In vitro maturation of NiSOD reveals a role for cytoplasmic histidine in processing and metalation

Basak, Priyanka; Cabelli, Diane E.; Chivers, Peter T.; Farquhar, Erik R.; Maroney, Michael J.

doi:10.1093/mtomcs/mfad054

Title: In vitro maturation of NiSOD reveals a role for cytoplasmic histidine in processing and metalation

Journal Article · Mon Sep 18 00:00:00 EDT 2023 · Metallomics (Online)

DOI:https://doi.org/10.1093/mtomcs/mfad054· OSTI ID:2007526

Basak, Priyanka ^[1]; Cabelli, Diane E. ^[2];

^[3];

^[4];

^[1]

University of Massachusetts, Amherst, MA (United States)
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Durham University (United Kingdom)
Brookhaven National Laboratory (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)

The importance of cellular low molecular weight (LMW) ligands in metalloenzyme maturation is largely unexplored. Maturation of NiSOD requires post-translational N-terminal processing of the proenzyme, SodN, by its cognate protease, SodX. Here we provide evidence for the participation of L-histidine in the protease-dependent maturation of Nickel-dependent Superoxide Dismutase (NiSOD) from Streptomyces coelicolor. Furthermore, in vitro studies using purified proteins cloned from S. coelicolor and overexpressed in E. coli support a model where a ternary complex formed between the substrate (SodN), the protease (SodX) and L-Histidine creates a novel Ni-binding site that is capable of the N-terminal processing of SodN and specifically incorporates Ni into the apo-NiSOD product. Thus, L-Histidine serves many of the functions associated with a metallochaperone or, conversely, eliminates the need for a metallochaperone in NiSOD maturation.

This content will become publicly available on Wed Sep 18 00:00:00 EDT 2024

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS); National Institutes of Health (NIH)

