An Iml3-Chl4 Heterodimer Links the Core Centromere to Factors Required for Accurate Chromosome Segregation

Cell Reports

Volumn 5, Issue 1, 2013, Pages 29-36

  Hinshaw, Stephen M ^a   Harrison, Stephen C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HETERODIMER; HISTONE H3; PROTEIN CENP C; PROTEIN CENP N; PROTEIN CHL4; PROTEIN IML3; PROTEIN MIF2; PROTEIN SGO1; UNCLASSIFIED DRUG;

ARTICLE; CENTROMERE; CHROMATIN; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CRYSTALLIZATION; FUNGAL STRAIN; MICROTUBULE; NONHUMAN; NUCLEOSOME; PLASMID; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; ULTRACENTRIFUGATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CENTROMERE; CHROMOSOME SEGREGATION; CRYSTALLOGRAPHY, X-RAY; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84885852996     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.08.036     Document Type: Article

References (39)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Bock L.J., Pagliuca C., Kobayashi N., Grove R.A., Oku Y., Shrestha K., Alfieri C., Golfieri C., Oldani A., Dal Maschio M., et al. Cnn1 inhibits the interactions between the KMN complexes of the yeast kinetochore. Nat. Cell Biol. 2012, 14:614-624.
3. Carroll C.W., Silva M.C., Godek K.M., Jansen L.E., Straight A.F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 2009, 11:896-902.
4. Carroll C.W., Milks K.J., Straight A.F. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J.Cell Biol. 2010, 189:1143-1155.
5. Cheeseman I.M., Anderson S., Jwa M., Green E.M., Kang J.S., Yates J.R., Chan C.S., Drubin D.G., Barnes G. Hierarchical assembly ofthe budding yeast kinetochore from multiple subcomplexes. Cell 2002, 111:163-172.
6. Cohen R.L., Espelin C.W., De Wulf P., Sorger P.K., Harrison S.C., Simons K.T. Structural and functional dissection of Mif2p, a conserved DNA-binding kinetochore protein. Mol. Biol. Cell 2008, 19:4480-4491.
7. De Wulf P., McAinsh A.D., Sorger P.K. Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 2003, 17:2902-2921.
8. Fernius J., Hardwick K.G. Bub1 kinase targets Sgo1 to ensure efficient chromosome biorientation in budding yeast mitosis. PLoS Genet. 2007, 3:e213.
9. Fernius J., Marston A.L. Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet. 2009, 5:e1000629.
10. Fernius J., Nerusheva O.O., Galander S., Alves Fde.L., Rappsilber J., Marston A.L. Cohesin-dependent association of scc2/4 with the centromere initiates pericentromeric cohesion establishment. Curr. Biol. 2013, 23:599-606.
11. Ghosh S.K., Sau S., Lahiri S., Lohia A., Sinha P. The Iml3 protein of the budding yeast is required for the prevention of precocious sister chromatid separation in meiosis I and for sister chromatid disjunction in meiosis II. Curr. Genet. 2004, 46:82-91.
12. Ha J.Y., Kim H.K., Kim J., Kim K.H., Oh S.J., Lee H.H., Yoon H.J., Song H.K., Suh S.W. The recombination-associated protein RdgC adopts a novel toroidal architecture for DNA binding. Nucleic Acids Res. 2007, 35:2671-2681.
13. Holm L., Rosenström P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010, 38(Web Server issue):W545-W549.
14. Indjeian V.B., Murray A.W. Budding yeast mitotic chromosomes have an intrinsic bias to biorient on the spindle. Curr. Biol. 2007, 17:1837-1846.
15. Joglekar A.P., Bouck D.C., Molk J.N., Bloom K.S., Salmon E.D. Molecular architecture of a kinetochore-microtubule attachment site. Nat. Cell Biol. 2006, 8:581-585.
16. Katis V.L., Galova M., Rabitsch K.P., Gregan J., Nasmyth K. Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332. Curr. Biol. 2004, 14:560-572.
17. Kawashima S.A., Yamagishi Y., Honda T., Ishiguro K., Watanabe Y. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 2010, 327:172-177.
18. Kiburz B.M., Reynolds D.B., Megee P.C., Marston A.L., Lee B.H., Lee T.I., Levine S.S., Young R.A., Amon A. The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes Dev. 2005, 19:3017-3030.
19. Kiburz B.M., Amon A., Marston A.L. Shugoshin promotes sister kinetochore biorientation in Saccharomyces cerevisiae. Mol. Biol. Cell 2008, 19:1199-1209.
20. Kim J.L., Nikolov D.B., Burley S.K. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 1993, 365:520-527.
21. Kitajima T.S., Kawashima S.A., Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 2004, 427:510-517.
22. Longtine M.S., McKenzie A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
23. Marston A.L., Tham W.H., Shah H., Amon A. A genome-wide screen identifies genes required for centromeric cohesion. Science 2004, 303:1367-1370.
24. McClelland S.E., Borusu S., Amaro A.C., Winter J.R., Belwal M., McAinsh A.D., Meraldi P. The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. EMBO J. 2007, 26:5033-5047.
25. Mellone B.G., Grive K.J., Shteyn V., Bowers S.R., Oderberg I., Karpen G.H. Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet. 2011, 7:e1002068.
26. Ng T.M., Waples W.G., Lavoie B.D., Biggins S. Pericentromeric sister chromatid cohesion promotes kinetochore biorientation. Mol. Biol. Cell 2009, 20:3818-3827.
27. Okada M., Cheeseman I.M., Hori T., Okawa K., McLeod I.X., Yates J.R., Desai A., Fukagawa T. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 2006, 8:446-457.
28. Otwinowski Z., Minor V. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
29. Owen D.J., Vallis Y., Pearse B.M., McMahon H.T., Evans P.R. The structure and function of the beta 2-adaptin appendage domain. EMBO J. 2000, 19:4216-4227.
30. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S.cerevisiae. Cell 1991, 66:1239-1256.
31. Painter J., Merritt E.A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:439-450.
32. Pot I., Measday V., Snydsman B., Cagney G., Fields S., Davis T.N., Muller E.G., Hieter P. Chl4p and iml3p are two new members of the budding yeast outer kinetochore. Mol. Biol. Cell 2003, 14:460-476.
33. Przewloka M.R., Venkei Z., Bolanos-Garcia V.M., Debski J., Dadlez M., Glover D.M. CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 2011, 21:399-405.
34. Schleiffer A., Maier M., Litos G., Lampert F., Hornung P., Mechtler K., Westermann S. CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat. Cell Biol. 2012, 14:604-613.
35. Screpanti E., De Antoni A., Alushin G.M., Petrovic A., Melis T., Nogales E., Musacchio A. Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 2011, 21:391-398.
36. Tanaka T., Fuchs J., Loidl J., Nasmyth K. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat. Cell Biol. 2000, 2:492-499.
37. Vistica J., Dam J., Balbo A., Yikilmaz E., Mariuzza R.A., Rouault T.A., Schuck P. Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem. 2004, 326:234-256.
38. Weber S.A., Gerton J.L., Polancic J.E., DeRisi J.L., Koshland D., Megee P.C. The kinetochore is an enhancer of pericentric cohesin binding. PLoS Biol. 2004, 2:E260.
39. Wu H., Min J., Zeng H., McCloskey D.E., Ikeguchi Y., Loppnau P., Michael A.J., Pegg A.E., Plotnikov A.N. Crystal structure of human spermine synthase: implications of substrate binding and catalytic mechanism. J.Biol. Chem. 2008, 283:16135-16146.