1,140
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Deacetylation of H4 lysine16 affects acetylation of lysine residues in histone H3 and H4 and promotes transcription of constitutive genes

ORCID Icon, &
Pages 597-617 | Received 05 Apr 2020, Accepted 24 Jul 2020, Published online: 23 Aug 2020

References

  • Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–395.
  • Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–1080.
  • Shukla A, Chaurasia P, Bhaumik SR. Histone methylation and ubiquitination with their cross-talk and roles in gene expression and stability. Cell Mol Life Sci. 2009;66:1419–1433.
  • Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41–45.
  • Smerdon MJ. DNA repair and the role of chromatin structure. Curr Opin Cell Biol. 1991;3:422–428.
  • Bannister AJ, Kouzarides T. The CBP co-activator is a histone acetyltransferase. Nature. 1996;384:641–643.
  • Luger K, Mader AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–260.
  • Millar CB, Kurdistani SK, Grunstein M. Acetylation of yeast histone H4 lysine 16: a switch for protein interactions in heterochromatin and euchromatin. Cold Spring Harb Symp Quant Biol. 2004;69:193–200.
  • Shogren-Knaak M, Peterson CL. Switching on chromatin: mechanistic role of histone H4-K16 acetylation. Cell Cycle. 2006;5:1361–1365.
  • Bhaumik SR, Smith E, Shilatifard A. Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol. 2007;14:1008–1016.
  • Fulton MD, Zhang J, He M, et al. Intricate effects of alpha- amino and lysine modifications on arginine methylation of the N-terminal tail of histone H4. Biochemistry. 2017;56:3539–3548.
  • Green EM, Mas G, Young NL, et al. Methylation of H4 lysines 5, 8 and 12 by yeast Set5 calibrates chromatin stress responses. Nat Struct Mol Biol. 2012;19:361–363.
  • Green EM, Morrison AJ, Gozani O. New marks on the block: set5 methylates H4 lysines 5, 8 and 12. Nucleus. 2012;3:335–339.
  • Shogren-Knaak M, Ishii H, Sun JM, et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science. 2006;311:844–847.
  • Zhang R, Erler J, Langowski J. Histone acetylation regulates chromatin accessibility: role of H4K16 in inter-nucleosome interaction. Biophys J. 2017;112:450–459.
  • Hecht A, Laroche T, Strahl-Bolsinger S, et al. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell. 1995;80:583–592.
  • Johnson A, Li G, Sikorski TW, et al. Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol Cell. 2009;35:769–781.
  • Kimura A, Umehara T, Horikoshi M. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat Genet. 2002;32:370–377.
  • Oppikofer M, Kueng S, Martino F, et al. A dual role of H4K16 acetylation in the establishment of yeast silent chromatin. Embo J. 2011;30:2610–2621.
  • Suka N, Luo K, Grunstein M. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet. 2002;32:378–383.
  • Kayne PS, Kim UJ, Han M, et al. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell. 1988;55:27–39.
  • Bird AW, Yu DY, Pray-Grant MG, et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature. 2002;419:411–415.
  • Ray A, Khan P, Nag Chaudhuri R. Regulated acetylation and deacetylation of H4 K16 is essential for efficient NER in saccharomyces cerevisiae. DNA Repair (Amst). 2018;72:39–55.
  • Durrin LK, Mann RK, Kayne PS, et al. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell. 1991;65:1023–1031.
  • Heise F, Chung HR, Weber JM, et al. Genome-wide H4 K16 acetylation by SAS-I is deposited independently of transcription and histone exchange. Nucleic Acids Res. 2012;40:65–74.
  • Horikoshi N, Kumar P, Sharma GG, et al. Genome-wide distribution of histone H4 lysine 16 acetylation sites and their relationship to gene expression. Genome Integr. 2013;4:3.
  • Kurdistani SK, Tavazoie S, Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell. 2004;117:721–733.
  • Taylor GC, Eskeland R, Hekimoglu-Balkan B, et al. H4K16 acetylation marks active genes and enhancers of embryonic stem cells, but does not alter chromatin compaction. Genome Res. 2013;23:2053–2065.
  • Wang A, Kurdistani SK, Grunstein M. Requirement of Hos2 histone deacetylase for gene activity in yeast. Science. 2002;298:1412–1414.
