Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer

Chreifi, Georges; Baxter, Elizabeth L.; Doukov, Tzanko; Cohen, Aina E.; McPhillips, Scott E.; Song, Jinhu; Meharenna, Yergalem T.; Soltis, S. Michael; Poulos, Thomas L.

doi:10.1073/pnas.1521664113

Title: Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer

Abstract

Significance A major problem in determining the crystal structures of metalloenzymes is that the reducing power of X-rays often changes the oxidation state of the metal center, thereby complicating important mechanistic conclusions on enzyme function. This reduction is especially problematic in studying Fe(IV)=O intermediates, which are powerful oxidants used by many metalloenzymes. This problem can be circumvented using the Stanford Linear Coherent Light Source (LCLS), which generates intense X-ray pulses on the femtosecond time scale and enables structure determinations with no reduction of metal centers. Here, we report the crystal structure of the Fe(IV)=O peroxidase intermediate called compound I using data obtained from the LCLS. We also present kinetic and computational results that, together with crystal structures, provide important mechanistic insights.

Authors:

Chreifi, Georges ^[1]; Baxter, Elizabeth L. ^[2]; Doukov, Tzanko ^[2]; Cohen, Aina E. ^[2]; McPhillips, Scott E. ^[2]; Song, Jinhu ^[2]; Meharenna, Yergalem T. ^[1]; Soltis, S. Michael ^[2]; Poulos, Thomas L. ^[3]

Department of Molecular Biology and Biochemistry, University of California, Irvine, CA 92697-3900,
Macromolecular Crystallographic Group, The Stanford Synchrotron Radiation Lightsource, National Accelerator Laboratory, Stanford University, Stanford, CA 94309,
Department of Molecular Biology and Biochemistry, University of California, Irvine, CA 92697-3900,, Department of Pharmaceutical Sciences, University of California, Irvine, CA 92697-3900,, Department of Chemistry, University of California, Irvine, CA 92697-3900

Publication Date:: 2016-01-19

Sponsoring Org.:: USDOE

OSTI Identifier:: 1236656

Grant/Contract Number:: AC02-76SF00515

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 113 Journal Issue: 5; Journal ID: ISSN 0027-8424

Publisher:: Proceedings of the National Academy of Sciences

Country of Publication:: United States

Language:: English

Citation Formats


                    Chreifi, Georges, Baxter, Elizabeth L., Doukov, Tzanko, Cohen, Aina E., McPhillips, Scott E., Song, Jinhu, Meharenna, Yergalem T., Soltis, S. Michael, and Poulos, Thomas L. Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer.  United States: N. p., 2016. 
Web.  doi:10.1073/pnas.1521664113.

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                    Chreifi, Georges, Baxter, Elizabeth L., Doukov, Tzanko, Cohen, Aina E., McPhillips, Scott E., Song, Jinhu, Meharenna, Yergalem T., Soltis, S. Michael, & Poulos, Thomas L. Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer.  United States.  https://doi.org/10.1073/pnas.1521664113

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                    Chreifi, Georges, Baxter, Elizabeth L., Doukov, Tzanko, Cohen, Aina E., McPhillips, Scott E., Song, Jinhu, Meharenna, Yergalem T., Soltis, S. Michael, and Poulos, Thomas L. Tue .  
"Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer".  United States.  https://doi.org/10.1073/pnas.1521664113.

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@article{osti_1236656,

  title        = {Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer},

  author       = {Chreifi, Georges and Baxter, Elizabeth L. and Doukov, Tzanko and Cohen, Aina E. and McPhillips, Scott E. and Song, Jinhu and Meharenna, Yergalem T. and Soltis, S. Michael and Poulos, Thomas L.},

  abstractNote = {Significance A major problem in determining the crystal structures of metalloenzymes is that the reducing power of X-rays often changes the oxidation state of the metal center, thereby complicating important mechanistic conclusions on enzyme function. This reduction is especially problematic in studying Fe(IV)=O intermediates, which are powerful oxidants used by many metalloenzymes. This problem can be circumvented using the Stanford Linear Coherent Light Source (LCLS), which generates intense X-ray pulses on the femtosecond time scale and enables structure determinations with no reduction of metal centers. Here, we report the crystal structure of the Fe(IV)=O peroxidase intermediate called compound I using data obtained from the LCLS. We also present kinetic and computational results that, together with crystal structures, provide important mechanistic insights.},

  doi          = {10.1073/pnas.1521664113},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 5,

  volume       = 113,

  place        = {United States},

  year         = {2016},

  month        = {1}

}

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Title: Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer

Abstract

Citation Formats

Goniometer-based femtosecond crystallography with X-ray free electron lasers journal, October 2014

Design of a Ruthenium−Cytochrome c Derivative To Measure Electron Transfer to the Radical Cation and Oxyferryl Heme in Cytochrome c Peroxidase † journal, January 1996

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Free energy of charges in solvated proteins: microscopic calculations using a reversible charging process journal, December 1986

Overview of the CCP 4 suite and current developments journal, March 2011

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Processing of X-ray snapshots from crystals in random orientations journal, July 2014

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Resonance Raman spectroscopy of oxoiron(IV) porphyrin π-cation radical and oxoiron(IV) hemes in peroxidase intermediates journal, April 2006

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Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: a novel role of the transmembrane domain journal, August 2005

