Crystallographic characterization of a tri-Asp metal-binding site at the three-fold symmetry axis of LarE

Fellner, Matthias; Huizenga, Kamren G.; Hausinger, Robert P.; Hu, Jian

doi:10.1038/s41598-020-62847-6

Title: Crystallographic characterization of a tri-Asp metal-binding site at the three-fold symmetry axis of LarE

Journal Article · Thu Apr 02 00:00:00 EDT 2020 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-020-62847-6· OSTI ID:1608895

Fellner, Matthias ^[1]; Huizenga, Kamren G. ^[2]; Hausinger, Robert P. ^[2]; Hu, Jian ^[2]

Univ. of Otago, Dunedin, Otago (New Zealand); Michigan State Univ., East Lansing, MI (United States)
Michigan State Univ., East Lansing, MI (United States)

Detailed crystallographic characterization of a tri-aspartate metal-binding site previously identified on the three-fold symmetry axis of a hexameric enzyme, LarE from Lactobacillus plantarum, was conducted. By screening an array of monovalent, divalent, and trivalent metal ions, we demonstrated that this metal binding site stoichiometrically binds Ca²⁺, Mn²⁺, Fe²⁺/Fe³⁺, Co²⁺, Ni²⁺, Cu²⁺, Zn²⁺, and Cd²⁺, but not monovalent metal ions, Cr³⁺, Mg²⁺, Y³⁺, Sr²⁺ or Ba²⁺. Extensive database searches resulted in only 13 similar metal binding sites in other proteins, indicative of the rareness of tri-aspartate architectures, which allows for engineering such a selective multivalent metal ion binding site into target macromolecules for structural and biophysical characterization.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE; National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: CHE1516126; CHE1807073; GM128959

OSTI ID:: 1608895

Journal Information:: Scientific Reports, Vol. 10, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (44)

