Cytochrome P460 Cofactor Maturation Proceeds via Peroxide-Dependent Post-translational Modification

Bollmeyer, Melissa M.; Coleman, Rachael E.; Majer, Sean H.; Ferrao, Silas D.; Lancaster, Kyle M.

doi:10.1021/jacs.3c03608

Cytochrome P460 Cofactor Maturation Proceeds via Peroxide-Dependent Post-translational Modification

Journal Article · 20 June 2023 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.3c03608· OSTI ID:2423359

Bollmeyer, Melissa M. ^[1]; ^[1]; ^[1]; Ferrao, Silas D. ^[1]; ^[1]

Department of Chemistry and Chemical Biology, Baker Laboratory, Cornell University, 162 Sciences Drive, Ithaca, New York 14853, United States

Not provided.

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

Sponsoring Organization:: USDOE

DOE Contract Number:: AC02-06CH11357

OSTI ID:: 2423359

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 26 Vol. 145; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

References (53)

Heme Oxygenase Reveals Its Strategy for Catalyzing Three Successive Oxygenation Reactions Matsui, Toshitaka; Unno, Masaki; Ikeda-Saito, Masao Accounts of Chemical Research, Vol. 43, Issue 2 https://doi.org/10.1021/ar9001685	journal	February 2010
Cytochrome P460 of Nitrosomonas europaea. Formation of the heme-lysine cross-link in a heterologous host and mutagenic conversion to a non-cross-linked cytochrome c ' Bergmann, David J.; Hooper, Alan B. European Journal of Biochemistry, Vol. 270, Issue 9 https://doi.org/10.1046/j.1432-1033.2003.03550.x	journal	May 2003
Redox Proteomics: Chemical Principles, Methodological Approaches and Biological/Biomedical Promises Bachi, Angela; Dalle-Donne, Isabella; Scaloni, Andrea Chemical Reviews, Vol. 113, Issue 1 https://doi.org/10.1021/cr300073p	journal	November 2012
Magnetic spectroscopic (EPR, ESEEM, Mössbauer, MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins Walker, F. Ann Coordination Chemistry Reviews, Vol. 185-186 https://doi.org/10.1016/S0010-8545(99)00029-6	journal	May 1999
Catalytic Mechanism of Heme Oxygenase through EPR and ENDOR of Cryoreduced Oxy-Heme Oxygenase and Its Asp 140 Mutants Davydov, Roman; Kofman, Viktoria; Fujii, Hiroshi Journal of the American Chemical Society, Vol. 124, Issue 8 https://doi.org/10.1021/ja0122391	journal	February 2002
Role of Arginine 38 in Horseradish Peroxidase Rodriguez-Lopez, Jose Neptuno; Smith, Andrew T.; Thorneley, Roger N. F. Journal of Biological Chemistry, Vol. 271, Issue 8 https://doi.org/10.1074/jbc.271.8.4023	journal	February 1996
The chemistry and biochemistry of heme c: functional bases for covalent attachment Bowman, Sarah E. J.; Bren, Kara L. Natural Product Reports, Vol. 25, Issue 6 https://doi.org/10.1039/b717196j	journal	January 2008
A noncanonical heme oxygenase specific for the degradation of c-type heme Li, Shuxin; Isiorho, Eta A.; Owens, Victoria L. Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100666	journal	January 2021
Spectroscopic Evidence for Electronic Control of Heme Hydroxylation by IsdG Conger, Matthew A.; Cornetta, Amanda R.; Liptak, Matthew D. Inorganic Chemistry, Vol. 58, Issue 22 https://doi.org/10.1021/acs.inorgchem.9b02530	journal	November 2019
A Ferric–Peroxo Intermediate in the Oxidation of Heme by IsdI Takayama, Shin-ichi J.; Loutet, Slade A.; Mauk, A. Grant Biochemistry, Vol. 54, Issue 16 https://doi.org/10.1021/acs.biochem.5b00239	journal	April 2015
Autocatalytic Radical Reactions in Physiological Prosthetic Heme Modification Colas, Christophe; Ortiz de Montellano, Paul R. Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr0204303	journal	June 2003
