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PLOS ONE  2013 

Mutations in Non-Acid Patch Residues Disrupt H2A.Z’s Association with Chromatin through Multiple Mechanisms

DOI: 10.1371/journal.pone.0076394

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Abstract:

The incorporation of histone variants into nucleosomes is a critical mechanism for regulating essential DNA-templated processes and for establishing distinct chromatin architectures with specialised functions. H2A.Z is an evolutionarily conserved H2A variant that has diverse roles in transcriptional regulation, heterochromatin boundary definition, chromosome stability and DNA repair. The H2A.Z C-terminus diverges in sequence from canonical H2A and imparts unique functions to H2A.Z in the yeast S. cerevisiae. Although mediated in part through the acid patch-containing M6 region, many molecular determinants of this divergent structure-function relationship remain unclear. Here, by using an unbiased random mutagenesis screen of H2A.Z alleles, we identify point mutations in the C-terminus outside of the M6 region that disrupt the normal function of H2A.Z in response to cytotoxic stress. These functional defects correlate with reduced chromatin association, which we attribute to reduced physical stability within chromatin, but also to altered interactions with the SWR and INO80 chromatin remodeling complexes. Together with experimental data, computational modelling of these residue changes in the context of protein structure suggests the importance of C-terminal domain integrity and configuration for maintaining the level of H2A.Z in nucleosomes.

