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Direct visualization of a Fe(IV)-OH intermediate in a heme enzyme.

<div class='caption-title'>Formation of Compound II.</div>
<div class='caption-title'>Neutron crystal structure of Compound II.</div>
<div class='caption-title'>Comparison of Compound I and Compound II intermediates in peroxidases and P450s.</div>
Kwon H, Basran J, Casadei CM, Fielding AJ, Schrader TE, Ostermann A, Devos JM, Aller P, Blakeley MP, Moody PCE, Raven EL
OpenAccess logo Nat Commun 7 13445 (2016)
Cited: 37 times
EuropePMC logo PMID: 27897163

Abstract

Catalytic heme enzymes carry out a wide range of oxidations in biology. They have in common a mechanism that requires formation of highly oxidized ferryl intermediates. It is these ferryl intermediates that provide the catalytic engine to drive the biological activity. Unravelling the nature of the ferryl species is of fundamental and widespread importance. The essential question is whether the ferryl is best described as a Fe(IV)=O or a Fe(IV)-OH species, but previous spectroscopic and X-ray crystallographic studies have not been able to unambiguously differentiate between the two species. Here we use a different approach. We report a neutron crystal structure of the ferryl intermediate in Compound II of a heme peroxidase; the structure allows the protonation states of the ferryl heme to be directly observed. This, together with pre-steady state kinetic analyses, electron paramagnetic resonance spectroscopy and single crystal X-ray fluorescence, identifies a Fe(IV)-OH species as the reactive intermediate. The structure establishes a precedent for the formation of Fe(IV)-OH in a peroxidase.

Articles - 5jqr mentioned but not cited (3)

  1. Direct visualization of a Fe(IV)-OH intermediate in a heme enzyme. Kwon H, Basran J, Casadei CM, Fielding AJ, Schrader TE, Ostermann A, Devos JM, Aller P, Blakeley MP, Moody PCE, Raven EL. Nat Commun 7 13445 (2016)
  2. Local Electric Fields as a Natural Switch of Heme-Iron Protein Reactivity. Bím D, Alexandrova AN. ACS Catal 11 6534-6546 (2021)
  3. Comparative analysis of ascorbate peroxidases (APXs) from selected plants with a special focus on Oryza sativa employing public databases. Wu B, Wang B. PLoS One 14 e0226543 (2019)


Reviews citing this publication (7)

  1. Oxygen Activation and Radical Transformations in Heme Proteins and Metalloporphyrins. Huang X, Groves JT. Chem Rev 118 2491-2553 (2018)
  2. Synthetic Fe/Cu Complexes: Toward Understanding Heme-Copper Oxidase Structure and Function. Adam SM, Wijeratne GB, Rogler PJ, Diaz DE, Quist DA, Liu JJ, Karlin KD. Chem Rev 118 10840-11022 (2018)
  3. Neutron Crystallography for the Study of Hydrogen Bonds in Macromolecules. Oksanen E, Chen JC, Fisher SZ. Molecules 22 E596 (2017)
  4. Aspartate or arginine? Validated redox state X-ray structures elucidate mechanistic subtleties of FeIV = O formation in bacterial dye-decolorizing peroxidases. Lučić M, Wilson MT, Svistunenko DA, Owen RL, Hough MA, Worrall JAR. J Biol Inorg Chem 26 743-761 (2021)
  5. Interactions of reactive sulfur species with metalloproteins. Domán A, Dóka É, Garai D, Bogdándi V, Balla G, Balla J, Nagy P. Redox Biol 60 102617 (2023)
  6. Metalloprotein catalysis: structural and mechanistic insights into oxidoreductases from neutron protein crystallography. Schröder GC, Meilleur F. Acta Crystallogr D Struct Biol 77 1251-1269 (2021)
  7. Heme-copper and Heme O2-derived synthetic (bioinorganic) chemistry toward an understanding of cytochrome c oxidase dioxygen chemistry. Panda S, Phan H, Karlin KD. J Inorg Biochem 249 112367 (2023)

Articles citing this publication (27)

