Structural and Dynamic Features of Acinetobacter baumannii OXA-66 β-Lactamase Explain Its Stability and Evolution of Novel Variants

Klamer, Zachary L.; June, Cynthia M.; Wawrzak, Zdzislaw; Taracila, Magdalena A.; Grey, Joshua A.; Benn, Alyssa M. I.; Russell, Christopher P.; Bonomo, Robert A.; Powers, Rachel A.; Leonard, David A.; Szarecka, Agnieszka

doi:10.1016/j.jmb.2024.168603

Title: Structural and Dynamic Features of Acinetobacter baumannii OXA-66 β-Lactamase Explain Its Stability and Evolution of Novel Variants

Journal Article · 31 May 2024 · Journal of Molecular Biology

DOI: https://doi.org/10.1016/j.jmb.2024.168603 · OSTI ID:2350995

; June, Cynthia M.; Wawrzak, Zdzislaw; Taracila, Magdalena A.; Grey, Joshua A.; Benn, Alyssa M. I.; Russell, Christopher P.; Bonomo, Robert A.; Powers, Rachel A.; Leonard, David A.;

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Sponsoring Organization:: USDOE

OSTI ID:: 2350995

Journal Information:: Journal of Molecular Biology, Journal Name: Journal of Molecular Biology Journal Issue: 12 Vol. 436; ISSN 0022-2836

Publisher:: ElsevierCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (65)

Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
ProDy: Protein Dynamics Inferred from Theory and Experiments Bakan, A.; Meireles, L. M.; Bahar, I. Bioinformatics, Vol. 27, Issue 11, p. 1575-1577 https://doi.org/10.1093/bioinformatics/btr168	journal	April 2011
Acinetobacter baumannii Antibiotic Resistance Mechanisms Kyriakidis, Ioannis; Vasileiou, Eleni; Pana, Zoi Dorothea Pathogens, Vol. 10, Issue 3 https://doi.org/10.3390/pathogens10030373	journal	March 2021
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Stability effects of mutations and protein evolvability Tokuriki, Nobuhiko; Tawfik, Dan S. Current Opinion in Structural Biology, Vol. 19, Issue 5 https://doi.org/10.1016/j.sbi.2009.08.003	journal	October 2009
Structural Basis for Enhancement of Carbapenemase Activity in the OXA-51 Family of Class D β-Lactamases Smith, Clyde A.; Antunes, Nuno Tiago; Stewart, Nichole K. ACS Chemical Biology, Vol. 10, Issue 8 https://doi.org/10.1021/acschembio.5b00090	journal	June 2015
Identification of Acinetobacter baumannii by Detection of the bla _OXA-51-like Carbapenemase Gene Intrinsic to This Species Turton, Jane F.; Woodford, Neil; Glover, Judith Journal of Clinical Microbiology, Vol. 44, Issue 8 https://doi.org/10.1128/JCM.01021-06	journal	August 2006
Software news and updates carma: A molecular dynamics analysis program Glykos, Nicholas M. Journal of Computational Chemistry, Vol. 27, Issue 14 https://doi.org/10.1002/jcc.20482	journal	January 2006
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Progress and Challenges in Implementing the Research on ESKAPE Pathogens Rice, Louis B. Infection Control & Hospital Epidemiology, Vol. 31, Issue S1 https://doi.org/10.1086/655995	journal	November 2010
OXA -Lactamases Evans, B. A.; Amyes, S. G. B. Clinical Microbiology Reviews, Vol. 27, Issue 2 https://doi.org/10.1128/CMR.00117-13	journal	April 2014
Acinetobacter baumannii: a universal threat to public health? Giamarellou, Helen; Antoniadou, Anastasia; Kanellakopoulou, Kyriaki International Journal of Antimicrobial Agents, Vol. 32, Issue 2 https://doi.org/10.1016/j.ijantimicag.2008.02.013	journal	August 2008
Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology Poirel, L.; Nordmann, P. Clinical Microbiology and Infection, Vol. 12, Issue 9 https://doi.org/10.1111/j.1469-0691.2006.01456.x	journal	September 2006
Structural insights into the enhanced carbapenemase efficiency of OXA‐655 compared to OXA‐10 Leiros, Hanna‐Kirsti S.; Thomassen, Ane Molden; Samuelsen, Ørjan FEBS Open Bio, Vol. 10, Issue 9 https://doi.org/10.1002/2211-5463.12935	journal	August 2020
Structures of the Class D Carbapenemase OXA-24 from Acinetobacter baumannii in Complex with Doripenem Schneider, Kyle D.; Ortega, Caleb J.; Renck, Nicholas A. Journal of Molecular Biology, Vol. 406, Issue 4 https://doi.org/10.1016/j.jmb.2010.12.042	journal	March 2011
The β-lactamase threat in Enterobacteriaceae, Pseudomonas and Acinetobacter Livermore, David M.; Woodford, Neil Trends in Microbiology, Vol. 14, Issue 9 https://doi.org/10.1016/j.tim.2006.07.008	journal	September 2006
OXA-235, a Novel Class D β-Lactamase Involved in Resistance to Carbapenems in Acinetobacter baumannii Higgins, Paul G.; Pérez-Llarena, Francisco J.; Zander, Esther Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 5 https://doi.org/10.1128/AAC.02413-12	journal	May 2013
Eleven novel OXA-51-like enzymes from clinical isolates of Acinetobacter baumannii Evans, B. A.; Brown, S.; Hamouda, A. Clinical Microbiology and Infection, Vol. 13, Issue 11 https://doi.org/10.1111/j.1469-0691.2007.01828.x	journal	November 2007
Crystal Structure of Carbapenemase OXA-58 from Acinetobacter baumannii Smith, Clyde A.; Antunes, Nuno Tiago; Toth, Marta Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 4 https://doi.org/10.1128/AAC.01983-13	journal	January 2014
Mapping the determinants of catalysis and substrate specificity of the antibiotic resistance enzyme CTX-M β-lactamase Judge, Allison; Hu, Liya; Sankaran, Banumathi Communications Biology, Vol. 6, Issue 1 https://doi.org/10.1038/s42003-023-04422-z	journal	January 2023
The structure of a doripenem-bound OXA-51 class D β-lactamase variant with enhanced carbapenemase activity: Structure of OXA-51 I129L with Doripenem Bound June, Cynthia M.; Muckenthaler, Taylor J.; Schroder, Emma C. Protein Science, Vol. 25, Issue 12 https://doi.org/10.1002/pro.3040	journal	September 2016
Role of the Hydrophobic Bridge in the Carbapenemase Activity of Class D β-Lactamases Stewart, Nichole K.; Smith, Clyde A.; Antunes, Nuno T. Antimicrobial Agents and Chemotherapy, Vol. 63, Issue 2 https://doi.org/10.1128/AAC.02191-18	journal	December 2018