References

[1]  Jackson JD, Falciano VT, Gorovsky MA (1996) A likely histone H2A.F/Z variant in Saccharomyces cerevisiae. Trends Biochem Sci 21: 466–467. doi:10.1016/S0968-0004(96)20028-3. PubMed: 9009827.
[2]  Adam M, Robert F, Larochelle M, Gaudreau L (2001) H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol 21: 6270–6279. doi:10.1128/MCB.21.18.6270–6279.2001. PubMed: 11509669.
[3]  Larochelle M, Gaudreau L (2003) H2A.Z has a function reminiscent of an activator required for preferential binding to intergenic DNA. EMBO J 22: 4512–4522. doi:10.1093/emboj/cdg427. PubMed: 12941702.
[4]  Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL et al. (2004) A Protein Complex Containing the Conserved Swi2/Snf2-Related ATPase Swr1p Deposits Histone Variant. p. H2A.Z into Euchromatin. Plos Biol 2: e131. doi:10.1371/journal.pbio.0020131.st003.
[5]  Krogan NJ, Keogh M-C, Datta N, Sawa C, Ryan OW et al. (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12: 1565–1576. doi:10.1016/S1097-2765(03)00497-0. PubMed: 14690608.
[6]  Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725–736. doi:10.1016/S0092-8674(03)00123-5. PubMed: 12628191.
[7]  Brickner JH, Walter P (2004) Gene Recruitment of the Activated INO1 Locus to the Nuclear Membrane. PLOS Biol 2: e342. doi:10.1371/journal.pbio.0020342. PubMed: 15455074.
[8]  Santisteban MS, Kalashnikova T, Smith MM (2000) Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes. Cell 103: 411–422. doi:10.1016/S0092-8674(00)00133-1. PubMed: 11081628.
[9]  Kalocsay M, Hiller NJ, Jentsch S (2009) Chromosome-wide Rad51 Spreading and SUMO-H2A.Z-Dependent Chromosome Fixation in Response to a Persistent DNA Double-Strand Break. Mol Cell 33: 335–343. doi:10.1016/j.molcel.2009.01.016. PubMed: 19217407.
[10]  Gardner JM, Smoyer CJ, Stensrud ES, Alexander R, Gogol M et al. (2011) Targeting of the SUN protein Mps3 to the inner nuclear membrane by the histone variant H2A.Z. J Cell Biol 193: 489–507. doi:10.1083/jcb.201011017. PubMed: 21518795.
[11]  Mizuguchi G, Shen X, Landry J, Wu WH, Sen S et al. (2004) ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex. PubMed: 14645854.
[12]  Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global Regulation of H2A.Z Localization by the INO80 Chromatin-Remodeling Enzyme Is Essential for Genome Integrity. Cell 144: 200–213. doi:10.1016/j.cell.2010.12.021. PubMed: 21241891.
[13]  Watanabe S, Radman-Livaja M, Rando OJ, Peterson CL (2013) A Histone Acetylation Switch Regulates H2A.Z Deposition by the SWR-C Remodeling Enzyme. Science 340: 195–199. doi:10.1126/science.1229758. PubMed: 23580526.
[14]  Wu WH, Alami S, Luk E, Wu CH, Sen S et al. (2005) Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat Struct Mol Biol 12: 1064–1071. doi:10.1038/nsmb1023. PubMed: 16299513.
[15]  Wu WH, Wu CH, Ladurner A, Mizuguchi G, Wei D et al. (2009) N Terminus of Swr1 Binds to Histone H2AZ and Provides a Platform for Subunit Assembly in the Chromatin Remodeling Complex. J Biol Chem 284: 6200–6207. doi:10.1074/jbc.M808830200. PubMed: 19088068.
[16]  Shen X, Mizuguchi G, Hamiche A, Wu C (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406: 541–544. doi:10.1038/35020123. PubMed: 10952318.
[17]  Shen X, Ranallo R, Choi E, Wu C (2003) Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol Cell 12: 147–155. doi:10.1016/S1097-2765(03)00264-8. PubMed: 12887900.
[18]  Suto RK, Clarkson MJ, Tremethick DJ, Luger K (2000) Crystal structure of a nucleosome core particle containing the variant histone. p. H2A.Z. Nat Struct Biol 7: 1121–1124. doi:10.1038/8. 1971.
[19]  Clarkson MJ, Wells JR, Gibson F, Saint R, Tremethick DJ (1999) Regions of variant histone His2AvD required for Drosophila development. Nature 399: 694–697. doi:10.1038/21436. PubMed: 10385122.
[20]  Jensen K, Santisteban MS, Urekar C, Smith MM (2011) Histone H2A.Z acid patch residues required for deposition and function. Mol Genet Genomics 285: 287–296. doi:10.1007/s00438-011-0604-5. PubMed: 21359583.
[21]  Mehta M, Braberg H, Wang S, Lozsa A, Shales M et al. (2010) Individual Lysine Acetylations on the N Terminus of Saccharomyces cerevisiae H2A.Z Are Highly but Not Differentially Regulated. J Biol Chem 285: 39855–39865. doi:10.1074/jbc.M110.185967. PubMed: 20952395.
