Class D β-lactamases do exist in Gram-positive bacteria

Toth, Marta; Antunes, Nuno Tiago; Stewart, Nichole K.; Frase, Hilary; Bhattacharya, Monolekha; Smith, Clyde A.; Vakulenko, Sergei B.

doi:10.1038/nchembio.1950

Title: Class D β-lactamases do exist in Gram-positive bacteria

Journal Article · Mon Nov 09 00:00:00 EST 2015 · Nature Chemical Biology

DOI:https://doi.org/10.1038/nchembio.1950· OSTI ID:1257221

Toth, Marta ^[1]; Antunes, Nuno Tiago ^[1]; Stewart, Nichole K. ^[1]; Frase, Hilary ^[1]; Bhattacharya, Monolekha ^[1]; Smith, Clyde A. ^[2]; Vakulenko, Sergei B. ^[1]

Univ. of Notre Dame, IN (United States). Dept. of Chemistry and Biochemistry
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Production of β-lactamases of one of four molecular classes (A, B, C and D) is the major mechanism of bacterial resistance to β-lactams, the largest class of antibiotics, which have saved countless lives since their inception 70 years ago. Although several hundred efficient class D enzymes have been identified in Gram-negative pathogens over the last four decades, none have been reported in Gram-positive bacteria. Here we demonstrate that efficient class D β-lactamases capable of hydrolyzing a wide array of β-lactam substrates are widely disseminated in various species of environmental Gram-positive organisms. Class D enzymes of Gram-positive bacteria have a distinct structural architecture and employ a unique substrate-binding mode that is quite different from that of all currently known class A, C and D β-lactamases. In conclusion, these enzymes thus constitute a previously unknown reservoir of novel antibiotic-resistance enzymes.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; P41GM103393

OSTI ID:: 1257221

Journal Information:: Nature Chemical Biology, Vol. 12, Issue 1; ISSN 1552-4450

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 47 works

Citation information provided by
Web of Science

References (47)