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Crystal Structure of the OXA-48 β-Lactamase Reveals Mechanistic Diversity among Class D Carbapenemases Docquier, Jean-Denis; Calderone, Vito; De Luca, Filomena Chemistry & Biology, Vol. 16, Issue 5 https://doi.org/10.1016/j.chembiol.2009.04.010	journal	May 2009
Carbapenemases: Transforming Acinetobacter baumannii into a Yet More Dangerous Menace Ramirez, Maria Soledad; Bonomo, Robert A.; Tolmasky, Marcelo E. Biomolecules, Vol. 10, Issue 5 https://doi.org/10.3390/biom10050720	journal	May 2020
Functional and Structural Characterization of OXA-935, a Novel OXA-10-Family β-Lactamase from Pseudomonas aeruginosa Pincus, Nathan B.; Rosas-Lemus, Monica; Gatesy, Samuel W. M. Antimicrobial Agents and Chemotherapy, Vol. 66, Issue 10 https://doi.org/10.1128/aac.00985-22	journal	October 2022
Characterisation of OXA-51, a novel class D carbapenemase found in genetically unrelated clinical strains of Acinetobacter baumannii from Argentina Brown, S.; Young, H. K.; Amyes, S. G. B. Clinical Microbiology and Infection, Vol. 11, Issue 1 https://doi.org/10.1111/j.1469-0691.2004.01016.x	journal	January 2005
Calculation of protein extinction coefficients from amino acid sequence data Gill, Stanley C.; von Hippel, Peter H. Analytical Biochemistry, Vol. 182, Issue 2 https://doi.org/10.1016/0003-2697(89)90602-7	journal	November 1989
Urinary tract colonization is enhanced by a plasmid that regulates uropathogenic Acinetobacter baumannii chromosomal genes Di Venanzio, Gisela; Flores-Mireles, Ana L.; Calix, Juan J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10706-y	journal	June 2019
Structural Basis of Activity against Aztreonam and Extended Spectrum Cephalosporins for Two Carbapenem-Hydrolyzing Class D β-Lactamases from Acinetobacter baumannii Mitchell, Joshua M.; Clasman, Jozlyn R.; June, Cynthia M. Biochemistry, Vol. 54, Issue 10 https://doi.org/10.1021/bi501547k	journal	March 2015
Multiple Global Suppressors of Protein Stability Defects Facilitate the Evolution of Extended-Spectrum TEM β-Lactamases Brown, Nicholas G.; Pennington, Jeanine M.; Huang, Wanzhi Journal of Molecular Biology, Vol. 404, Issue 5 https://doi.org/10.1016/j.jmb.2010.10.008	journal	December 2010
How Protein Stability and New Functions Trade Off Tokuriki, Nobuhiko; Stricher, Francois; Serrano, Luis PLoS Computational Biology, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pcbi.1000002	journal	February 2008
Characterization of the Naturally Occurring Oxacillinase ofAcinetobacter baumannii Héritier, Claire; Poirel, Laurent; Fournier, Pierre-Edouard Antimicrobial Agents and Chemotherapy, Vol. 49, Issue 10 https://doi.org/10.1128/AAC.49.10.4174-4179.2005	journal	October 2005
OXA-23 β-Lactamase Overexpression in Acinetobacter baumannii Drives Physiological Changes Resulting in New Genetic Vulnerabilities Colquhoun, Jennifer M.; Farokhyfar, Marjan; Hutcheson, Anna R. mBio, Vol. 12, Issue 6 https://doi.org/10.1128/mBio.03137-21	journal	December 2021
Arginine Modulates Carbapenem Deactivation by OXA-24/40 in Acinetobacter baumannii VanPelt, Jamie; Stoffel, Shannon; Staude, Michael W. Journal of Molecular Biology, Vol. 433, Issue 19 https://doi.org/10.1016/j.jmb.2021.167150	journal	September 2021
Nosocomial outbreaks caused by Acinetobacter baumannii and Pseudomonas aeruginosa: Results of a systematic review Wieland, Katja; Chhatwal, Patrick; Vonberg, Ralf-Peter American Journal of Infection Control, Vol. 46, Issue 6 https://doi.org/10.1016/j.ajic.2017.12.014	journal	June 2018
Confronting multidrug-resistant Acinetobacter baumannii: a review Neonakis, Ioannis K.; Spandidos, Demetrios A.; Petinaki, Efthimia International Journal of Antimicrobial Agents, Vol. 37, Issue 2 https://doi.org/10.1016/j.ijantimicag.2010.10.014	journal	February 2011
Conformational stability of OXA-51 β-lactamase explains its role in carbapenem resistance ofAcinetobacter baumannii Tiwari, Vishvanath; Moganty, Rajeswari R. Journal of Biomolecular Structure and Dynamics, Vol. 32, Issue 9 https://doi.org/10.1080/07391102.2013.819789	journal	July 2013
OXA-51-like β-lactamases and their association with particular epidemic lineages of Acinetobacter baumannii Evans, B. A.; Hamouda, A.; Towner, K. J. Clinical Microbiology and Infection, Vol. 14, Issue 3 https://doi.org/10.1111/j.1469-0691.2007.01919.x	journal	March 2008
Tn2008-driven carbapenem resistance in Acinetobacter baumannii isolates from a period of increased incidence of infections in a Southwest Virginia hospital (USA) Rao, Jayasimha; Susanti, Dwi; Childress, Johnathon C. Journal of Global Antimicrobial Resistance, Vol. 12 https://doi.org/10.1016/j.jgar.2017.08.017	journal	March 2018
