Functional and Structural Characterization of Diverse NfsB Chloramphenicol Reductase Enzymes from Human Pathogens

Mullowney, Michael W.; Maltseva, Natalia I.; Endres, Michael; Kim, Youngchang; Joachimiak, Andrzej; Crofts, Terence S.; Culyba, ed., Matthew J.

doi:10.1128/spectrum.00139-22

Title: Functional and Structural Characterization of Diverse NfsB Chloramphenicol Reductase Enzymes from Human Pathogens

Journal Article · 22 February 2022 · Microbiology Spectrum

DOI: https://doi.org/10.1128/spectrum.00139-22 · OSTI ID:1846232

^[1];

^[2]; Endres, Michael ^[3];

^[2];

^[4];

^[5]; Culyba, ed., Matthew J.

Department of Chemistry, Northwestern University, Evanston, Illinois, USA
Center for Structural Genomics of Infectious Diseases, Consortium for Advanced Science and Engineering, University of Chicago, Chicago, Illinois, USA, Structure Biology Center, Argonne National Laboratory, Argonne, Illinois, USA
Structure Biology Center, Argonne National Laboratory, Argonne, Illinois, USA
Center for Structural Genomics of Infectious Diseases, Consortium for Advanced Science and Engineering, University of Chicago, Chicago, Illinois, USA, Structure Biology Center, Argonne National Laboratory, Argonne, Illinois, USA, Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, Illinois, USA
Department of Molecular Biosciences, Northwestern University, Evanston, Illinois, USA

The question of how new enzyme activities evolve is of great biological interest and, in the context of antibiotic resistance, of great medical importance. Here, we have tested the hypothesis that new antibiotic resistance mechanisms may evolve from promiscuous housekeeping enzymes that have antibiotic modification side activities.

View Journal Article

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1846232

Journal Information:: Microbiology Spectrum, Journal Name: Microbiology Spectrum; ISSN 2165-0497