Structures of Ceftazidime and Its Transition-State Analogue in Complex with AmpC β-Lactamase: Implications for Resistance Mutations and Inhibitor Design ^† ^, ^‡ Powers, Rachel A.; Caselli, Emilia; Focia, Pamela J. Biochemistry, Vol. 40, Issue 31 https://doi.org/10.1021/bi0109358	journal	August 2001
The ybxI Gene of Bacillus subtilis 168 Encodes a Class D -Lactamase of Low Activity Colombo, M. -L.; Hanique, S.; Baurin, S. L. Antimicrobial Agents and Chemotherapy, Vol. 48, Issue 2 https://doi.org/10.1128/AAC.48.2.484-490.2004	journal	January 2004
OXA-type carbapenemases Walther-Rasmussen, Jan; Høiby, Niels Journal of Antimicrobial Chemotherapy, Vol. 57, Issue 3 https://doi.org/10.1093/jac/dki482	journal	January 2006
Analysis of the plasticity of location of the Arg244 positive charge within the active site of the TEM-1 β-lactamase Marciano, David C.; Brown, Nicholas G.; Palzkill, Timothy Protein Science, Vol. 18, Issue 10 https://doi.org/10.1002/pro.220	journal	October 2009
Probing Active Site Chemistry in SHV β-Lactamase Variants at Ambler Position 244: UNDERSTANDING UNIQUE PROPERTIES OF INHIBITOR RESISTANCE Thomson, Jodi M.; Distler, Anne M.; Prati, Fabio Journal of Biological Chemistry, Vol. 281, Issue 36 https://doi.org/10.1074/jbc.M603222200	journal	June 2006
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
Crystal structures of the class D β-lactamase OXA-13 in the native form and in complex with meropenem Pernot, Lucile; Frénois, Frédéric; Rybkine, Tania Journal of Molecular Biology, Vol. 310, Issue 4 https://doi.org/10.1006/jmbi.2001.4805	journal	July 2001
The Oxyanion Hole in Serine β-Lactamase Catalysis: Interactions of Thiono Substrates with the Active Site Curley, Kieran; Pratt, R. F. Bioorganic Chemistry, Vol. 28, Issue 6 https://doi.org/10.1006/bioo.2000.1184	journal	December 2000
Critical involvement of a carbamylated lysine in catalytic function of class D -lactamases Golemi, D.; Maveyraud, L.; Vakulenko, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 25 https://doi.org/10.1073/pnas.241442898	journal	November 2001
An Antibiotic-Resistance Enzyme from a Deep-Sea Bacterium Toth, Marta; Smith, Clyde; Frase, Hilary Journal of the American Chemical Society, Vol. 132, Issue 2 https://doi.org/10.1021/ja908850p	journal	January 2010
Structural Basis for Carbapenemase Activity of the OXA-23 β-Lactamase from Acinetobacter baumannii Smith, Clyde A.; Antunes, Nuno Tiago; Stewart, Nichole K. Chemistry & Biology, Vol. 20, Issue 9 https://doi.org/10.1016/j.chembiol.2013.07.015	journal	September 2013
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
The First Structural and Mechanistic Insights for Class D β-Lactamases: Evidence for a Novel Catalytic Process for Turnover of β-Lactam Antibiotics Golemi, Dasantila; Maveyraud, Laurent; Vakulenko, Sergei Journal of the American Chemical Society, Vol. 122, Issue 25 https://doi.org/10.1021/ja0013881	journal	June 2000
The Structure of <latex>$\beta$</latex>-Lactamases Ambler, R. P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 289, Issue 1036 https://doi.org/10.1098/rstb.1980.0049	journal	May 1980
Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants Kabsch, W. Journal of Applied Crystallography, Vol. 26, Issue 6 https://doi.org/10.1107/S0021889893005588	journal	December 1993
Proliferation and significance of clinically relevant β-lactamases: β-lactamase overview Bush, Karen Annals of the New York Academy of Sciences, Vol. 1277, Issue 1 https://doi.org/10.1111/nyas.12023	journal	January 2013
ampC cephalosporinase of Escherichia coli K-12 has a different evolutionary origin from that of beta-lactamases of the penicillinase type. Jaurin, B.; Grundstrom, T. Proceedings of the National Academy of Sciences, Vol. 78, Issue 8 https://doi.org/10.1073/pnas.78.8.4897	journal	August 1981
Crystal Structure of 6α-(Hydroxymethyl)penicillanate Complexed to the TEM-1 β-Lactamase from Escherichia coli : Evidence on the Mechanism of Action of a Novel Inhibitor Designed by a Computer-Aided Process Maveyraud, Laurent; Massova, Irina; Birck, Catherine Journal of the American Chemical Society, Vol. 118, Issue 32 https://doi.org/10.1021/ja9609718	journal	January 1996
Comparison of -lactamases of classes A and D: 1.5-A crystallographic structure of the class D OXA-1 oxacillinase Sun, T. Protein Science, Vol. 12, Issue 1 https://doi.org/10.1110/ps.0224303	journal	January 2003
Crystal Structures of Substrate and Inhibitor Complexes with AmpC β-Lactamase: Possible Implications for Substrate-Assisted Catalysis Patera, Alexandra; Blaszczak, Larry C.; Shoichet, Brian K. Journal of the American Chemical Society, Vol. 122, Issue 43 https://doi.org/10.1021/ja001676x	journal	November 2000
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
Class D β-Lactamases: A Reappraisal after Five Decades Leonard, David A.; Bonomo, Robert A.; Powers, Rachel A. Accounts of Chemical Research, Vol. 46, Issue 11 https://doi.org/10.1021/ar300327a	journal	July 2013