Metal Preferences and Metallation Foster, Andrew W.; Osman, Deenah; Robinson, Nigel J. Journal of Biological Chemistry, Vol. 289, Issue 41 https://doi.org/10.1074/jbc.R114.588145	journal	August 2014
Short-distance probes for protein backbone structure based on energy transfer between bimane and transition metal ions Taraska, J. W.; Puljung, M. C.; Zagotta, W. N. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0905207106	journal	September 2009
Nickel-pincer cofactor biosynthesis involves LarB-catalyzed pyridinium carboxylation and LarE-dependent sacrificial sulfur insertion Desguin, Benoît; Soumillion, Patrice; Hols, Pascal Proceedings of the National Academy of Sciences, Vol. 113, Issue 20 https://doi.org/10.1073/pnas.1600486113	journal	April 2016
A structural perspective on the PP-loop ATP pyrophosphatase family Fellner, Matthias; Hausinger, Robert P.; Hu, Jian Critical Reviews in Biochemistry and Molecular Biology, Vol. 53, Issue 6 https://doi.org/10.1080/10409238.2018.1516728	journal	October 2018
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
The worldwide Protein Data Bank (wwPDB): ensuring a single, uniform archive of PDB data Berman, H.; Henrick, K.; Nakamura, H. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl971	journal	January 2007
Structural insights into the catalytic mechanism of a sacrificial sulfur insertase of the N-type ATP pyrophosphatase family, LarE Fellner, Matthias; Desguin, Benoît; Hausinger, Robert P. Proceedings of the National Academy of Sciences, Vol. 114, Issue 34 https://doi.org/10.1073/pnas.1704967114	journal	August 2017
A tethered niacin-derived pincer complex with a nickel-carbon bond in lactate racemase Desguin, Benoît; Zhang, Tuo; Soumillion, Patrice Science, Vol. 349, Issue 6243 https://doi.org/10.1126/science.aab2272	journal	July 2015
Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides Shannon, R. D. Acta Crystallographica Section A, Vol. 32, Issue 5, p. 751-767 https://doi.org/10.1107/S0567739476001551	journal	September 1976
The crystallographic structure of Panicum Mosaic Virus (PMV) Makino, Debora L.; Larson, Steven B.; McPherson, Alexander Journal of Structural Biology, Vol. 181, Issue 1 https://doi.org/10.1016/j.jsb.2012.10.012	journal	January 2013
Structures of C1q-like Proteins Reveal Unique Features among the C1q/TNF Superfamily Ressl, Susanne; Vu, Brandon K.; Vivona, Sandro Structure, Vol. 23, Issue 4 https://doi.org/10.1016/j.str.2015.01.019	journal	April 2015
MetalPDB in 2018: a database of metal sites in biological macromolecular structures Putignano, Valeria; Rosato, Antonio; Banci, Lucia Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx989	journal	October 2017
Transition metal ion FRET uncovers K+ regulation of a neurotransmitter/sodium symporter Billesbølle, Christian B.; Mortensen, Jonas S.; Sohail, Azmat Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12755	journal	September 2016
Functional and Structural Characterization of an Unusual Cofactor-Independent Oxygenase Baas, Bert-Jan; Poddar, Harshwardhan; Geertsema, Edzard M. Biochemistry, Vol. 54, Issue 5 https://doi.org/10.1021/bi501200j	journal	January 2015
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
Three-dimensional structure and ligand-binding site of carp fishelectin (FEL) Capaldi, Stefano; Faggion, Beniamino; Carrizo, Maria E. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/S1399004715004174	journal	April 2015
ZincBind—the database of zinc binding sites Ireland, Sam M.; Martin, Andrew C. R. Database, Vol. 2019 https://doi.org/10.1093/database/baz006	journal	January 2019
MIPS: metal interactions in protein structures Hemavathi, K.; Kalaivani, M.; Udayakumar, A. Journal of Applied Crystallography, Vol. 43, Issue 1 https://doi.org/10.1107/S002188980903982x	journal	December 2009
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
Discovery of a Novel Class of Potent Human Deoxyuridine Triphosphatase Inhibitors Remarkably Enhancing the Antitumor Activity of Thymidylate Synthase Inhibitors Miyahara, Seiji; Miyakoshi, Hitoshi; Yokogawa, Tatsushi Journal of Medicinal Chemistry, Vol. 55, Issue 7 https://doi.org/10.1021/jm201628y	journal	March 2012
Recognition- and Reactivity-Based Fluorescent Probes for Studying Transition Metal Signaling in Living Systems Aron, Allegra T.; Ramos-Torres, Karla M.; Cotruvo, Joseph A. Accounts of Chemical Research, Vol. 48, Issue 8 https://doi.org/10.1021/acs.accounts.5b00221	journal	July 2015
Factors Governing the Metal Coordination Number in Metal Complexes from Cambridge Structural Database Analyses Dudev, Minko; Wang, Jonathan; Dudev, Todor The Journal of Physical Chemistry B, Vol. 110, Issue 4 https://doi.org/10.1021/jp054975n	journal	February 2006
Analysis of the Active Site Cysteine Residue of the Sacrificial Sulfur Insertase LarE from Lactobacillus plantarum Fellner, Matthias; Rankin, Joel A.; Desguin, Benoît Biochemistry, Vol. 57, Issue 38 https://doi.org/10.1021/acs.biochem.8b00601	journal	August 2018
Biosynthesis of the nickel-pincer nucleotide cofactor of lactate racemase requires a CTP-dependent cyclometallase Desguin, Benoît; Fellner, Matthias; Riant, Olivier Journal of Biological Chemistry, Vol. 293, Issue 32 https://doi.org/10.1074/jbc.RA118.003741	journal	June 2018
Channel specificity: structural basis for sugar discrimination and differential flux rates in maltoporin 1 1Edited by R. Huber Wang, Yan-Fei; Dutzler, Raimund; Rizkallah, Pierre J. Journal of Molecular Biology, Vol. 272, Issue 1 https://doi.org/10.1006/jmbi.1997.1224	journal	September 1997
Structure of maltoporin from Salmonella typhimurium ligated with a nitrophenyl-maltotrioside Meyer, Joachim E. W.; Hofnung, Maurice; Schulz, Georg E. Journal of Molecular Biology, Vol. 266, Issue 4 https://doi.org/10.1006/jmbi.1996.0823	journal	March 1997
MetalS3, a database-mining tool for the identification of structurally similar metal sites Valasatava, Yana; Rosato, Antonio; Cavallaro, Gabriele JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 6 https://doi.org/10.1007/s00775-014-1128-3	journal	April 2014
Structure of the infectious salmon anemia virus receptor complex illustrates a unique binding strategy for attachment Cook, Jonathan D.; Sultana, Azmiri; Lee, Jeffrey E. Proceedings of the National Academy of Sciences, Vol. 114, Issue 14 https://doi.org/10.1073/pnas.1617993114	journal	March 2017
Characterization of metalloproteins by high-throughput X-ray absorption spectroscopy Shi, W.; Punta, M.; Bohon, J. Genome Research, Vol. 21, Issue 6 https://doi.org/10.1101/gr.115097.110	journal	April 2011
Monodentate versus Bidentate Carboxylate Binding in Magnesium and Calcium Proteins: What Are the Basic Principles? Dudev, Todor; Lim, Carmay The Journal of Physical Chemistry B, Vol. 108, Issue 14 https://doi.org/10.1021/jp0310347	journal	April 2004
Lactate Racemase Nickel-Pincer Cofactor Operates by a Proton-Coupled Hydride Transfer Mechanism Rankin, Joel A.; Mauban, Robert C.; Fellner, Matthias Biochemistry, Vol. 57, Issue 23 https://doi.org/10.1021/acs.biochem.8b00100	journal	February 2018
MetalMine: a database of functional metal-binding sites in proteins Nakamura, Kensuke; Hirai, Aki; Altaf-Ul-Amin, Md. Plant Biotechnology, Vol. 26, Issue 5 https://doi.org/10.5511/plantbiotechnology.26.517	journal	January 2009
Lactate racemase is a nickel-dependent enzyme activated by a widespread maturation system Desguin, Benoît; Goffin, Philippe; Viaene, Eric Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4615	journal	April 2014
Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server Zheng, Heping; Chordia, Mahendra D.; Cooper, David R. Nature Protocols, Vol. 9, Issue 1 https://doi.org/10.1038/nprot.2013.172	journal	December 2013
Nickel–pincer nucleotide cofactor Hausinger, Robert P.; Desguin, Benoît; Fellner, Matthias Current Opinion in Chemical Biology, Vol. 47 https://doi.org/10.1016/j.cbpa.2018.06.019	journal	December 2018
A stability ruler for metal ion complexes Martin, R. Bruce Journal of Chemical Education, Vol. 64, Issue 5 https://doi.org/10.1021/ed064p402	journal	May 1987
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Many-body effect determines the selectivity for Ca ²⁺ and Mg ²⁺ in proteins Jing, Zhifeng; Liu, Chengwen; Qi, Rui Proceedings of the National Academy of Sciences, Vol. 115, Issue 32 https://doi.org/10.1073/pnas.1805049115	journal	July 2018
Structural Basis of Biological NO Generation by Octaheme Oxidoreductases Maalcke, Wouter J.; Dietl, Andreas; Marritt, Sophie J. Journal of Biological Chemistry, Vol. 289, Issue 3 https://doi.org/10.1074/jbc.M113.525147	journal	December 2013
Engineering Novel Metalloproteins: Design of Metal-Binding Sites into Native Protein Scaffolds Lu, Yi; Berry, Steven M.; Pfister, Thomas D. Chemical Reviews, Vol. 101, Issue 10 https://doi.org/10.1021/cr0000574	journal	October 2001
The structure of enzyme IIAlactose from Lactococcus lactis reveals a new fold and points to possible interactions of a multicomponent system Sliz, Piotr; Engelmann, Roswitha; Hengstenberg, Wolfgang Structure, Vol. 5, Issue 6 https://doi.org/10.1016/S0969-2126(97)00232-3	journal	June 1997
Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination Dokmanić, Ivan; Šikić, Mile; Tomić, Sanja Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 3 https://doi.org/10.1107/S090744490706595X	journal	February 2008
An Artificial Metalloenzyme: Creation of a Designed Copper Binding Site in a Thermostable Protein Podtetenieff, John; Taglieber, Andreas; Bill, Eckhard Angewandte Chemie International Edition, Vol. 49, Issue 30 https://doi.org/10.1002/anie.201002106	journal	June 2010

