Overcoming universal restrictions on metal selectivity by protein design

Choi, Tae Su; Tezcan, F. Akif

doi:10.1038/s41586-022-04469-8

Overcoming universal restrictions on metal selectivity by protein design

Journal Article · 02 March 2022 · Nature (London)

DOI:https://doi.org/10.1038/s41586-022-04469-8· OSTI ID:1982151

;

Not provided.

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC02-05CH11231

OSTI ID:: 1982151

Journal Information:: Nature (London), Vol. 603, Issue 7901; ISSN 0028-0836

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

References (65)

Metalloproteins and metal sensing Waldron, Kevin J.; Rutherford, Julian C.; Ford, Dianne Nature, Vol. 460, Issue 7257 https://doi.org/10.1038/nature08300	journal	August 2009
How do bacterial cells ensure that metalloproteins get the correct metal? Waldron, Kevin J.; Robinson, Nigel J. Nature Reviews Microbiology, Vol. 7, Issue 1 https://doi.org/10.1038/nrmicro2057	journal	January 2009
Competition among Metal Ions for Protein Binding Sites: Determinants of Metal Ion Selectivity in Proteins Dudev, Todor; Lim, Carmay Chemical Reviews, Vol. 114, Issue 1 https://doi.org/10.1021/cr4004665	journal	September 2013
Key Structural Motifs Balance Metal Binding and Oxidative Reactivity in a Heterobimetallic Mn/Fe Protein Kisgeropoulos, Effie C.; Griese, Julia J.; Smith, Zachary R. Journal of the American Chemical Society, Vol. 142, Issue 11 https://doi.org/10.1021/jacs.0c00333	journal	February 2020
The Bacillus anthracis class Ib ribonucleotide reductase subunit NrdF intrinsically selects manganese over iron Grāve, Kristīne; Griese, Julia J.; Berggren, Gustav JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 4 https://doi.org/10.1007/s00775-020-01782-3	journal	April 2020
Metalloregulatory proteins: Metal selectivity and allosteric switching Reyes-Caballero, Hermes; Campanello, Gregory C.; Giedroc, David P. Biophysical Chemistry, Vol. 156, Issue 2-3 https://doi.org/10.1016/j.bpc.2011.03.010	journal	July 2011
Metallochaperones, an Intracellular Shuttle Service for Metal Ions O'Halloran, Thomas V.; Culotta, Valeria Cizewski Journal of Biological Chemistry, Vol. 275, Issue 33 https://doi.org/10.1074/jbc.R000006200	journal	May 2000
Protein-folding location can regulate manganese-binding versus copper- or zinc-binding Tottey, Steve; Waldron, Kevin J.; Firbank, Susan J. Nature, Vol. 455, Issue 7216 https://doi.org/10.1038/nature07340	journal	October 2008
De Novo Design of Four-Helix Bundle Metalloproteins: One Scaffold, Diverse Reactivities Lombardi, Angela; Pirro, Fabio; Maglio, Ornella Accounts of Chemical Research https://doi.org/10.1021/acs.accounts.8b00674	journal	April 2019
Design of functional metalloproteins Lu, Yi; Yeung, Natasha; Sieracki, Nathan Nature, Vol. 460, Issue 7257 https://doi.org/10.1038/nature08304	journal	August 2009
Protein Design: Toward Functional Metalloenzymes Yu, Fangting; Cangelosi, Virginia M.; Zastrow, Melissa L. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr400458x	journal	January 2014
Artificial Metalloenzymes: Reaction Scope and Optimization Strategies Schwizer, Fabian; Okamoto, Yasunori; Heinisch, Tillmann Chemical Reviews, Vol. 118, Issue 1 https://doi.org/10.1021/acs.chemrev.7b00014	journal	May 2017
Design and Construction of Functional Supramolecular Metalloprotein Assemblies Churchfield, Lewis A.; Tezcan, F. Akif Accounts of Chemical Research, Vol. 52, Issue 2 https://doi.org/10.1021/acs.accounts.8b00617	journal	January 2019
An artificial di-iron oxo-protein with phenol oxidase activity Faiella, Marina; Andreozzi, Concetta; de Rosales, Rafael Torres Martin Nature Chemical Biology, Vol. 5, Issue 12 https://doi.org/10.1038/nchembio.257	journal	November 2009