  1. Direct Observation of Oxygen Rebound with an Iron-Hydroxide Complex. Zaragoza JPT, Yosca TH, Siegler MA, Moënne-Loccoz P, Green MT, Goldberg DP. J Am Chem Soc 139 13640-13643 (2017)
  2. Living with Oxygen. Gray HB, Winkler JR. Acc Chem Res 51 1850-1857 (2018)
  3. Serial Femtosecond Zero Dose Crystallography Captures a Water-Free Distal Heme Site in a Dye-Decolorising Peroxidase to Reveal a Catalytic Role for an Arginine in FeIV =O Formation. Lučić M, Svistunenko DA, Wilson MT, Chaplin AK, Davy B, Ebrahim A, Axford D, Tosha T, Sugimoto H, Owada S, Dworkowski FSN, Tews I, Owen RL, Hough MA, Worrall JAR. Angew Chem Int Ed Engl 59 21656-21662 (2020)
  4. Effects of Noncovalent Interactions on High-Spin Fe(IV)-Oxido Complexes. Oswald VF, Lee JL, Biswas S, Weitz AC, Mittra K, Fan R, Li J, Zhao J, Hu MY, Alp EE, Bominaar EL, Guo Y, Green MT, Hendrich MP, Borovik AS. J Am Chem Soc 142 11804-11817 (2020)
  5. Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands. Ehudin MA, Gee LB, Sabuncu S, Braun A, Moënne-Loccoz P, Hedman B, Hodgson KO, Solomon EI, Karlin KD. J Am Chem Soc 141 5942-5960 (2019)
  6. Manganese and Cobalt in the Nonheme-Metal-Binding Site of a Biosynthetic Model of Heme-Copper Oxidase Superfamily Confer Oxidase Activity through Redox-Inactive Mechanism. Reed JH, Shi Y, Zhu Q, Chakraborty S, Mirts EN, Petrik ID, Bhagi-Damodaran A, Ross M, Moënne-Loccoz P, Zhang Y, Lu Y. J Am Chem Soc 139 12209-12218 (2017)
  7. Visualizing the protons in a metalloenzyme electron proton transfer pathway. Kwon H, Basran J, Devos JM, Suardíaz R, van der Kamp MW, Mulholland AJ, Schrader TE, Ostermann A, Blakeley MP, Moody PCE, Raven EL. Proc Natl Acad Sci U S A 117 6484-6490 (2020)
  8. XFEL Crystal Structures of Peroxidase Compound II. Kwon H, Basran J, Pathak C, Hussain M, Freeman SL, Fielding AJ, Bailey AJ, Stefanou N, Sparkes HA, Tosha T, Yamashita K, Hirata K, Murakami H, Ueno G, Ago H, Tono K, Yamamoto M, Sawai H, Shiro Y, Sugimoto H, Raven EL, Moody PCE. Angew Chem Int Ed Engl 60 14578-14585 (2021)
  9. Unravelling the mechanisms controlling heme supply and demand. Leung GC, Fung SS, Gallio AE, Blore R, Alibhai D, Raven EL, Hudson AJ. Proc Natl Acad Sci U S A 118 e2104008118 (2021)
  10. An Aromatic Dyad Motif in Dye Decolourising Peroxidases Has Implications for Free Radical Formation and Catalysis. Chaplin AK, Chicano TM, Hampshire BV, Wilson MT, Hough MA, Svistunenko DA, Worrall JAR. Chemistry 25 6141-6153 (2019)
  11. Ascorbate Peroxidase Compound II Is an Iron(IV) Oxo Species. Ledray AP, Krest CM, Yosca TH, Mittra K, Green MT. J Am Chem Soc (2020)
  12. Enhanced Rates of C-H Bond Cleavage by a Hydrogen-Bonded Synthetic Heme High-Valent Iron(IV) Oxo Complex. Ehudin MA, Quist DA, Karlin KD. J Am Chem Soc 141 12558-12569 (2019)
  13. Neutron crystallography reveals mechanisms used by Pseudomonas aeruginosa for host-cell binding. Gajdos L, Blakeley MP, Haertlein M, Forsyth VT, Devos JM, Imberty A. Nat Commun 13 194 (2022)
  14. High-resolution neutron crystallography visualizes an OH-bound resting state of a copper-containing nitrite reductase. Fukuda Y, Hirano Y, Kusaka K, Inoue T, Tamada T. Proc Natl Acad Sci U S A 117 4071-4077 (2020)