[22]  Wang AY, Aristizabal MJ, Ryan C, Krogan NJ, Kobor MS (2011) Key Functional Regions in the Histone Variant H2A.Z C-Terminal Docking Domain. Mol Cell Biol 31: 3871–3884. doi:10.1128/MCB.05182-11. PubMed: 21791612.
[23]  Millar CB, Xu F, Zhang K, Grunstein M (2006) Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 20: 711–722. doi:10.1101/gad.1395506. PubMed: 16543223.
[24]  Babiarz JE (2006) Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomy cescerevisiae. Genes Dev 20: 700–710. doi:10.1101/gad.1386306. PubMed: 16543222.
[25]  Keogh MC (2006) The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev 20: 660–665. doi:10.1101/gad.1388106. PubMed: 16543219.
[26]  Halley JE, Kaplan T, Wang AY, Kobor MS, Rine J (2010) Roles for H2A.Z and Its Acetylation in GAL1 Transcription and Gene Induction, but Not GAL1-Transcriptional Memory. PLOS Biol 8: e1000401. doi:10.1371/journal.pbio.1000401.t006.
[27]  Wan Y, Saleem RA, Ratushny AV, Roda O, Smith JJ et al. (2009) Role of the Histone Variant. p. H2A. Z/Htz1p in TBP Recruitment, Chromatin Dynamics, and Regulated Expression of Oleate-Responsive Genes. Molecular and Cellular Biology 29: 2346–2358 doi:10.1128/MCB.01233-08.
[28]  Kawano A, Hayashi Y, Noguchi S, Handa H, Horikoshi M et al. (2011) Global analysis for functional residues of histone variant Htz1 using the comprehensive point mutant library. Genes Cells 16: 590–607. doi:10.1111/j.1365-2443.2011.01512.x. PubMed: 21470346.
[29]  Morillo-Huesca M, Clemente-Ruiz M, Andújar E, Prado F (2010) The SWR1 Histone Replacement Complex Causes Genetic Instability and Genome-Wide Transcription Misregulation in the Absence of H2A.Z. PLOS ONE 5: e12143. doi:10.1371/journal.pone.0012143.g006. PubMed: 20711347.
[30]  Sharp JA, Fouts ET, Krawitz DC, Kaufman PD (2001) Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencingJudith A Sharp: 1–11.
[31]  Zabaronick SR, Tyler JK (2005) The Histone Chaperone Anti-Silencing Function 1 Is a Global Regulator of Transcription Independent of Passage through S Phase. Mol Cell Biol 25: 652–660. doi:10.1128/MCB.25.2.652-660.2005. PubMed: 15632066.
[32]  Ramey CJ, Howar S, Adkins M, Linger J, Spicer J et al. (2004) Activation of the DNA Damage Checkpoint in Yeast Lacking the Histone Chaperone Anti-Silencing Function 1. Mol Cell Biol 24: 10313–10327. doi:10.1128/MCB.24.23.10313-10327.2004. PubMed: 15542840.
[33]  Schwabish MA, Struhl K (2006) Asf1 Mediates Histone Eviction and Deposition during Elongation by RNA Polymerase II. Mol Cell 22: 415–422. doi:10.1016/j.molcel.2006.03.014. PubMed: 16678113.
[34]  Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806–810. doi:10.1038/nature05649. PubMed: 17314980.
[35]  Wratting D, Thistlethwaite A, Harris M, Zeef LA, Millar CB (2012) A Conserved Function for the H2A.Z C Terminus. J Biol Chem 287: 19148–19157. doi:10.1074/jbc.M111.317990. PubMed: 22493515.
[36]  Luk E, Vu N-D, Patteson K, Mizuguchi G, Wu W-H et al. (2007) Chz1, a Nuclear Chaperone for Histone H2AZ. Mol Cell 25: 357–368. doi:10.1016/j.molcel.2006.12.015. PubMed: 17289584.
[37]  Zhou Z, Feng H, Hansen DF, Kato H, Luk E et al. (2008) NMR structure of chaperone Chz1 complexed with histones. ZH H2A: 2B. Nature Structural & Molecular Biology 15: 868–869 doi:10.1038/nsmb.1465.
[38]  Word JM, Lovell SC, LaBean TH, Taylor HC, Zalis ME et al. (1999) Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. J Mol Biol 285: 1711–1733. doi:10.1006/jmbi.1998.2400. PubMed: 9917407.
[39]  Zhang H, Roberts DN, Cairns BR (2005) Genome-Wide Dynamics of Htz1, a Histone H2A Variant that Poises Repressed/Basal Promoters for Activation through Histone Loss. Cell 123: 219–231. doi:10.1016/j.cell.2005.08.036. PubMed: 16239141.
[40]  Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961. doi:10.1002/(SICI)1097-0061(199807)14:10<953?::AID-YEA293>3.0.CO;2-U. PubMed: 9717241.
[41]  Word JM, Lovell SC, Richardson JS, Richardson DC (1999) Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J Mol Biol 285: 1735–1747. doi:10.1006/jmbi.1998.2401. PubMed: 9917408.
[42]  Chen VB, Davis IW, Richardson DC (2009) KING (Kinemage, Next Generation): A versatile interactive molecular and scientific visualization program. Protein Sci 18: 2403–2409. doi:10.1002/pro.250. PubMed: 19768809.

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