Grant/Contract Number:: SC0012704; R01-GM069696

OSTI ID:: 2007526

Report Number(s):: BNL-224865-2023-JAAM

Journal Information:: Metallomics (Online), Vol. 15, Issue 11; ISSN 1756-591X

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Analytical Methods for Imaging Metals in Biology: From Transition Metal Metabolism to Transition Metal Signaling Ackerman, Cheri M.; Lee, Sumin; Chang, Christopher J. Analytical Chemistry, Vol. 89, Issue 1 https://doi.org/10.1021/acs.analchem.6b04631	journal	December 2016
Metal homeostasis and resistance in bacteria Chandrangsu, Pete; Rensing, Christopher; Helmann, John D. Nature Reviews Microbiology, Vol. 15, Issue 6 https://doi.org/10.1038/nrmicro.2017.15	journal	March 2017
Low-molecular-mass labile metal pools in Escherichia coli: advances using chromatography and mass spectrometry Brawley, Hayley N.; Lindahl, Paul A. JBIC Journal of Biological Inorganic Chemistry, Vol. 26, Issue 4 https://doi.org/10.1007/s00775-021-01864-w	journal	May 2021
Metal ion ligands in hyperaccumulating plants Callahan, Damien L.; Baker, Alan J. M.; Kolev, Spas D. JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 1 https://doi.org/10.1007/s00775-005-0056-7	journal	December 2005
Identification of nickel chelators in three hyperaccumulating plants: An X-ray spectroscopic study Montargès-Pelletier, Emmanuelle; Chardot, Vanessa; Echevarria, Guillaume Phytochemistry, Vol. 69, Issue 8 https://doi.org/10.1016/j.phytochem.2008.02.009	journal	May 2008
LC–MS and GC–MS metabolite profiling of nickel(II) complexes in the latex of the nickel-hyperaccumulating tree Sebertia acuminata and identification of methylated aldaric acid as a new nickel(II) ligand Callahan, Damien L.; Roessner, Ute; Dumontet, Vincent Phytochemistry, Vol. 69, Issue 1 https://doi.org/10.1016/j.phytochem.2007.07.001	journal	January 2008
A tight tunable range for Ni(II) sensing and buffering in cells Foster, Andrew W.; Pernil, Rafael; Patterson, Carl J. Nature Chemical Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nchembio.2310	journal	February 2017
Identification of Ni-(l-His)2 as a substrate for NikABCDE-dependent nickel uptake in Escherichia coli Chivers, Peter T.; Benanti, Erin L.; Heil-Chapdelaine, Vanessa Metallomics, Vol. 4, Issue 10 https://doi.org/10.1039/c2mt20139a	journal	January 2012
Nickel recognition by bacterial importer proteins Chivers, Peter T. Metallomics, Vol. 7, Issue 4 https://doi.org/10.1039/C4MT00310A	journal	January 2015
A novel nickel-containing superoxide dismutase from Streptomyces spp Youn, Hong-Duk; Kim, Eun-Ja; Roe, Jung-Hye Biochemical Journal, Vol. 318, Issue 3 https://doi.org/10.1042/bj3180889	journal	September 1996
Nickel Superoxide Dismutase Structure and Mechanism ^† Barondeau, David P.; Kassmann, Carey J.; Bruns, Cami K. Biochemistry, Vol. 43, Issue 25 https://doi.org/10.1021/bi0496081	journal	June 2004
Expression, Reconstitution, and Mutation of Recombinant Streptomyces c oelicolor NiSOD Bryngelson, Peter A.; Arobo, Sumonu E.; Pinkham, Jennifer L. Journal of the American Chemical Society, Vol. 126, Issue 2 https://doi.org/10.1021/ja0387507	journal	January 2004
Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor Ahn, Bo-Eun; Cha, Joonseok; Lee, Eun-Jin Molecular Microbiology, Vol. 59, Issue 6 https://doi.org/10.1111/j.1365-2958.2006.05065.x	journal	March 2006
Superoxide dismutases: Ancient enzymes and new insights Miller, Anne-Frances FEBS Letters, Vol. 586, Issue 5 https://doi.org/10.1016/j.febslet.2011.10.048	journal	November 2011
Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton Cuvelier, M. L.; Allen, A. E.; Monier, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1001665107	journal	July 2010