Inhibition of the NMC-A β-Lactamase by a Penicillanic Acid Derivative and the Structural Bases for the Increase in Substrate Profile of This Antibiotic Resistance Enzyme Mourey, Lionel; Miyashita, Kazuyuki; Swarén, Peter Journal of the American Chemical Society, Vol. 120, Issue 36 https://doi.org/10.1021/ja9817996	journal	September 1998
Precise insertion of antibiotic resistance determinants into Tn21-like transposons: nucleotide sequence of the OXA-1 beta-lactamase gene. Ouellette, M.; Bissonnette, L.; Roy, P. H. Proceedings of the National Academy of Sciences, Vol. 84, Issue 21 https://doi.org/10.1073/pnas.84.21.7378	journal	November 1987
The 1.4 Å Crystal Structure of the Class D β-Lactamase OXA-1 Complexed with Doripenem Schneider, Kyle D.; Karpen, Mary E.; Bonomo, Robert A. Biochemistry, Vol. 48, Issue 50 https://doi.org/10.1021/bi901690r	journal	December 2009
PATRIC, the bacterial bioinformatics database and analysis resource Wattam, Alice R.; Abraham, David; Dalay, Oral Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1099	journal	November 2013
Beta-Lactam Antibiotics Induce a Lethal Malfunctioning of the Bacterial Cell Wall Synthesis Machinery Cho, Hongbaek; Uehara, Tsuyoshi; Bernhardt, Thomas G. Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.11.017	journal	December 2014
Solvent content of protein crystals Matthews, B. W. Journal of Molecular Biology, Vol. 33, Issue 2 https://doi.org/10.1016/0022-2836(68)90205-2	journal	April 1968
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
An introduction to data reduction: space-group determination, scaling and intensity statistics Evans, Philip R. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S090744491003982X	journal	March 2011
Crystal Structure of the Narrow-Spectrum OXA-46 Class D -Lactamase: Relationship between Active-Site Lysine Carbamylation and Inhibition by Polycarboxylates Docquier, J. D.; Benvenuti, M.; Calderone, V. Antimicrobial Agents and Chemotherapy, Vol. 54, Issue 5 https://doi.org/10.1128/AAC.01517-09	journal	February 2010
The β-lactamases of Gram-negative bacteria and their rôle in resistance to β-lactam antibiotics Sykes, R. B.; Matthew, M. Journal of Antimicrobial Chemotherapy, Vol. 2, Issue 2 https://doi.org/10.1093/jac/2.2.115	journal	January 1976
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
A standard numbering scheme for the class A β-lactamases Ambler, R. P.; Coulson, A. F. W.; Frère, J. M. Biochemical Journal, Vol. 276, Issue 1 https://doi.org/10.1042/bj2760269	journal	May 1991
Kinetic and Structural Requirements for Carbapenemase Activity in GES-Type β-Lactamases Stewart, Nichole K.; Smith, Clyde A.; Frase, Hilary Biochemistry, Vol. 54, Issue 2 https://doi.org/10.1021/bi501052t	journal	December 2014
Penicillin Binding Proteins: key players in bacterial cell cycle and drug resistance processes Macheboeuf, Pauline; Contreras-Martel, Carlos; Job, Viviana FEMS Microbiology Reviews, Vol. 30, Issue 5 https://doi.org/10.1111/j.1574-6976.2006.00024.x	journal	September 2006
Class D β-Lactamases: Are They All Carbapenemases? Antunes, Nuno T.; Lamoureaux, Toni L.; Toth, Marta Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 4 https://doi.org/10.1128/AAC.02522-13	journal	January 2014
Molecular Epidemiology of Multidrug-Resistant Acinetobacter baumannii in a Tertiary Care Hospital in Naples, Italy, Shows the Emergence of a Novel Epidemic Clone Giannouli, M.; Cuccurullo, S.; Crivaro, V. Journal of Clinical Microbiology, Vol. 48, Issue 4 https://doi.org/10.1128/JCM.02263-09	journal	February 2010
Penicillin-Binding Proteins and the Mechanism of Action of Beta-Lactam Antibiotics1 Waxman, D. J.; Strominger, J. L. Annual Review of Biochemistry, Vol. 52, Issue 1 https://doi.org/10.1146/annurev.bi.52.070183.004141	journal	June 1983
Resistance to ?-lactam antibiotics Poole, K. Cellular and Molecular Life Sciences, Vol. 61, Issue 17 https://doi.org/10.1007/s00018-004-4060-9	journal	August 2004
Hydrolytic Mechanism of OXA-58 Enzyme, a Carbapenem-hydrolyzing Class D β-Lactamase from Acinetobacter baumannii Verma, Vidhu; Testero, Sebastian A.; Amini, Kaveh Journal of Biological Chemistry, Vol. 286, Issue 43 https://doi.org/10.1074/jbc.m111.280115	journal	August 2011
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/s0907444913000061	journal	June 2013
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
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
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
Structural Basis for Imipenem Inhibition of Class C -Lactamases Beadle, B. M.; Shoichet, B. K. Antimicrobial Agents and Chemotherapy, Vol. 46, Issue 12 https://doi.org/10.1128/aac.46.12.3978-3980.2002	journal	December 2002
Molecular Specificities of R Factor-Determined Beta-Lactamases: Correlation with Plasmid Compatibility Hedges, R. W.; Datta, Naomi; Kontomichalou, Polyxeni Journal of Bacteriology, Vol. 117, Issue 1 https://doi.org/10.1128/jb.117.1.56-62.1974	journal	January 1974