Structural Characterization of Synthetic and Protein-Bound Porphyrins in Terms of the Lowest-Frequency Normal Coordinates of the Macrocycle Jentzen, Walter; Song, Xing-Zhi; Shelnutt, John A. The Journal of Physical Chemistry B, Vol. 101, Issue 9 https://doi.org/10.1021/jp963142h	journal	February 1997
Epsilonproteobacterial hydroxylamine oxidoreductase ( ε Hao): characterization of a ‘missing link’ in the multihaem cytochrome c family : Epsilonproteobacterial hydroxylamine oxidoreductase Haase, Doreen; Hermann, Bianca; Einsle, Oliver Molecular Microbiology, Vol. 105, Issue 1 https://doi.org/10.1111/mmi.13690	journal	May 2017
Structure and catalytic mechanism of heme oxygenase Unno, Masaki; Matsui, Toshitaka; Ikeda-Saito, Masao Natural Product Reports, Vol. 24, Issue 3 https://doi.org/10.1039/b604180a	journal	January 2007
Influences of the heme-lysine crosslink in cytochrome P460 over redox catalysis and nitric oxide sensitivity Vilbert, Avery C.; Caranto, Jonathan D.; Lancaster, Kyle M. Chemical Science, Vol. 9, Issue 2 https://doi.org/10.1039/C7SC03450D	journal	January 2018
Ruffling is essential for Staphylococcus aureus IsdG-catalyzed degradation of heme to staphylobilin Schuelke-Sanchez, Ariel E.; Cornetta, Amanda R.; Kocian, Taylor A. J. Journal of Inorganic Biochemistry, Vol. 230 https://doi.org/10.1016/j.jinorgbio.2022.111775	journal	May 2022
Roles of distal aspartate and arginine of B-class dye-decolorizing peroxidase in heterolytic hydrogen peroxide cleavage Pfanzagl, Vera; Nys, Kevin; Bellei, Marzia Journal of Biological Chemistry, Vol. 293, Issue 38 https://doi.org/10.1074/jbc.RA118.004773	journal	August 2018
Protein post-translational modifications in bacteria Macek, Boris; Forchhammer, Karl; Hardouin, Julie Nature Reviews Microbiology, Vol. 17, Issue 11 https://doi.org/10.1038/s41579-019-0243-0	journal	September 2019
Probing lysine posttranslational modifications by unnatural amino acids Maas, Marijn N.; Hintzen, Jordi C. J.; Mecinović, Jasmin Chemical Communications, Vol. 58, Issue 52 https://doi.org/10.1039/D2CC00708H	journal	January 2022
Unique Electronic Structures of the Highly Ruffled Hemes in Heme-Degrading Enzymes of Staphylococcus aureus, IsdG and IsdI, by Resonance Raman and Electron Paramagnetic Resonance Spectroscopies Takahashi, Satoshi; Nambu, Shusuke; Matsui, Toshitaka Biochemistry, Vol. 59, Issue 40 https://doi.org/10.1021/acs.biochem.0c00731	journal	September 2020
Quantum Mechanical/Molecular Mechanical Study of Mechanisms of Heme Degradation by the Enzyme Heme Oxygenase: The Strategic Function of the Water Cluster Chen, Hui; Moreau, Yohann; Derat, Etienne Journal of the American Chemical Society, Vol. 130, Issue 6 https://doi.org/10.1021/ja076679p	journal	February 2008
Elucidation of the heme active site electronic structure affecting the unprecedented nitrite dismutase activity of the ferriheme b proteins, the nitrophorins He, Chunmao; Ogata, Hideaki; Lubitz, Wolfgang Chemical Science, Vol. 7, Issue 8 https://doi.org/10.1039/C6SC01019A	journal	January 2016
The Heme–Lys Cross-Link in Cytochrome P460 Promotes Catalysis by Enforcing Secondary Coordination Sphere Architecture Coleman, Rachael E.; Vilbert, Avery C.; Lancaster, Kyle M. Biochemistry, Vol. 59, Issue 24 https://doi.org/10.1021/acs.biochem.0c00261	journal	June 2020
A Superoxo-Ferrous State in a Reduced Oxy-Ferrous Hemoprotein and Model Compounds Davydov, Roman; Satterlee, James D.; Fujii, Hiroshi Journal of the American Chemical Society, Vol. 125, Issue 52 https://doi.org/10.1021/ja037037e	journal	December 2003