Crystal structure of nickel-containing superoxide dismutase reveals another type of active site Wuerges, J.; Lee, J. -W.; Yim, Y. -I. Proceedings of the National Academy of Sciences, Vol. 101, Issue 23 https://doi.org/10.1073/pnas.0308514101	journal	June 2004
Examination of the Nickel Site Structure and Reaction Mechanism in Streptomyces seoulensis Superoxide Dismutase Choudhury, Suranjan B.; Lee, Jin-Won; Davidson, Gerard Biochemistry, Vol. 38, Issue 12 https://doi.org/10.1021/bi982537j	journal	March 1999
Superoxide Dismutases and Superoxide Reductases Sheng, Yuewei; Abreu, Isabel A.; Cabelli, Diane E. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr4005296	journal	January 2014
Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Müller Kim, Eun-Ja; Chung, Hye-Jung; Suh, Bumsu Molecular Microbiology, Vol. 27, Issue 1 https://doi.org/10.1046/j.1365-2958.1998.00674.x	journal	January 1998
CbiX-homologous protein (CbiXhp), a metal-binding protein, fromStreptomyces seoulensisis involved in expression of nickel-containing superoxide dismutase Kim, In-Kwon; Yim, Yang-In; Kim, Young-Min FEMS Microbiology Letters, Vol. 228, Issue 1 https://doi.org/10.1016/S0378-1097(03)00719-5	journal	November 2003
In Vivo Production of Active Nickel Superoxide Dismutase from Prochlorococcus marinus MIT9313 Is Dependent on Its Cognate Peptidase Eitinger, Thomas Journal of Bacteriology, Vol. 186, Issue 22 https://doi.org/10.1128/JB.186.22.7821-7825.2004	journal	November 2004
Proteolytic cleavage orchestrates cofactor insertion and protein assembly in [NiFe]-hydrogenase biosynthesis Senger, Moritz; Stripp, Sven T.; Soboh, Basem Journal of Biological Chemistry, Vol. 292, Issue 28 https://doi.org/10.1074/jbc.M117.788125	journal	July 2017
[NiFe]-Hydrogenase Maturation Lacasse, Michael J.; Zamble, Deborah B. Biochemistry, Vol. 55, Issue 12 https://doi.org/10.1021/acs.biochem.5b01328	journal	March 2016
Spontaneous, non-enzymatic breakdown of peptides during enzymatic protein hydrolysis Butré, Claire I.; Buhler, Sofie; Sforza, Stefano Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8 https://doi.org/10.1016/j.bbapap.2015.03.004	journal	August 2015
The Role of Mixed Amine/Amide Ligation in Nickel Superoxide Dismutase Huang, Hsin-Ting; Dillon, Stephanie; Ryan, Kelly C. Inorganic Chemistry, Vol. 57, Issue 20 https://doi.org/10.1021/acs.inorgchem.8b01499	journal	October 2018
Pro5 is not essential for the formation of ‘Ni-hook’ in nickel superoxide dismutase Basak, Priyanka; Zambelli, Barbara; Cabelli, Diane E. Journal of Inorganic Biochemistry, Vol. 234 https://doi.org/10.1016/j.jinorgbio.2022.111858	journal	September 2022
Spectroscopic and Computational Studies of Ni Superoxide Dismutase: Electronic Structure Contributions to Enzymatic Function Fiedler, Adam T.; Bryngelson, Peter A.; Maroney, Michael J. Journal of the American Chemical Society, Vol. 127, Issue 15 https://doi.org/10.1021/ja042521i	journal	April 2005
UniProt: a worldwide hub of protein knowledge Consortium, The UniProt Nucleic Acids Research https://doi.org/10.1093/nar/gky1049		November 2018
Periodic acid–Schiff’s reagent assay for carbohydrates in a microtiter plate format Kilcoyne, Michelle; Gerlach, Jared Q.; Farrell, Mark P. Analytical Biochemistry, Vol. 416, Issue 1 https://doi.org/10.1016/j.ab.2011.05.006	journal	September 2011
Quick measurement of protein sulfhydryls with Ellman's reagent and with 4,4′-dithiodipyridine Riener, Christian K.; Kada, Gerald; Gruber, Hermann J. Analytical and Bioanalytical Chemistry, Vol. 373, Issue 4-5 https://doi.org/10.1007/s00216-002-1347-2	journal	July 2002
Removal and replacement of metal ions in metallopeptidases Auld, David S. Proteolytic Enzymes: Aspartic and Metallo Peptidases https://doi.org/10.1016/0076-6879(95)48016-1	book	January 1995
Crystal structure of a bacterial signal peptidase in complex with a β-lactam inhibitor Paetzel, Mark; Dalbey, Ross E.; Strynadka, Natalie C. J. Nature, Vol. 396, Issue 6707 https://doi.org/10.1038/24196	journal	November 1998
