Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes
Abstract
Abstract McrBC complexes are motor-driven nucleases functioning in bacterial self-defense by cleaving foreign DNA. The GTP-specific AAA + protein McrB powers translocation along DNA and its hydrolysis activity is stimulated by its partner nuclease McrC. Here, we report cryo-EM structures of Thermococcus gammatolerans McrB and McrBC, and E. coli McrBC. The McrB hexamers, containing the necessary catalytic machinery for basal GTP hydrolysis, are intrinsically asymmetric. This asymmetry directs McrC binding so that it engages a single active site, where it then uses an arginine/lysine-mediated hydrogen-bonding network to reposition the asparagine in the McrB signature motif for optimal catalytic function. While the two McrBC complexes use different DNA-binding domains, these contribute to the same general GTP-recognition mechanism employed by all G proteins. Asymmetry also induces distinct inter-subunit interactions around the ring, suggesting a coordinated and directional GTP-hydrolysis cycle. Our data provide insights into the conserved molecular mechanisms governing McrB family AAA + motors.
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); Office of Research Infrastructure Programs (ORIP); USDOE Office of Science (SC)
- OSTI Identifier:
- 1833741
- Alternate Identifier(s):
- OSTI ID: 1763102
- Grant/Contract Number:
- AC02-06CH11357; GM120242; S10 RR029205
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cryoelectron microscopy; DNA-binding proteins; DNA restriction-modification enzymes; GTP-binding protein regulators; Hydrolases
Citation Formats
Niu, Yiming, Suzuki, Hiroshi, Hosford, Christopher J., Walz, Thomas, and Chappie, Joshua S. Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-19735-4.
Niu, Yiming, Suzuki, Hiroshi, Hosford, Christopher J., Walz, Thomas, & Chappie, Joshua S. Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes. United Kingdom. https://doi.org/10.1038/s41467-020-19735-4
Niu, Yiming, Suzuki, Hiroshi, Hosford, Christopher J., Walz, Thomas, and Chappie, Joshua S. Fri .
"Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes". United Kingdom. https://doi.org/10.1038/s41467-020-19735-4.
@article{osti_1833741,
title = {Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes},
author = {Niu, Yiming and Suzuki, Hiroshi and Hosford, Christopher J. and Walz, Thomas and Chappie, Joshua S.},
abstractNote = {Abstract McrBC complexes are motor-driven nucleases functioning in bacterial self-defense by cleaving foreign DNA. The GTP-specific AAA + protein McrB powers translocation along DNA and its hydrolysis activity is stimulated by its partner nuclease McrC. Here, we report cryo-EM structures of Thermococcus gammatolerans McrB and McrBC, and E. coli McrBC. The McrB hexamers, containing the necessary catalytic machinery for basal GTP hydrolysis, are intrinsically asymmetric. This asymmetry directs McrC binding so that it engages a single active site, where it then uses an arginine/lysine-mediated hydrogen-bonding network to reposition the asparagine in the McrB signature motif for optimal catalytic function. While the two McrBC complexes use different DNA-binding domains, these contribute to the same general GTP-recognition mechanism employed by all G proteins. Asymmetry also induces distinct inter-subunit interactions around the ring, suggesting a coordinated and directional GTP-hydrolysis cycle. Our data provide insights into the conserved molecular mechanisms governing McrB family AAA + motors.},
doi = {10.1038/s41467-020-19735-4},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Fri Nov 20 00:00:00 EST 2020},
month = {Fri Nov 20 00:00:00 EST 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-020-19735-4
https://doi.org/10.1038/s41467-020-19735-4
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Bacteriophage resistance mechanisms
journal, March 2010
- Labrie, Simon J.; Samson, Julie E.; Moineau, Sylvain
- Nature Reviews Microbiology, Vol. 8, Issue 5
Fundamental Characteristics of AAA+ Protein Family Structure and Function
journal, January 2016
- Miller, Justin M.; Enemark, Eric J.
