Nucleosome assembly factors CAF-1 and HIR modulate epigenetic switching frequencies in an H3K56 acetylation-associated manner in Candida albicans

Eukaryotic Cell

Volumn 12, Issue 4, 2013, Pages 591-603

  Stevenson, John S ^a   Liu, Haoping ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CHROMATIN ASSEMBLY FACTOR 1; FUNGAL PROTEIN; HISTONE; HISTONE DEACETYLASE; NICOTINAMIDE; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ACETYLATION; ARTICLE; CANDIDA ALBICANS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; MUTATION; NUCLEOSOME;

ACETYLATION; ACETYLTRANSFERASES; CANDIDA ALBICANS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN ASSEMBLY FACTOR-1; EPIGENESIS, GENETIC; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; HISTONES; MUTATION; NIACINAMIDE; NUCLEOSOMES; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

CANDIDA ALBICANS;

EID: 84875516407     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00334-12     Document Type: Article

References (66)

1. Kornberg RD. 1977. Structure of chromatin. Annu. Rev. Biochem. 46: 931-954.
2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389:251-260.
3. Millar CB, Grunstein M. 2006. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 7:657-666.
4. Zhou VW, Goren A, Bernstein BE. 2011. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12:7-18.
5. De Koning L, Corpet A, Haber JE, Almouzni G. 2007. Histone chaper-ones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol. 14:997-1007.
6. Eitoku M, Sato L, Senda T, Horikoshi M. 2008. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell. Mol. Life Sci. 65:414-444.
7. Kaufman PD, Kobayashi R, Stillman B. 1997. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevi-siae cells lacking chromatin assembly factor-I. Genes Dev. 11:345-357.
8. Stillman B. 1986. Chromatin assembly during SV40 DNA replication in vitro. Cell 45:555-565.
9. Shibahara K, Stillman B. 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96: 575-585.
10. Enomoto S, Berman J. 1998. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev. 12:219-232.
11. Enomoto S, McCune-Zierath PD, Gerami-Nejad M, Sanders MA, Berman J. 1997. RLF2, a subunit of yeast chromatin assembly factor-I, is required for telomeric chromatin function in vivo. Genes Dev. 11:358-370.
12. Monson EK, de Bruin D, Zakian VA. 1997. The yeast Cac1 protein is required for the stable inheritance of transcriptionally repressed chromatin at telomeres. Proc. Natl. Acad. Sci. U. S. A. 94:13081-13086.
13. Smith JS, Caputo E, Boeke JD. 1999. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol. 19:3184-3197.
14. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, Yates JR, III, Kaufman PD. 2005. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15:2044-2049.
15. Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL. 2005. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 19:2534-2539.
16. Osley MA, Lycan D. 1987. Transacting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol. Cell. Biol. 7:4204-4210.
17. Xu H, Kim UJ, Schuster T, Grunstein M. 1992. Identification of a new set of cell cycle-regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:5249-5259.
18. Anderson HE, Wardle J, Korkut SV, Murton HE, Lopez-Maury L, Bahler J, Whitehall SK. 2009. The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts. Mol. Cell. Biol. 29:5158-5167.
19. Formosa T, Ruone S, Adams MD, Olsen AE, Eriksson P, Yu Y, Rhoades AR, Kaufman PD, Stillman DJ. 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.
20. Nourani A, Robert F, Winston F. 2006. Evidence that Spt2/Sin1, an HMG-like factor, plays rolesin transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:1496-1509.
21. Kaufman PD, Cohen JL, Osley MA. 1998. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18:4793-4806.
22. Sharp JA, Franco AA, Osley MA, Kaufman PD. 2002. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev. 16:85-100.
23. Lopes da Rosa J, Holik J, Green EM, Rando OJ, Kaufman PD. 2011. Overlapping regulation ofCenH3 localization and histoneH3turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187:9-19.
24. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz David C, Pchelintsev Nikolay A, Adams Peter D, Jansen Lars ET, Almouzni G. 2011. Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol. Cell 44:928-941.
25. Houlard M, Berlivet S, Probst AV, Quivy Héry J-PP, Almouzni G, Gérard M. 2006. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet. 2:e181. doi:10.1371/journal.pgen.0020181.
26. Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S, Carey A, Brickman JM, Wynshaw-Boris A, Scambler PJ. 2002. Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnor-malitiesof mesoendodermal derivatives prior to early embryonic lethality. Mol. Cell. Biol. 22:2318-2328.
27. Alabert C, Groth A. 2012. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13:153-167.
28. Slutsky B, Staebell M, Anderson J, Risen L, Pfaller M, Soll DR. 1987. "White-opaque transition": a second high-frequency switching system in Candida albicans. J. Bacteriol. 169:189-197.
29. Lohse MB, Johnson AD. 2009. White-opaque switching in Candida albicans. Curr. Opin. Microbiol. 12:650-654.
30. Soll DR. 2009. Why does Candida albicans switch? FEMS Yeast Res. 9:973-989.
31. Huang G, Wang H, Chou S, Nie X, Chen J, Liu H. 2006. Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 103:12813-12818.
32. Srikantha T, Borneman AR, Daniels KJ, Pujol C, Wu W, Seringhaus MR, Gerstein M, Yi S, Snyder M, Soll DR. 2006. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 5:1674-1687.
33. Zordan RE, Galgoczy DJ, Johnson AD. 2006. Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc. Natl. Acad. Sci. U. S. A. 103:12807-12812.