Compound I of Heme Oxygenase Cannot Hydroxylate Its Heme meso-Carbon Matsui, Toshitaka; Kim, Sun Hee; Jin, Hiromichi Journal of the American Chemical Society, Vol. 128, Issue 4 https://doi.org/10.1021/ja057578z	journal	January 2006
Disruption of an Active Site Hydrogen Bond Converts Human Heme Oxygenase-1 into a Peroxidase Lightning, Luke Koenigs; Huang, Hong-wei; Moënne-Loccoz, Pierre Journal of Biological Chemistry, Vol. 276, Issue 14 https://doi.org/10.1074/jbc.M010349200	journal	December 2000
NMR and DFT Investigation of Heme Ruffling: Functional Implications for Cytochrome c Liptak, Matthew D.; Wen, Xin; Bren, Kara L. Journal of the American Chemical Society, Vol. 132, Issue 28 https://doi.org/10.1021/ja102098p	journal	July 2010
Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission Caranto, Jonathan D.; Vilbert, Avery C.; Lancaster, Kyle M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 51 https://doi.org/10.1073/pnas.1611051113	journal	November 2016
Resonance Raman spectra of heme proteins. Effects of oxidation and spin state Spiro, Thomas G.; Strekas, Thomas C. Journal of the American Chemical Society, Vol. 96, Issue 2 https://doi.org/10.1021/ja00809a004	journal	January 1974
Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria Klotz, Martin G.; Schmid, Markus C.; Strous, Marc Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01733.x	journal	November 2008
Cytochrome c ′ _β-Met Is a Variant in the P460 Superfamily Lacking the Heme–Lysyl Cross-Link: A Peroxidase Mimic Generating a Ferryl Intermediate Liew, Fong Ning; Brandys, Marisa A.; Biswas, Saborni Biochemistry, Vol. 59, Issue 5 https://doi.org/10.1021/acs.biochem.9b00810	journal	December 2019
One fold, two functions: cytochrome P460 and cytochrome c ′-β from the methanotroph Methylococcus capsulatus (Bath) Adams, Hannah R.; Krewson, Callie; Vardanega, Jenny E. Chemical Science, Vol. 10, Issue 10 https://doi.org/10.1039/C8SC05210G	journal	January 2019
[136] Assay of catalases and peroxidases Chance, Britton; Maehly, A. C. Methods in Enzymology, Vol. 2, p. 764-775 https://doi.org/10.1016/S0076-6879(55)02300-8	book	January 1955
Ascorbate Peroxidase Compound II Is an Iron(IV) Oxo Species Ledray, Aaron P.; Krest, Courtney M.; Yosca, Timothy H. Journal of the American Chemical Society, Vol. 142, Issue 48 https://doi.org/10.1021/jacs.0c09108	journal	November 2020
Controlling a burn: outer-sphere gating of hydroxylamine oxidation by a distal base in cytochrome P460 Smith, Meghan A.; Majer, Sean H.; Vilbert, Avery C. Chemical Science, Vol. 10, Issue 13 https://doi.org/10.1039/C9SC00195F	journal	January 2019
Nitric oxide interaction with insect nitrophorins and thoughts on the electron configuration of the FeNO complex Walker, F. Journal of Inorganic Biochemistry, Vol. 99, Issue 1 https://doi.org/10.1016/j.jinorgbio.2004.10.009	journal	January 2005
Influence of heme c attachment on heme conformation and potential Kleingardner, Jesse G.; Levin, Benjamin D.; Zoppellaro, Giorgio JBIC Journal of Biological Inorganic Chemistry, Vol. 23, Issue 7 https://doi.org/10.1007/s00775-018-1603-3	journal	August 2018
Cytochrome c as a Peroxidase: Activation of the Precatalytic Native State by H₂O₂-Induced Covalent Modifications Yin, Victor; Shaw, Gary S.; Konermann, Lars Journal of the American Chemical Society, Vol. 139, Issue 44 https://doi.org/10.1021/jacs.7b07106	journal	October 2017
The Crystal Structure of Cytochrome P460 of Nitrosomonas europaea Reveals a Novel Cytochrome Fold and Heme−Protein Cross-link ^† ^, ^‡ Pearson, Arwen R.; Elmore, Bradley O.; Yang, Cheng Biochemistry, Vol. 46, Issue 28 https://doi.org/10.1021/bi700086r	journal	July 2007