- Archaea, Vol. 2016
Molecular Organization of Intrinsic Restriction and Modification Genes BsuM of Bacillus subtilis Marburg
journal, January 2002
- Ohshima, Hideyuki; Matsuoka, Satoshi; Asai, Kei
- Journal of Bacteriology, Vol. 184, Issue 2
Structure of the EndoMS-DNA Complex as Mismatch Restriction Endonuclease
journal, November 2016
- Nakae, Setsu; Hijikata, Atsushi; Tsuji, Toshiyuki
- Structure, Vol. 24, Issue 11
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
The rotary mechanism of ATP synthase
journal, December 2000
- Stock, Daniela; Gibbons, Clyde; Arechaga, Ignacio
- Current Opinion in Structural Biology, Vol. 10, Issue 6
Development and Use of Personalized Bacteriophage-Based Therapeutic Cocktails To Treat a Patient with a Disseminated Resistant Acinetobacter baumannii Infection
journal, August 2017
- Schooley, Robert T.; Biswas, Biswajit; Gill, Jason J.
- Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 10
Realm of PD-(D/E)XK nuclease superfamily revisited: detection of novel families with modified transitive meta profile searches
journal, January 2007
- Knizewski, Lukasz; Kinch, Lisa N.; Grishin, Nick V.
- BMC Structural Biology, Vol. 7, Issue 1
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Structural insights into ATP hydrolysis by the MoxR ATPase RavA and the LdcI-RavA cage-like complex
journal, January 2020
- Jessop, Matthew; Arragain, Benoit; Miras, Roger
- Communications Biology, Vol. 3, Issue 1
I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010
- Roy, Ambrish; Kucukural, Alper; Zhang, Yang
- Nature Protocols, Vol. 5, Issue 4
Ratchet-like polypeptide translocation mechanism of the AAA+ disaggregase Hsp104
journal, June 2017
- Gates, Stephanie N.; Yokom, Adam L.; Lin, JiaBei
- Science, Vol. 357, Issue 6348
The Biology of CRISPR-Cas: Backward and Forward
journal, March 2018
- Hille, Frank; Richter, Hagen; Wong, Shi Pey
- Cell, Vol. 172, Issue 6
Evolutionary Relationships and Structural Mechanisms of aaa+ Proteins
journal, June 2006
- Erzberger, Jan P.; Berger, James M.
- Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1
McrBC: a multisubunit GTP-dependent restriction endonuclease
journal, May 1992
- Sutherland, Ellen; Coe, Linda; Raleigh, Elisabeth A.
- Journal of Molecular Biology, Vol. 225, Issue 2
The GTP-Dependent Restriction Enzyme McrBC from Escherichia coli Forms High-Molecular Mass Complexes with DNA and Produces a Cleavage Pattern with a Characteristic 10-Base Pair Repeat †
journal, April 2002
- Pieper, Uwe; Groll, Detlef H.; Wünsch, Sandra
- Biochemistry, Vol. 41, Issue 16
The crystal structure of the Helicobacter pylori LlaJI.R1 N-terminal domain provides a model for site-specific DNA binding
journal, June 2018
- Hosford, Christopher J.; Chappie, Joshua S.
- Journal of Biological Chemistry, Vol. 293, Issue 30
A Bayesian approach to beam-induced motion correction in cryo-EM single-particle analysis
journal, January 2019
- Zivanov, Jasenko; Nakane, Takanori; Scheres, Sjors H. W.
- IUCrJ, Vol. 6, Issue 1
Characterization of the interaction between the restriction endonuclease McrBC from E. coli and its cofactor GTP
journal, September 1997
- Pieper, Uwe; Brinkmann, Thilo; Krüger, Torsten
- Journal of Molecular Biology, Vol. 272, Issue 2
GTP and ATP hydrolysis in biology
journal, May 2016
- Wittinghofer, Alfred
- Biopolymers, Vol. 105, Issue 8
The Ras-RasGAP Complex: Structural Basis for GTPase Activation and Its Loss in Oncogenic Ras Mutants
journal, July 1997
- Scheffzek, K.