Hydrolytic catalysis and structural stabilization in a designed metalloprotein Zastrow, Melissa L.; Peacock, Anna F. A.; Stuckey, Jeanne A. Nature Chemistry, Vol. 4, Issue 2 https://doi.org/10.1038/nchem.1201	journal	November 2011
Evolution of a highly active and enantiospecific metalloenzyme from short peptides Studer, Sabine; Hansen, Douglas A.; Pianowski, Zbigniew L. Science, Vol. 362, Issue 6420 https://doi.org/10.1126/science.aau3744	journal	December 2018
Computational redesign of a mononuclear zinc metalloenzyme for organophosphate hydrolysis Khare, Sagar D.; Kipnis, Yakov; Greisen, Per Jr Nature Chemical Biology, Vol. 8, Issue 3 https://doi.org/10.1038/nchembio.777	journal	February 2012
Rational design of a structural and functional nitric oxide reductase Yeung, Natasha; Lin, Ying-Wu; Gao, Yi-Gui Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08620	journal	November 2009
A designed supramolecular protein assembly with in vivo enzymatic activity Song, Woon Ju; Tezcan, F. Akif Science, Vol. 346, Issue 6216 https://doi.org/10.1126/science.1259680	journal	December 2014
De Novo Design of an Allosteric Metalloprotein Assembly with Strained Disulfide Bonds Churchfield, Lewis A.; Medina-Morales, Annette; Brodin, Jeffrey D. Journal of the American Chemical Society, Vol. 138, Issue 40 https://doi.org/10.1021/jacs.6b08458	journal	September 2016
A protein engineered to bind uranyl selectively and with femtomolar affinity Zhou, Lu; Bosscher, Mike; Zhang, Changsheng Nature Chemistry, Vol. 6, Issue 3 https://doi.org/10.1038/nchem.1856	journal	January 2014
Engineering A Uranyl-Specific Binding Protein from NikR Wegner, Seraphine V.; Boyaci, Hande; Chen, Hao Angewandte Chemie International Edition, Vol. 48, Issue 13, p. 2339-2341 https://doi.org/10.1002/anie.200805262	journal	February 2009
Evolution of Metal Selectivity in Templated Protein Interfaces Brodin, Jeffrey D.; Medina-Morales, Annette; Ni, Thomas Journal of the American Chemical Society, Vol. 132, Issue 25 https://doi.org/10.1021/ja910844n	journal	June 2010
Probing the minimal determinants of zinc binding with computational protein design Guffy, Sharon L.; Der, Bryan S.; Kuhlman, Brian Protein Engineering Design and Selection, Vol. 29, Issue 8 https://doi.org/10.1093/protein/gzw026	journal	June 2016
Computational approaches for de novo design and redesign of metal-binding sites on proteins Akcapinar, Gunseli Bayram; Sezerman, Osman Ugur Bioscience Reports, Vol. 37, Issue 2 https://doi.org/10.1042/BSR20160179	journal	March 2017
Cooperative cluster formation in metallothionein Byrd, Jonathan; Winge, Dennis R. Archives of Biochemistry and Biophysics, Vol. 250, Issue 1 https://doi.org/10.1016/0003-9861(86)90721-6	journal	October 1986
Conserved properties of individual Ca ²⁺ -binding sites in calmodulin Halling, D. Brent; Liebeskind, Benjamin J.; Hall, Amelia W. Proceedings of the National Academy of Sciences, Vol. 113, Issue 9 https://doi.org/10.1073/pnas.1600385113	journal	February 2016
Transition Metal Sequestration by the Host-Defense Protein Calprotectin Zygiel, Emily M.; Nolan, Elizabeth M. Annual Review of Biochemistry, Vol. 87, Issue 1 https://doi.org/10.1146/annurev-biochem-062917-012312	journal	June 2018
An efficient, step-economical strategy for the design of functional metalloproteins Rittle, Jonathan; Field, Mackenzie J.; Green, Michael T. Nature Chemistry, Vol. 11, Issue 5 https://doi.org/10.1038/s41557-019-0218-9	journal	February 2019
Stability and Folding Kinetics of Structurally Characterized Cytochrome c - b ₅₆₂ ^† ^, ^‡ Faraone-Mennella, Jasmin; Tezcan, F. Akif; Gray, Harry B. Biochemistry, Vol. 45, Issue 35 https://doi.org/10.1021/bi060242x	journal	September 2006
Molecular Insights into Human Serum Albumin as a Receptor of Amyloid-β in the Extracellular Region Choi, Tae Su; Lee, Hyuck Jin; Han, Jong Yoon Journal of the American Chemical Society, Vol. 139, Issue 43 https://doi.org/10.1021/jacs.7b08584	journal	October 2017
