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

Campeciño, Julius O.; Dudycz, Lech W.; Tumelty, David; Berg, Volker; Cabelli, Diane E.; Maroney, Michael J.

doi:10.1021/jacs.5b03629

Title: 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

DOI:https://doi.org/10.1021/jacs.5b03629· OSTI ID:1224774

Campeciño, Julius O. ^[1]; Dudycz, Lech W. ^[2]; Tumelty, David ^[3]; Berg, Volker ^[1]; Cabelli, Diane E. ^[4]; Maroney, Michael J. ^[1]

Univ. of Massachusetts, Amherst, MA (United States)
Lex Company Research Lab., Shirley, MA (United States)
New England Peptide, Gardner, MA (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)

In this study, computational investigations have implicated the amidate ligand in nickel superoxide dismutase (NiSOD) in stabilizing Ni-centered redox catalysis and in preventing cysteine thiolate ligand oxidation. To test these predictions, we have used an experimental approach utilizing a semisynthetic scheme that employs native chemical ligation of a pentapeptide (HCDLP) to recombinant S. coelicolor NiSOD lacking these N-terminal residues, NΔ5-NiSOD. Wild-type enzyme produced in this manner exhibits the characteristic spectral properties of recombinant WT-NiSOD and is as catalytically active. The semisynthetic scheme was also employed to construct a variant where the amidate ligand was converted to a secondary amine, H1*-NiSOD, a novel strategy that retains a backbone N-donor atom. The H1*-NiSOD variant was found to have only ~1% of the catalytic activity of the recombinant wild-type enzyme, and had altered spectroscopic properties. X-ray absorption spectroscopy reveals a four-coordinate planar site with N₂S₂-donor ligands, consistent with electronic absorption spectroscopic results indicating that the Ni center in H1*-NiSOD is mostly reduced in the as-isolated sample, as opposed to 50:50 Ni(II)/Ni(III) mixture that is typical for the recombinant wild-type enzyme. The EPR spectrum of as-isolated H1*-NiSOD accounts for ~11% of the Ni in the sample and is similar to WT-NiSOD, but more axial, with g_z < g_x,y. ¹⁴N-hyperfine is observed on g_z, confirming the addition of the apical histidine ligand in the Ni(III) complex. Lastly, the altered electronic properties and implications for redox catalysis are discussed in light of predictions based on synthetic and computational models.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC00112704; SC0012704; AC02-98CH10886

OSTI ID:: 1224774

Alternate ID(s):: OSTI ID: 1335404

Report Number(s):: BNL-108507-2015-JA; BNL-111846-2016-JA; R&D Project: CO004; KC0304030

Journal Information:: Journal of the American Chemical Society, Vol. 137, Issue 28; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 17 works

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References (55)

