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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Potential role of the histone chaperone, CAF-1, in transcription

  • Published : 2009.04.30
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Abstract

The eukaryotic genome forms a chromatin structure that contains repeating nucleosome structures. Nucleosome packaging is regulated by chromatin remodeling factors such as histone chaperones. The Saccharomyces cerevisiae H3/H4 histone chaperones, CAF-1 and Asf1, regulate DNA replication and chromatin assembly. CAF-1 function is largely restricted to non-transcriptional processes in heterochromatin, whereas Asf1 regulates transcription together with another H3/H4 chaperone, HIR. This study examined the role of the yeast H3/H4 histone chaperones, Asf1, HIR, and CAF-1 in chromatin dynamics during transcription. Unexpectedly, CAF-1 was recruited to the actively transcribed region in a similar way to HIR and Asf1. In addition, the three histone chaperones genetically interacted with Set2-dependent H3 K36 methylation. Similar to histone chaperones, Set2 was required for tolerance to excess histone H3 but not to excess H2A, suggesting that CAF-1, Asf1, HIR, and Set2 function in a related pathway and target chromatin during transcription.

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References

  1. Luger, K., Mader, A. W., Richmond, R., Sargent, D. F. and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 https://doi.org/10.1038/38444
  2. Adams, C. R. and Kamakaka, R. T. (1999). Chromatin assembly: biochemical identities and genetic redundancy. Curr. Opi. Genet. Dev. 9, 185-190 https://doi.org/10.1016/S0959-437X(99)80028-8
  3. Mellor, J. (2006) Dynamic nucleosomes and gene transcription. Trends Genet. 22, 320-329 https://doi.org/10.1016/j.tig.2006.03.008
  4. Workman, J. L. (2006) Nucleosome displacement in transcription. Genes Dev. 20, 2009-2017 https://doi.org/10.1101/gad.1435706
  5. Smith, S.M. and Stillman, B. (1989) Purification and characterization of DAF-1 a human cell facor required for chromatin assembly during DNA replication in vitro. Cell 58, 15-25 https://doi.org/10.1016/0092-8674(89)90398-X
  6. Green, E. M., Antczak, A. J., Bailey, A. O., Franco, A. A., Wu, K. J., Yates, J. R. and Kaufman, P. D. (2005) Replicationindependent histone deposition by the HIR complex and Asf1. Curr. Biol. 15, 2044-2049 https://doi.org/10.1016/j.cub.2005.10.053
  7. Prochasson, P., Florens, L., Swanson, S. K., Washburn, M. P. and Workman, J. L. (2005) The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 19, 2534-2439 https://doi.org/10.1101/gad.1341105
  8. Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y. (2004) Histone H3.1 and H3.3 complex mediate nucleosome assembly pathway dependent or independent of DNA synthesis. Cell 116, 51-61 https://doi.org/10.1016/S0092-8674(03)01064-X
  9. Sharp, J. A., Fouts, E. T., Krawitz, D. C. and Kaufman, P. D. (2001) Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11, 463-473 https://doi.org/10.1016/S0960-9822(01)00140-3
  10. Formosa, T., Ruone, S., Adams, M. D., Osen, A. E., Eriksson, P., Yu, Y., Rhoades, A. R., Kaufman, P. D. and Stillman, D.J. (2002) Defects in SPT16 or POB3(yFACT) in saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162, 1557-1571
  11. Adkins, M. W. and Tyler, J. K. (2004) The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J. Biol. Chem. 279, 52069-52074 https://doi.org/10.1074/jbc.M406113200
  12. Korber, P., Barbaric, S., Luckenbach, T., Schmid, A., Schermer, U. J., Blaschke, D. and Horz, W. (2006) The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J. Biol. Chem. 281, 5539-5545 https://doi.org/10.1074/jbc.M513340200
