Histone H4 facilitates the proteolysis of the budding yeast CENP-ACse4 centromeric histone variant

Genetics

Volumn 205, Issue 1, 2017, Pages 113-124

  Deyter, Gary M R ^a,b   Hildebrand, Erica M ^a,c   Barber, Adrienne D ^a   Biggins, Sue ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

CENP ACse4; Centromere; H4; Nucleosome; Proteolysis; Psh1

Indexed keywords

CENTROMERE PROTEIN A; HISTONE H2B; HISTONE H3; HISTONE H4; MYC PROTEIN; PSH1 PROTEIN; SPACER DNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; AUTOANTIGEN; CHROMATIN; DNA BINDING PROTEIN; EUCHROMATIN; HISTONE; NONHISTONE PROTEIN; NUCLEOSOME; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL MUTANT; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENOMIC INSTABILITY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; CENTROMERE; CHROMATIN; EUCHROMATIN; GENETICS; KINETOCHORE; METABOLISM; UBIQUITINATION;

AUTOANTIGENS; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; EUCHROMATIN; HISTONES; KINETOCHORES; NUCLEOSOMES; PROTEIN BINDING; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 85008439762     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.194027     Document Type: Article

References (52)

1. Akiyoshi, B., K. K. Sarangapani, A. F. Powers, C. R. Nelson, S. L. Reichow et al., 2010 Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468: 576-579.
2. Amato, A., T. Schillaci, L. Lentini, and A. Di Leonardo, 2009 CENP-A overexpression promotes genome instability in pRb-depleted human cells. Mol. Cancer 8: 119.
3. Biggins, S., F. F. Severin, N. Bhalla, I. Sassoon, A. A. Hyman et al., 1999 The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13: 532-544.
4. Black, B. E., and D. W. Cleveland, 2011 Epigenetic centromere propagation and the nature of CENP-A nucleosomes. Cell 144: 471-479.
5. Collins, K. A., S. Furuyama, and S. Biggins, 2004 Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 14: 1968-1972.
6. Da Rosa, J. L., J. Holik, E. M. Green, O. J. Rando, and P. D. Kaufman, 2011 Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187: 9-19.
7. Dai, J., E. M. Hyland, D. S. Yuan, H. Huang, J. S. Bader et al., 2008 Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134: 1066-1078.
8. Dechassa, M. L., K. Wyns, and K. Luger, 2014 Scm3 deposits a (Cse4-H4)2 tetramer onto DNA through a Cse4-H4 dimer intermediate. Nucleic Acids Res. 42: 5532-5542.
9. Deyter, G. M. R., and S. Biggins, 2014 The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev. 28: 1815-1826.
10. Duina, A. A., A. Rufiange, J. Bracey, J. Hall, A. Nourani et al., 2007 Evidence that the localization of the elongation factor Spt16 across transcribed genes is dependent upon histone H3 integrity in Saccharomyces cerevisiae. Genetics 177: 101-112.
11. Eriksson, P. R., D. Ganguli, V. Nagarajavel, and D. J. Clark, 2012 Regulation of histone gene expression in budding yeast. Genetics 191: 7-20.
12. Gietz, R. D., and A. Sugino, 1988 New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534.
13. Gross, S., F. Catez, H. Masumoto, and P. Lomonte, 2012 Centromere architecture breakdown induced by the viral E3 ubiquitin ligase ICP0 protein of herpes simplex virus type 1. PLoS One 7: e44227.
14. Hainer, S. J., and J. A. Martens, 2011 Identification of histone mutants that are defective for transcription-coupled nucleosome occupancy. Mol. Cell. Biol. 31: 3557-3568.
15. Hardwick, K., and A. W. Murray, 1995 Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol. 131: 709-720.
16. Heun, P., S. Erhardt, M. D. Blower, S. Weiss, A. D. Skora et al., 2006 Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 10: 303-315.
17. Hewawasam, G., M. Shivaraju, M. Mattingly, S. Venkatesh, S. Martin-Brown et al., 2010 Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol. Cell 40: 444-454.
18. Hildebrand, E. M., and S. Biggins, 2016 Regulation of budding yeast CENP-A levels prevents misincorporation at promoter nucleosomes and transcriptional defects. PLoS Genet. 12: e1005930.
19. Jung, I., J. Seo, H. S. Lee, L. W. Stanton, D. Kim et al., 2015 Global mapping of the regulatory interactions of histone residues. FEBS Lett. 589: 4061-4070.
20. Kawashima, S., Y. Nakabayashi, K. Matsubara, N. Sano, T. Enomoto et al., 2011 Global analysis of core histones reveals nucleosomal surfaces required for chromosome bi-orientation. EMBO J. 30: 3353-3367.
21. Kupiec, M., 2014 Biology of telomeres: lessons from budding yeast. FEMS Microbiol. Rev. 38: 144-171.
22. Kurat, C. F., J. Recht, E. Radovani, T. Durbic, B. Andrews et al., 2014 Regulation of histone gene transcription in yeast. Cell. Mol. Life Sci. 71: 599-613.
23. Li, M., and Y. Fang, 2015 Histone variants: the artists of eukaryotic chromatin. Sci. China Life Sci. 58: 232-239.