Scalable Access to Arylomycins via C–H Functionalization Logic Peters, David S.; Romesberg, Floyd E.; Baran, Phil S. Journal of the American Chemical Society, Vol. 140, Issue 6 https://doi.org/10.1021/jacs.8b00087	journal	February 2018
Bacterial Signal Peptidases Paetzel, Mark Subcellular Biochemistry https://doi.org/10.1007/978-3-030-18768-2_7	book	January 2019
Crystallographic and Biophysical Analysis of a Bacterial Signal Peptidase in Complex with a Lipopeptide-based Inhibitor Paetzel, Mark; Goodall, Jonathon J.; Kania, Malgosia Journal of Biological Chemistry, Vol. 279, Issue 29 https://doi.org/10.1074/jbc.M401686200	journal	July 2004
The Phyre2 web portal for protein modeling, prediction and analysis Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M. Nature Protocols, Vol. 10, Issue 6 https://doi.org/10.1038/nprot.2015.053	journal	May 2015
Role of Conserved Tyrosine Residues in NiSOD Catalysis: A Case of Convergent Evolution Herbst, Robert W.; Guce, Abigail; Bryngelson, Peter A. Biochemistry, Vol. 48, Issue 15 https://doi.org/10.1021/bi802029t	journal	March 2009
Isothermal Titration Calorimetry Measurements of Ni(II) and Cu(II) Binding to His, GlyGlyHis, HisGlyHis, and Bovine Serum Albumin: A Critical Evaluation Zhang, Yi; Akilesh, Shreeram; Wilcox, Dean E. Inorganic Chemistry, Vol. 39, Issue 14 https://doi.org/10.1021/ic000036s	journal	June 2000
Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli Bennett, Bryson D.; Kimball, Elizabeth H.; Gao, Melissa Nature Chemical Biology, Vol. 5, Issue 8 https://doi.org/10.1038/nchembio.186	journal	June 2009
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
Stereoselectivity in the metal complex catalyzed hydrolysis of amino acid esters—II The role of a catalyst structure Blackburn, John R.; Jones, Mark M. Journal of Inorganic and Nuclear Chemistry, Vol. 35, Issue 5 https://doi.org/10.1016/0022-1902(73)80251-9	journal	May 1973
X-ray spectroscopic studies of nickel complexes, with application to the structure of nickel sites in hydrogenases Colpas, Gerard J.; Maroney, Michael J.; Bagyinka, Csaba. Inorganic Chemistry, Vol. 30, Issue 5 https://doi.org/10.1021/ic00005a010	journal	March 1991
EXAFS, EPR, and Electronic Absorption Spectroscopic Study of the .alpha. Metallo Subunit of CO Dehydrogenase from Clostridium thermoaceticum Xia, Jinqiang; Dong, Jun; Wang, Shengke Journal of the American Chemical Society, Vol. 117, Issue 27 https://doi.org/10.1021/ja00132a004	journal	July 1995
On the structure of the nickel/iron/sulfur center of the carbon monoxide dehydrogenase from Rhodospirillum rubrum: an x-ray absorption spectroscopy study. Tan, G. O.; Ensign, S. A.; Ciurli, S. Proceedings of the National Academy of Sciences, Vol. 89, Issue 10 https://doi.org/10.1073/pnas.89.10.4427	journal	May 1992
Structural investigations of nickel complexes with nitrogen and sulfur donor ligands Colpas, Gerard J.; Kumar, Manoj; Day, Roberta O. Inorganic Chemistry, Vol. 29, Issue 23 https://doi.org/10.1021/ic00348a037	journal	November 1990
Nickel Superoxide Dismutase: Structural and Functional Roles of His1 and Its H-Bonding Network Ryan, Kelly C.; Guce, Abigail I.; Johnson, Olivia E. Biochemistry, Vol. 54, Issue 4 https://doi.org/10.1021/bi501258u	journal	January 2015
Ni(II) and Co(II) Sensing by Escherichia coli RcnR Iwig, Jeffrey S.; Leitch, Sharon; Herbst, Robert W. Journal of the American Chemical Society, Vol. 130, Issue 24 https://doi.org/10.1021/ja710067d	journal	May 2008
Promiscuous Nickel Import in Human Pathogens: Structure, Thermodynamics, and Evolution of Extracytoplasmic Nickel-Binding Proteins Lebrette, Hugo; Brochier-armanet, Céline; Zambelli, Barbara Structure, Vol. 22, Issue 10 https://doi.org/10.1016/j.str.2014.07.012	journal	October 2014
