Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida
Abstract
PqqB is an enzyme involved in the biosynthesis of pyrroloquinoline quinone and a distal member of the metallo-β-lactamase (MBL) superfamily. PqqB lacks two residues in the conserved signature motif HxHxDH that makes up the key metal-chelating elements that can bind up to two metal ions at the active site of MBLs and other members of its superfamily. Here, we report crystal structures of PqqB bound to Mn2+, Mg2+, Cu2+, and Zn2+. These structures demonstrate that PqqB can still bind metal ions at the canonical MBL active site. The fact that PqqB can adapt its side chains to chelate a wide spectrum of metal ions with different coordination features on a uniform main chain scaffold demonstrates its metal-binding plasticity. This plasticity may provide insights into the structural basis of promiscuous activities found in ensembles of metal complexes within this superfamily. Furthermore, PqqB belongs to a small subclass of MBLs that contain an additional CxCxxC motif that binds a structural Zn2+. Our data support a key role for this motif in dimerization.
- Authors:
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institutes of Health (NIH)
- OSTI Identifier:
- 1418055
- Resource Type:
- Journal Article
- Journal Name:
- JBIC Journal of Biological Inorganic Chemistry
- Additional Journal Information:
- Journal Volume: 22; Journal Issue: 7; Journal ID: ISSN 0949-8257
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Tu, Xiongying, Latham, John A., Klema, Valerie J., Evans, Robert L., Li, Chao, Klinman, Judith P., and Wilmot, Carrie M. Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida. United States: N. p., 2017.
Web. doi:10.1007/s00775-017-1486-8.
Tu, Xiongying, Latham, John A., Klema, Valerie J., Evans, Robert L., Li, Chao, Klinman, Judith P., & Wilmot, Carrie M. Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida. United States. https://doi.org/10.1007/s00775-017-1486-8
Tu, Xiongying, Latham, John A., Klema, Valerie J., Evans, Robert L., Li, Chao, Klinman, Judith P., and Wilmot, Carrie M. 2017.
"Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida". United States. https://doi.org/10.1007/s00775-017-1486-8.
@article{osti_1418055,
title = {Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida},
author = {Tu, Xiongying and Latham, John A. and Klema, Valerie J. and Evans, Robert L. and Li, Chao and Klinman, Judith P. and Wilmot, Carrie M.},
abstractNote = {PqqB is an enzyme involved in the biosynthesis of pyrroloquinoline quinone and a distal member of the metallo-β-lactamase (MBL) superfamily. PqqB lacks two residues in the conserved signature motif HxHxDH that makes up the key metal-chelating elements that can bind up to two metal ions at the active site of MBLs and other members of its superfamily. Here, we report crystal structures of PqqB bound to Mn2+, Mg2+, Cu2+, and Zn2+. These structures demonstrate that PqqB can still bind metal ions at the canonical MBL active site. The fact that PqqB can adapt its side chains to chelate a wide spectrum of metal ions with different coordination features on a uniform main chain scaffold demonstrates its metal-binding plasticity. This plasticity may provide insights into the structural basis of promiscuous activities found in ensembles of metal complexes within this superfamily. Furthermore, PqqB belongs to a small subclass of MBLs that contain an additional CxCxxC motif that binds a structural Zn2+. Our data support a key role for this motif in dimerization.},
doi = {10.1007/s00775-017-1486-8},
url = {https://www.osti.gov/biblio/1418055},
journal = {JBIC Journal of Biological Inorganic Chemistry},
issn = {0949-8257},
number = 7,
volume = 22,
place = {United States},
year = {Sat Aug 19 00:00:00 EDT 2017},
month = {Sat Aug 19 00:00:00 EDT 2017}
}
Works referenced in this record:
A Metallo-β-lactamase Enzyme in Action: Crystal Structures of the Monozinc Carbapenemase CphA and its Complex with Biapenem
journal, January 2005
- Garau, Gianpiero; Bebrone, Carine; Anne, Christine
- Journal of Molecular Biology, Vol. 345, Issue 4
Pyrroloquinoline Quinone Stimulates Mitochondrial Biogenesis through cAMP Response Element-binding Protein Phosphorylation and Increased PGC-1α Expression
journal, October 2009
- Chowanadisai, Winyoo; Bauerly, Kathryn A.; Tchaparian, Eskouhie
- Journal of Biological Chemistry, Vol. 285, Issue 1
Structure of New Delhi metallo-β-lactamase 1 (NDM-1)
journal, September 2011
- Green, Victoria L.; Verma, Anil; Owens, Raymond J.
- Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 67, Issue 10
Pyrroloquinoline quinone (PQQ) producing Escherichia coli Nissle 1917 (EcN) alleviates age associated oxidative stress and hyperlipidemia, and improves mitochondrial function in ageing rats
journal, June 2015
- Singh, Ashish Kumar; Pandey, Sumeet Kumar; Saha, Gourav
- Experimental Gerontology, Vol. 66
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
Intrigues and Intricacies of the Biosynthetic Pathways for the Enzymatic Quinocofactors: PQQ, TTQ, CTQ, TPQ, and LTQ
journal, December 2013
- Klinman, Judith P.; Bonnot, Florence
- Chemical Reviews, Vol. 114, Issue 8
The Structure of the Dizinc Subclass B2 Metallo- -Lactamase CphA Reveals that the Second Inhibitory Zinc Ion Binds in the Histidine Site
journal, August 2009
- Bebrone, C.; Delbruck, H.; Kupper, M. B.
- Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 10
Pyrroloquinoline Quinone (PQQ) Inhibits Lipopolysaccharide Induced Inflammation in Part via Downregulated NF-κB and p38/JNK Activation in Microglial and Attenuates Microglia Activation in Lipopolysaccharide Treatment Mice
journal, October 2014
- Yang, Chongfei; Yu, Lifeng; Kong, Lingbo
- PLoS ONE, Vol. 9, Issue 10
MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009
- Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism
journal, August 2011
- Zhang, HongMin; Hao, Quan
- The FASEB Journal, Vol. 25, Issue 8
Structure of PhnP, a Phosphodiesterase of the Carbon-Phosphorus Lyase Pathway for Phosphonate Degradation
journal, April 2009
- Podzelinska, Kateryna; He, Shu-Mei; Wathier, Matthew
- Journal of Biological Chemistry, Vol. 284, Issue 25
Structure and Mechanism of PhnP, a Phosphodiesterase of the Carbon-Phosphorus Lyase Pathway
journal, October 2011
- He, Shu-Mei; Wathier, Matthew; Podzelinska, Kateryna
- Biochemistry, Vol. 50, Issue 40
Distribution and Properties of the Genes Encoding the Biosynthesis of the Bacterial Cofactor, Pyrroloquinoline Quinone
journal, March 2012
- Shen, Yao-Qing; Bonnot, Florence; Imsand, Erin M.
- Biochemistry, Vol. 51, Issue 11
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
journal, September 1998
- Brünger, A. T.; Adams, P. D.; Clore, G. M.
- Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5
The Structure of a Biosynthetic Intermediate of Pyrroloquinoline Quinone (PQQ) and Elucidation of the Final Step of PQQ Biosynthesis
journal, May 2004
- Magnusson, Olafur T.; Toyama, Hirohide; Saeki, Megumi
- Journal of the American Chemical Society, Vol. 126, Issue 17
Crystal structure of PqqB from <i>Pseudomonas putida</i> at 2.2 Å resolution
journal, January 2012
- Metlitzky, Moritz; Puehringer, Sandra; J. Fisher, Stuart
- Journal of Biophysical Chemistry, Vol. 03, Issue 02
Evolution of Enzyme Superfamilies: Comprehensive Exploration of Sequence–Function Relationships
journal, November 2016
- Baier, F.; Copp, J. N.; Tokuriki, N.
- Biochemistry, Vol. 55, Issue 46
Pyrroloquinoline Quinone (PQQ) Prevents Cognitive Deficit Caused by Oxidative Stress in Rats
journal, January 2008
- Ohwada, Kei; Takeda, Hironobu; Yamazaki, Makiko
- Journal of Clinical Biochemistry and Nutrition, Vol. 42, 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
Zn(II) Dependence of the Aeromonas hydrophila AE036 Metallo-β-lactamase Activity and Stability †
journal, September 1997
- Hernandez Valladares, Maria; Felici, Antonio; Weber, Georges
- Biochemistry, Vol. 36, Issue 38
Distinct Metal Isoforms Underlie Promiscuous Activity Profiles of Metalloenzymes
journal, April 2015
- Baier, Florian; Chen, John; Solomonson, Matthew
- ACS Chemical Biology, Vol. 10, Issue 7
Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily
journal, December 2007
- Bebrone, Carine
- Biochemical Pharmacology, Vol. 74, Issue 12
A structural view of the antibiotic degradation enzyme NDM-1 from a superbug
journal, May 2011
- Guo, Yu; Wang, Jing; Niu, Guojun
- Protein & Cell, Vol. 2, Issue 5
Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance
journal, August 2011
- King, Dustin; Strynadka, Natalie
- Protein Science, Vol. 20, Issue 9
Connectivity between Catalytic Landscapes of the Metallo-β-Lactamase Superfamily
journal, June 2014
- Baier, Florian; Tokuriki, Nobuhiko
- Journal of Molecular Biology, Vol. 426, Issue 13
Dioxygen activation by nonheme iron enzymes with the 2-His-1-carboxylate facial triad that generate high-valent oxoiron oxidants
journal, January 2017
- Kal, Subhasree; Que, Lawrence
- JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 2-3
Structure of Apo- and Monometalated Forms of NDM-1—A Highly Potent Carbapenem-Hydrolyzing Metallo-β-Lactamase
journal, September 2011
- Kim, Youngchang; Tesar, Christine; Mire, Joseph
- PLoS ONE, Vol. 6, Issue 9
Synthesis of pyrroloquinoline quinone in vivo and in vitro and detection of an intermediate in the biosynthetic pathway.
journal, September 1995
- Velterop, J. S.; Sellink, E.; Meulenberg, J. J.
- Journal of Bacteriology, Vol. 177, Issue 17
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4