  15. Capture of activated dioxygen intermediates at the copper-active site of a lytic polysaccharide monooxygenase. Schröder GC, O'Dell WB, Webb SP, Agarwal PK, Meilleur F. Chem Sci 13 13303-13320 (2022)
  16. A sorghum ascorbate peroxidase with four binding sites has activity against ascorbate and phenylpropanoids. Zhang B, Lewis JA, Vermerris W, Sattler SE, Kang C. Plant Physiol 192 102-118 (2023)
  17. Activity of Cytosolic Ascorbate Peroxidase (APX) from Panicum virgatum against Ascorbate and Phenylpropanoids. Zhang B, Lewis JA, Kovacs F, Sattler SE, Sarath G, Kang C. Int J Mol Sci 24 1778 (2023)
  18. Back-exchange of deuterium in neutron crystallography: characterization by IR spectroscopy. Yee AW, Blakeley MP, Moulin M, Haertlein M, Mitchell E, Forsyth VT. J Appl Crystallogr 50 660-664 (2017)
  19. Complementarity of neutron, XFEL and synchrotron crystallography for defining the structures of metalloenzymes at room temperature. Moreno-Chicano T, Carey LM, Axford D, Beale JH, Doak RB, Duyvesteyn HME, Ebrahim A, Henning RW, Monteiro DCF, Myles DA, Owada S, Sherrell DA, Straw ML, Šrajer V, Sugimoto H, Tono K, Tosha T, Tews I, Trebbin M, Strange RW, Weiss KL, Worrall JAR, Meilleur F, Owen RL, Ghiladi RA, Hough MA. IUCrJ 9 610-624 (2022)
  20. Cryotrapping peroxide in the active site of human mitochondrial manganese superoxide dismutase crystals for neutron diffraction. Azadmanesh J, Lutz WE, Coates L, Weiss KL, Borgstahl GEO. Acta Crystallogr F Struct Biol Commun 78 8-16 (2022)
  21. Mechanistic insights into the chemistry of compound I formation in heme peroxidases: quantum chemical investigations of cytochrome c peroxidase. Aboelnga MM. RSC Adv 12 15543-15554 (2022)
  22. Serial Femtosecond Crystallography Reveals the Role of Water in the One- or Two-Electron Redox Chemistry of Compound I in the Catalytic Cycle of the B-Type Dye-Decolorizing Peroxidase DtpB. Lučić M, Wilson MT, Tosha T, Sugimoto H, Shilova A, Axford D, Owen RL, Hough MA, Worrall JAR. ACS Catal 12 13349-13359 (2022)
  23. Common Reactivity and Properties of Heme Peroxidases: A DFT Study of Their Origin. Ramos DR, Furtmüller PG, Obinger C, Peña-Gallego Á, Pérez-Juste I, Santaballa JA. Antioxidants (Basel) 12 303 (2023)
  24. Crystal structure of Trypanosoma cruzi heme peroxidase and characterization of its substrate specificity and compound I intermediate. Freeman SL, Skafar V, Kwon H, Fielding AJ, Moody PCE, Martínez A, Issoglio FM, Inchausti L, Smircich P, Zeida A, Piacenza L, Radi R, Raven EL. J Biol Chem 298 102204 (2022)
  25. Monitoring the heme iron state in horseradish peroxidase to detect ultratrace amounts of hydrogen peroxide in alcohols. Ravanfar R, Abbaspourrad A. RSC Adv 11 9901-9910 (2021)
  26. Introductory Journal Article Neutron scattering for the study of biological systems - major opportunities within a rapidly changing landscape. Forsyth VT, Moody P. Acta Crystallogr D Struct Biol 74 1126-1128 (2018)
  27. Understanding the Key Roles of pH Buffer in Accelerating Lignin Degradation by Lignin Peroxidase. Fang W, Feng S, Jiang Z, Liang W, Li P, Wang B. JACS Au 3 536-549 (2023)


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