Nickel superoxide dismutase: structural and functional roles of Cys2 and Cys6 Ryan, Kelly C.; Johnson, Olivia E.; Cabelli, Diane E. JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 5 https://doi.org/10.1007/s00775-010-0645-y	journal	March 2010
Nickel Coordination Compounds: Classification and Analysis of Crystallographic and Structural data Melnik,, Milan; Sramko,, Tibor; Dunaj--Jurco,, Michal Reviews in Inorganic Chemistry, Vol. 14, Issue 1-4 https://doi.org/10.1515/REVIC.1994.14.1-4.1	journal	September 1994
New octahedral thiolato complexes of divalent nickel: syntheses, structures, and properties of (Et4N)[Ni(SC5H4N)3] and (Ph4P)[Ni(SC4H3N2)3].CH3CN Rosenfield, Steven G.; Berends, Hilde P.; Gelmini, Lucio Inorganic Chemistry, Vol. 26, Issue 17 https://doi.org/10.1021/ic00264a015	journal	August 1987
Nickel serves as a substrate recognition motif for the endopeptidase involved in hydrogenase maturation: Nickel recognition by maturation endopeptidase Theodoratou, Ekaterini; Paschos, Athanasios; Magalon, Axel European Journal of Biochemistry, Vol. 267, Issue 7 https://doi.org/10.1046/j.1432-1327.2000.01202.x	journal	April 2000
In vivo and in vitro nickel-dependent processing of the [NiFe] hydrogenase in Azotobacter vinelandii Menon, A. L.; Robson, R. L. Journal of Bacteriology, Vol. 176, Issue 2 https://doi.org/10.1128/jb.176.2.291-295.1994	journal	January 1994
Fidelity of metal insertion into hydrogenases Magalon, Axel; Blokesch, Melanie; Zehelein, Eva FEBS Letters, Vol. 499, Issue 1-2 https://doi.org/10.1016/S0014-5793(01)02525-X	journal	June 2001
Maturation of [NiFe]-hydrogenases in Escherichia coli: The HypC Cycle Blokesch, Melanie; Böck, August Journal of Molecular Biology, Vol. 324, Issue 2, p. 287-296 https://doi.org/10.1016/S0022-2836(02)01070-7	journal	November 2002
Nickel Ligation of the N-Terminal Amine of HypA Is Required for Urease Maturation in Helicobacter pylori Hu, Heidi Q.; Johnson, Ryan C.; Merrell, D. Scott Biochemistry, Vol. 56, Issue 8 https://doi.org/10.1021/acs.biochem.6b00912	journal	February 2017
The Periodate-Schiff Reaction: Specificity, Kinetics, and Reaction Products with pure Substrates Dahlqvist, Arne; Olsson, Inge; NordÉN, ÅKe Journal of Histochemistry & Cytochemistry, Vol. 13, Issue 6 https://doi.org/10.1177/13.6.423	journal	July 1965
A Semisynthetic Strategy Leads to Alteration of the Backbone Amidate Ligand in the NiSOD Active Site Campeciño, Julius O.; Dudycz, Lech W.; Tumelty, David Journal of the American Chemical Society, Vol. 137, Issue 28 https://doi.org/10.1021/jacs.5b03629	journal	July 2015
SIXPack a Graphical User Interface for XAS Analysis Using IFEFFIT Webb, S. M. Physica Scripta https://doi.org/10.1238/Physica.Topical.115a01011	journal	January 2005

Similar Records

A semisynthetic strategy leads to alteration of the backbone amidate ligand in the NiSOD active site

Journal Article · Wed Jul 01 00:00:00 EDT 2015 · Journal of the American Chemical Society · OSTI ID:2007526

Campeciño, Julius O.; Dudycz, Lech W.; Tumelty, David; +3 more

The Role of Conserved Tyrosine Residues in NiSOD Catalysis: A Case of Convergent Evolution

Journal Article · Thu Jan 01 00:00:00 EST 2009 · Biochemistry · OSTI ID:2007526

Herbst, R; Guce, A; Bryngelson, P; +5 more

A Superoxide Dismutase Maquette That Reproduces the Spectroscopic and Functional Properties of the Metalloenzyme

Journal Article · Sun Jan 01 00:00:00 EST 2006 · Inorg. Chem. · OSTI ID:2007526

Shearer, J; Long, L

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
nickel superoxide dismutase
enzyme maturation

Title: In vitro maturation of NiSOD reveals a role for cytoplasmic histidine in processing and metalation

Citation Formats

References (59)

Similar Records

Related Subjects