Structural and histone binding studies of the chromo barrel domain of TIP60
Abstract
Tat-interactive protein 60 consists of an N-terminal chromo barrel domain (TIP60-CB) and a C-terminal acetyltransferase domain and acetylates histone and nonhistone proteins in diverse cellular processes. While TIP60-CB is thought to recognize histone tails, molecular details of this interaction remain unclear. In this work, we attempted a quantitative analysis of the interaction between the human TIP60-CB and histone peptides, but did not observe any detectable binding by either fluorescence polarization or isothermal titration calorimetry assays. We also determined the crystal structure of the TIP60-CB alone. Analysis of the apo-tructure reveals a putative peptide-binding site that might be occluded by the basic side chain of a residue in a unique β hairpin between the two N-terminal strands of the β barrel, leading to the inability of TIP60-CB to bind histones.
- Authors:
-
- Central China Normal Univ., Wuhan (China)
- Central China Normal Univ., Wuhan (China); Univ. of Toronto, ON (Canada)
- Univ. of Toronto, ON (Canada)
- Wuhan Sports Univ. (China)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Natural Science Foundation of China (NSFC); Hubei Chenguang Talented Youth Development Foundation; AbbVie; Bayer Pharma AG; Boehringer Ingelheim; Canada Foundation for Innovation; Eshelman Institute for Innovation; Genome Canada; Ontario Genomics Institute; Innovative Medicines Initiative; Janssen; Merck KGaA; MSD; Novartis Pharma AG; Ontario Ministry of Research, Innovation and Science (MRIS); Pfizer; São Paulo Research Foundation (FAPESP); Takeda; Wellcome
- OSTI Identifier:
- 1439636
- Alternate Identifier(s):
- OSTI ID: 1464428
- Grant/Contract Number:
- AC02-06CH11357; 31500613; 115766
- Resource Type:
- Accepted Manuscript
- Journal Name:
- FEBS Letters
- Additional Journal Information:
- Journal Volume: 592; Journal Issue: 7; Journal ID: ISSN 0014-5793
- Publisher:
- Federation of European Biochemical Societies
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; chromo barrel domain; histone methylation; TIP60
Citation Formats
Zhang, Yuzhe, Lei, Ming, Yang, Xiajie, Feng, Yue, Yang, Yuan, Loppnau, Peter, Li, Yanjun, Yang, Yi, Min, Jinrong, and Liu, Yanli. Structural and histone binding studies of the chromo barrel domain of TIP60. United States: N. p., 2018.
Web. doi:10.1002/1873-3468.13021.
Zhang, Yuzhe, Lei, Ming, Yang, Xiajie, Feng, Yue, Yang, Yuan, Loppnau, Peter, Li, Yanjun, Yang, Yi, Min, Jinrong, & Liu, Yanli. Structural and histone binding studies of the chromo barrel domain of TIP60. United States. https://doi.org/10.1002/1873-3468.13021
Zhang, Yuzhe, Lei, Ming, Yang, Xiajie, Feng, Yue, Yang, Yuan, Loppnau, Peter, Li, Yanjun, Yang, Yi, Min, Jinrong, and Liu, Yanli. Sun .
"Structural and histone binding studies of the chromo barrel domain of TIP60". United States. https://doi.org/10.1002/1873-3468.13021. https://www.osti.gov/servlets/purl/1439636.