Models of the Low-Spin Iron(III) Hydroperoxide Intermediate of Heme Oxygenase: Magnetic Resonance Evidence for Thermodynamic Stabilization of the d _x _y Electronic State at Ambient Temperatures Rivera, Mario; Caignan, Gregori A.; Astashkin, Andrei V. Journal of the American Chemical Society, Vol. 124, Issue 21 https://doi.org/10.1021/ja017334o	journal	May 2002
Oxygen and One Reducing Equivalent Are Both Required for the Conversion of α-Hydroxyhemin to Verdoheme in Heme Oxygenase Matera, Kathryn Mansfield; Takahashi, Satoshi; Fujii, Hiroshi Journal of Biological Chemistry, Vol. 271, Issue 12 https://doi.org/10.1074/jbc.271.12.6618	journal	March 1996
Heme P460: A (Cross) Link to Nitric Oxide Coleman, Rachael E.; Lancaster, Kyle M. Accounts of Chemical Research, Vol. 53, Issue 12 https://doi.org/10.1021/acs.accounts.0c00573	journal	November 2020
Oxygen Activation and Radical Transformations in Heme Proteins and Metalloporphyrins Huang, Xiongyi; Groves, John T. Chemical Reviews, Vol. 118, Issue 5 https://doi.org/10.1021/acs.chemrev.7b00373	journal	December 2017
Application of Badger's Rule to Heme and Non-Heme Iron−Oxygen Bonds: An Examination of Ferryl Protonation States Green, Michael T. Journal of the American Chemical Society, Vol. 128, Issue 6 https://doi.org/10.1021/ja054074s	journal	February 2006
Protein Posttranslational Modifications: The Chemistry of Proteome Diversifications Walsh, Christopher T.; Garneau-Tsodikova, Sylvie; Gatto, Gregory J. Angewandte Chemie International Edition, Vol. 44, Issue 45 https://doi.org/10.1002/anie.200501023	journal	November 2005
Dynamic ruffling distortion of the heme substrate in non-canonical heme oxygenase enzymes Graves, Amanda B.; Horak, Erik H.; Liptak, Matthew D. Dalton Transactions, Vol. 45, Issue 24 https://doi.org/10.1039/C6DT00702C	journal	January 2016
Structural Characterization of Cytochrome c′β‐Met from an Ammonia-Oxidizing Bacterium Abendroth, Jan; Buchko, Garry W.; Liew, Fong Ning Biochemistry, Vol. 61, Issue 7 https://doi.org/10.1021/acs.biochem.1c00640	journal	March 2022
The broad diversity of heme-protein cross-links: An overview Lin, Ying-Wu Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8 https://doi.org/10.1016/j.bbapap.2015.04.019	journal	August 2015
Transcription of nitrification genes by the methane-oxidizing bacterium, Methylococcus capsulatus strain Bath Poret-Peterson, Amisha T.; Graham, James E.; Gulledge, Jay The ISME Journal, Vol. 2, Issue 12 https://doi.org/10.1038/ismej.2008.71	journal	July 2008
Cytochromes P460 and c ′-beta; A new family of high-spin cytochromes c Elmore, Bradley O.; Bergmann, David J.; Klotz, Martin G. FEBS Letters, Vol. 581, Issue 5 https://doi.org/10.1016/j.febslet.2007.01.068	journal	February 2007
Escherichia coli genes required for cytochrome c maturation. Thöny-Meyer, L.; Fischer, F.; Künzler, P. Journal of Bacteriology, Vol. 177, Issue 15 https://doi.org/10.1128/jb.177.15.4321-4326.1995	journal	August 1995
Characterization of a nitrite-reducing octaheme hydroxylamine oxidoreductase that lacks the tyrosine cross-link Ferousi, Christina; Schmitz, Rob A.; Maalcke, Wouter J. Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100476	journal	January 2021
Theory Favors a Stepwise Mechanism of Porphyrin Degradation by a Ferric Hydroperoxide Model of the Active Species of Heme Oxygenase Kumar, Devesh; de Visser, Samuël P.; Shaik, Sason Journal of the American Chemical Society, Vol. 127, Issue 22 https://doi.org/10.1021/ja0446956	journal	May 2005

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