Detrimental incorporation of excess Cenp-A/Cid and Cenp-C into Drosophilacentromeres is prevented by limiting amounts of the bridging factor Cal1

Journal of Cell Science

Volumn 123, Issue 21, 2010, Pages 3768-3779

  Schittenhelm, Ralf B ^a,c   Althoff, Friederike ^a   Heidmann, Stefan ^b   Lehner, Christian F ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c ETH ZURICH   (Switzerland)

Author keywords

Cal1; Centromere; Chromosome instability; Kinetochore; Mitosis

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN C; HISTONE H3; NUCLEAR PROTEIN; PROTEIN CAL1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CENTROMERE; CHROMOSOMAL INSTABILITY; COPY NUMBER VARIATION; DROSOPHILA; GENETIC CODE; GENETIC VARIABILITY; IN VIVO STUDY; INSECT GENETICS; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STOICHIOMETRY; YEAST;

ANIMALS; CELLS, CULTURED; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HISTONES; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; TWO-HYBRID SYSTEM TECHNIQUES; YEASTS;

EUKARYOTA; SACCHAROMYCETALES;

EID: 78149309083     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.067934     Document Type: Article

References (59)

1. Ahmad, K. and Henikoff, S. (2002). Histone H3 variants specify modes of chromatin assembly. Proc. Natl. Acad. Sci. USA 99, 16477-16484.
2. Allshire, R. C. and Karpen, G. H. (2008). Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937.
3. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
4. Blower, M. D., Sullivan, B. A. and Karpen, G. H. (2002). Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2, 319-330.
5. Camahort, R., Shivaraju, M., Mattingly, M., Li, B., Nakanishi, S., Zhu, D., Shilatifard, A., Workman, J. L. and Gerton, J. L. (2009). Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell 35, 794-805.
6. Cheeseman, I. M., Niessen, S., Anderson, S., Hyndman, F., Yates, J. R., 3rd, Oegema, K. and Desai, A. (2004). A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18, 2255-2268. (Pubitemid 39209574)
7. Cohen, R. L., Espelin, C. W., De Wulf, P., Sorger, P. K., Harrison, S. C. and Simons, K. T. (2008). Structural and functional dissection of Mif2p, a conserved DNA-binding kinetochore protein. Mol. Biol. Cell 19, 4480-4491.
8. Collins, K. A., Furuyama, S. and Biggins, S. (2004). Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 14, 1968-1972.
9. Dalal, Y., Wang, H., Lindsay, S. and Henikoff, S. (2007). Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol. 5, e218.
10. Dunleavy, E. M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y. and Almouzni-Pettinotti, G. (2009). HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497.
11. Edgar, B. A. and O'Farrell, P. H. (1989). Genetic control of cell division patterns in the Drosophila embryo. Cell 57, 177-183.
12. Erhardt, S., Mellone, B. G., Betts, C. M., Zhang, W., Karpen, G. H. and Straight, A. F. (2008). Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J. Cell Biol. 183, 805-818.
13. Fitzgerald-Hayes, M., Buhler, J. M., Cooper, T. G. and Carbon, J. (1982). Isolation and subcloning analysis of functional centromere DNA (CEN11) from Saccharomyces cerevisiae chromosome XI. Mol. Cell. Biol. 2, 82-87.
14. Foltz, D. R., Jansen, L. E., Bailey, A. O., Yates, J. R., 3rd, Bassett, E. A., Wood, S., Black, B. E. and Cleveland, D. W. (2009). Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137, 472-484.
15. Fujita, Y., Hayashi, T., Kiyomitsu, T., Toyoda, Y., Kokubu, A., Obuse, C. and Yanagida, M. (2007). Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell 12, 17-30. (Pubitemid 46002597)
16. Furuyama, T. and Henikoff, S. (2009). Centromeric nucleosomes induce positive DNA supercoils. Cell 138, 104-113.
17. Furuyama, T., Dalal, Y. and Henikoff, S. (2006). Chaperone-mediated assembly of centromeric chromatin in vitro. Proc. Natl. Acad. Sci. USA 103, 6172-6177.