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Permeability of currently available microtiter plate sealing tapes fail to fulfil the requirements for aerobic microbial cultivation Sieben, Michaela; Giese, Heiner; Grosch, Jan-Hendrik Biotechnology Journal, Vol. 11, Issue 12 https://doi.org/10.1002/biot.201600054	journal	September 2016
Methionine in proteins: The Cinderella of the proteinogenic amino acids Aledo, Juan C. Protein Science, Vol. 28, Issue 10 https://doi.org/10.1002/pro.3698	journal	August 2019
Controlled Intracellular Processing of Fusion Proteins by TEV Protease Kapust, Rachel B.; Waugh, David S. Protein Expression and Purification, Vol. 19, Issue 2 https://doi.org/10.1006/prep.2000.1251	journal	July 2000
Protein Production for Structural Genomics Using E. coli Expression Makowska-Grzyska, Magdalena; Kim, Youngchang; Maltseva, Natalia Structural Genomics and Drug Discovery https://doi.org/10.1007/978-1-4939-0354-2_7	book	January 2014
New LIC vectors for production of proteins from genes containing rare codons Eschenfeldt, William H.; Makowska-Grzyska, Magdalena; Stols, Lucy Journal of Structural and Functional Genomics, Vol. 14, Issue 4 https://doi.org/10.1007/s10969-013-9163-9	journal	September 2013
A new Coupling Component for Sulfanilamide Determination Bratton, A. Calvin; Marshall, E. K. Journal of Biological Chemistry, Vol. 128, Issue 2 https://doi.org/10.1016/S0021-9258(18)73708-3	journal	May 1939
Bacterial resistance to antibiotics: Enzymatic degradation and modification Wright, G. Advanced Drug Delivery Reviews, Vol. 57, Issue 10 https://doi.org/10.1016/j.addr.2005.04.002	journal	July 2005
Investigating the promiscuity of the chloramphenicol nitroreductase from Haemophilus influenzae towards the reduction of 4-nitrobenzene derivatives Green, Keith D.; Fosso, Marina Y.; Mayhoub, Abdelrahman S. Bioorganic & Medicinal Chemistry Letters, Vol. 29, Issue 9 https://doi.org/10.1016/j.bmcl.2019.02.025	journal	May 2019
Discovery and Characterization of a Nitroreductase Capable of Conferring Bacterial Resistance to Chloramphenicol Crofts, Terence S.; Sontha, Pratyush; King, Amber O. Cell Chemical Biology, Vol. 26, Issue 4 https://doi.org/10.1016/j.chembiol.2019.01.007	journal	April 2019
Molecular basis of bacterial resistance to chloramphenicol and florfenicol Schwarz, Stefan; Kehrenberg, Corinna; Doublet, Benoît FEMS Microbiology Reviews, Vol. 28, Issue 5 https://doi.org/10.1016/j.femsre.2004.04.001	journal	November 2004
Crossroads of Antibiotic Resistance and Biosynthesis Wencewicz, Timothy A. Journal of Molecular Biology, Vol. 431, Issue 18 https://doi.org/10.1016/j.jmb.2019.06.033	journal	August 2019
The antibiotic resistome: what's new? Perry, Julie Ann; Westman, Erin Louise; Wright, Gerard D. Current Opinion in Microbiology, Vol. 21 https://doi.org/10.1016/j.mib.2014.09.002	journal	October 2014
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Mechanism-Informed Refinement Reveals Altered Substrate-Binding Mode for Catalytically Competent Nitroreductase Pitsawong, Warintra; Haynes, Chad A.; Koder, Ronald L. Structure, Vol. 25, Issue 7 https://doi.org/10.1016/j.str.2017.05.002	journal	July 2017
High-throughput protein purification and quality assessment for crystallization Kim, Youngchang; Babnigg, Gyorgy; Jedrzejczak, Robert Methods, Vol. 55, Issue 1 https://doi.org/10.1016/j.ymeth.2011.07.010	journal	September 2011
Re-estimating annual deaths due to multidrug-resistant organism infections Burnham, Jason P.; Olsen, Margaret A.; Kollef, Marin H. Infection Control & Hospital Epidemiology, Vol. 40, Issue 1 https://doi.org/10.1017/ice.2018.304	journal	November 2018
Plazomicin Retains Antibiotic Activity against Most Aminoglycoside Modifying Enzymes Cox, Georgina; Ejim, Linda; Stogios, Peter J. ACS Infectious Diseases, Vol. 4, Issue 6 https://doi.org/10.1021/acsinfecdis.8b00001	journal	April 2018
The Moderately Efficient Enzyme: Evolutionary and Physicochemical Trends Shaping Enzyme Parameters Bar-Even, Arren; Noor, Elad; Savir, Yonatan Biochemistry, Vol. 50, Issue 21 https://doi.org/10.1021/bi2002289	journal	May 2011
Synthesis and Evaluation of Hetero- and Homodimers of Ribosome-Targeting Antibiotics: Antimicrobial Activity, in Vitro Inhibition of Translation, and Drug Resistance Berkov-Zrihen, Yifat; Green, Keith D.; Labby, Kristin J. Journal of Medicinal Chemistry, Vol. 56, Issue 13 https://doi.org/10.1021/jm400707f	journal	July 2013
Reduction of Chloromycetin by a Cell-free Bacterial Extract and its Relation to Nitrite Reduction Egami, Fujio; Ebata, Mituo; Sato, Ryo Nature, Vol. 167, Issue 4238 https://doi.org/10.1038/167118a0	journal	January 1951
Announcing the worldwide Protein Data Bank Berman, Helen; Henrick, Kim; Nakamura, Haruki Nature Structural & Molecular Biology, Vol. 10, Issue 12 https://doi.org/10.1038/nsb1203-980	journal	December 2003
The evolution of substrate discrimination in macrolide antibiotic resistance enzymes Pawlowski, Andrew C.; Stogios, Peter J.; Koteva, Kalinka Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02680-0	journal	January 2018
Structures of Nitroreductase in Three States: EFFECTS OF INHIBITOR BINDING AND REDUCTION Haynes, Chad A.; Koder, Ronald L.; Miller, Anne-Frances Journal of Biological Chemistry, Vol. 277, Issue 13 https://doi.org/10.1074/jbc.M111334200	journal	January 2002