- Science, Vol. 277, Issue 5324
New tools for automated high-resolution cryo-EM structure determination in RELION-3
journal, November 2018
- Zivanov, Jasenko; Nakane, Takanori; Forsberg, Björn O.
- eLife, Vol. 7
Revenge of the phages: defeating bacterial defences
journal, August 2013
- Samson, Julie E.; Magadán, Alfonso H.; Sabri, Mourad
- Nature Reviews Microbiology, Vol. 11, Issue 10
Mechanistic insights into the recycling machine of the SNARE complex
journal, January 2015
- Zhao, Minglei; Wu, Shenping; Zhou, Qiangjun
- Nature, Vol. 518, Issue 7537
Classification and evolution of P-loop GTPases and related ATPases
journal, March 2002
- Leipe, Detlef D.; Wolf, Yuri I.; Koonin, Eugene V.
- Journal of Molecular Biology, Vol. 317, Issue 1
Hexameric assembly of the AAA+ protein McrB is necessary for GTPase activity
journal, December 2018
- Nirwan, Neha; Singh, Pratima; Mishra, Gyana Gourab
- Nucleic Acids Research, Vol. 47, Issue 2
Crystal Structure of the YcjX Stress Protein Reveals a Ras-Like GTP-Binding Protein
journal, August 2019
- Tsai, Joshua T.; Sung, Nuri; Lee, Jungsoon
- Journal of Molecular Biology, Vol. 431, Issue 17
The I-TASSER Suite: protein structure and function prediction
journal, December 2014
- Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
- Nature Methods, Vol. 12, Issue 1
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
GEFs and GAPs: Critical Elements in the Control of Small G Proteins
journal, June 2007
- Bos, Johannes L.; Rehmann, Holger; Wittinghofer, Alfred
- Cell, Vol. 129, Issue 5
Mechanisms of Conformational Change for a Replicative Hexameric Helicase of SV40 Large Tumor Antigen
journal, October 2004
- Gai, Dahai; Zhao, Rui; Li, Dawei
- Cell, Vol. 119, Issue 1
ESCRT-III Family Members Stimulate Vps4 ATPase Activity Directly or via Vta1
journal, January 2008
- Azmi, Ishara F.; Davies, Brian A.; Xiao, Junyu
- Developmental Cell, Vol. 14, Issue 1
Gctf: Real-time CTF determination and correction
journal, January 2016
- Zhang, Kai
- Journal of Structural Biology, Vol. 193, Issue 1
Biosynthesis and Function of Modified Bases in Bacteria and Their Viruses
journal, May 2016
- Weigele, Peter; Raleigh, Elisabeth A.
- Chemical Reviews, Vol. 116, Issue 20
Structure of the mitochondrial inner membrane AAA+ protease YME1 gives insight into substrate processing
journal, November 2017
- Puchades, Cristina; Rampello, Anthony J.; Shin, Mia
- Science, Vol. 358, Issue 6363
Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy
journal, October 2003
- Rosenthal, Peter B.; Henderson, Richard
- Journal of Molecular Biology, Vol. 333, Issue 4
Restriction modification system analysis and development of in vivo methylation for the transformation of Clostridium cellulovorans
journal, November 2015
- Yang, Xiaorui; Xu, Mengmeng; Yang, Shang-Tian
- Applied Microbiology and Biotechnology, Vol. 100, Issue 5
Defining the Location and Function of Domains of McrB by Deletion Mutagenesis
journal, January 1999
- Pieper, Uwe; Schweitzer, Thomas; Groll, Detlef H.
- Biological Chemistry, Vol. 380, Issue 10
McrB: a prokaryotic protein specifically recognizing DNA containing modified cytosine residues.
journal, June 1995
- Krüger, T.; Wild, C.; Noyer-Weidner, M.
- The EMBO Journal, Vol. 14, Issue 11
Automatic protein structure solution from weak X-ray data
journal, November 2013
- Skubák, Pavol; Pannu, Navraj S.
