Functional and Physical Interactions between Yeast 14-3-3 Proteins, Acetyltransferases, and Deacetylases in Response to DNA Replication Perturbations

REFERENCES

• Aitken, A. 2006. 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 16:162–172.
   PubMed Web of Science ®Google Scholar
• Aparicio, J. G., C. J. Viggiani, D. G. Gibson, and O. M. Aparicio. 2004. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:4769–4780.
   PubMedGoogle Scholar
• Bird, A. W., D. Y. Yu, M. G. Pray-Grant, Q. Qiu, K. E. Harmon, P. C. Megee, P. A. Grant, M. M. Smith, and M. F. Christman. 2002. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419:411–415.
   PubMed Web of Science ®Google Scholar
• Burke, T. W., J. G. Cook, M. Asano, and J. R. Nevins. 2001. Replication factors MCM2 and ORC1 interact with the histone acetyltransferase HBO1. J. Biol. Chem. 276:15397–15408.
   PubMed Web of Science ®Google Scholar
• Celic, I., H. Masumoto, W. P. Griffith, P. Meluh, R. J. Cotter, J. D. Boeke, and A. Verreault. 2006. The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr. Biol. 16:1280–1289.
   PubMed Web of Science ®Google Scholar
• Cheung, P., K. G. Tanner, W. L. Cheung, P. Sassone-Corsi, J. M. Denu, and C. D. Allis. 2000. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5:905–915.
   PubMed Web of Science ®Google Scholar
• Choy, J. S., and S. J. Kron. 2002. NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol. Cell. Biol. 22:8215–8225.
   PubMed Web of Science ®Google Scholar
• Clarke, A. S., J. E. Lowell, S. J. Jacobson, and L. Pillus. 1999. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19:2515–2526.
   PubMed Web of Science ®Google Scholar
• Cobb, J. A., L. Bjergbaek, K. Shimada, C. Frei, and S. M. Gasser. 2003. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22:4325–4336.
   PubMed Web of Science ®Google Scholar
• Desany, B. A., A. A. Alcasabas, J. B. Bachant, and S. J. Elledge. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12:2956–2970.
   PubMed Web of Science ®Google Scholar
• Dohmen, R. J., P. Wu, and A. Varshavsky. 1994. Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science 263:1273–1276.
   PubMed Web of Science ®Google Scholar
• Downs, J. A., S. Allard, O. Jobin-Robitaille, A. Javaheri, A. Auger, N. Bouchard, S. J. Kron, S. P. Jackson, and J. Cote. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16:979–990.
   PubMed Web of Science ®Google Scholar
• Doyon, Y., and J. Cote. 2004. The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14:147–154.
   PubMed Web of Science ®Google Scholar
• Edmondson, D. G., J. K. Davie, J. Zhou, B. Mirnikjoo, K. Tatchell, and S. Y. Dent. 2002. Site-specific loss of acetylation upon phosphorylation of histone H3. J. Biol. Chem. 277:29496–29502.
   PubMedGoogle Scholar
• Gelperin, D., J. Weigle, K. Nelson, P. Roseboom, K. Irie, K. Matsumoto, and S. Lemmon. 1995. 14-3-3 proteins: potential roles in vesicular transport and Ras signaling in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 92:11539–11543.
   PubMedGoogle Scholar
• Grozinger, C. M., and S. L. Schreiber. 2000. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc. Natl. Acad. Sci. USA 97:7835–7840.
   PubMed Web of Science ®Google Scholar
• Hasan, S., N. El-Andaloussi, U. Hardeland, P. O. Hassa, C. Burki, R. Imhof, P. Schar, and M. O. Hottiger. 2002. Acetylation regulates the DNA end-trimming activity of DNA polymerase β. Mol. Cell 10:1213–1222.
   PubMedGoogle Scholar
• Iizuka, M., and B. Stillman. 1999. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J. Biol. Chem. 274:23027–23034.
   PubMed Web of Science ®Google Scholar
• Iizuka, M., T. Matsui, H. Takisawa, and M. M. Smith. 2006. Regulation of replication licensing by acetyltransferase Hbo1. Mol. Cell. Biol. 26:1098–1108.
   PubMed Web of Science ®Google Scholar
• Imhof, A., and A. P. Wolffe. 1999. Purification and properties of the Xenopus Hat1 acetyltransferase: association with the 14-3-3 proteins in the oocyte nucleus. Biochemistry 38:13085–13093.
   PubMed Web of Science ®Google Scholar
• Jazayeri, A., A. D. McAinsh, and S. P. Jackson. 2004. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 101:1644–1649.