  • Yu Y, Teng Y, Liu H, et al. UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc Natl Acad Sci U S A. 2005;102:8650–8655.
  • Fraga MF, Ballestar E, Villar-Garea A, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 2005;37:391–400.
  • Rando OJ, Winston F. Chromatin and transcription in yeast. Genetics. 2012;190:351–387.
  • Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128:707–719.
  • Lee TI, Causton HC, Holstege FC, et al. Redundant roles for the TFIID and SAGA complexes in global transcription. Nature. 2000;405:701–704.
  • Bhaumik SR, Green MR. SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev. 2001;15:1935–1945.
  • Bhaumik SR, Green MR. Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo. Mol Cell Biol. 2002;22:7365–7371.
  • Li XY, Bhaumik SR, Green MR. Distinct classes of yeast promoters revealed by differential TAF recruitment. Science. 2000;288:1242–1244.
  • Basehoar AD, Zanton SJ, Pugh BF. Identification and distinct regulation of yeast TATA box-containing genes. Cell. 2004;116:699–709.
  • Huisinga KL, Pugh BF. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell. 2004;13:573–585.
  • Nagai S, Davis RE, Mattei PJ, et al. Chromatin potentiates transcription. Proc Natl Acad Sci U S A. 2017;114:1536–1541.
  • Warfield L, Ramachandran S, Baptista T, et al. Transcription of nearly all yeast RNA polymerase II-transcribed genes is dependent on transcription factor TFIID. Mol Cell. 2017;68:118–129 e115.
  • Baptista T, Grunberg S, Minoungou N, et al. SAGA is a general cofactor for RNA polymerase II transcription. Mol Cell. 2017;68:130–143 e135.
  • Bonnet J, Wang CY, Baptista T, et al. The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription. Genes Dev. 2014;28:1999–2012.
  • Natsume-Kitatani Y, Mamitsuka H. Classification of promoters based on the combination of core promoter elements exhibits different histone modification patterns. PloS One. 2016;11:e0151917.
  • Burke RL, Tekamp-Olson P, Najarian R. The isolation, characterization, and sequence of the pyruvate kinase gene of Saccharomyces cerevisiae. J Biol Chem. 1983;258:2193–2201.
  • Fraenkel DG. The top genes: on the distance from transcript to function in yeast glycolysis. Curr Opin Microbiol. 2003;6:198–201.
  • Pearce AK, Crimmins K, Groussac E, et al. Pyruvate kinase (Pyk1) levels influence both the rate and direction of carbon flux in yeast under fermentative conditions. Microbiology. 2001;147:391–401.
  • Parsons MC, Weil PA. Cloning of TFC1, the Saccharomyces cerevisiae gene encoding the 95-kDa subunit of transcription factor TFIIIC. J Biol Chem. 1992;267:2894–2901.
  • Swanson RN, Conesa C, Lefebvre O, et al. Isolation of TFC1, a gene encoding one of two DNA-binding subunits of yeast transcription factor tau (TFIIIC). Proc Natl Acad Sci U S A. 1991;88:4887–4891.
  • Uprety B, Lahudkar S, Malik S, et al. The 19S proteasome subcomplex promotes the targeting of NuA4 HAT to the promoters of ribosomal protein genes to facilitate the recruitment of TFIID for transcriptional initiation in vivo. Nucleic Acids Res. 2012;40:1969–1983.
  • Klebanow ER, Poon D, Zhou S, et al. Isolation and characterization of TAF25, an essential yeast gene that encodes an RNA polymerase II-specific TATA-binding protein-associated factor. J Biol Chem. 1996;271:13706–13715.
  • Tora L. A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev. 2002;16:673–675.
  • Gilon T, Chomsky O, Kulka RG. Degradation signals recognized by the Ubc6p- Ubc7p ubiquitin-conjugating enzyme pair. Mol Cell Biol. 2000;20:7214–7219.
  • Sommer T, Jentsch S. A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature. 1993;365:176–179.
  • Pruyne D, Bretscher A. Polarization of cell growth in yeast. J Cell Sci. 2000;113(Pt 4):571–585.
  • Pruyne D, Bretscher A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci. 2000;113(Pt 3):365–375.
  • Archambault J, Friesen JD. Genetics of eukaryotic RNA polymerases I, II, and III. Microbiol Rev. 1993;57:703–724.
  • Liu CL, Kaplan T, Kim M, et al. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 2005;3:e328.