@article{osti_1439636,
title = {Structural and histone binding studies of the chromo barrel domain of TIP60},
author = {Zhang, Yuzhe and Lei, Ming and Yang, Xiajie and Feng, Yue and Yang, Yuan and Loppnau, Peter and Li, Yanjun and Yang, Yi and Min, Jinrong and Liu, Yanli},
abstractNote = {Tat-interactive protein 60 consists of an N-terminal chromo barrel domain (TIP60-CB) and a C-terminal acetyltransferase domain and acetylates histone and nonhistone proteins in diverse cellular processes. While TIP60-CB is thought to recognize histone tails, molecular details of this interaction remain unclear. In this work, we attempted a quantitative analysis of the interaction between the human TIP60-CB and histone peptides, but did not observe any detectable binding by either fluorescence polarization or isothermal titration calorimetry assays. We also determined the crystal structure of the TIP60-CB alone. Analysis of the apo-tructure reveals a putative peptide-binding site that might be occluded by the basic side chain of a residue in a unique β hairpin between the two N-terminal strands of the β barrel, leading to the inability of TIP60-CB to bind histones.},
doi = {10.1002/1873-3468.13021},
journal = {FEBS Letters},
number = 7,
volume = 592,
place = {United States},
year = {Sun Mar 25 00:00:00 EDT 2018},
month = {Sun Mar 25 00:00:00 EDT 2018}
}
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Works referenced in this record:
Recent developments in classical density modification
journal, March 2010
- Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
SIRT1 Regulates Autoacetylation and Histone Acetyltransferase Activity of TIP60
journal, January 2010
- Wang, Jiadong; Chen, Junjie
- Journal of Biological Chemistry, Vol. 285, Issue 15
Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains
journal, August 2003
- Fischle, W.
- Genes & Development, Vol. 17, Issue 15
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Structural basis for selective binding of m6A RNA by the YTHDC1 YTH domain
journal, September 2014
- Xu, Chao; Wang, Xiao; Liu, Ke
- Nature Chemical Biology, Vol. 10, Issue 11
Acetylation by Tip60 Is Required for Selective Histone Variant Exchange at DNA Lesions
journal, December 2004
- Kusch, T.
- Science, Vol. 306, Issue 5704
Sgf29 binds histone H3K4me2/3 and is required for SAGA complex recruitment and histone H3 acetylation: Sgf29 functions as an H3K4me2/3 binder in SAGA
journal, June 2011
- Bian, Chuanbing; Xu, Chao; Ruan, Jianbin
- The EMBO Journal, Vol. 30, Issue 14
Structure and function of the nucleosome-binding PWWP domain
journal, November 2014
- Qin, Su; Min, Jinrong
- Trends in Biochemical Sciences, Vol. 39, Issue 11
Epigenetic virtues of chromodomains
journal, September 2011
- Blus, Bartlomiej J.; Wiggins, Kimberly; Khorasanizadeh, Sepideh
- Critical Reviews in Biochemistry and Molecular Biology, Vol. 46, Issue 6
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994
- Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
- Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
Structural basis for recognition of arginine methylated Piwi proteins by the extended Tudor domain
journal, October 2010
- Liu, K.; Chen, C.; Guo, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 43
Novel Structural and Functional Mode of a Knot Essential for RNA Binding Activity of the Esa1 Presumed Chromodomain
journal, May 2008
- Shimojo, Hideaki; Sano, Norihiko; Moriwaki, Yoshihito
- Journal of Molecular Biology, Vol. 378, Issue 5
Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank
journal, September 2004
- Yang, Huanwang; Guranovic, Vladimir; Dutta, Shuchismita
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 10
Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9
journal, February 2002
- Nielsen, Peter R.; Nietlispach, Daniel; Mott, Helen R.
- Nature, Vol. 416, Issue 6876
Structural and Histone Binding Ability Characterizations of Human PWWP Domains
journal, June 2011
- Wu, Hong; Zeng, Hong; Lam, Robert
- PLoS ONE, Vol. 6, Issue 6
Structure and function of histone methylation binding proteinsThis paper is one of a selection of papers published in this Special Issue, entitled CSBMCB’s 51st Annual Meeting – Epigenetics and Chromatin Dynamics, and has undergone the Journal’s usual peer review process.
journal, February 2009
- Adams-Cioaba, Melanie A.; Min, Jinrong
- Biochemistry and Cell Biology, Vol. 87, Issue 1
How good are my data and what is the resolution?
journal, June 2013
- Evans, Philip R.; Murshudov, Garib N.
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
Tip60 acetylates six lysines of a specific class in core histones in vitro
journal, December 1998
- Kimura, Akatsuki; Horikoshi, Masami
- Genes to Cells, Vol. 3, Issue 12
KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling
journal, May 2013
- Kaidi, Abderrahmane; Jackson, Stephen P.
