2xif › Citations

Nature of the ferryl heme in compounds I and II.

Gumiero A, Metcalfe CL, Pearson AR, Raven EL, Moody PC
J Biol Chem 286 1260-8 (2011)
Related entries: 2xi6, 2xih, 2xil, 2xj5, 2xj6, 2xj8

Cited: 57 times
EuropePMC logo PMID: 21062738

Abstract

Heme enzymes are ubiquitous in biology and catalyze a vast array of biological redox processes. The formation of high valent ferryl intermediates of the heme iron (known as Compounds I and Compound II) is implicated for a number of catalytic heme enzymes, but these species are formed only transiently and thus have proved somewhat elusive. In consequence, there has been conflicting evidence as to the nature of these ferryl intermediates in a number of different heme enzymes, in particular the precise nature of the bond between the heme iron and the bound oxygen atom. In this work, we present high resolution crystal structures of both Compound I and Compound II intermediates in two different heme peroxidase enzymes, cytochrome c peroxidase and ascorbate peroxidase, allowing direct and accurate comparison of the bonding interactions in the different intermediates. A consistent picture emerges across all structures, showing lengthening of the ferryl oxygen bond (and presumed protonation) on reduction of Compound I to Compound II. These data clarify long standing inconsistencies on the nature of the ferryl heme species in these intermediates.

Articles - 2xif mentioned but not cited (5)

  1. Nature of the ferryl heme in compounds I and II. Gumiero A, Metcalfe CL, Pearson AR, Raven EL, Moody PC. J Biol Chem 286 1260-1268 (2011)
  2. 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)
  3. Molecular cloning and in-silico characterization of high temperature stress responsive pAPX gene isolated from heat tolerant Indian wheat cv. Raj 3765. Padaria JC, Vishwakarma H, Biswas K, Jasrotia RS, Singh GP. BMC Res Notes 7 713 (2014)
  4. Modeling and phylogenetic analysis of cytosolic ascorbate peroxidase (OsAPX1) from rice reveal signature motifs that may play a role in stress tolerance. Pandey S, Negi YK, Chinreddy S, Sathelly K, Arora S, Kaul T. Bioinformation 10 119-123 (2014)
  5. Molecular model of thylakoid membrane bound (SlAPX6) ascorbate peroxidase from Solanum lycopersicum. Tripathi K, Pandey S, Malik M, Sathelly K, Kaul T. Bioinformation 12 44-47 (2016)


Reviews citing this publication (11)

  1. Oxygen Activation and Radical Transformations in Heme Proteins and Metalloporphyrins. Huang X, Groves JT. Chem Rev 118 2491-2553 (2018)
  2. Myeloperoxidase: a leukocyte-derived protagonist of inflammation and cardiovascular disease. Nussbaum C, Klinke A, Adam M, Baldus S, Sperandio M. Antioxid Redox Signal 18 692-713 (2013)
  3. 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)
  4. The reaction mechanisms of heme catalases: an atomistic view by ab initio molecular dynamics. Alfonso-Prieto M, Vidossich P, Rovira C. Arch Biochem Biophys 525 121-130 (2012)
  5. Functional and protective hole hopping in metalloenzymes. Gray HB, Winkler JR. Chem Sci 12 13988-14003 (2021)
  6. Production of dioxygen in the dark: dismutases of oxyanions. DuBois JL, Ojha S. Met Ions Life Sci 15 45-87 (2015)
  7. 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)
  8. MauG: a di-heme enzyme required for methylamine dehydrogenase maturation. Wilmot CM, Yukl ET. Dalton Trans 42 3127-3135 (2013)
  9. MauG, a diheme enzyme that catalyzes tryptophan tryptophylquinone biosynthesis by remote catalysis. Shin S, Davidson VL. Arch Biochem Biophys 544 112-118 (2014)
  10. Mechanistic Insight on the Activity and Substrate Selectivity of Nonheme Iron Dioxygenases. de Visser SP. Chem Rec 18 1501-1516 (2018)
  11. Understanding heme proteins with hyperfine spectroscopy. Van Doorslaer S. J Magn Reson 280 79-88 (2017)

Articles citing this publication (41)

