Asf1-like Structure of the Conserved Yaf9 YEATS Domain and Role in H2A.Z Deposition and Acetylation

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2009 Dec 8

PMID 19966225

Citations 38

Authors

Alice Y Wang

Julia M Schulze

Emmanuel Skordalakes

Jennifer W Gin

James M Berger

Jasper Rine

Michael S Kobor

Affiliations

Soon will be listed here.

Abstract

Chromatin can be modified by posttranslational modifications of histones, ATP-dependent remodeling, and incorporation of histone variants. The Saccharomyces cerevisiae protein Yaf9 is a subunit of both the essential histone acetyltransferase complex NuA4 and the ATP-dependent chromatin remodeling complex SWR1-C, which deposits histone variant H2A.Z into euchromatin. Yaf9 contains a YEATS domain, found in proteins associated with multiple chromatin-modifying enzymes and transcription complexes across eukaryotes. Here, we established the conservation of YEATS domain function from yeast to human, and determined the structure of this region from Yaf9 by x-ray crystallography to 2.3 A resolution. The Yaf9 YEATS domain consisted of a beta-sandwich characteristic of the Ig fold and contained three distinct conserved structural features. The structure of the Yaf9 YEATS domain was highly similar to that of the histone chaperone Asf1, a similarity that extended to an ability of Yaf9 to bind histones H3 and H4 in vitro. Using structure-function analysis, we found that the YEATS domain was required for Yaf9 function, histone variant H2A.Z chromatin deposition at specific promoters, and H2A.Z acetylation.

Citing Articles

The polySUMOylation axis promotes nucleolar release of Tof2 for mitotic exit.

Gutierrez-Morton E, Haluska C, Collins L, Rizkallah R, Tomko Jr R, Wang Y Cell Rep. 2024; 43(7):114492.

PMID: 39002125 PMC: 11298248. DOI: 10.1016/j.celrep.2024.114492.

Small-molecule tools for YEATS domain proteins.

Erb M Curr Opin Chem Biol. 2023; 77:102404.

PMID: 37924571 PMC: 10842393. DOI: 10.1016/j.cbpa.2023.102404.

GAS41 promotes H2A.Z deposition through recognition of the N terminus of histone H3 by the YEATS domain.

Kikuchi M, Takase S, Konuma T, Noritsugu K, Sekine S, Ikegami T Proc Natl Acad Sci U S A. 2023; 120(43):e2304103120.

PMID: 37844223 PMC: 10614846. DOI: 10.1073/pnas.2304103120.

Computational and Functional Analysis of Structural Features in the ZAKα Kinase.

Johansen V, Snieckute G, Vind A, Blasius M, Bekker-Jensen S Cells. 2023; 12(6).

PMID: 36980309 PMC: 10047201. DOI: 10.3390/cells12060969.

Epigenetic Reprogramming of the Glucose Metabolic Pathways by the Chromatin Effectors During Cancer.

Mondal P, Tiwary N, Sengupta A, Dhang S, Roy S, Das C Subcell Biochem. 2022; 100:269-336.

PMID: 36301498 DOI: 10.1007/978-3-031-07634-3_9.

References

Li B, Pattenden S, Lee D, Gutierrez J, Chen J, Seidel C . Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci U S A. 2005; 102(51):18385-90. PMC: 1317944. DOI: 10.1073/pnas.0507975102. View

Wu W, Wu C, Ladurner A, Mizuguchi G, Wei D, Xiao H . N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J Biol Chem. 2008; 284(10):6200-7. PMC: 2649089. DOI: 10.1074/jbc.M808830200. View

Babiarz J, Halley J, Rine J . Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev. 2006; 20(6):700-10. PMC: 1413290. DOI: 10.1101/gad.1386306. View

Mizuguchi G, Shen X, Landry J, Wu W, Sen S, Wu C . ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 2003; 303(5656):343-8. DOI: 10.1126/science.1090701. View

Zeisig D, Bittner C, Zeisig B, Garcia-Cuellar M, Hess J, Slany R . The eleven-nineteen-leukemia protein ENL connects nuclear MLL fusion partners with chromatin. Oncogene. 2005; 24(35):5525-32. DOI: 10.1038/sj.onc.1208699. View

Guillemette B, Gaudreau L . Reuniting the contrasting functions of H2A.Z. Biochem Cell Biol. 2006; 84(4):528-35. DOI: 10.1139/o06-077. View

Daser A, Rabbitts T . Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev. 2004; 18(9):965-74. DOI: 10.1101/gad.1195504. View

Bork P, Holm L, Sander C . The immunoglobulin fold. Structural classification, sequence patterns and common core. J Mol Biol. 1994; 242(4):309-20. DOI: 10.1006/jmbi.1994.1582. View

Keogh M, Mennella T, Sawa C, Berthelet S, Krogan N, Wolek A . The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev. 2006; 20(6):660-5. PMC: 1413285. DOI: 10.1101/gad.1388106. View

10.

Kobor M, Venkatasubrahmanyam S, Meneghini M, Gin J, Jennings J, Link A . A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2004; 2(5):E131. PMC: 374244. DOI: 10.1371/journal.pbio.0020131. View

11.

Park J, Roeder R . GAS41 is required for repression of the p53 tumor suppressor pathway during normal cellular proliferation. Mol Cell Biol. 2006; 26(11):4006-16. PMC: 1489109. DOI: 10.1128/MCB.02185-05. View

12.

Millar C, Xu F, Zhang K, Grunstein M . Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev. 2006; 20(6):711-22. PMC: 1413291. DOI: 10.1101/gad.1395506. View

13.

Kusch T, Workman J . Histone variants and complexes involved in their exchange. Subcell Biochem. 2007; 41:91-109. View

14.

Rufiange A, Jacques P, Bhat W, Robert F, Nourani A . Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell. 2007; 27(3):393-405. DOI: 10.1016/j.molcel.2007.07.011. View

15.

Williams S, Truong D, Tyler J . 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(26):9000-5. PMC: 2449354. DOI: 10.1073/pnas.0800057105. View

16.

Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A . Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell. 2008; 134(2):244-55. PMC: 2597342. DOI: 10.1016/j.cell.2008.06.018. View

17.

Zhang H, Richardson D, Roberts D, Utley R, Erdjument-Bromage H, Tempst P . The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near telomeres. Mol Cell Biol. 2004; 24(21):9424-36. PMC: 522225. DOI: 10.1128/MCB.24.21.9424-9436.2004. View

18.

Schulze J, Jackson J, Nakanishi S, Gardner J, Hentrich T, Haug J . Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol Cell. 2009; 35(5):626-41. PMC: 3222332. DOI: 10.1016/j.molcel.2009.07.017. View

19.

Krogan N, Keogh M, Datta N, Sawa C, Ryan O, Ding H . A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell. 2003; 12(6):1565-76. DOI: 10.1016/s1097-2765(03)00497-0. View

20.

Baker N, Sept D, Joseph S, Holst M, McCammon J . Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A. 2001; 98(18):10037-41. PMC: 56910. DOI: 10.1073/pnas.181342398. View