Carbapenem-Hydrolyzing GES-Type Extended-Spectrum β-Lactamase in Acinetobacter baumannii Bonnin, Rémy A.; Nordmann, Patrice; Potron, Anaïs Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 1 https://doi.org/10.1128/AAC.00773-10	journal	January 2011
Diversity, Epidemiology, and Genetics of Class D -Lactamases Poirel, L.; Naas, T.; Nordmann, P. Antimicrobial Agents and Chemotherapy, Vol. 54, Issue 1 https://doi.org/10.1128/AAC.01512-08	journal	August 2009
The CCP4 suite programs for protein crystallography Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology Feig, Michael; Karanicolas, John; Brooks, Charles L. Journal of Molecular Graphics and Modelling, Vol. 22, Issue 5 https://doi.org/10.1016/j.jmgm.2003.12.005	journal	May 2004
Common Clinical Substitutions Enhance the Carbapenemase Activity of OXA-51-Like Class D β-Lactamases from Acinetobacter spp. Mitchell, Joshua M.; Leonard, David A. Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 11 https://doi.org/10.1128/AAC.03651-14	journal	August 2014
Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C. Journal of Computational Physics, Vol. 23, Issue 3 https://doi.org/10.1016/0021-9991(77)90098-5	journal	March 1977
Crystal Structure of OXA-58 with the Substrate-Binding Cleft in a Closed State: Insights into the Mobility and Stability of the OXA-58 Structure Saino, Hiromichi; Sugiyabu, Tomohiro; Ueno, Go PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0145869	journal	December 2015
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Crystal structure of the carbapenemase OXA-24 reveals insights into the mechanism of carbapenem hydrolysis Santillana, E.; Beceiro, A.; Bou, G. Proceedings of the National Academy of Sciences, Vol. 104, Issue 13 https://doi.org/10.1073/pnas.0607557104	journal	March 2007
Variability in carbapenemase activity of intrinsic OxaAb (OXA-51-like) β-lactamase enzymes inAcinetobacter baumannii Takebayashi, Yuiko; Findlay, Jacqueline; Heesom, Kate J. Journal of Antimicrobial Chemotherapy, Vol. 76, Issue 3 https://doi.org/10.1093/jac/dkaa502	journal	December 2020
Molecular Dynamics at the Root of Expansion of Function in the M69L Inhibitor-Resistant TEM β-Lactamase from Escherichia c oli Meroueh, Samy O.; Roblin, Pierre; Golemi, Dasantila Journal of the American Chemical Society, Vol. 124, Issue 32 https://doi.org/10.1021/ja026547q	journal	July 2002
Clinical Variants of the Native Class D β-Lactamase of Acinetobacter baumannii Pose an Emerging Threat through Increased Hydrolytic Activity against Carbapenems Schroder, Emma C.; Klamer, Zachary L.; Saral, Aysegul Antimicrobial Agents and Chemotherapy, Vol. 60, Issue 10 https://doi.org/10.1128/AAC.01277-16	journal	August 2016
Systematic mutagenesis of the active site omega loop of TEM-1 beta-lactamase Petrosino, J. F.; Palzkill, T. Journal of Bacteriology, Vol. 178, Issue 7 https://doi.org/10.1128/jb.178.7.1821-1828.1996	journal	April 1996
Natural Variants of the KPC-2 Carbapenemase have Evolved Increased Catalytic Efficiency for Ceftazidime Hydrolysis at the Cost of Enzyme Stability Mehta, Shrenik C.; Rice, Kacie; Palzkill, Timothy PLOS Pathogens, Vol. 11, Issue 6 https://doi.org/10.1371/journal.ppat.1004949	journal	June 2015
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii: Role of ISAba1 in expression of OXA carbapenemase genes Turton, Jane F.; Ward, M. Elaina; Woodford, Neil FEMS Microbiology Letters, Vol. 258, Issue 1 https://doi.org/10.1111/j.1574-6968.2006.00195.x	journal	May 2006
Multidrug ResistantAcinetobacter baumanii: A 15-Year Trend Analysis Russell, Dana L.; Uslan, Daniel Z.; Rubin, Zachary A. Infection Control & Hospital Epidemiology, Vol. 39, Issue 5 https://doi.org/10.1017/ice.2018.52	journal	March 2018
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
blaOXA-51-type β-lactamase genes are ubiquitous and vary within a strain in Acinetobacter baumannii Merkier, Andrea Karina; Centrón, Daniela International Journal of Antimicrobial Agents, Vol. 28, Issue 2 https://doi.org/10.1016/j.ijantimicag.2006.03.023	journal	August 2006
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
Structures of the Class D Carbapenemases OXA-23 and OXA-146: Mechanistic Basis of Activity against Carbapenems, Extended-Spectrum Cephalosporins, and Aztreonam Kaitany, Kip-Chumba J.; Klinger, Neil V.; June, Cynthia M. Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 10 https://doi.org/10.1128/AAC.00762-13	journal	July 2013

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