Bacterial sensors define intracellular free energies for correct enzyme metalation Osman, Deenah; Martini, Maria Alessandra; Foster, Andrew W. Nature Chemical Biology, Vol. 15, Issue 3 https://doi.org/10.1038/s41589-018-0211-4	journal	January 2019
Calculating metalation in cells reveals CobW acquires CoII for vitamin B12 biosynthesis while related proteins prefer ZnII Young, Tessa R.; Martini, Maria Alessandra; Foster, Andrew W. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21479-8	journal	February 2021
Directed evolution of artificial metalloenzymes for in vivo metathesis Jeschek, Markus; Reuter, Raphael; Heinisch, Tillmann Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19114	journal	August 2016
Mechanism of potassium-channel selectivity revealed by Na+ and Li+ binding sites within the KcsA pore Thompson, Ameer N.; Kim, Ilsoo; Panosian, Timothy D. Nature Structural & Molecular Biology, Vol. 16, Issue 12 https://doi.org/10.1038/nsmb.1703	journal	November 2009
Entropy redistribution controls allostery in a metalloregulatory protein Capdevila, Daiana A.; Braymer, Joseph J.; Edmonds, Katherine A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1620665114	journal	March 2017
Protein Dynamism and Evolvability Tokuriki, N.; Tawfik, D. S. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1169375	journal	April 2009
The ensemble nature of allostery Motlagh, Hesam N.; Wrabl, James O.; Li, Jing Nature, Vol. 508, Issue 7496 https://doi.org/10.1038/nature13001	journal	April 2014
The Role of Protein Loops and Linkers in Conformational Dynamics and Allostery Papaleo, Elena; Saladino, Giorgio; Lambrughi, Matteo Chemical Reviews, Vol. 116, Issue 11 https://doi.org/10.1021/acs.chemrev.5b00623	journal	February 2016
Overproduction of theBradyrhizobium japonicum c-Type Cytochrome Subunits of thecbb3Oxidase inEscherichia coli Arslan, Engin; Schulz, Henk; Zufferey, Rachel Biochemical and Biophysical Research Communications, Vol. 251, Issue 3 https://doi.org/10.1006/bbrc.1998.9549	journal	October 1998
An integrated high-throughput data acquisition system for biological solution X-ray scattering studies Martel, Anne; Liu, Ping; Weiss, Thomas M. Journal of Synchrotron Radiation, Vol. 19, Issue 3 https://doi.org/10.1107/S0909049512008072	journal	March 2012
ATSAS 3.0 : expanded functionality and new tools for small-angle scattering data analysis Manalastas-Cantos, Karen; Konarev, Petr V.; Hajizadeh, Nelly R. Journal of Applied Crystallography, Vol. 54, Issue 1 https://doi.org/10.1107/S1600576720013412	journal	February 2021
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
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
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
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
A genetic approach to analyzing membrane protein topology Manoil, C.; Beckwith, J. Science, Vol. 233, Issue 4771 https://doi.org/10.1126/science.3529391	journal	September 1986
A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives Dapprich, Stefan; Komáromi, István; Byun, K. Suzie Journal of Molecular Structure: THEOCHEM, Vol. 461-462 https://doi.org/10.1016/S0166-1280(98)00475-8	journal	April 1999
Geometry optimization with QM/MM, ONIOM, and other combined methods. I. Microiterations and constraints Vreven, Thom; Morokuma, Keiji; Farkas, Ödön Journal of Computational Chemistry, Vol. 24, Issue 6 https://doi.org/10.1002/jcc.10156	journal	April 2003
Matrix Metalloproteinase 2 Inhibition: Combined Quantum Mechanics and Molecular Mechanics Studies of the Inhibition Mechanism of (4-Phenoxyphenylsulfonyl)methylthiirane and Its Oxirane Analogue Tao, Peng; Fisher, Jed F.; Shi, Qicun Biochemistry, Vol. 48, Issue 41 https://doi.org/10.1021/bi901118r	journal	September 2009