- Nature, Vol. 498, Issue 7452
Molecular Basis of the Interaction of Saccharomyces cerevisiae Eaf3 Chromo Domain with Methylated H3K36
journal, November 2008
- Sun, Bingfa; Hong, Jing; Zhang, Peng
- Journal of Biological Chemistry, Vol. 283, Issue 52
Homozygous disruption of the tip60 gene causes early embryonic lethality
journal, November 2009
- Hu, Yaofei; Fisher, Joseph B.; Koprowski, Stacy
- Developmental Dynamics, Vol. 238, Issue 11
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
The Tudor domain ‘Royal Family’: Tudor, plant Agenet, Chromo, PWWP and MBT domains
journal, February 2003
- Maurer-Stroh, Sebastian; Dickens, Nicholas J.; Hughes-Davies, Luke
- Trends in Biochemical Sciences, Vol. 28, Issue 2
Regulation of Arabidopsis Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate FT Expression
journal, September 2014
- Bu, Zhongyuan; Yu, Yu; Li, Zepeng
- PLoS Genetics, Vol. 10, Issue 9
Tip60 is a haplo-insufficient tumour suppressor required for an oncogene-induced DNA damage response
journal, August 2007
- Gorrini, Chiara; Squatrito, Massimo; Luise, Chiara
- Nature, Vol. 448, Issue 7157
Involvement of the TIP60 Histone Acetylase Complex in DNA Repair and Apoptosis
journal, August 2000
- Ikura, Tsuyoshi; Ogryzko, Vasily V.; Grigoriev, Mikhail
- Cell, Vol. 102, Issue 4
A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model
journal, October 1993
- Bayly, Christopher I.; Cieplak, Piotr; Cornell, Wendy
- The Journal of Physical Chemistry, Vol. 97, Issue 40
Tudor, MBT and chromo domains gauge the degree of lysine methylation
journal, January 2006
- Kim, Jeesun; Daniel, Jeremy; Espejo, Alexsandra
- EMBO reports
Readout of Epigenetic Modifications
journal, June 2013
- Patel, Dinshaw J.; Wang, Zhanxin
- Annual Review of Biochemistry, Vol. 82, Issue 1
An RNAi Screen of Chromatin Proteins Identifies Tip60-p400 as a Regulator of Embryonic Stem Cell Identity
journal, July 2008
- Fazzio, Thomas G.; Huff, Jason T.; Panning, Barbara
- Cell, Vol. 134, Issue 1
Protein structure alignment by incremental combinatorial extension (CE) of the optimal path
journal, September 1998
- Shindyalov, I. N.; Bourne, P. E.
- Protein Engineering Design and Selection, Vol. 11, Issue 9
The Buccaneer software for automated model building. 1. Tracing protein chains
journal, August 2006
- Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9
In situ proteolysis for protein crystallization and structure determination
journal, November 2007
- Dong, Aiping; Xu, Xiaohui; Edwards, Aled M.
- Nature Methods, Vol. 4, Issue 12
Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60
journal, September 2009
- Sun, Yingli; Jiang, Xiaofeng; Xu, Ye
- Nature Cell Biology, Vol. 11, Issue 11
Structure of HP1 Chromodomain Bound to a Lysine 9-Methylated Histone H3 Tail
journal, February 2002
- Jacobs, S. A.
