Structure of HhaI endonuclease with cognate DNA at an atomic resolution of 1.0 Å
Abstract
HhaI, a Type II restriction endonuclease, recognizes the symmetric sequence 5'-GCG↓C-3' in duplex DNA and cleaves (‘↓’) to produce fragments with 2-base, 3'-overhangs. We determined the structure of HhaI in complex with cognate DNA at an ultra-high atomic resolution of 1.0 Å. Most restriction enzymes act as dimers with two catalytic sites, and cleave the two strands of duplex DNA simultaneously, in a single binding event. HhaI, in contrast, acts as a monomer with only one catalytic site, and cleaves the DNA strands sequentially, one after the other. HhaI comprises three domains, each consisting of a mixed five-stranded β sheet with a defined function. The first domain contains the catalytic-site; the second contains residues for sequence recognition; and the third contributes to non-specific DNA binding. The active-site belongs to the ‘PD-D/EXK’ superfamily of nucleases and contains the motif SD-X11-EAK. The first two domains are similar in structure to two other monomeric restriction enzymes, HinP1I (G↓CGC) and MspI (C↓CGG), which produce fragments with 5'-overhangs. The third domain, present only in HhaI, shifts the positions of the recognition residues relative to the catalytic site enabling this enzyme to cleave the recognition sequence at a different position. The structure of M.HhaI, the biologicalmore »
- Authors:
-
- Univ. of Texas, Houston, TX (United States). Anderson Cancer Center
- New England Biolabs, Inc., Ipswich, MA (United States)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1603149
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 48; Journal Issue: 3; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Horton, John R., Yang, Jie, Zhang, Xing, Petronzio, Theresa, Fomenkov, Alexey, Wilson, Geoffrey G., Roberts, Richard J., and Cheng, Xiaodong. Structure of HhaI endonuclease with cognate DNA at an atomic resolution of 1.0 Å. United States: N. p., 2019.
Web. doi:10.1093/nar/gkz1195.
Horton, John R., Yang, Jie, Zhang, Xing, Petronzio, Theresa, Fomenkov, Alexey, Wilson, Geoffrey G., Roberts, Richard J., & Cheng, Xiaodong. Structure of HhaI endonuclease with cognate DNA at an atomic resolution of 1.0 Å. United States. https://doi.org/10.1093/nar/gkz1195
Horton, John R., Yang, Jie, Zhang, Xing, Petronzio, Theresa, Fomenkov, Alexey, Wilson, Geoffrey G., Roberts, Richard J., and Cheng, Xiaodong. Fri .
"Structure of HhaI endonuclease with cognate DNA at an atomic resolution of 1.0 Å". United States. https://doi.org/10.1093/nar/gkz1195. https://www.osti.gov/servlets/purl/1603149.
@article{osti_1603149,
title = {Structure of HhaI endonuclease with cognate DNA at an atomic resolution of 1.0 Å},
author = {Horton, John R. and Yang, Jie and Zhang, Xing and Petronzio, Theresa and Fomenkov, Alexey and Wilson, Geoffrey G. and Roberts, Richard J. and Cheng, Xiaodong},
abstractNote = {HhaI, a Type II restriction endonuclease, recognizes the symmetric sequence 5'-GCG↓C-3' in duplex DNA and cleaves (‘↓’) to produce fragments with 2-base, 3'-overhangs. We determined the structure of HhaI in complex with cognate DNA at an ultra-high atomic resolution of 1.0 Å. Most restriction enzymes act as dimers with two catalytic sites, and cleave the two strands of duplex DNA simultaneously, in a single binding event. HhaI, in contrast, acts as a monomer with only one catalytic site, and cleaves the DNA strands sequentially, one after the other. HhaI comprises three domains, each consisting of a mixed five-stranded β sheet with a defined function. The first domain contains the catalytic-site; the second contains residues for sequence recognition; and the third contributes to non-specific DNA binding. The active-site belongs to the ‘PD-D/EXK’ superfamily of nucleases and contains the motif SD-X11-EAK. The first two domains are similar in structure to two other monomeric restriction enzymes, HinP1I (G↓CGC) and MspI (C↓CGG), which produce fragments with 5'-overhangs. The third domain, present only in HhaI, shifts the positions of the recognition residues relative to the catalytic site enabling this enzyme to cleave the recognition sequence at a different position. The structure of M.HhaI, the biological methyltransferase partner of HhaI, was determined earlier. Together, these two structures represent the first natural pair of restriction-modification enzymes to be characterized in atomic detail.},
doi = {10.1093/nar/gkz1195},
journal = {Nucleic Acids Research},
number = 3,
volume = 48,
place = {United States},
year = {2019},
month = {12}
}
Works referenced in this record:
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, November 2014
- Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
- Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299
PvuII endonuclease contains two calcium ions in active sites11Edited by A. R. Fersht
journal, July 2000
- Horton, John R.; Cheng, Xiaodong
- Journal of Molecular Biology, Vol. 300, Issue 5
Electron diffraction and the hydrogen atom
journal, January 2017
- McCusker, Lynne B.