  • Bell O, Wirbelauer C, Hild M, et al. Localized H3K36 methylation states define histone H4K16 acetylation during transcriptional elongation in Drosophila. Embo J. 2007;26:4974–4984.
  • Gaucher J, Boussouar F, Montellier E, et al. Bromodomain-dependent stage-specific male genome programming by Brdt. Embo J. 2012;31:3809–3820.
  • Gates LA, Shi J, Rohira AD, et al. Acetylation on histone H3 lysine 9 mediates a switch from transcription initiation to elongation. J Biol Chem. 2017;292:14456–14472.
  • Owen DJ, Ornaghi P, Yang JC, et al. The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. Embo J. 2000;19:6141–6149.
  • Dion MF, Altschuler SJ, Wu LF, et al. Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci U S A. 2005;102:5501–5506.
  • Shukla A, Bajwa P, Bhaumik SR. SAGA-associated Sgf73p facilitates formation of the preinitiation complex assembly at the promoters either in a HAT-dependent or independent manner in vivo. Nucleic Acids Res. 2006;34:6225–6232.
  • Uprety B, Sen R, Bhaumik SR. Eaf1p is required for recruitment of NuA4 in targeting TFIID to the promoters of the ribosomal protein genes for transcriptional initiation in vivo. Mol Cell Biol. 2015;35:2947–2964.
  • Bernier M, Luo Y, Nwokelo KC, et al. Linker histone H1 and H3K56 acetylation are antagonistic regulators of nucleosome dynamics. Nat Commun. 2015;6:10152.
  • Hyland EM, Cosgrove MS, Molina H, et al. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol. 2005;25:10060–10070.
  • Maas NL, Miller KM, DeFazio LG, et al. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell. 2006;23:109–119.
  • Masumoto H, Hawke D, Kobayashi R, et al. A role for cell-cycle- regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature. 2005;436:294–298.
  • Rufiange A, Jacques PE, Bhat W, et al. Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell. 2007;27:393–405.
  • Topal S, Vasseur P, Radman-Livaja M, et al. Distinct transcriptional roles for histone H3-K56 acetylation during the cell cycle in Yeast. Nat Commun. 2019;10:4372.
  • Xu F, Zhang K, Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell. 2005;121:375–385.
  • Yang J, Zhang X, Feng J, et al. The histone chaperone FACT contributes to DNA replication-coupled nucleosome assembly. Cell Rep. 2016;14:1128–1141.
  • Schneider J, Bajwa P, Johnson FC, et al. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem. 2006;281:37270–37274.
  • Durairaj G, Chaurasia P, Lahudkar S, et al. Regulation of chromatin assembly/disassembly by Rtt109p, a histone H3 Lys56-specific acetyltransferase, in vivo. J Biol Chem. 2010;285:30472–30479.
  • Watanabe S, Resch M, Lilyestrom W, et al. Structural characterization of H3K56Q nucleosomes and nucleosomal arrays. Biochim Biophys Acta. 2010;1799:480–486.
  • Allard S, Utley RT, Savard J, et al. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. Embo J. 1999;18:5108–5119.
  • Reiter C, Heise F, Chung HR, et al. A link between Sas2- mediated H4 K16 acetylation, chromatin assembly in S-phase by CAF-I and Asf1, and nucleosome assembly by Spt6 during transcription. FEMS Yeast Res. 2015;15:fov073.
  • Jacobson RH, Ladurner AG, King DS, et al. Structure and function of a human TAFII250 double bromodomain module. Science. 2000;288:1422–1425.
  • Matangkasombut O, Buratowski S. Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation. Mol Cell. 2003;11:353–363.
  • Pamblanco M, Poveda A, Sendra R, et al. Bromodomain factor 1 (Bdf1) protein interacts with histones. FEBS Lett. 2001;496:31–35.
  • Martinez-Campa C, Politis P, Moreau JL, et al. Precise nucleosome positioning and the TATA box dictate requirements for the histone H4 tail and the bromodomain factor Bdf1. Mol Cell. 2004;15:69–81.
  • Weiner A, Hsieh TH, Appleboim A, et al. High-resolution chromatin dynamics during a yeast stress response. Mol Cell. 2015;58:371–386.
  • Hsieh TH, Weiner A, Lajoie B, et al. Mapping nucleosome resolution chromosome folding in yeast by micro-C. Cell. 2015;162:108–119.