Cited By (3)

Human coronaviruses OC43 and HKU1 bind to 9- O -acetylated sialic acids via a conserved receptor-binding site in spike protein domain A Hulswit, Ruben J. G.; Lang, Yifei; Bakkers, Mark J. G. Proceedings of the National Academy of Sciences, Vol. 116, Issue 7 https://doi.org/10.1073/pnas.1809667116	journal	January 2019
Infectious salmon anaemia virus—molecular biology and pathogenesis of the infection Rimstad, E.; Markussen, T. Journal of Applied Microbiology, Vol. 129, Issue 1 https://doi.org/10.1111/jam.14567	journal	January 2020
Tilapia Lake Virus Does Not Hemagglutinate Avian and Piscine Erythrocytes and NH4Cl Does Not Inhibit Viral Replication In Vitro Chengula, Augustino Alfred; Mutoloki, Stephen; Evensen, Øystein Viruses, Vol. 11, Issue 12 https://doi.org/10.3390/v11121152	journal	December 2019

Similar Records

Analysis of the Active Site Cysteine Residue of the Sacrificial Sulfur Insertase LarE from Lactobacillus plantarum

Journal Article · Wed Aug 29 00:00:00 EDT 2018 · Biochemistry · OSTI ID:1608895

Fellner, Matthias; Rankin, Joel A.; Desguin, Benoît; +2 more

Structural insights into the catalytic mechanism of a sacrificial sulfur insertase of the N-type ATP pyrophosphatase family, LarE

Journal Article · Mon Aug 07 00:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1608895

Fellner, Matthias; Desguin, Benoît; Hausinger, Robert P.; +1 more

METAL-TYROSYL COORDINATION IN TRANSFERRIN. 2. DIFFERENCE ULTRAVIOLET SPECTROSCOPY OF DI-, TRI-, AND TETRAVALENT METAL IONS WITH ETHYLENE-BIS(0-DYDROXYPHENYLGLY-CINE).

Journal Article · Fri Aug 01 00:00:00 EDT 1980 · Journal of the American Chemical Society · OSTI ID:1608895

Pecoraro, Vincent L.; Harris, Wesley R.; Carrano, Carl J.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biochemistry
structural biology

Title: Crystallographic characterization of a tri-Asp metal-binding site at the three-fold symmetry axis of LarE

Citation Formats

References (44)

Cited By (3)

Similar Records

Related Subjects