1016/j.molcel.2009.06.031.
62. Yamagishi Y, Honda T, Tanno Y, Watanabe Y. 2010. Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330:239-243. doi: 10.1126/science.1194498.
63. Yamagishi Y, Sakuno T, Shimura M, Watanabe Y. 2008. Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251-255. doi: 10.1038/nature07217.
64. Yoon HJ, Carbon J. 1999. Participation of Bir1p, a member of the inhibitor of apoptosis family in yeast chromosome segregation events. Proceedings of the National Academy of Sciences of the United States of America 96:13208-13213. doi: 10.1073/pnas.96.23.13208.
65. Yu HG, Koshland D. 2007. The Aurora kinase Ipl1 maintains the centromeric localization of PP2A to protect cohesin during meiosis. Journal of Cell Biology 176:911-918. doi: 10.1083/jcb.200609153.