   PubMedGoogle Scholar
• Kushnirov, V. V. 2000. Rapid and reliable protein extraction from yeast. Yeast 16:857–860.
   PubMed Web of Science ®Google Scholar
• Li, X., S. Song, Y. Liu, S. H. Ko, and H. Y. Kao. 2004. Phosphorylation of the histone deacetylase 7 modulates its stability and association with 14-3-3 proteins. J. Biol. Chem. 279:34201–34208.
   PubMedGoogle Scholar
• Lo, W. S., R. C. Trievel, J. R. Rojas, L. Duggan, J. Y. Hsu, C. D. Allis, R. Marmorstein, and S. L. Berger. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5:917–926.
   PubMed Web of Science ®Google Scholar
• Loewith, R., M. Meijer, S. P. Lees-Miller, K. Riabowol, and D. Young. 2000. Three yeast proteins related to the human candidate tumor suppressor p33ING1 are associated with histone acetyltransferase activities. Mol. Cell. Biol. 20:3807–3816.
   PubMed Web of Science ®Google Scholar
• Longhese, M. P., M. Clerici, and G. Lucchini. 2003. The S-phase checkpoint and its regulation in Saccharomyces cerevisiae. Mutat. Res. 532:41–58.
   PubMedGoogle Scholar
• Longhese, M. P., V. Paciotti, H. Neecke, and G. Lucchini. 2000. Checkpoint proteins influence telomeric silencing and length maintenance in budding yeast. Genetics 155:1577–1591.
   PubMedGoogle Scholar
• Lopes, M., C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, C. S. Newlon, and M. Foiani. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412:557–561.
   PubMed Web of Science ®Google Scholar
• Lottersberger, F., A. Panza, G. Lucchini, S. Piatti, and M. P. Longhese. 2006. The Saccharomyces cerevisiae 14-3-3 proteins are required for the G1/S transition, actin cytoskeleton organization and cell wall integrity. Genetics 173:661–675.
   PubMedGoogle Scholar
• Lottersberger, F., F. Rubert, V. Baldo, G. Lucchini, and M. P. Longhese. 2003. Functions of Saccharomyces cerevisiae 14-3-3 proteins in response to DNA damage and to DNA replication stress. Genetics 165:1717–1732.
   PubMedGoogle Scholar
• Lucca, C., F. Vanoli, C. Cotta-Ramusino, A. Pellicioli, G. Liberi, J. Haber, and M. Foiani. 2004. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23:1206–1213.
   PubMed Web of Science ®Google Scholar
• Maas, N. L., K. M. Miller, L. G. DeFazio, and D. P. Toczyski. 2006. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23:109–119.
   PubMed Web of Science ®Google Scholar
• Macdonald, N., J. P. Welburn, M. E. Noble, A. Nguyen, M. B. Yaffe, D. Clynes, J. G. Moggs, G. Orphanides, S. Thomson, J. W. Edmunds, A. L. Clayton, J. A. Endicott, and L. C. Mahadevan. 2005. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol. Cell 20:199–211.
   PubMed Web of Science ®Google Scholar
• Mann, R. K., and M. Grunstein. 1992. Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J. 11:3297–3306.
   PubMed Web of Science ®Google Scholar
• Masumoto, H., D. Hawke, R. Kobayashi, and A. Verreault. 2005. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294–298.
   PubMed Web of Science ®Google Scholar
• Millar, C. B., and M. Grunstein. 2006. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 7:657–666.
   PubMed Web of Science ®Google Scholar
• Muslin, A. J., J. W. Tanner, P. M. Allen, and A. S. Shaw. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889–897.
   PubMed Web of Science ®Google Scholar
• Naryzhny, S. N., and H. Lee. 2004. The post-translational modifications of proliferating cell nuclear antigen: acetylation, not phosphorylation, plays an important role in the regulation of its function. J. Biol. Chem. 279:20194–20199.
   PubMed Web of Science ®Google Scholar
• Neecke, H., G. Lucchini, and M. P. Longhese. 1999. Cell cycle progression in the presence of irreparable DNA damage is controlled by a Mec1- and Rad53-dependent checkpoint in budding yeast. EMBO J. 18:4485–4497.
   PubMedGoogle Scholar
• Ozdemir, A., S. Spicuglia, E. Lasonder, M. Vermeulen, C. Campsteijn, H. G. Stunnenberg, and C. Logie. 2005. Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J. Biol. Chem. 280:25949–25952.
   PubMed Web of Science ®Google Scholar
• Paciotti, V., M. Clerici, G. Lucchini, and M. P. Longhese. 2000. The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14:2046–2059.
   PubMed Web of Science ®Google Scholar
• Paulovich, A. G., and L. H. Hartwell. 1995. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82:841–847.