Density‐functional thermochemistry. III. The role of exact exchange Becke, Axel D. The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652 https://doi.org/10.1063/1.464913	journal	April 1993
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Lee, Chengteh; Yang, Weitao; Parr, Robert G. Physical Review B, Vol. 37, Issue 2 https://doi.org/10.1103/PhysRevB.37.785	journal	January 1988
The effect of d-functions on molecular orbital energies for hydrocarbons Hariharan, P. C.; Pople, J. A. Chemical Physics Letters, Vol. 16, Issue 2 https://doi.org/10.1016/0009-2614(72)80259-8	journal	October 1972
6-31G ^* basis set for atoms K through Zn Rassolov, Vitaly A.; Pople, John A.; Ratner, Mark A. The Journal of Chemical Physics, Vol. 109, Issue 4 https://doi.org/10.1063/1.476673	journal	July 1998
6-31G* basis set for third-row atoms Rassolov, Vitaly A.; Ratner, Mark A.; Pople, John A. Journal of Computational Chemistry, Vol. 22, Issue 9 https://doi.org/10.1002/jcc.1058	journal	January 2001
Lennard-Jones parameters for the combined QM/MM method using the B3LYP/6-31G*/AMBER potential Freindorf, Marek; Shao, Yihan; Furlani, Thomas R. Journal of Computational Chemistry, Vol. 26, Issue 12 https://doi.org/10.1002/jcc.20264	journal	September 2005
The Amber biomolecular simulation programs Case, David A.; Cheatham, Thomas E.; Darden, Tom Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20290	journal	January 2005
Hybrid Models for Combined Quantum Mechanical and Molecular Mechanical Approaches Bakowies, Dirk; Thiel, Walter The Journal of Physical Chemistry, Vol. 100, Issue 25 https://doi.org/10.1021/jp9536514	journal	January 1996
Simulation of formamide hydrolysis by hydroxide ion in the gas phase and in aqueous solution Weiner, Scott J.; Singh, U. Chandra; Kollman, Peter A. Journal of the American Chemical Society, Vol. 107, Issue 8 https://doi.org/10.1021/ja00294a003	journal	April 1985
Metal‐Templated Design of Chemically Switchable Protein Assemblies with High‐Affinity Coordination Sites Kakkis, Albert; Gagnon, Derek; Esselborn, Julian Angewandte Chemie International Edition, Vol. 59, Issue 49 https://doi.org/10.1002/anie.202009226	journal	September 2020
Molar absorption coefficients and stability constants of metal complexes of 4-(2-pyridylazo)resorcinol (PAR): Revisiting common chelating probe for the study of metalloproteins Kocyła, Anna; Pomorski, Adam; Krężel, Artur Journal of Inorganic Biochemistry, Vol. 152 https://doi.org/10.1016/j.jinorgbio.2015.08.024	journal	November 2015
Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase Kuzmič, Petr Analytical Biochemistry, Vol. 237, Issue 2 https://doi.org/10.1006/abio.1996.0238	journal	June 1996
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
Molecular weight–gyration radius relation of globular proteins: a comparison of light scattering, small-angle X-ray scattering and structure-based data Smilgies, Detlef-M.; Folta-Stogniew, Ewa Journal of Applied Crystallography, Vol. 48, Issue 5 https://doi.org/10.1107/S1600576715015551	journal	September 2015

Similar Records

Overcoming Steric Restrictions of VRC01 HIV-1 Neutralizing Antibodies through Immunization

Journal Article · 2019 · Cell Reports · OSTI ID:1623651

Parks, K. Rachael; MacCamy, Anna J.; Trichka, Josephine; +16 more

Design of a Flexible, Zn-Selective Protein Scaffold that Displays Anti-Irving–Williams Behavior

Journal Article · 2022 · Journal of the American Chemical Society · OSTI ID:2422667

Choi, Tae Su; Tezcan, F. Akif

Exploring the repeat protein universe through computational protein design

Journal Article · 2015 · Nature (London) · OSTI ID:1378707

Brunette, TJ; Parmeggiani, Fabio; Huang, Po-Ssu; +6 more

Related Subjects

Science & Technology - Other Topics

Overcoming universal restrictions on metal selectivity by protein design

Citation Formats

References (65)

Similar Records

Related Subjects