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
Backbone-Engineered High-Potential Iron Proteins: Effects of Active-Site Hydrogen Bonding on Reduction Potential Low, Donald W.; Hill, Michael G. Journal of the American Chemical Society, Vol. 122, Issue 44 https://doi.org/10.1021/ja001218o	journal	November 2000
Structural comparison of alkylated derivatives of (bmmp-dmed)Ni and (bmmp-dmed)Zn Grapperhaus, Craig A.; Mullins, Christopher S.; Mashuta, Mark S. Inorganica Chimica Acta, Vol. 358, Issue 3 https://doi.org/10.1016/j.ica.2004.09.035	journal	February 2005
Analysis of Backbone Hydrogen Bonding in a β-Turn of Staphylococcal Nuclease Shin, Injae; Ting, Alice Y.; Schultz, Peter G. Journal of the American Chemical Society, Vol. 119, Issue 51 https://doi.org/10.1021/ja972820q	journal	December 1997
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
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
Amino Acids and Peptides. L. Development of a Novel N.PI.-Protecting Group for Histidine, N.PI.-2-Adamantyloxymethylhistidine, and Its Application to Peptide Synthesis. Okada, Yoshio; Wang, Jidong; Yamamoto, Takeshi Chemical and Pharmaceutical Bulletin, Vol. 45, Issue 3 https://doi.org/10.1248/cpb.45.452	journal	January 1997
Mycobacterium tuberculosis NmtR Harbors a Nickel Sensing Site with Parallels to Escherichia coli RcnR Reyes-Caballero, Hermes; Lee, Chul Won; Giedroc, David P. Biochemistry, Vol. 50, Issue 37 https://doi.org/10.1021/bi200737a	journal	September 2011
Communication between the Zinc and Nickel Sites in Dimeric HypA: Metal Recognition and pH Sensing Herbst, Robert W.; Perovic, Iva; Martin-Diaconescu, Vlad Journal of the American Chemical Society, Vol. 132, Issue 30 https://doi.org/10.1021/ja1005724	journal	August 2010
Probing Intermolecular Main Chain Hydrogen Bonding in Serine Proteinase−Protein Inhibitor Complexes: Chemical Synthesis of Backbone-Engineered Turkey Ovomucoid Third Domain Lu, Wuyuan; Qasim, M. A.; Laskowski,, Michael Biochemistry, Vol. 36, Issue 4 https://doi.org/10.1021/bi9625612	journal	January 1997
Oxygen Capture by Sulfur in Nickel Thiolates Grapperhaus, Craig A.; Darensbourg, Marcetta Y. Accounts of Chemical Research, Vol. 31, Issue 8 https://doi.org/10.1021/ar950048v	journal	May 1998
An Experimental Approach to Evaluating the Role of Backbone Interactions in Proteins Using Unnatural Amino Acid Mutagenesis ^† Koh, John T.; Cornish, Virginia W.; Schultz, Peter G. Biochemistry, Vol. 36, Issue 38 https://doi.org/10.1021/bi9707685	journal	September 1997
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
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
Unraveling the Helicobacter pylori UreG zinc binding site using X-ray absorption spectroscopy (XAS) and structural modeling Martin-Diaconescu, Vlad; Bellucci, Matteo; Musiani, Francesco JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 3 https://doi.org/10.1007/s00775-011-0857-9	journal	November 2011
Site-specific incorporation of nonnatural residues during in vitro protein biosynthesis with semi-synthetic aminoacyl-tRNAs Bain, J. D.; Diala, Edward S.; Glabe, Charles G. Biochemistry, Vol. 30, Issue 22 https://doi.org/10.1021/bi00236a013	journal	June 1991
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
The Influence of Amine/Amide versus Bisamide Coordination in Nickel Superoxide Dismutase Neupane, Kosh P.; Shearer, Jason Inorganic Chemistry, Vol. 45, Issue 26 https://doi.org/10.1021/ic061156o	journal	December 2006
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
Synthesis of highly epimerizable N-protected α-amino aldehydes of high enantiomeric excess Myers, Andrew G.; Zhong, Boyu; Movassaghi, Mohammad Tetrahedron Letters, Vol. 41, Issue 9 https://doi.org/10.1016/S0040-4039(99)02293-5	journal	February 2000
Design and chemical synthesis of a sequence-specific DNA-cleaving protein Mack, David P.; Iverson, Brent L.; Dervan, Peter B. Journal of the American Chemical Society, Vol. 110, Issue 22 https://doi.org/10.1021/ja00230a067	journal	October 1988
