Two distinct pathways responsible for the loading of CENP-A to centromeres in the fission yeast cell cycle

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 360, Issue 1455, 2005, Pages 595-607

  Takahashi, Kohta ^a,b   Takayama, Yuko ^a,b   Masuda, Fumie ^a   Kobayashi, Yasuyo ^a   Saitoh, Shigeaki ^a   Tanaka, T ^c   Heriche, J K ^d   Allshire, R ^e  

^a KURUME UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

CENP A histone; Centromere; Chromosome segregation; Fission yeast; GATA factor

Indexed keywords

CHROMOSOME; YEAST;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE;

AMS2 PROTEIN, S POMBE; AUTOANTIGEN; CELL CYCLE PROTEIN; CENTROMERE PROTEIN A; DNA BINDING PROTEIN; HISTONE; MIS6 PROTEIN, S POMBE; NONHISTONE PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; TRANSCRIPTION FACTOR GATA;

BIOLOGICAL MODEL; CELL CYCLE; CENTROMERE; CHROMATIN; CHROMOSOME SEGREGATION; METABOLISM; PHYSIOLOGY; REVIEW; SCHIZOSACCHAROMYCES;

AUTOANTIGENS; CELL CYCLE; CELL CYCLE PROTEINS; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; GATA TRANSCRIPTION FACTORS; HISTONES; MODELS, BIOLOGICAL; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 20544448498     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2004.1614     Document Type: Conference Paper

References (64)