18. Gassmann, R., Essex, A., Hu, J. S., Maddox, P. S., Motegi, F., Sugimoto, A., O'Rourke, S. M., Bowerman, B., McLeod, I., Yates, J. R., 3rd et al. (2008). A new mechanism controlling kinetochore-microtubule interactions revealed by comparison of two dynein-targeting components: SPDL-1 and the Rod/Zwilch/Zw10 complex. Genes Dev. 22, 2385-2399.
19. Goshima, G., Wollman, R., Goodwin, S. S., Zhang, N., Scholey, J. M., Vale, R. D. and Stuurman, N. (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421.
20. Hayashi, T., Fujita, Y., Iwasaki, O., Adachi, Y., Takahashi, K. and Yanagida, M. (2004). Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118, 715-729.
21. Heeger, S., Leismann, O., Schittenhelm, R., Schraidt, O., Heidmann, S. and Lehner, C. F. (2005). Genetic inteactions of Separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog. Genes Dev. 19, 2041-2053.
22. Heun, P., Erhardt, S., Blower, M. D., Weiss, S., Skora, A. D. and Karpen, G. H. (2006). Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 10, 303-315.
23. Hori, T., Amano, M., Suzuki, A., Backer, C. B., Welburn, J. P., Dong, Y., McEwen, B. F., Shang, W. H., Suzuki, E., Okawa, K. et al. (2008). CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135, 1039-1052.
24. Jäger, H., Herzig, B., Herzig, A., Sticht, H., Lehner, C. F. and Heidmann, S. (2004). Structure predictions and interaction studies indicate homology of separase N-terminal regulatory domains and Drosophila THR. Cell Cycle 3, 182-188. (Pubitemid 40268695)
25. Jäger, H., Rauch, M. and Heidmann, S. (2005). The Drosophila melanogaster condensin subunit Cap-G interacts with the centromere-specific histone H3 variant CID. Chromosoma 113, 350-361.
26. Jansen, L. E., Black, B. E., Foltz, D. R. and Cleveland, D. W. (2007). Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805.
27. Joglekar, A. P., Bouck, D. C., Molk, J. N., Bloom, K. S. and Salmon, E. D. (2006). Molecular architecture of a kinetochore-microtubule attachment site. Nat. Cell Biol. 8, 581-585.
28. Joglekar, A. P., Bouck, D., Finley, K., Liu, X., Wan, Y., Berman, J., He, X., Salmon, E. D. and Bloom, K. S. (2008). Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J. Cell Biol. 181, 587-594.
29. Lam, A. L., Boivin, C. D., Bonney, C. F., Rudd, M. K. and Sullivan, B. A. (2006). Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc. Natl. Acad. Sci. USA 103, 4186-4191.
30. Maddox, P. S., Hyndman, F., Monen, J., Oegema, K. and Desai, A. (2007). Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176, 757-763.
31. Maiato, H., Hergert, P. J., Moutinho-Pereira, S., Dong, Y., Vandenbeldt, K. J., Rieder, C. L. and McEwen, B. F. (2006). The ultrastructure of the kinetochore and kinetochore fiber in Drosophila somatic cells. Chromosoma 115, 469-480.
32. Meluh, P. B., Yang, P., Glowczewski, L., Koshland, D. and Smith, M. M. (1998). Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94, 607-613.
33. Meraldi, P., McAinsh, A. D., Rheinbay, E. and Sorger, P. K. (2006). Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol. 7, R23.
34. Metaxakis, A., Oehler, S., Klinakis, A. and Savakis, C. (2005). Minos as a genetic and genomic tool in Drosophila melanogaster. Genetics 171, 571-581. (Pubitemid 43156447)
35. Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M. M. and Wu, C. (2007). Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129, 1153-1164.
36. Moreno-Moreno, O., Torras-Llort, M. and Azorin, F. (2006). Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res. 34, 6247-6255.
37. Okada, M., Cheeseman, I. M., Hori, T., Okawa, K., McLeod, I. X., Yates, J. R., 3rd, Desai, A. and Fukagawa, T. (2006). The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8, 446-457.
38. Pandey, R., Heidmann, S. and Lehner, C. F. (2005). Epithelial re-organization and dynamics of progression through mitosis in Drosophila separase complex mutants. J. Cell Sci. 118, 733-742.