- Science, Vol. 295, Issue 5562
Family-wide Characterization of Histone Binding Abilities of Human CW Domain-containing Proteins
journal, March 2016
- Liu, Yanli; Tempel, Wolfram; Zhang, Qi
- Journal of Biological Chemistry, Vol. 291, Issue 17
MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009
- Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
Structural Insight into Recognition of Methylated Histone Tails by Retinoblastoma-binding Protein 1
journal, January 2012
- Gong, Weibin; Zhou, Tao; Mo, Jinjin
- Journal of Biological Chemistry, Vol. 287, Issue 11
Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain
journal, July 2010
- Kim, Daesung; Blus, Bartlomiej J.; Chandra, Vikas
- Nature Structural & Molecular Biology, Vol. 17, Issue 8
Deciphering key features in protein structures with the new ENDscript server
journal, April 2014
- Robert, Xavier; Gouet, Patrice
- Nucleic Acids Research, Vol. 42, Issue W1
Structural Basis for the Recognition of Methylated Histone H3K36 by the Eaf3 Subunit of Histone Deacetylase Complex Rpd3S
journal, November 2008
- Xu, Chao; Cui, Gaofeng; Botuyan, Maria Victoria
- Structure, Vol. 16, Issue 11
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
iotbx.cif : a comprehensive CIF toolbox
journal, October 2011
- Gildea, Richard J.; Bourhis, Luc J.; Dolomanov, Oleg V.
- Journal of Applied Crystallography, Vol. 44, Issue 6
How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers
journal, November 2007
- Taverna, Sean D.; Li, Haitao; Ruthenburg, Alexander J.
- Nature Structural & Molecular Biology, Vol. 14, Issue 11
REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011
- Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3
journal, November 2006
- Zhang, Peng; Du, Jiamu; Sun, Bingfa
- Nucleic Acids Research, Vol. 34, Issue 22
L3MBTL1 recognition of mono- and dimethylated histones
journal, November 2007
- Min, Jinrong; Allali-Hassani, Abdellah; Nady, Nataliya
- Nature Structural & Molecular Biology, Vol. 14, Issue 12
High-resolution X-ray and NMR Structures of the SMN Tudor Domain: Conformational Variation in the Binding Site for Symmetrically Dimethylated Arginine Residues
journal, March 2003
- Sprangers, Remco; Groves, Matthew R.; Sinning, Irmgard
- Journal of Molecular Biology, Vol. 327, Issue 2
Epigenetic targets and drug discovery
journal, September 2014
- Liu, Yanli; Liu, Ke; Qin, Su
- Pharmacology & Therapeutics, Vol. 143, Issue 3
DNA Damage-Induced Acetylation of Lysine 3016 of ATM Activates ATM Kinase Activity
journal, October 2007
- Sun, Y.; Xu, Y.; Roy, K.
- Molecular and Cellular Biology, Vol. 27, Issue 24
Molecular replacement with MOLREP
journal, December 2009
- Vagin, Alexei; Teplyakov, Alexei
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
Structure and function of histone methylation-binding proteins in plants
journal, June 2016
- Liu, Yanli; Min, Jinrong
- Biochemical Journal, Vol. 473, Issue 12
Recognition of enhancer element–specific histone methylation by TIP60 in transcriptional activation
journal, November 2011
- Jeong, Kwang Won; Kim, Kyunghwan; Situ, Alan Jialun
- Nature Structural & Molecular Biology, Vol. 18, Issue 12
Crystal Structure of the Malignant Brain Tumor (MBT) Repeats in Sex Comb on Midleg-like 2 (SCML2)
journal, September 2003
- Sathyamurthy, Aruna; Allen, Mark D.; Murzin, Alexey G.
- Journal of Biological Chemistry, Vol. 278, Issue 47
Expression of Tip60, an androgen receptor coactivator, and its role in prostate cancer development
journal, April 2003
- Halkidou, Kalipso; Gnanapragasam, Vincent J.; Mehta, Piyush B.
- Oncogene, Vol. 22, Issue 16
Structure of the Chromo Barrel Domain from the MOF Acetyltransferase
journal, June 2005
- Nielsen, Peter R.; Nietlispach, Daniel; Buscaino, Alessia
- Journal of Biological Chemistry, Vol. 280, Issue 37
Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27
journal, August 2003
- Min, J.
- Genes & Development, Vol. 17, Issue 15
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Works referencing / citing this record:
Family-Wide Characterization of Histone Binding Abilities of PHD Domains of AL Proteins in Arabidopsis thaliana
journal, September 2018
- Liang, Xiao; Lei, Ming; Li, Fangzhou
- The Protein Journal, Vol. 37, Issue 6