  1. Heme enzymes. Neutron cryo-crystallography captures the protonation state of ferryl heme in a peroxidase. Casadei CM, Gumiero A, Metcalfe CL, Murphy EJ, Basran J, Concilio MG, Teixeira SC, Schrader TE, Fielding AJ, Ostermann A, Blakeley MP, Raven EL, Moody PC. Science 345 193-197 (2014)
  2. Dose-resolved serial synchrotron and XFEL structures of radiation-sensitive metalloproteins. Ebrahim A, Moreno-Chicano T, Appleby MV, Chaplin AK, Beale JH, Sherrell DA, Duyvesteyn HME, Owada S, Tono K, Sugimoto H, Strange RW, Worrall JAR, Axford D, Owen RL, Hough MA. IUCrJ 6 543-551 (2019)
  3. Living with Oxygen. Gray HB, Winkler JR. Acc Chem Res 51 1850-1857 (2018)
  4. Structure-Based Mechanism for Oxidative Decarboxylation Reactions Mediated by Amino Acids and Heme Propionates in Coproheme Decarboxylase (HemQ). Celis AI, Gauss GH, Streit BR, Shisler K, Moraski GC, Rodgers KR, Lukat-Rodgers GS, Peters JW, DuBois JL. J Am Chem Soc 139 1900-1911 (2017)
  5. Setting an upper limit on the myoglobin iron(IV)hydroxide pK(a): insight into axial ligand tuning in heme protein catalysis. Yosca TH, Behan RK, Krest CM, Onderko EL, Langston MC, Green MT. J Am Chem Soc 136 9124-9131 (2014)
  6. Ferryl protonation in oxoiron(IV) porphyrins and its role in oxygen transfer. Boaz NC, Bell SR, Groves JT. J Am Chem Soc 137 2875-2885 (2015)
  7. Proton delivery to ferryl heme in a heme peroxidase: enzymatic use of the Grotthuss mechanism. Efimov I, Badyal SK, Metcalfe CL, Macdonald I, Gumiero A, Raven EL, Moody PC. J Am Chem Soc 133 15376-15383 (2011)
  8. X-ray-induced photoreduction of heme metal centers rapidly induces active-site perturbations in a protein-independent manner. Pfanzagl V, Beale JH, Michlits H, Schmidt D, Gabler T, Obinger C, Djinović-Carugo K, Hofbauer S. J Biol Chem 295 13488-13501 (2020)
  9. Reactivity of an FeIV-Oxo Complex with Protons and Oxidants. Hill EA, Weitz AC, Onderko E, Romero-Rivera A, Guo Y, Swart M, Bominaar EL, Green MT, Hendrich MP, Lacy DC, Borovik AS. J Am Chem Soc 138 13143-13146 (2016)
  10. Geometric and electronic structures of the His-Fe(IV)=O and His-Fe(IV)-Tyr hemes of MauG. Jensen LM, Meharenna YT, Davidson VL, Poulos TL, Hedman B, Wilmot CM, Sarangi R. J Biol Inorg Chem 17 1241-1255 (2012)
  11. 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)
  12. Assessment of malathion toxicity on cytophysiological activity, DNA damage and antioxidant enzymes in root of Allium cepa model. Srivastava AK, Singh D. Sci Rep 10 886 (2020)
  13. Cryo-EM structures of intermediates suggest an alternative catalytic reaction cycle for cytochrome c oxidase. Kolbe F, Safarian S, Piórek Ż, Welsch S, Müller H, Michel H. Nat Commun 12 6903 (2021)
  14. 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)
  15. Carboxyl group of Glu113 is required for stabilization of the diferrous and bis-Fe(IV) states of MauG. Abu Tarboush N, Yukl ET, Shin S, Feng M, Wilmot CM, Davidson VL. Biochemistry 52 6358-6367 (2013)
  16. Decarboxylation involving a ferryl, propionate, and a tyrosyl group in a radical relay yields heme b. Streit BR, Celis AI, Moraski GC, Shisler KA, Shepard EM, Rodgers KR, Lukat-Rodgers GS, DuBois JL. J Biol Chem 293 3989-3999 (2018)
  17. 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)
  18. Roles of multiple-proton transfer pathways and proton-coupled electron transfer in the reactivity of the bis-FeIV state of MauG. Ma Z, Williamson HR, Davidson VL. Proc Natl Acad Sci U S A 112 10896-10901 (2015)
  19. 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)
  20. A structural and dynamic investigation of the inhibition of catalase by nitric oxide. Candelaresi M, Gumiero A, Adamczyk K, Robb K, Bellota-Antón C, Sangal V, Munnoch J, Greetham GM, Towrie M, Hoskisson PA, Parker AW, Tucker NP, Walsh MA, Hunt NT. Org Biomol Chem 11 7778-7788 (2013)