- Science, Vol. 355, Issue 6321
Structure of PvuII endonuclease with cognate DNA.
journal, September 1994
- Cheng, X.; Balendiran, K.; Schildkraut, I.
- The EMBO Journal, Vol. 13, Issue 17
Crystal structure and mechanism of action of the N6-methyladenine-dependent type IIM restriction endonuclease R.DpnI
journal, June 2012
- Siwek, Wojciech; Czapinska, Honorata; Bochtler, Matthias
- Nucleic Acids Research, Vol. 40, Issue 15
Modification-dependent restriction endonuclease, MspJI, flips 5-methylcytosine out of the DNA helix
journal, September 2014
- Horton, John R.; Wang, Hua; Mabuchi, Megumu Yamada
- Nucleic Acids Research, Vol. 42, Issue 19
Crystal Structure ofCitrobacter freundiiRestriction EndonucleaseCfr10I at 2.15 Å Resolution
journal, January 1996
- Bozic, Damir; Grazulis, Saulius; Siksnys, Virginijus
- Journal of Molecular Biology, Vol. 255, Issue 1
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, October 2009
- Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
- Nucleic Acids Research, Vol. 38, Issue suppl_1
Structure of restriction endonuclease BamHI and its relationship to EcoRI
journal, April 1994
- Newman, M.; Strzelecka, T.; Dorner, L. F.
- Nature, Vol. 368, Issue 6472
Crystal structure of restriction endonuclease BglI bound to its interrupted DNA recognition sequence
journal, September 1998
- Newman, Matthew; Lunnen, Keith; Wilson, Geoffrey
- The EMBO Journal, Vol. 17, Issue 18
Restriction endonuclease MvaI is a monomer that recognizes its target sequence asymmetrically
journal, March 2007
- Kaus-Drobek, Magdalena; Czapinska, Honorata; Sokołowska, Monika
- Nucleic Acids Research, Vol. 35, Issue 6
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
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013
- Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
- Nature Methods, Vol. 10, Issue 6
Refinement of Eco RI endonuclease crystal structure: a revised protein chain tracing
journal, September 1990
- Kim, Y.; Grable, J.; Love, R.
- Science, Vol. 249, Issue 4974
Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012
- Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
Sau 3AI, a Monomeric Type II Restriction Endonuclease That Dimerizes on the DNA and Thereby Induces DNA Loops
journal, April 2001
- Friedhoff, Peter; Lurz, Rudi; Lüder, Gerhild
- Journal of Biological Chemistry, Vol. 276, Issue 26
A specific endonuclease from Haemophilus haemolyticus
journal, May 1976
- Roberts, Richard J.; Myers, Phyllis A.; Morrison, Alan
- Journal of Molecular Biology, Vol. 103, Issue 1
The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015
- Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
- Nature Protocols, Vol. 10, Issue 6
The crystal structure of EcoRV endonuclease and of its complexes with cognate and non-cognate DNA fragments.
journal, May 1993
- Winkler, F. K.; Banner, D. W.; Oefner, C.
- The EMBO Journal, Vol. 12, Issue 5
UbaLAI is a monomeric Type IIE restriction enzyme
text, January 2017
- Sasnauskas, Giedrius; Tamulaitienė, Giedrė; Tamulaitis, Gintautas
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
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
A public database of macromolecular diffraction experiments
journal, October 2016
- Grabowski, Marek; Langner, Karol M.; Cymborowski, Marcin
- Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 11
Structure and cleavage activity of the tetrameric MspJI DNA modification-dependent restriction endonuclease
journal, July 2012
- Horton, John R.; Mabuchi, Megumu Yamada; Cohen-Karni, Devora
- Nucleic Acids Research, Vol. 40, Issue 19
Structure of HinP1I endonuclease reveals a striking similarity to the monomeric restriction enzyme MspI
journal, March 2005
- Yang, Z.
- Nucleic Acids Research, Vol. 33, Issue 6
RefSeq: an update on prokaryotic genome annotation and curation
journal, November 2017
- Haft, Daniel H.; DiCuccio, Michael; Badretdin, Azat
- Nucleic Acids Research, Vol. 46, Issue D1
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard
journal, May 2009
- Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6
Cloning of restriction and modification genes in E. coli: The HhaII system from Haemophilus haemolyticus
journal, April 1978
- Mann, Michael B.; Nagaraja Rao, R.; Smith, H. O.