   PubMed Web of Science ®Google Scholar
• Pozuelo Rubio, M., K. M. Geraghty, B. H. C. Wong, N. T. Wood, D. G. Campbell, N. Morrice, and C. Mackintosh. 2004. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379:395–408.
   PubMedGoogle Scholar
• Qin, S., and M. R. Parthun. 2006. Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol. Cell. Biol. 26:3649–3658.
   PubMedGoogle Scholar
• Roberts, R. L., H. U. Mosch, and G. R. Fink. 1997. 14-3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae. Cell 89:1055–1065.
   PubMed Web of Science ®Google Scholar
• Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Sanchez, Y., B. A. Desany, W. J. Jones, Q. Liu, B. Wang, and S. J. Elledge. 1996. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271:357–360.
   PubMed Web of Science ®Google Scholar
• Santocanale, C., and J. F. Diffley. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395:615–618.
   PubMed Web of Science ®Google Scholar
• Scott, K. L., and S. E. Plon. 2003. Loss of Sin3/Rpd3 histone deacetylase restores the DNA damage response in checkpoint-deficient strains of Saccharomyces cerevisiae. Mol. Cell. Biol. 23:4522–4531.
   PubMed Web of Science ®Google Scholar
• Sekito, T., J. Thornton, and R. A. Butow. 2000. Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol. Biol. Cell 11:2103–2115.
   PubMedGoogle Scholar
• Shirahige, K., Y. Hori, K. Shiraishi, M. Yamashita, K. Takahashi, C. Obuse, T. Tsurimoto, and H. Yoshikawa. 1998. Regulation of DNA-replication origins during cell-cycle progression. Nature 395:618–621.
   PubMed Web of Science ®Google Scholar
• Smith, E. R., A. Eisen, W. Gu, M. Sattah, A. Pannuti, J. Zhou, R. G. Cook, J. C. Lucchesi, and C. D. Allis. 1998. ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc. Natl. Acad. Sci. USA 95:3561–3565.
   PubMed Web of Science ®Google Scholar
• Sweeney, F. D., F. Yang, A. Chi, J. Shabanowitz, D. F. Hunt, and D. Durocher. 2005. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15:1364–1375.
   PubMed Web of Science ®Google Scholar
• Tamburini, B. A., and J. K. Tyler. 2005. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25:4903–4913.
   PubMed Web of Science ®Google Scholar
• Tercero, J. A., and J. F. Diffley. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553–557.
   PubMed Web of Science ®Google Scholar
• Tercero, J. A., M. P. Longhese, and J. F. Diffley. 2003. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11:1323–1336.
   PubMed Web of Science ®Google Scholar
• Tsukuda, T., A. B. Fleming, J. A. Nickoloff, and M. A. Osley. 2005. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379–383.
   PubMed Web of Science ®Google Scholar
• Utley, R. T., N. Lacoste, O. Jobin-Robitaille, S. Allard, and J. Cote. 2005. Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell. Biol. 25:8179–8190.
   PubMed Web of Science ®Google Scholar
• van Attikum, H., O. Fritsch, B. Hohn, and S. M. Gasser. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777–788.
   PubMed Web of Science ®Google Scholar
• van Heusden, G. P., D. J. Griffiths, J. C. Ford, T. F. Chin-A-Woeng, P. A. Schrader, A. M. Carr, and H. Y. Steensma. 1995. The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. Eur. J. Biochem. 229:45–53.
   PubMedGoogle Scholar
• Vogelauer, M., L. Rubbi, I. Lucas, B. J. Brewer, and M. Grunstein. 2002. Histone acetylation regulates the time of replication origin firing. Mol. Cell 10:1223–1233.
   PubMed Web of Science ®Google Scholar
• Wang, A. H., M. J. Kruhlak, J. Wu, N. R. Bertos, M. Vezmar, B. I. Posner, D. P. Bazett-Jones, and X. J. Yang. 2000. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol. 20:6904–6912.
   PubMed Web of Science ®Google Scholar
• Wurtele, H., and A. Verreault. 2006. Histone post-translational modifications and the response to DNA double-strand breaks. Curr. Opin. Cell Biol. 18:137–144.
   PubMedGoogle Scholar
• Yaffe, M. B., K. Rittinger, S. Volinia, P. R. Caron, A. Aitken, H. Leffers, S. J. Gamblin, S. J. Smerdon, and L. C. Cantley. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91:961–971.
   PubMed Web of Science ®Google Scholar
• Zhao, X., E. G. Muller, and R. Rothstein. 1998. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2:329–340.
   PubMed Web of Science ®Google Scholar