39. Parks, A. L., Cook, K. R., Belvin, M., Dompe, N. A., Fawcett, R., Huppert, K., Tan, L. R., Winter, C. G., Bogart, K. P., Deal, J. E. et al. (2004). Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288-292. (Pubitemid 38282755)
40. Perpelescu, M., Nozaki, N., Obuse, C., Yang, H. and Yoda, K. (2009). Active establishment of centromeric CENP-A chromatin by RSF complex. J. Cell Biol. 185, 397-407.
41. Pidoux, A. L., Choi, E. S., Abbott, J. K., Liu, X., Kagansky, A., Castillo, A. G., Hamilton, G. L., Richardson, W., Rappsilber, J., He, X. et al. (2009). Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol. Cell 33, 299-311.
42. Przewloka, M. R., Zhang, W., Costa, P., Archambault, V., D'Avino, P. P., Lilley, K. S., Laue, E. D., McAinsh, A. D. and Glover, D. M. (2007). Molecular analysis of core kinetochore composition and assembly in Drosophila melanogaster. PLoS ONE 2, e478.
43. Santaguida, S. and Musacchio, A. (2009). The life and miracles of kinetochores. EMBO J. 28, 2511-2531.
44. Schittenhelm, R. B., Heeger, S., Althoff, F., Walter, A., Heidmann, S., Mechtler, K. and Lehner, C. F. (2007). Spatial organization of a ubiquitous eukaryotic kinetochore protein network in Drosophila chromosomes. Chromosoma 116, 385-402.
45. Schittenhelm, R. B., Chaleckis, R. and Lehner, C. F. (2009). Essential functional domains and intrakinetochore localization of Drosophila Spc105. EMBO J. 28, 2374-2386.
46. Schuh, M., Lehner, C. F. and Heidmann, S. (2007). Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17, 237-243.
47. Sonnichsen, B., Koski, L. B., Walsh, A., Marschall, P., Neumann, B., Brehm, M., Alleaume, A. M., Artelt, J., Bettencourt, P., Cassin, E. et al. (2005). Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434, 462-469. (Pubitemid 40477050)
48. Sugimoto, K., Kuriyama, K., Shibata, A. and Himeno, M. (1997). Characterization of internal DNA-binding and C-terminal dimerization domains of human centromere/kinetochore autoantigen CENP-C in vitro: role of DNA-binding and self-associating activities in kinetochore organization. Chromosome Res. 5, 132-141.
49. Sun, X., Wahlstrom, J. and Karpen, G. (1997). Molecular structure of a functional Drosophila centromere. Cell 91, 1007-1019. (Pubitemid 28027833)
50. Takahashi, K., Chen, E. S. and Yanagida, M. (2000). Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288, 2215-2219. (Pubitemid 30429607)
51. Talbert, P. B., Bryson, T. D. and Henikoff, S. (2004). Adaptive evolution of centromere proteins in plants and animals. J. Biol. 3, 18.
52. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L. et al. (2004). A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287. (Pubitemid 38282754)
53. Torras-Llort, M., Moreno-Moreno, O. and Azorin, F. (2009). Focus on the centre: the role of chromatin on the regulation of centromere identity and function. EMBO J. 28, 2337-2348.
54. Trazzi, S., Perini, G., Bernardoni, R., Zoli, M., Reese, J. C., Musacchio, A. and Della Valle, G. (2009). The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation. PLoS ONE 4, e5832.
55. Vagnarelli, P., Ribeiro, S. A. and Earnshaw, W. C. (2008). Centromeres: old tales and new tools. FEBS Lett. 582, 1950-1959.
56. Van Hooser, A. A., Ouspenski, II, Gregson, H. C., Starr, D. A., Yen, T. J., Goldberg, M. L., Yokomori, K., Earnshaw, W. C., Sullivan, K. F. and Brinkley, B. R. (2001). Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114, 3529-3542.
57. Williams, J. S., Hayashi, T., Yanagida, M. and Russell, P. (2009). Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol. Cell 33, 287-298.
58. Winey, M., Mamay, C. L., O'Toole, E. T., Mastronarde, D. N., Giddings, T. H., Jr, McDonald, K. L. and McIntosh, J. R. (1995). Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J. Cell Biol. 129, 1601-1615.
59. Yang, C. H., Tomkiel, J., Saitoh, H., Johnson, D. H. and Earnshaw, W. C. (1996). Identification of overlapping DNA-binding and centromere-targeting domains in the human kinetochore protein CENP-C. Mol. Cell. Biol. 16, 3576-3586.