- Gene, Vol. 3, Issue 2
Cloning of the HhaI and HinPI restriction-modification systems
journal, December 1988
- Barsomian, Janet M.; Card, Charles O.; Wilson, Geoffrey G.
- Gene, Vol. 74, Issue 1
Carbon-Oxygen Hydrogen Bonding in Biological Structure and Function
journal, October 2012
- Horowitz, Scott; Trievel, Raymond C.
- Journal of Biological Chemistry, Vol. 287, Issue 50
UbaLAI is a monomeric Type IIE restriction enzyme
journal, July 2017
- Sasnauskas, Giedrius; Tamulaitienė, Giedrė; Tamulaitis, Gintautas
- Nucleic Acids Research, Vol. 45, Issue 16
Allosteric Regulation of DNA Cleavage and Sequence-Specificity through Run-On Oligomerization
journal, October 2013
- Lyumkis, Dmitry; Talley, Heather; Stewart, Andrew
- Structure, Vol. 21, Issue 10
NCBI prokaryotic genome annotation pipeline
journal, June 2016
- Tatusova, Tatiana; DiCuccio, Michael; Badretdin, Azat
- Nucleic Acids Research, Vol. 44, Issue 14
Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing
journal, December 2011
- Clark, Tyson A.; Murray, Iain A.; Morgan, Richard D.
- Nucleic Acids Research, Vol. 40, Issue 4
DNA nicking by HinP1I endonuclease: bending, base flipping and minor groove expansion
journal, February 2006
- Horton, J. R.
- Nucleic Acids Research, Vol. 34, Issue 3
Target site cleavage by the monomeric restriction enzyme BcnI requires translocation to a random DNA sequence and a switch in enzyme orientation
journal, July 2011
- Sasnauskas, Giedrius; Kostiuk, Georgij; Tamulaitis, Gintautas
- Nucleic Acids Research, Vol. 39, Issue 20
Type II restriction endonucleases—a historical perspective and more
journal, May 2014
- Pingoud, Alfred; Wilson, Geoffrey G.; Wende, Wolfgang
- Nucleic Acids Research, Vol. 42, Issue 12
A view of consecutive binding events from structures of tetrameric endonuclease Sfi I bound to DNA : The structure of
journal, November 2005
- Vanamee, Éva Scheuring; Viadiu, Hector; Kucera, Rebecca
- The EMBO Journal, Vol. 24, Issue 23
Structural basis of the methylation specificity of R.DpnI
journal, June 2014
- Mierzejewska, Karolina; Siwek, Wojciech; Czapinska, Honorata
- Nucleic Acids Research, Vol. 42, Issue 13
Degenerate sequence recognition by the monomeric restriction enzyme: single mutation converts BcnI into a strand-specific nicking endonuclease
journal, January 2011
- Kostiuk, Georgij; Sasnauskas, Giedrius; Tamulaitiene, Giedre
- Nucleic Acids Research, Vol. 39, Issue 9
Two crystal forms of the restriction enzyme MspI-DNA complex show the same novel structure
journal, October 2005
- Xu, Qian Steven; Roberts, Richard J.; Guo, Hwai-Chen
- Protein Science, Vol. 14, Issue 10
Structural basis for human PRDM9 action at recombination hot spots
journal, February 2016
- Patel, Anamika; Horton, John R.; Wilson, Geoffrey G.
- Genes & Development, Vol. 30, Issue 3
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Monomeric Restriction Endonuclease BcnI in the Apo Form and in an Asymmetric Complex with Target DNA
journal, June 2007
- Sokolowska, Monika; Kaus-Drobek, Magdalena; Czapinska, Honorata
- Journal of Molecular Biology, Vol. 369, Issue 3
How restriction enzymes became the workhorses of molecular biology
journal, April 2005
- Roberts, R. J.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
Direct detection of DNA methylation during single-molecule, real-time sequencing
journal, May 2010
- Flusberg, Benjamin A.; Webster, Dale R.; Lee, Jessica H.
- Nature Methods, Vol. 7, Issue 6
Cloning, sequencing, in vivo promoter mapping, and expression in Escherichia coli of the gene for the HhaI methyltransferase.
journal, April 1987
- Caserta, M.; Zacharias, W.; Nwankwo, D.
- Journal of Biological Chemistry, Vol. 262, Issue 10
IND-enzymes: a repository for hydrolytic enzymes derived from thermophilic and psychrophilic bacterial species with potential industrial usage
journal, May 2021
- Sunny, Jithin S.; Nisha, Khairun; Natarajan, Anuradha
- Extremophiles, Vol. 25, Issue 4
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard.
text, January 2009
- Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy
- Apollo - University of Cambridge Repository