1. Ahmad, K. & Henikoff, S. 2002 The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200.
2. Allshire, R. 2004 Centromere and kinetochore structure and function. In The molecular biology of Schizosaccharomyces pombe ch. 10. pp. 149-169. Berlin: Springer.
3. Amor, D. J. & Choo, K. H. 2002 Neocentromeres: role in human disease, evolution, and centromere study. Am. J. Hum. Genet. 71, 695-714.
4. Amor, D. J., Bentley, K., Ryan, J., Perry, J., Wong, L., Slater, H. & Choo, K. H. 2004 Human centromere repositioning "in progress". Proc. Natl Acad. Sci. USA 101, 6542-6547.
5. Baum, M., Ngan, V. K. & Clarke, L. 1994 The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol. Biol. Cell 5, 747-761.
6. Bernard, P., Maure, J. F., Partridge, J. F., Genier, S., Javerzat, J. P. & Allshire, R. C. 2001 Requirement of heterochromatin for cohesion at centromeres. Science 294, 2539-2542.
7. Black, B. E., Foltz, D. R., Chakravarthy, S., Luger, K., Woods, V. L., Jr & Cleveland, D. W. 2004 Structural determinants for generating centromeric chromatin. Nature 430, 578-582.
8. Blower, M. D. & Karpen, G. H. 2001 The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nature Cell Biol. 3, 730-739.
9. Boyes, J., Omichinski, J., Clark, D., Pikaart, M. & Felsenfeld, G. 1998 Perturbation of nucleosome structure by the erythroid transcription factor GATA-1. J. Mol. Biol. 279, 529-544.
10. Buchwitz, B. J., Ahmad, K., Moore, L. L., Roth, M. B. & Henikoff, S. 1999 A histone-H3-like protein in C. elegans. Nature 401, 547-548.
11. Chen, E. S., Saitoh, S., Yanagida, M. & Takahashi, K. 2003a A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. Mol. Cell 11, 175-187.
12. Chen, E. S., Yanagida, M. & Takahashi, K. 2003b Does a GATA factor make the bed for centromeric nucleosomes? Cell Cycle 2, 277-278.
13. Chikashige, Y., Kinoshita, N., Nakaseko, Y., Matsumoto, T., Murakami, S., Niwa, O. & Yanagida, M. 1989 Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell 57, 739-751.
14. Choo, K. H. 2001 Domain organization at the centromere and neocentromere. Dev. Cell 1, 165-177.
15. Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarnik, M. & Zaret, K. S. 2002 Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9, 279-289.
16. Clarke, L. & Baum, M. P. 1990 Functional analysis of a centromere from fission yeast: a role for centromere-specific repeated DNA sequences. Mol. Cell Biol. 10, 1863-1872.
17. Cleveland, D. W., Mao, Y. & Sullivan, K. F. 2003 Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421.
18. DeLuca, J. G., Howell, B. J., Canman, J. C., Hickey, J. M., Fang, G. & Salmon, E. D. 2003 Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores. Curr. Biol. 13, 2103-2109.
19. Earnshaw, W. C. & Migeon, B. R. 1985 Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92, 290-296.
20. Egel, R. 2004 The molecular biology of Schizosaccharomyces pombe - genetics, genomics and beyond. Berlin: Springer.
21. Ekwall, K., Olsson, T., Turner, B. M., Cranston, G. & Allshire, R. C. 1997 Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell 91, 1021-1032.
22. Goshima, G., Saitoh, S. & Yanagida, M. 1999 Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation. Genes Dev. 13, 1664-1677.
23. Goshima, G., Kiyomitsu, T., Yoda, K. & Yanagida, M. 2003 Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J. Cell Biol. 160, 25-39.
24. Hahnenberger, K. M., Carbon, J. & Clarke, L. 1991 Identification of DNA regions required for mitotic and meiotic functions within the centromere of Schizosaccharomyces pombe chromosome I. Mol. Cell Biol. 11, 2206-2215.
25. Hayashi, T., Fujita, Y., Iwasaki, O., Adachi, Y., Takahashi, K. & Yanagida, M. 2004 Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118, 715-729.
26. Henikoff, S., Ahmad, K. & Malik, H. S. 2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098-1102.
27. Howman, E. V., Fowler, K. J., Newson, A. J., Redward, S., MacDonald, A. C., Kalitsis, P. & Choo, K. H. 2000 Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl Acad. Sci. USA 97, 1148-1153.
28. Karpen, G. H. & Allshire, R. C. 1997 The case for epigenetic effects on centromere identity and function. Trends Genet. 13, 489-496.
29. Krude, T. 1999 Chromatin assembly during DNA replication in somatic cells. Eur. J. Biochem. 263, 1-5.
30. Liu, S. T., Hittle, J. C., Jablonski, S. A., Campbell, M. S., Yoda, K. & Yen, T. J. 2003 Human CENP-I specifies localization of CENP-F, MAD1 and MAD2 to kinetochores and is essential for mitosis. Nature Cell Biol. 5, 341-345.
31. Martin-Lluesma, S., Stucke, V. M. & Nigg, E. A. 2002 Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297, 2267-2270.
32. Matsumoto, S. & Yanagida, M. 1985 Histone gene organization of fission yeast: a common upstream sequence. EMBO J. 4, 3531-3538.
33. Matsumoto, T., Murakami, S., Niwa, O. & Yanagida, M. 1990 Construction and characterization of centric circular and acentric linear chromosomes in fission yeast. Curr. Genet. 18, 323-330.