34. Zordan RE, Miller MG, Galgoczy DJ, Tuch BB, Johnson AD. 2007. Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol. 5:e256-e256. doi:10.1371/journal.pbio.0050256.
35. Tuch BB, Mitrovich QM, Homann OR, Hernday AD, Monighetti CK, De La Vega FM, Johnson AD. 2010. The transcriptomes of two heritable cell types illuminate the circuit governing their differentiation. PLoS Genet. 6:e1001070-e1001070. doi:10.1371/journal.pgen.1001070.
36. Hnisz D, Schwarzmüller T, Kuchler K. 2009. Transcriptional loops meet chromatin: a dual-layer network controls white-opaque switching in Candida albicans. Mol. Microbiol. 74:1-15.
37. Stevenson JS, Liu H. 2011. Regulation of white and opaque cell-type formation in Candida albicans by Rtt109 and Hst3. Mol. Microbiol. 81: 1078-1091.
38. Chen C-C, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK. 2008. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231-243.
39. Driscoll R, Hudson A, Jackson SP. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315:649-652.
40. Han J, Zhou H, Horazdovsky B, Zhang K, Xu Zhang R-MZ. 2007. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315:653-655.
41. Kaplan T, Liu CL, Erkmann JA, Holik J, Grunstein M, Kaufman PD, Friedman N, Rando OJ. 2008. Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet. 4:e1000270-e1000270. doi:10.1371/journal.pgen.1000270.
42. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z. 2008. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244-255.
43. Masumoto H, Hawke D, Kobayashi R, Verreault A. 2005. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294-298.
44. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlingame AL, Hunt DF, Kaufman PD, Allis CD. 2006. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc. Natl. Acad. Sci. U. S. A. 103:6988-6993.
45. Sharp JA, Fouts ET, Krawitz DC, Kaufman PD. 2001. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochro-matic silencing. Curr. Biol. 11:463-473.
46. Lopes da Rosa J, Boyartchuk VL, Zhu LJ, Kaufman PD. 2010. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107:1594-1599.
47. Wurtele H, Tsao S, Lepine G, Mullick A, Tremblay J, Drogaris P, Lee Thibault E-HP, Verreault A, Raymond M. 2010. Modulation of histone H3 lysine 56 acetylation as an antifungal therapeutic strategy. Nat. Med. 16:774-780.
48. Rauceo JM, Blankenship JR, Fanning S, Hamaker JJ, Deneault Smith J-SFJ, Nantel A, Mitchell AP. 2008. Regulation of the Candida albicans cell wall damage response by transcription factor Sko1 and PAS kinase Psk1. Mol. Biol. Cell 19:2741-2751.
49. Ramírez-Zavala B, Reuss O, Park Ohlsen Y-NK, Morschhäuser J. 2008. Environmental induction of white-opaque switching in Candida albicans. PLoS Pathog. 4:e1000089-e1000089. doi:10.1371/journal.ppat.1000089.
50. Reuss O, Vik A, Kolter R, Morschhäuser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119-127.
51. Sherwood PW, Tsang SV, Osley MA. 1993. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:28-38.
52. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 1999. Ploidy regulation of gene expression. Science 285:251-254.
53. Janbon G, Sherman F, Rustchenko E. 1998. Monosomy of a specific chromosome determines l-sorbose utilization: a novel regulatory mechanism in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 95:5150-5155.
54. Kapitzky L, Beltrao P, Berens TJ, Gassner N, Zhou C, Wuster A, Wu J, Babu MM, Elledge SJ, Toczyski D, Lokey RS, Krogan NJ. 2010. Cross-species chemogenomic profiling reveals evolutionarily conserved drug mode of action. Mol. Syst. Biol. 6:451.
55. Sinha H, David L, Pascon RC, Clauder-Munster S, Krishnakumar S, Nguyen M, Shi G, Dean J, Davis RW, Oefner PJ, McCusker JH, Steinmetz LM. 2008. Sequential elimination of major-effect contributors identifies additional quantitative trait loci conditioning high-temperature growth in yeast. Genetics 180:1661-1670.
56. Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, Pleiss JA, Friedman N, Rando OJ. 2012. Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol. 10:e1001369. doi:10.1371/journal.pbio.1001369.
57. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A. 2006. The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr. Biol. 16:1280-1289.
58. Maas NL, Miller KM, DeFazio LG, Toczyski DP. 2006. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23:109-119.
59. Huang G, Yi S, Sahni N, Daniels KJ, Srikantha T, Soll DR. 2010. N-acetylglucosamine induces white to opaque switching,amating prerequisite in Candida albicans. PLoS Pathog. 6:e1000806-e1000806. doi:10.1371/journal.ppat.1000806.
60. Baum M, Sanyal K, Mishra PK, Thaler N, Carbon J. 2006. Formation of functional centromeric chromatin is specified epigenetically in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 103:14877-14882.
61. Sanyal K, Baum M, Carbon J. 2004. Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc. Natl. Acad. Sci. U. S. A. 101:11374-11379.
62. Charoensawan V, Janga SC, Bulyk ML, Babu MM, Teichmann SA. 2012. DNA sequence preferences of transcriptional activators correlate more strongly than repressors with nucleosomes. Mol. Cell 47:183-192.
63. Kaufman PD, Rando OJ. 2010. Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol. 22:284-290.
64. Radman-Livaja M, Verzijlbergen KF, Weiner A, van Welsem T, Friedman N, Rando OJ, van Leeuwen F. 2011. Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol. 9:e1001075. doi:10.1371/journal.pbio.1001075.
65. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B. 2010. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328:94-98.
66. Hathaway NA, Bell O, Hodges C, Miller EL, Neel DS, Crabtree GR. 2012. Dynamics and memory of heterochromatin in living cells. Cell 149: 1447-1460.