  13. Kim, H. J., Seol, J. H., Han, J. W., Youn, H. D. and Cho, E. J. (2007) Histone chaperones regulate histone exchange during transcription. EMBO J. 26, 4467-4474 https://doi.org/10.1038/sj.emboj.7601870
  14. Nourani, A., Robert, F. and Winston, F. (2006) Evidence that Spt2/Sin1, an HMG-like factor, plays roles in transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol. Cell Biol. 26, 1496-1509 https://doi.org/10.1128/MCB.26.4.1496-1509.2006
  15. Schwabish, M. A. and Struhl, K. (2004) Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell Biol. 24, 10111-10117 https://doi.org/10.1128/MCB.24.23.10111-10117.2004
  16. Kaplan, C. D., Holland, M. J. and Winston, F. (2005) Interaction between transcription elongation factors and mRNA 3'-end formation at the Saccharomyces cerevisiae GAL10-GAL7 Locus. J. Biol. Chem. 280, 913-922 https://doi.org/10.1074/jbc.M411108200
  17. Kim, M., Ahn, S. H., Krogan, N. J., Greenblatt, J. F. and Buratowski, S. (2004) Transitions in RNA polymerase II elongation complexes at the 3' ends of genes. EMBO J. 23, 354-364 https://doi.org/10.1038/sj.emboj.7600053
  18. Prather, D., Krogan, N. J., Emili, A., Greenblatt, J. F. and Winston, F. (2005) Identification and characterization of Elf1, a conserved transcription elongation factor in Saccharomyecs cerevisiae. Mol. Cell Biol. 25, 10122-1013 https://doi.org/10.1128/MCB.25.22.10122-10135.2005
  19. Krawitz, D. C., Kama, T. and Kaufman, P. D. (2002) Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol. Cell Biol. 22, 614-625 https://doi.org/10.1128/MCB.22.2.614-625.2002
  20. Hirschhorn, J. N., Brown, S. A., Clark, C. D. and Winston, F. (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6, 2288-2298 https://doi.org/10.1101/gad.6.12a.2288
  21. Schwabish, M. A. and Struhl, K. (2007) The Swi/Snf complex is important for histone eviction during transcriptional activation and RNA polymerase II elongation in vivo. Mol. Cell Biol. 27, 6987-6995 https://doi.org/10.1128/MCB.00717-07
  22. Eriksson, P. R., Mendiratta, G., Mclaughlin, N. B., Wolfsberg, T. G., Marino-Ramirez, L., Pompa, T. A., Jainerin, M., Landsman, D., Shen, C. H. and Clark, D. J. (2005) Global regulation by the yeast spt10 protein is mediated through chromatin structure and the histone upstream activating sequence elements. Mol. Cell Biol. 25, 9127-9137 https://doi.org/10.1128/MCB.25.20.9127-9137.2005
  23. Xu, F., Zhang, K. and Grunstein, M. (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121, 375-385 https://doi.org/10.1016/j.cell.2005.03.011
  24. DeSilva, H., Lee, K. and Osley, M. A. (1998) Functional dissection of yeast Hir1p, a WD repeat-containing transcriptional corepressor. Genetics 148, 657-667
  25. Carrozza, M. J., Li, B., Florens, L., Suganuma, T., Swanson,S. K., Lee, K. K., Shia, W. J., Anderson, S., Yates, J., Washburn, M. P. and Workman, J. L. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581-592 https://doi.org/10.1016/j.cell.2005.10.023
  26. Keogh, M. C., Kurdistani, S. K., Morris, S. A., Ahn, S. H., Podolny, V., Collins, S. R., Schuldiner, M., Chin, K., Punna, T., Thompson, N. J., Boone, C., Emili, A., Weissman, J. S., Hughes, T. R., Strahl, B. D., Grunstein, M., Greenblatt, J. F., Buratowski, S. and Krogan, N. J. (2005) Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593-605 https://doi.org/10.1016/j.cell.2005.10.025
  27. Seol, J. H., Kim, H. J., Yang, Y. J., Kim, S. T., Youn, H. D., Han, J. W., Lee, H. W. and Cho, E. J. (2006) Different roles of histone H3 lysine 4 methylation in chromatin maintenance. Bio. Biophy. Res. Comm. 349, 463-470 https://doi.org/10.1016/j.bbrc.2006.08.122
  28. Cho, E. J., Kobor, M. S., Kim, M., Greenblatt, J. and Buratowski, S. (2001) Opposing effects of Ctk1 kinase and Fcp1 phosphatase at serine 2 of the RNA polymerase II C-terminal domain. Genes Dev. 24, 3319-3329

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