- Nature Communications, Vol. 4, Issue 1
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
The Recognition of Methylated DNA by the GTP-Dependent Restriction Endonuclease McrBC Resides in the N-Terminal Domain of Mcr B
journal, January 1997
- Gast, Frank-Ulrich; Brinkmann, Thilo; Pieper, Uwe
- Biological Chemistry, Vol. 378, Issue 9
DNA translocation mechanism of the MCM complex and implications for replication initiation
journal, July 2019
- Meagher, Martin; Epling, Leslie B.; Enemark, Eric J.
- Nature Communications, Vol. 10, Issue 1
Characterisation of molecular motions in cryo-EM single-particle data by multi-body refinement in RELION
journal, June 2018
- Nakane, Takanori; Kimanius, Dari; Lindahl, Erik
- eLife, Vol. 7
The Rap–RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues
journal, February 2008
- Scrima, Andrea; Thomas, Christoph; Deaconescu, Delia
- The EMBO Journal, Vol. 27, Issue 7
Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase
journal, December 2003
- Iwata, M.; Imamura, H.; Stambouli, E.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 1
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification
journal, March 2010
- Sheldrick, George M.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
The recognition domain of the methyl-specific endonuclease McrBC flips out 5-methylcytosine
journal, May 2012
- Sukackaite, Rasa; Grazulis, Saulius; Tamulaitis, Gintautas
- Nucleic Acids Research, Vol. 40, Issue 15
The GTPase superfamily: conserved structure and molecular mechanism
journal, January 1991
- Bourne, Henry R.; Sanders, David A.; McCormick, Frank
- Nature, Vol. 349, Issue 6305
Katanin spiral and ring structures shed light on power stroke for microtubule severing
journal, August 2017
- Zehr, Elena; Szyk, Agnieszka; Piszczek, Grzegorz
- Nature Structural & Molecular Biology, Vol. 24, Issue 9
Recognition of modified cytosine variants by the DNA‐binding domain of methyl‐directed endonuclease McrBC
journal, September 2018
- Zagorskaitė, Evelina; Manakova, Elena; Sasnauskas, Giedrius
- FEBS Letters, Vol. 592, Issue 19
Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase
journal, April 2001
- Yasuda, Ryohei; Noji, Hiroyuki; Yoshida, Masasuke
- Nature, Vol. 410, Issue 6831
Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase
journal, April 2017
- Monroe, Nicole; Han, Han; Shen, Peter S.
- eLife, Vol. 6
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
journal, February 2017
- Punjani, Ali; Rubinstein, John L.; Fleet, David J.
- Nature Methods, Vol. 14, Issue 3
Substrate processing by the Cdc48 ATPase complex is initiated by ubiquitin unfolding
journal, June 2019
- Twomey, Edward C.; Ji, Zhejian; Wales, Thomas E.
- Science, Vol. 365, Issue 6452
Scalable web services for the PSIPRED Protein Analysis Workbench
journal, June 2013
- Buchan, Daniel W. A.; Minneci, Federico; Nugent, Tim C. O.
- Nucleic Acids Research, Vol. 41, Issue W1
DNA curvature and flexibility in vitro and in vivo
journal, February 2010
- Peters, Justin P.; Maher, L. James
- Quarterly Reviews of Biophysics, Vol. 43, Issue 1
AAA+: A Class of Chaperone-Like ATPases Associated with the Assembly, Operation, and Disassembly of Protein Complexes
journal, January 1999
- Neuwald, Andrew F.; Aravind, L.; Spouge, John L.
- Genome Research, Vol. 9, Issue 1
The AAA+ superfamily of functionally diverse proteins
journal, January 2008
- Snider, Jamie; Thibault, Guillaume; Houry, Walid A.