Cited By (11)

¹³ C-Carbamylation as a mechanistic probe for the inhibition of class D β-lactamases by avibactam and halide ions Lohans, Christopher T.; Wang, David Y.; Jorgensen, Christian Organic & Biomolecular Chemistry, Vol. 15, Issue 28 https://doi.org/10.1039/c7ob01514c	journal	January 2017
Asymmetric synthesis of δ-amino acid derivatives via diastereoselective vinylogous Mannich reactions between N-tert-butanesulfinyl imines and dioxinone-derived lithium dienolate Li, Guijun; Xu, Xiaoliang; Tian, Hongchang RSC Advances, Vol. 7, Issue 80 https://doi.org/10.1039/c7ra10529k	journal	January 2017
An active β‐lactamase is a part of an orchestrated cell wall stress resistance network of Bacillus subtilis and related rhizosphere species Bucher, Tabitha; Keren‐Paz, Alona; Hausser, Jean Environmental Microbiology, Vol. 21, Issue 3 https://doi.org/10.1111/1462-2920.14526	journal	January 2019
Past and Present Perspectives on β-Lactamases Bush, Karen Antimicrobial Agents and Chemotherapy, Vol. 62, Issue 10 https://doi.org/10.1128/aac.01076-18	journal	July 2018
Therapeutic Efficacy of LN-1-255 in Combination with Imipenem in Severe Infection Caused by Carbapenem-Resistant Acinetobacter baumannii Vázquez-Ucha, Juan Carlos; Martínez-Guitián, Marta; Maneiro, María Antimicrobial Agents and Chemotherapy, Vol. 63, Issue 10 https://doi.org/10.1128/aac.01092-19	journal	August 2019
Activity of the β-Lactamase Inhibitor LN-1-255 against Carbapenem-Hydrolyzing Class D β-Lactamases from Acinetobacter baumannii Vázquez-Ucha, Juan Carlos; Maneiro, María; Martínez-Guitián, Marta Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 11 https://doi.org/10.1128/aac.01172-17	journal	August 2017
Regulation and Anaerobic Function of the Clostridioides difficile β-Lactamase Sandhu, Brindar K.; Edwards, Adrianne N.; Anderson, Sarah E. Antimicrobial Agents and Chemotherapy, Vol. 64, Issue 1 https://doi.org/10.1128/aac.01496-19	journal	October 2019
Intrinsic Class D β-Lactamases of Clostridium difficile Toth, Marta; Stewart, Nichole K.; Smith, Clyde mBio, Vol. 9, Issue 6 https://doi.org/10.1128/mbio.01803-18	journal	December 2018
Systematic Identification and Classification of β-Lactamases Based on Sequence Similarity Criteria: β-Lactamase Annotation Silveira, Melise Chaves; Azevedo da Silva, Rangeline; Faria da Mota, Fábio Evolutionary Bioinformatics, Vol. 14 https://doi.org/10.1177/1176934318797351	journal	January 2018
β-Lactamases and β-Lactamase Inhibitors in the 21st Century Tooke, Catherine L.; Hinchliffe, Philip; Bragginton, Eilis C. Journal of Molecular Biology, Vol. 431, Issue 18 https://doi.org/10.1016/j.jmb.2019.04.002	journal	August 2019
An overview of the antimicrobial resistance mechanisms of bacteria C. Reygaert, Wanda AIMS Microbiology, Vol. 4, Issue 3 https://doi.org/10.3934/microbiol.2018.3.482	journal	January 2018

Similar Records

Structural Basis of Activity against Aztreonam and Extended Spectrum Cephalosporins for Two Carbapenem-Hydrolyzing Class D β-Lactamases from Acinetobacter baumannii

Journal Article · Tue Feb 24 00:00:00 EST 2015 · Biochemistry · OSTI ID:1257221

Mitchell, Joshua M.; Clasman, Jozlyn R.; June, Cynthia M.; +9 more

A close look onto structural models and primary ligands of metallo-β-lactamases

Journal Article · Sat Aug 25 00:00:00 EDT 2018 · Drug Resistance Updates · OSTI ID:1257221

Raczynska, Joanna E.; Shabalin, Ivan G.; Minor, Wladek; +2 more

A DNA aptamer reveals an allosteric site for inhibition in metallo-β-lactamases

Journal Article · Mon Apr 22 00:00:00 EDT 2019 · PLoS ONE · OSTI ID:1257221

Khan, Nazmul H.; Bui, Anthony A.; Xiao, Yang; +4 more

Related Subjects

60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
Bacteria
Enzymes
X-ray crystallography

Title: Class D β-lactamases do exist in Gram-positive bacteria

Citation Formats

References (47)

Cited By (11)

Similar Records

Related Subjects