Nickel-Specific Response in the Transcriptional Regulator, Escherichia coli NikR Leitch, Sharon; Bradley, Michael J.; Rowe, Jessica L. Journal of the American Chemical Society, Vol. 129, Issue 16 https://doi.org/10.1021/ja068505y	journal	April 2007
A Nickel Superoxide Dismutase Maquette That Reproduces the Spectroscopic and Functional Properties of the Metalloenzyme Shearer, Jason; Long, Linh M. Inorganic Chemistry, Vol. 45, Issue 6 https://doi.org/10.1021/ic0514344	journal	March 2006
Characterization of Semisynthetic and Naturally N ^α -Acetylated α-Synuclein in Vitro and in Intact Cells : IMPLICATIONS FOR AGGREGATION AND CELLULAR PROPERTIES OF α-SYNUCLEIN Fauvet, Bruno; Fares, Mohamed-Bilal; Samuel, Filsy Journal of Biological Chemistry, Vol. 287, Issue 34 https://doi.org/10.1074/jbc.M112.383711	journal	June 2012
[Me ₄ N](Ni ^II (BEAAM)): A Synthetic Model for Nickel Superoxide Dismutase That Contains Ni in a Mixed Amine/Amide Coordination Environment Shearer, Jason; Zhao, Ningfeng Inorganic Chemistry, Vol. 45, Issue 24 https://doi.org/10.1021/ic061604s	journal	November 2006
Superoxide as an intracellular radical sink Winterbourn, Christine C. Free Radical Biology and Medicine, Vol. 14, Issue 1 https://doi.org/10.1016/0891-5849(93)90512-S	journal	January 1993
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
Density functional theory investigations of NiN2S2 reactivity as a function of nitrogen donor type and N–H···S hydrogen bonding inspired by nickel-containing superoxide dismutase Mullins, C. S.; Grapperhaus, C. A.; Kozlowski, P. M. JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 5 https://doi.org/10.1007/s00775-006-0109-6	journal	May 2006
Metallopeptide Based Mimics with Substituted Histidines Approximate a Key Hydrogen Bonding Network in the Metalloenzyme Nickel Superoxide Dismutase Shearer, Jason; Neupane, Kosh P.; Callan, Paige E. Inorganic Chemistry, Vol. 48, Issue 22 https://doi.org/10.1021/ic9010407	journal	November 2009
Peptide Backbone Chemistry and Membrane Channel Function: Effects of a Single Amide-to-Ester Replacement on Gramicidin Channel Structure and Function ^† Jude, Anthony R.; Providence, Lyndon L.; Schmutzer, Sigrid E. Biochemistry, Vol. 40, Issue 5 https://doi.org/10.1021/bi001562y	journal	February 2001
Direct Production of Proteins with N-Terminal Cysteine for Site-Specific Conjugation Gentle, Ian E.; De Souza, David P.; Baca, Manuel Bioconjugate Chemistry, Vol. 15, Issue 3 https://doi.org/10.1021/bc049965o	journal	May 2004
Oxidation of nickel thiolate ligands by dioxygen Mirza, Shaukat A.; Pressler, Michelle A.; Kumar, Manoj Inorganic Chemistry, Vol. 32, Issue 6 https://doi.org/10.1021/ic00058a038	journal	March 1993
Probing the Role of Backbone Hydrogen Bonds in Protein–Peptide Interactions by Amide-to-Ester Mutations Eildal, Jonas N. N.; Hultqvist, Greta; Balle, Thomas Journal of the American Chemical Society, Vol. 135, Issue 35 https://doi.org/10.1021/ja402875h	journal	June 2013
Fe(III) and Co(III) Centers with Carboxamido Nitrogen and Modified Sulfur Coordination: Lessons Learned from Nitrile Hydratase Harrop, Todd C.; Mascharak, Pradip K. Accounts of Chemical Research, Vol. 37, Issue 4 https://doi.org/10.1021/ar0301532	journal	February 2004
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
Subtle Bite-Angle Influences on N ₂ S ₂ Ni Complexes Smee, Jason J.; Miller, Matthew L.; Grapperhaus, Craig A. Inorganic Chemistry, Vol. 40, Issue 14 https://doi.org/10.1021/ic0008619	journal	July 2001
An Efficient Fmoc-SPPS Approach for the Generation of Thioester Peptide Precursors for Use in Native Chemical Ligation Blanco-Canosa, Juan B.; Dawson, Philip E. Angewandte Chemie International Edition, Vol. 47, Issue 36 https://doi.org/10.1002/anie.200705471	journal	August 2008
Desulfurization of cysteine-containing peptides resulting from sample preparation for protein characterization by mass spectrometry: Desulfurization of cysteine-containing peptides Wang, Zhouxi; Rejtar, Tomas; Zhou, Zhaohui Sunny Rapid Communications in Mass Spectrometry, Vol. 24, Issue 3 https://doi.org/10.1002/rcm.4383	journal	January 2010