- Genome Biology, Vol. 9, Issue 4
Structure-based mechanism for activation of the AAA+ GTPase McrB by the endonuclease McrC
journal, July 2019
- Nirwan, Neha; Itoh, Yuzuru; Singh, Pratima
- Nature Communications, Vol. 10, Issue 1
A Mutational Analysis of the PD...D/EXK Motif Suggests That McrC Harbors the Catalytic Center for DNA Cleavage by the GTP-Dependent Restriction Enzyme McrBC from Escherichia coli †
journal, April 2002
- Pieper, Uwe; Pingoud, Alfred
- Biochemistry, Vol. 41, Issue 16
The SWISS-MODEL Repository—new features and functionality
journal, November 2016
- Bienert, Stefan; Waterhouse, Andrew; de Beer, Tjaart A. P.
- Nucleic Acids Research, Vol. 45, Issue D1
Conformational transitions and structural deformability of EcoRV endonuclease revealed by crystallographic analysis
journal, October 1997
- Perona, John J.; Martin, Amy M.
- Journal of Molecular Biology, Vol. 273, Issue 1
I-TASSER server: new development for protein structure and function predictions
journal, April 2015
- Yang, Jianyi; Zhang, Yang
- Nucleic Acids Research, Vol. 43, Issue W1
The GTP-binding Domain of McrB: More Than Just a Variation on a Common Theme?
journal, September 1999
- Pieper, Uwe; Schweitzer, Thomas; Groll, Detlef H.
- Journal of Molecular Biology, Vol. 292, Issue 3
The McrBC endonuclease translocates DNA in a reaction dependent on GTP hydrolysis 1 1Edited by J. Karn
journal, July 1999
- Panne, Daniel; Raleigh, Elisabeth A.; Bickle, Thomas A.
- Journal of Molecular Biology, Vol. 290, Issue 1
A Type IV Modification Dependent Restriction Nuclease that Targets Glucosylated Hydroxymethyl Cytosine Modified DNAs
journal, February 2007
- Bair, Catherine L.; Black, Lindsay W.
- Journal of Molecular Biology, Vol. 366, Issue 3
G domain dimerization controls dynamin's assembly-stimulated GTPase activity
journal, April 2010
- Chappie, Joshua S.; Acharya, Sharmistha; Leonard, Marilyn
- Nature, Vol. 465, Issue 7297
The McrBC restriction endonuclease assembles into a ring structure in the presence of G nucleotides
journal, June 2001
- Panne, D.
- The EMBO Journal, Vol. 20, Issue 12
CTFFIND4: Fast and accurate defocus estimation from electron micrographs
journal, November 2015
- Rohou, Alexis; Grigorieff, Nikolaus
- Journal of Structural Biology, Vol. 192, Issue 2
Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus
journal, May 2019
- Dedrick, Rebekah M.; Guerrero-Bustamante, Carlos A.; Garlena, Rebecca A.
- Nature Medicine, Vol. 25, Issue 5
Mechanism of DNA translocation in a replicative hexameric helicase
journal, July 2006
- Enemark, Eric J.; Joshua-Tor, Leemor
- Nature, Vol. 442, Issue 7100
Phage-Encoded Anti-CRISPR Defenses
journal, November 2018
- Stanley, Sabrina Y.; Maxwell, Karen L.
- Annual Review of Genetics, Vol. 52, Issue 1
Negative staining and image classification — powerful tools in modern electron microscopy
journal, January 2004
- Ohi, Melanie; Li, Ying; Cheng, Yifan
- Biological Procedures Online, Vol. 6, Issue 1
Mechanism localisation and control of restriction cleavage of phage T4 and λ chromosomes in vivo
journal, April 1976
- Dharmalingam, K.; Goldberg, Edward B.
- Nature, Vol. 260, Issue 5550
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
journal, February 2017
- Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul
- Nature Methods, Vol. 14, Issue 4
Scaling and assessment of data quality
journal, December 2005
- Evans, Philip
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82
SerialEM: A Program for Automated Tilt Series Acquisition on Tecnai Microscopes Using Prediction of Specimen Position
journal, July 2003
- Mastronarde, David N.