Structural and Mechanistic Studies of Escherichia coli Nitroreductase with the Antibiotic Nitrofurazone Race, Paul R.; Lovering, Andrew L.; Green, Richard M. Journal of Biological Chemistry, Vol. 280, Issue 14 https://doi.org/10.1074/jbc.M409652200	journal	April 2005
Experimental Animal Models for Anaerobic Infections Onderdonk, A. B.; Kasper, D. L.; Mansheim, B. J. Clinical Infectious Diseases, Vol. 1, Issue 2 https://doi.org/10.1093/clinids/1.2.291	journal	March 1979
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Building Phylogenetic Trees from Molecular Data with MEGA Hall, B. G. Molecular Biology and Evolution, Vol. 30, Issue 5 https://doi.org/10.1093/molbev/mst012	journal	March 2013
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements Lutz, R. Nucleic Acids Research, Vol. 25, Issue 6, p. 1203-1210 https://doi.org/10.1093/nar/25.6.1203	journal	March 1997
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes Davis, I. W.; Murray, L. W.; Richardson, J. S. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh398	journal	July 2004
Gene Cloning, Purification, and Characterization of NfsB, a Minor Oxygen-Insensitive Nitroreductase from Escherichia coli, Similar in Biochemical Properties to FRase I, the Major Flavin Reductase in Vibrio fischeri Zenno, S.; Koike, H.; Tanokura, M. Journal of Biochemistry, Vol. 120, Issue 4 https://doi.org/10.1093/oxfordjournals.jbchem.a021473	journal	October 1996
The Ferredoxin-dependent Reduction of Chloramphenicol by Clostridium acetobutylicum O'Brien, R. W.; Morris, J. G. Journal of General Microbiology, Vol. 67, Issue 3 https://doi.org/10.1099/00221287-67-3-265	journal	August 1971
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
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
The Buccaneer software for automated model building. 1. Tracing protein chains Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9 https://doi.org/10.1107/S0907444906022116	journal	August 2006
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444909038360	journal	March 2010
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
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
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Reduction of polynitroaromatic compounds: the bacterial nitroreductases Roldán, María Dolores; Pérez-Reinado, Eva; Castillo, Francisco FEMS Microbiology Reviews, Vol. 32, Issue 3 https://doi.org/10.1111/j.1574-6976.2008.00107.x	journal	May 2008
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Chloramphenicol Is a Substrate for a Novel Nitroreductase Pathway in Haemophilus influenzae Smith, Arnold L.; Erwin, Alice L.; Kline, Toni Antimicrobial Agents and Chemotherapy, Vol. 51, Issue 8 https://doi.org/10.1128/AAC.00087-07	journal	August 2007
Structure and Function of CinD (YtjD) of Lactococcus lactis , a Copper-Induced Nitroreductase Involved in Defense against Oxidative Stress Mermod, Mélanie; Mourlane, Frédéric; Waltersperger, Sandro Journal of Bacteriology, Vol. 192, Issue 16 https://doi.org/10.1128/JB.00372-10	journal	August 2010
Genetics of Nitrofurazone Resistance in Escherichia coli McCalla, D. R.; Kaiser, Christel; Green, M. H. L. Journal of Bacteriology, Vol. 133, Issue 1 https://doi.org/10.1128/jb.133.1.10-16.1978	journal	January 1978
Reduction of Chloromycetin and Related Compounds by Escherichia coli Smith, Grant N.; Worrel, C. S. Journal of Bacteriology, Vol. 65, Issue 3 https://doi.org/10.1128/jb.65.3.313-317.1953	journal	March 1953
Relationship Between “Chloramphenicol Reductase Activity” and Chloramphenicol Resistance in Escherichia Coli, Merkel, Joseph R.; Steers, Edward Journal of Bacteriology, Vol. 66, Issue 4 https://doi.org/10.1128/jb.66.4.389-396.1953	journal	October 1953
Acquired Antibiotic Resistance Genes: An Overview van Hoek, Angela H. A. M.; Mevius, Dik; Guerra, Beatriz Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00203	journal	January 2011
Chloramphenicol Derivatives as Antibacterial and Anticancer Agents: Historic Problems and Current Solutions Dinos, George; Athanassopoulos, Constantinos; Missiri, Dionissia Antibiotics, Vol. 5, Issue 2 https://doi.org/10.3390/antibiotics5020020	journal	June 2016
Intracellular complexities of acquiring a new enzymatic function revealed by mass-randomisation of active-site residues Hall, Kelsi R.; Robins, Katherine J.; Williams, Elsie M. eLife, Vol. 9 https://doi.org/10.7554/eLife.59081	journal	November 2020

Similar Records

Structural and functional characterization of three Type B and C chloramphenicol acetyltransferases from Vibrio species

Journal Article · 2019 · Protein Science · OSTI ID:1615515

Alcala, Ashley; Ramirez, Guadalupe; Solis, Allan; +10 more

Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-offs

Journal Article · 2010 · J. Mol. Biol. · OSTI ID:1008800

Wang, Xiaojun; Minasov, George; Shoichet, Brian K

Systems-Wide Prediction of Enzyme Promiscuity Reveals a New Underground Alternative Route for Pyridoxal 5’-Phosphate Production in E. coli

Journal Article · 2016 · PLoS Computational Biology (Online) · OSTI ID:1258643

Oberhardt, Matthew A.; Zarecki, Raphy; Reshef, Leah; +8 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Haemophilus influenzae
Neisseria
NfsB
antibiotic resistance
chloramphenicol
crystal structure
nitroreductase

Title: Functional and Structural Characterization of Diverse NfsB Chloramphenicol Reductase Enzymes from Human Pathogens

Citation Formats

References (51)

Similar Records

Related Subjects