Probing Variable Axial Ligation in Nickel Superoxide Dismutase Utilizing Metallopeptide-Based Models: Insight into the Superoxide Disproportionation Mechanism Neupane, Kosh P.; Gearty, Kristie; Francis, Ashish Journal of the American Chemical Society, Vol. 129, Issue 47 https://doi.org/10.1021/ja0731625	journal	November 2007
Probing Variable Amine/Amide Ligation in Ni ^II N ₂ S ₂ Complexes Using Sulfur K-Edge and Nickel L-Edge X-ray Absorption Spectroscopies: Implications for the Active Site of Nickel Superoxide Dismutase Shearer, Jason; Dehestani, Ahmad; Abanda, Franklin Inorganic Chemistry, Vol. 47, Issue 7 https://doi.org/10.1021/ic7019878	journal	March 2008
Singlet Oxygen and the Production of Sulfur Oxygenates of Nickel(II) and Palladium(II) Thiolates Grapperhaus, Craig A.; Maguire, Michael J.; Tuntulani, Thawatchai Inorganic Chemistry, Vol. 36, Issue 9 https://doi.org/10.1021/ic970050d	journal	April 1997
Amino Terminal Cu(II)- and Ni(II)-Binding (ATCUN) Motif of Proteins and Peptides: Metal Binding, DNA Cleavage, and Other Properties Harford, Catherine; Sarkar, Bibudhendra Accounts of Chemical Research, Vol. 30, Issue 3 https://doi.org/10.1021/ar9501535	journal	March 1997
Superoxide Dismutase from Escherichia coli B Keele, Bernard B.; McCord, J. M.; Fridovich, I. Journal of Biological Chemistry, Vol. 245, Issue 22 https://doi.org/10.1016/S0021-9258(18)62675-4	journal	November 1970
Modulation of Reactivity in Native Chemical Ligation through the Use of Thiol Additives Dawson, Philip E.; Churchill, Michael J.; Ghadiri, M. Reza Journal of the American Chemical Society, Vol. 119, Issue 19 https://doi.org/10.1021/ja962656r	journal	May 1997
Unique Reactivity of a Tetradentate N ₂ S ₂ Complex of Nickel: Intermediates in the Production of Sulfur Oxygenates Kaasjager, Vincent E.; Bouwman, Elisabeth; Gorter, S. Inorganic Chemistry, Vol. 41, Issue 7 https://doi.org/10.1021/ic010784x	journal	April 2002
Bisamidate and Mixed Amine/Amidate NiN ₂ S ₂ Complexes as Models for Nickel-Containing Acetyl Coenzyme A Synthase and Superoxide Dismutase: An Experimental and Computational Study Mathrubootham, Vaidyanathan; Thomas, Jason; Staples, Richard Inorganic Chemistry, Vol. 49, Issue 12 https://doi.org/10.1021/ic9023053	journal	June 2010
Mitochondrial free radical generation, oxidative stress, and aging11This article is dedicated to the memory of our dear friend, colleague, and mentor Lars Ernster (1920–1998), in gratitude for all he gave to us. Cadenas, Enrique; Davies, Kelvin J. A. Free Radical Biology and Medicine, Vol. 29, Issue 3-4 https://doi.org/10.1016/S0891-5849(00)00317-8	journal	August 2000
Nickel-mediated sequence-specific oxidative cleavage of DNA by a designed metalloprotein Mack, David P.; Dervan, Peter B. Journal of the American Chemical Society, Vol. 112, Issue 11 https://doi.org/10.1021/ja00167a102	journal	May 1990
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
Sequence-specific oxidative cleavage of DNA by a designed metalloprotein, nickel(II).cntdot.GGH(Hin139-190) Mack, David P.; Dervan, Peter B. Biochemistry, Vol. 31, Issue 39 https://doi.org/10.1021/bi00154a011	journal	October 1992
Superoxide dismutases—a review of the metal-associated mechanistic variations Abreu, Isabel A.; Cabelli, Diane E. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2 https://doi.org/10.1016/j.bbapap.2009.11.005	journal	February 2010
Protein Backbone Engineering through Total Chemical Synthesis: New Insight into the Mechanism of HIV-1 Protease Catalysis Baca, Manuel; Kent, Stephen B. H. Tetrahedron, Vol. 56, Issue 48 https://doi.org/10.1016/S0040-4020(00)00835-8	journal	November 2000
Structure of Thiocyanate Hydrolase: A New Nitrile Hydratase Family Protein with a Novel Five-coordinate Cobalt(III) Center Arakawa, Takatoshi; Kawano, Yoshiaki; Kataoka, Shingo Journal of Molecular Biology, Vol. 366, Issue 5 https://doi.org/10.1016/j.jmb.2006.12.011	journal	March 2007
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
Amino Acid Derivatives. I. Carboallyloxy Derivatives of α-Amino Acids ^1,2 Stevens, Carl M.; Watanabe, Ronald Journal of the American Chemical Society, Vol. 72, Issue 2 https://doi.org/10.1021/ja01158a020	journal	February 1950

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