- Microscopy and Microanalysis, Vol. 9, Issue S02
Structure of a AAA+ unfoldase in the process of unfolding substrate
journal, April 2017
- Ripstein, Zev A.; Huang, Rui; Augustyniak, Rafal
- eLife, Vol. 6
Non-traditional Antibacterial Therapeutic Options and Challenges
journal, July 2019
- Theuretzbacher, Ursula; Piddock, Laura J. V.
- Cell Host & Microbe, Vol. 26, Issue 1
Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme
journal, May 2000
- Stewart, Fiona J.; Panne, Daniel; Bickle, Thomas A.
- Journal of Molecular Biology, Vol. 298, Issue 4
In vivo restriction by LlaI is encoded by three genes, arranged in an operon with llaIM, on the conjugative Lactococcus plasmid pTR2030.
journal, January 1995
- O'Sullivan, D. J.; Zagula, K.; Klaenhammer, T. R.
- Journal of bacteriology, Vol. 177, Issue 1
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM
journal, March 2011
- Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Invited review: Small GTPases and their GAPs
journal, May 2016
- Mishra, Ashwini K.; Lambright, David G.
- Biopolymers, Vol. 105, Issue 8
Structure of RGS4 Bound to AlF4−-Activated Giα1: Stabilization of the Transition State for GTP Hydrolysis
journal, April 1997
- Tesmer, John J. G.; Berman, David M.; Gilman, Alfred G.
- Cell, Vol. 89, Issue 2
Substrate-engaged 26 S proteasome structures reveal mechanisms for ATP-hydrolysis–driven translocation
journal, October 2018
- de la Peña, Andres H.; Goodall, Ellen A.; Gates, Stephanie N.
- Science, Vol. 362, Issue 6418
Phage Therapy: A Renewed Approach to Combat Antibiotic-Resistant Bacteria
journal, February 2019
- Kortright, Kaitlyn E.; Chan, Benjamin K.; Koff, Jonathan L.
- Cell Host & Microbe, Vol. 25, Issue 2
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
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
Nucleoside triphosphate-binding proteins: different scaffolds to achieve phosphoryl transfer
journal, February 1999
- Vetter, Ingrid R.; Wittinghofer, Alfred
- Quarterly Reviews of Biophysics, Vol. 32, Issue 1
A quantitative approach to data-collection strategies
journal, December 2005
- Bourenkov, Gleb P.; Popov, Alexander N.
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1
Crystallization and preliminary X-ray diffraction studies of Hje, a Holliday junction resolving enzyme from Sulfolobus solfataricus
journal, December 2002
- Middleton, Claire L.; Parker, Joanne L.; Richard, Derek J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 1
Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology
journal, November 2007
- Forgac, Michael
- Nature Reviews Molecular Cell Biology, Vol. 8, Issue 11
A Nonhereditary, Host-Induced Variation of Bacterial Viruses1
journal, January 1952
- Luria, S. E.; Human, Mary L.
- Journal of Bacteriology, Vol. 64, Issue 4
Structure of small G proteins and their regulators.
journal, December 2001
- Paduch, M.; Jeleń, F.; Otlewski, J.
- Acta Biochimica Polonica, Vol. 48, Issue 4
A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens
journal, August 2013
- Wittebole, Xavier; De Roock, Sophie; Opal, Steven M.
- Virulence, Vol. 5, Issue 1
Automated electron microscope tomography using robust prediction of specimen movements
journal, October 2005
- Mastronarde, David N.
- Journal of Structural Biology, Vol. 152, Issue 1
Evolutionary history and higher order classification of AAA+ ATPases
journal, April 2004
- Iyer, Lakshminarayan M.; Leipe, Detlef D.; Koonin, Eugene V.
- Journal of Structural Biology, Vol. 146, Issue 1-2
Structure and function of the AAA+ nucleotide binding pocket
journal, January 2012
- Wendler, Petra; Ciniawsky, Susanne; Kock, Malte
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 1