24. Liang, D., S. L. Burkhart, R. K. Singh, M. H. Kabbaj, and A. Gunjan, 2012 Histone dosage regulates DNA damage sensitivity in a checkpoint-independent manner by the homologous recombination pathway. Nucleic Acids Res. 40: 9604-9620.
25. Lomonte, P., K. F. Sullivan, and R. D. Everett, 2001 Degradation of nucleosome-associated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. J. Biol. Chem. 276: 5829-5835.
26. Longtine, M. S., McKenzie, A., III, D. J. Demarini, N. G. Shah, A. Wach et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
27. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond, 1997 Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
28. Minshull, J., A. Straight, A. Rudner, A. Dernburg, A. Belmont et al., 1996 Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr. Biol. 6: 1609-1620.
29. Moreno-Moreno, O., M. Torras-Llort, and F. Azorin, 2006 Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res. 34: 6247-6255.
30. Moreno-Moreno, O., S. Medina-Giró, M. Torras-Llort, and F. Azorín, 2011 The F box protein partner of paired regulates stability of Drosophila centromeric histone H3, CenH3CID. Curr. Biol. 21: 1488-1493.
31. Ng, T. M., W. G. Waples, B. D. Lavoie, and S. Biggins, 2009 Pericentromeric sister chromatid cohesion promotes kinetochore biorientation. Mol. Biol. Cell 20: 3818-3827.
32. Ng, T. M., T. L. Lenstra, N. Duggan, S. Jiang, S. Ceto et al., 2013 Kinetochore function and chromosome segregation rely on critical residues in histones H3 and H4 in budding yeast. Genetics 195: 795-807.
33. Nguyen, H. T., W. Wharton, Harper J. A., II,, J. R. Dornhoffer, and A. A. Duina, 2013 A nucleosomal region important for ensuring proper interactions between the transcription elongation factor Spt16 and transcribed genes in Saccharomyces cerevisiae. G3 (Bethesda) 3: 929-940.
34. Ohkuni, K., R. Abdulle, and K. Kitagawa, 2014 Degradation of centromeric histone H3 variant Cse4 requires the Fpr3 peptidylprolyl cis-trans isomerase. Genetics 196: 1041-1045.
35. Ohkuni, K., Y. Takahashi, A. Fulp, J. Lawrimore, W. C. Au et al., 2016 SUMO-Targeted Ubiquitin Ligase (STUbL) Slx5 regulates proteolysis of centromeric histone H3 variant Cse4 and prevents its mislocalization to euchromatin. Mol. Biol. Cell 27: 1500-1510.
36. Palmer, D. K., K. O’Day, M. H. Wener, B. S. Andrews, and R. L. Margolis, 1987 A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J. Cell Biol. 104: 805-815.
37. Rando, O. J., and F. Winston, 2012 Chromatin and transcription in yeast. Genetics 190: 351-387.
38. Ranjitkar, P., M. O. Press, X. Yi, R. Baker, M. J. MacCoss et al., 2010 An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell 40: 455-464.
39. Rose, M. D., F. Winston, and P. Heiter, 1990 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Sekulic, N., E. A. Bassett, D. J. Rogers, and B. E. Black, 2010 The structure of (CENP-A-H4)2 reveals physical features that mark centromeres. Nature 467: 347-351.
41. Sharp, J. A., A. A. Franco, M. A. Osley, and P. D. Kaufman, 2002 Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev. 16: 85-100.
42. Sherman, F., G. Fink, and C. Lawrence, 1974 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Singh, R. K., M.-H. M. Kabbaj, J. Paik, and A. Gunjan, 2009 Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 11: 925-933.
44. Smith, M. M., P. Yang, M. S. Santisteban, P. W. Boone, A. T. Goldstein et al., 1996 A novel histone H4 mutant defective in nuclear division and mitotic chromosome transmission. Mol. Cell. Biol. 16: 1017-1026.
45. Stoler, S., K. C. Keith, K. E. Curnick, and M. Fitzgerald-Hayes, 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.
46. Straight, A. F., A. S. Belmont, C. C. Robinett, and A. W. Murray, 1996 GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr. Biol. 6: 1599-1608.
47. Tachiwana, H., W. Kagawa, T. Shiga, A. Osakabe, Y. Miya et al., 2011 Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476: 232-235.
48. Tomonaga, T., K. Matsushita, S. Yamaguchi, T. Oohashi, H. Shimada et al., 2003 Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63: 3511-3516.
49. Van Hooser, A. A., I. I. Ouspenski, H. C. Gregson, D. A. Starr, T. J. Yen et al., 2001 Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114: 3529-3542.
50. Venkatesh, S., and J. L. Workman, 2015 Histone exchange, chromatin structure and the regulation of transcription. Nat. Rev. Mol. Cell Biol. 16: 178-189.
51. Verdaasdonk, J. S., and K. Bloom, 2011 Centromeres: unique chromatin structures that drive chromosome segregation. Nature Publishing Group 12: 320-332.
52. White, C. L., R. K. Suto, and K. Luger, 2001 Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J. 20: 5207-5218.