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Title: 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


Pyrroloquinoline Quinone Stimulates Mitochondrial Biogenesis through cAMP Response Element-binding Protein Phosphorylation and Increased PGC-1α Expression
journal, October 2009


Structure of New Delhi metallo-β-lactamase 1 (NDM-1)
journal, September 2011


Overview of the CCP 4 suite and current developments
journal, March 2011


Intrigues and Intricacies of the Biosynthetic Pathways for the Enzymatic Quinocofactors: PQQ, TTQ, CTQ, TPQ, and LTQ
journal, December 2013


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


MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009


Coot model-building tools for molecular graphics
journal, November 2004


Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism
journal, August 2011


Structure of PhnP, a Phosphodiesterase of the Carbon-Phosphorus Lyase Pathway for Phosphonate Degradation
journal, April 2009


Structure and Mechanism of PhnP, a Phosphodiesterase of the Carbon-Phosphorus Lyase Pathway
journal, October 2011


Distribution and Properties of the Genes Encoding the Biosynthesis of the Bacterial Cofactor, Pyrroloquinoline Quinone
journal, March 2012


Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
journal, September 1998


The Structure of a Biosynthetic Intermediate of Pyrroloquinoline Quinone (PQQ) and Elucidation of the Final Step of PQQ Biosynthesis
journal, May 2004


Crystal structure of PqqB from <i>Pseudomonas putida</i> at 2.2 Å resolution
journal, January 2012


Evolution of Enzyme Superfamilies: Comprehensive Exploration of Sequence–Function Relationships
journal, November 2016


Pyrroloquinoline Quinone (PQQ) Prevents Cognitive Deficit Caused by Oxidative Stress in Rats
journal, January 2008


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010


Zn(II) Dependence of the Aeromonas hydrophila AE036 Metallo-β-lactamase Activity and Stability
journal, September 1997


Distinct Metal Isoforms Underlie Promiscuous Activity Profiles of Metalloenzymes
journal, April 2015


A structural view of the antibiotic degradation enzyme NDM-1 from a superbug
journal, May 2011


Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance
journal, August 2011


Connectivity between Catalytic Landscapes of the Metallo-β-Lactamase Superfamily
journal, June 2014


Dioxygen activation by nonheme iron enzymes with the 2-His-1-carboxylate facial triad that generate high-valent oxoiron oxidants
journal, January 2017


Synthesis of pyrroloquinoline quinone in vivo and in vitro and detection of an intermediate in the biosynthetic pathway.
journal, September 1995


XDS
journal, January 2010


Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007


[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997


Phaser crystallographic software
journal, July 2007