34. Maundrell, K. 1993 Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123, 127-130.
35. Meluh, P. B., Yang, P., Glowczewski, L., Koshland, D. & Smith, M. M. 1998 Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94, 607-613.
36. Murakami, S., Matsumoto, T., Niwa, O. & Yanagida, M. 1991 Structure of the fission yeast centromere cen3: direct analysis of the reiterated inverted region. Chromosoma. 101, 214-221.
37. Nabeshima, K., Nakagawa, T., Straight, A. F., Murray, A., Chikashige, Y., Yamashita, Y. M., Hiraoka, Y. & Yanagida, M. 1998 Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol. Biol. Cell 9, 3211-3225.
38. Nakaseko, Y., Adachi, Y., Funahashi, S., Niwa, O. & Yanagida, M. 1986 Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 5, 1011-1021.
39. Nakaseko, Y., Kinoshita, N. & Yanagida, M. 1987 A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 15, 4705-4715.
40. Nakayama, J., Xiao, G., Noma, K., Malikzay, A., Bjerling, P., Ekwall, K., Kobayashi, R. & Grewal, S. I. 2003 Alp13, an MRG family protein, is a component of fission yeast Clr6 histone deacetylase required for genomic integrity. EMBO J. 22, 2776-2787.
41. Nishihashi, A., Haraguchi, T., Hiraoka, Y., Ikemura, T., Regnier, V., Dodson, H., Earnshaw, W. C. & Fukagawa, T. 2002 CENP-I is essential for centromere function in vertebrate cells. Dev. Cell 2, 463-476.
42. Niwa, O., Matsumoto, T., Chikashige, Y. & Yanagida, M. 1989 Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere. EMBO J. 8, 3045-3052.
43. Palmer, D. K., O'Day, K., Wener, M. H., Andrews, B. S. & Margolis, R. L. 1987 A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J. Cell Biol. 104, 805-815.
44. Palmer, D. K., O'Day, K., Trong, H. L., Charbonneau, H. & Margolis, R. L. 1991 Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc. Natl Acad. Sci. USA 88, 3734-3738.
45. Partridge, J. F., Borgstrom, B. & Allshire, R. C. 2000 Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 14, 783-791.
46. Pidoux, A. L., Richardson, W. & Allshire, R. C. 2003 Sim4: a novel fission yeast kinetochore protein required for centromeric silencing and chromosome segregation. J. Cell Biol. 161, 295-307.
47. Polizzi, C. & Clarke, L. 1991 The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J. Cell Biol. 112, 191-201.
48. Qian, Y. W. & Lee, E. Y. 1995 Dual retinoblastoma-binding proteins with properties related to a negative regulator of ras in yeast. J. Biol. Chem. 270, 25507-25513.
49. Qian, Y. W., Wang, Y. C., Hollingsworth, R. E., Jr, Jones, D., Ling, N. & Lee, E. Y. 1993 A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 364, 648-652.
50. Saitoh, S., Takahashi, K. & Yanagida, M. 1997 Mis6, a fission yeast inner centromere protein, acts during G1/S and forms specialized chromatin required for equal segregation. Cell 90, 131-143.
51. Scazzocchio, C. 2000 The fungal GATA factors. Curr. Opin. Microbiol. 3, 126-131.
52. Skoufias, D. A., Andreassen, P. R., Lacroix, F. B., Wilson, L. & Margolis, R. L. 2001 Mammalian mad2 and bub1/-bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl Acad. Sci. USA 98, 4492-4497.
53. Smith, M. M. 2002 Centromeres and variant histones: what, where, when and why? Curr. Opin. Cell Biol. 14, 279-285.
54. Steiner, N. C. & Clarke, L. 1994 A novel epigenetic effect can alter centromere function in fission yeast. Cell 79, 865-874.
55. Stoler, S., Keith, K. C., Curnick, K. E. & Fitzgerald-Hayes, M. 1995 A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev. 9, 573-586.
56. Sullivan, B. A. & Willard, H. F. 1998 Stable dicentric X chromosomes with two functional centromeres. Nat. Genet. 20, 227-228.
57. Sullivan, B. A., Blower, M. D. & Karpen, G. H. 2001 Determining centromere identity: cyclical stories and forking paths. Nat. Rev. Genet. 2, 584-596.
58. Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. 2004 Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51-61.
59. Takahashi, K., Murakami, S., Chikashige, Y., Funabiki, H., Niwa, O. & Yanagida, M. 1992 A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol. Biol. Cell 3, 819-835.
60. Takahashi, K., Yamada, H. & Yanagida, M. 1994 Fission yeast minichromosome loss mutants mis cause lethal aneuploidy and replication abnormality. Mol. Biol. Cell 5, 1145-1158.
61. Takahashi, K., Chen, E. S. & Yanagida, M. 2000 Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288, 2215-2219.
62. Verreault, A., Kaufman, P. D., Kobayashi, R. & Stillman, B. 1996 Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87, 95-104.
63. Warburton, P. E., Cooke, C. A., Bourassa, S., Vafa, O., Sullivan, B. A., Stetten, G., Gimelli, G., Warburton, D., Tyler-Smith, C., Sullivan, K. F., Poirier, G. G. & Earnshaw, W. C. 1997 Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 7, 901-904.
64. Watanabe, Y. & Nurse, P. 1999 Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400, 461-464.