  21. Rewiring the "Push-Pull" Catalytic Machinery of a Heme Enzyme Using an Expanded Genetic Code. Ortmayer M, Fisher K, Basran J, Wolde-Michael EM, Heyes DJ, Levy C, Lovelock SL, Anderson JLR, Raven EL, Hay S, Rigby SEJ, Green AP. ACS Catal 10 2735-2746 (2020)
  22. 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)
  23. The Chemical Basis of Intracerebral Hemorrhage and Cell Toxicity With Contributions From Eryptosis and Ferroptosis. Derry PJ, Vo ATT, Gnanansekaran A, Mitra J, Liopo AV, Hegde ML, Tsai AL, Tour JM, Kent TA. Front Cell Neurosci 14 603043 (2020)
  24. 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)
  25. Combining X-ray and neutron crystallography with spectroscopy. Kwon H, Smith O, Raven EL, Moody PC. Acta Crystallogr D Struct Biol 73 141-147 (2017)
  26. Mechanism of protein oxidative damage that is coupled to long-range electron transfer to high-valent haems. Ma Z, Williamson HR, Davidson VL. Biochem J 473 1769-1775 (2016)
  27. Therapeutic Potential of Ocimum tenuiflorum as MPO Inhibitor with Implications for Atherosclerosis Prevention. Narasimhulu CA, Vardhan S. J Med Food 18 507-515 (2015)
  28. Intramolecular Oxidative O-Demethylation of an Oxoferryl Porphyrin Complexed with a Per-O-methylated β-Cyclodextrin Dimer. Kitagishi H, Kurosawa S, Kano K. Chem Asian J 11 3213-3219 (2016)
  29. A Suicide Mutation Affecting Proton Transfers to High-Valent Hemes Causes Inactivation of MauG during Catalysis. Ma Z, Williamson HR, Davidson VL. Biochemistry 55 5738-5745 (2016)
  30. Generation of novel functional metalloproteins via hybrids of cytochrome c and peroxidase. Ying T, Zhong F, Wang ZH, Xie J, Tan X, Huang ZX. Protein Eng Des Sel 26 401-407 (2013)
  31. Structural Characterization of Neisseria gonorrhoeae Bacterial Peroxidase-Insights into the Catalytic Cycle of Bacterial Peroxidases. Nóbrega CS, Carvalho AL, Romão MJ, Pauleta SR. Int J Mol Sci 24 6246 (2023)
  32. Energy dispersive spectrometry and first principles studies on the oxidation of pentlandite. Xiong X, Lu X, Li G, Cheng H, Xu Q, Li S. Phys Chem Chem Phys 20 12791-12798 (2018)
  33. Exploring the Factors which Result in Cytochrome P450 Catalyzed Desaturation Versus Hydroxylation. Coleman T, Doherty DZ, Zhang T, Podgorski MN, Qiao R, Lee JHZ, Bruning JB, De Voss JJ, Zhou W, Bell SG. Chem Asian J 17 e202200986 (2022)
  34. 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)
  35. Methoxyphenol derivatives as reversible inhibitors of myeloperoxidase as potential antiatherosclerotic agents. Jayaraj P, Narasimhulu CA, Maiseyeu A, Durairaj R, Rao S, Rajagopalan S, Parthasarathy S, Desikan R. Future Med Chem 12 95-110 (2020)
  36. The pKa value of the proximal water molecule trans to a high-valent MnV[double bond, length as m-dash]O porphyrin: towards the control of reactivity by pH. Saint-Germes L, Bar L, Dejeu J, Spinelli N, Defrancq E, Pratviel G. Dalton Trans 46 12088-12094 (2017)
  37. 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)
  38. Converting the bis-FeIV state of the diheme enzyme MauG to Compound I decreases the reorganization energy for electron transfer. Dow BA, Davidson VL. Biochem J 473 67-72 (2016)
  39. Probing the conformational mobility of the active site of a heme peroxidase. Gumiero A, Badyal SK, Leeks T, Moody PC, Raven EL. Dalton Trans 42 3170-3175 (2013)
  40. Letter Properties of the high-spin heme of MauG are altered by binding of preMADH at the protein surface 40 Å away. Feng M, Ma Z, Crudup BF, Davidson VL. FEBS Lett 591 1566-1572 (2017)
  41. 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)


Quick links