  • Goudarzi A, Zhang D, Huang H, et al. Dynamic competing histone H4 K5K8 acetylation and butyrylation are hallmarks of highly active gene promoters. Mol Cell. 2016;62:169–180.
  • Ma XJ, Wu J, Altheim BA, et al. Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci U S A. 1998;95:6693–6698.
  • Ruan K, Yamamoto TG, Asakawa H, et al. Histone H4 acetylation required for chromatin decompaction during DNA replication. Sci Rep. 2015;5:12720.
  • Chang CS, Pillus L. Collaboration between the essential Esa1 acetyltransferase and the Rpd3 deacetylase is mediated by H4K12 histone acetylation in Saccharomyces cerevisiae. Genetics. 2009;183:149–160.
  • De Nadal E, Zapater M, Alepuz PM, et al. The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature. 2004;427:370–374.
  • Kurdistani SK, Robyr D, Tavazoie S, et al. Genome-wide binding map of the histone deacetylase Rpd3 in yeast. Nat Genet. 2002;31:248–254.
  • Robert F, Pokholok DK, Hannett NM, et al. Global position and recruitment of HATs and HDACs in the yeast genome. Mol Cell. 2004;16:199–209.
  • Elias-Villalobos A, Helmlinger D, Ibeas JI. Histone deacetylases: revealing the molecular base of dimorphism in pathogenic fungi. Microb Cell. 2015;2:491–493.
  • Ferdoush J, Sen R, Kaja A, et al. Two distinct regulatory mechanisms of transcriptional initiation in response to nutrient signaling. Genetics. 2018;208:191–205.
  • Sharma VM, Tomar RS, Dempsey AE, et al. Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage-inducible genes. Mol Cell Biol. 2007;27:3199–3210.
  • Karmodiya K, Krebs AR, Oulad-Abdelghani M, et al. H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics. 2012;13:424.
  • Guo R, Chen J, Mitchell DL, et al. GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 2011;39:1390–1397.
  • Meyer B, Fabbrizi MR, Raj S, et al. Histone H3 lysine 9 acetylation obstructs ATM activation and promotes ionizing radiation sensitivity in normal stem cells. Stem Cell Reports. 2016;7:1013–1022.
  • Chen Y, Zhang Y, Ye H, et al. Structural basis for the acetylation of histone H3K9 and H3K27 mediated by the histone chaperone Vps75 in Pneumocystis carinii. Signal Transduct Target Ther. 2019;4:14.
  • Zhou W, Jiang D, Tian J, et al. Acetylation of H3K4, H3K9, and H3K27 mediated by p300 regulates the expression of GATA4 in cardiocytes. Genes Dis. 2019;6:318–325.
  • Abshiru N, Ippersiel K, Tang Y, et al. Chaperone-mediated acetylation of histones by Rtt109 identified by quantitative proteomics. J Proteomics. 2013;81:80–90.
  • Cote JM, Kuo YM, Henry RA, et al. Two factor authentication: Asf1 mediates crosstalk between H3 K14 and K56 acetylation. Nucleic Acids Res. 2019;47:7380–7391.
  • Simoneau A, Delgoshaie N, Celic I, et al. Interplay between histone H3 lysine 56 deacetylation and chromatin modifiers in response to DNA damage. Genetics. 2015;200:185–205.
  • Tan Y, Xue Y, Song C, et al. Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency. Proc Natl Acad Sci U S A. 2013;110:11493–11498.
  • Williams SK, Truong D, Tyler JK. Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A. 2008;105:9000–9005.
  • Xie W, Song C, Young NL, et al. Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell. 2009;33:417–427.
  • Kaplan T, Liu CL, Erkmann JA, et al. Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet. 2008;4:e1000270.
  • Gardner JM, Jaspersen SL. Manipulating the yeast genome: deletion, mutation, and tagging by PCR. Methods Mol Biol. 2014;1205:45–78.
  • Szymanski EP, Kerscher O. Budding yeast protein extraction and purification for the study of function, interactions, and post-translational modifications. J Vis Exp. 2013;80:e50921.
  • Song L, Crawford GE. DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harb Protoc. 2010;2010:pdb prot5384.
  • Zhong J, Luo K, Winter PS, et al. Mapping nucleosome positions using DNase-seq. Genome Res. 2016;26:351–364.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.