Effects of Concerted Hydrogen Bonding of Distal Histidine on Active Site Structures of Horseradish Peroxidase. Resonance Raman Studies with Asn70 Mutants † journal, February 1997

A Complete Mechanism for Steady-State Oxidation of Yeast Cytochrome c by Yeast Cytochrome c Peroxidase † journal, January 1996

Resonance Raman evidence for oxygen exchange between the FeIV = O heme and bulk water during enzymic catalysis of horseradish peroxidase and its relation with the heme-linked ionization. journal, April 1986

Crystallographic and Single-Crystal Spectral Analysis of the Peroxidase Ferryl Intermediate journal, April 2010

MOLREP an Automated Program for Molecular Replacement journal, December 1997

The catalytic pathway of horseradish peroxidase at high resolution journal, May 2002

Potential for biomolecular imaging with femtosecond X-ray pulses journal, August 2000

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Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin journal, March 1992

Proton Linkage in Formation of the Cytochrome c-Cytochrome c Peroxidase Complex: Electrostatic Properties of the High- and Low-Affinity Cytochrome Binding Sites on the Peroxidase journal, October 1994

Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER journal, March 2012

Constant pH Replica Exchange Molecular Dynamics in Explicit Solvent Using Discrete Protonation States: Implementation, Testing, and Validation journal, February 2014

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Goniometer-based femtosecond crystallography with X-ray free electron lasers
journal, October 2014

Design of a Ruthenium−Cytochrome c Derivative To Measure Electron Transfer to the Radical Cation and Oxyferryl Heme in Cytochrome c Peroxidase ^†
journal, January 1996

The crystal structure of cytochrome c peroxidase.
journal, January 1980

Free energy of charges in solvated proteins: microscopic calculations using a reversible charging process
journal, December 1986

Overview of the CCP 4 suite and current developments
journal, March 2011

Radiation damage in protein serial femtosecond crystallography using an x-ray free-electron laser
journal, December 2011

Crystal structure of the Leishmania major peroxidase-cytochrome c complex
journal, October 2012

Engineering Ascorbate Peroxidase Activity into Cytochrome c Peroxidase ^† ^‡
journal, September 2008

Heme Enzyme Structure and Function
journal, January 2014

Crystal Structure of Leishmania major Peroxidase and Characterization of the Compound I Tryptophan Radical
journal, May 2011

Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle
journal, July 2004

Neutron cryo-crystallography captures the protonation state of ferryl heme in a peroxidase
journal, July 2014

Enzymatic Mechanism of Leishmania major Peroxidase and the Critical Role of Specific Ionic Interactions
journal, May 2015

Leishmania major Peroxidase Is a Cytochrome c Peroxidase
journal, March 2012

Processing of X-ray snapshots from crystals in random orientations
journal, July 2014

The stereochemistry of peroxidase catalysis.
journal, September 1980

Application of Badger's Rule to Heme and Non-Heme Iron−Oxygen Bonds: An Examination of Ferryl Protonation States
journal, February 2006

REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011

On the Role of Water in Peroxidase Catalysis: A Theoretical Investigation of HRP Compound I Formation
journal, April 2010

A hypothetical model of the cytochrome c peroxidase . cytochrome c electron transfer complex.
journal, November 1980

Femtosecond X-ray protein nanocrystallography
journal, February 2011

Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c
journal, December 1992

Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy
journal, July 2014

Constant pH molecular dynamics in generalized Born implicit solvent
journal, December 2004

On the status of ferryl protonation
journal, April 2006

An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot
journal, November 2002

Resonance Raman spectroscopy of oxoiron(IV) porphyrin π-cation radical and oxoiron(IV) hemes in peroxidase intermediates
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Proximal ligand effects on electronic structure and spectra of compound I of peroxidases
journal, March 2001

Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: a novel role of the transmembrane domain
journal, August 2005

Effects of Concerted Hydrogen Bonding of Distal Histidine on Active Site Structures of Horseradish Peroxidase. Resonance Raman Studies with Asn70 Mutants ^†
journal, February 1997

A Complete Mechanism for Steady-State Oxidation of Yeast Cytochrome c by Yeast Cytochrome c Peroxidase ^†
journal, January 1996

Resonance Raman evidence for oxygen exchange between the FeIV = O heme and bulk water during enzymic catalysis of horseradish peroxidase and its relation with the heme-linked ionization.
journal, April 1986

Crystallographic and Single-Crystal Spectral Analysis of the Peroxidase Ferryl Intermediate
journal, April 2010

MOLREP an Automated Program for Molecular Replacement
journal, December 1997

The catalytic pathway of horseradish peroxidase at high resolution
journal, May 2002

Potential for biomolecular imaging with femtosecond X-ray pulses
journal, August 2000

XDS
journal, January 2010

Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin
journal, March 1992

Proton Linkage in Formation of the Cytochrome c-Cytochrome c Peroxidase Complex: Electrostatic Properties of the High- and Low-Affinity Cytochrome Binding Sites on the Peroxidase
journal, October 1994

Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER
journal, March 2012

Constant pH Replica Exchange Molecular Dynamics in Explicit Solvent Using Discrete Protonation States: Implementation, Testing, and Validation
journal, February 2014

Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements
journal, December 2011

High-Resolution Crystal Structures and Spectroscopy of Native and Compound I Cytochrome c Peroxidase ^†
journal, May 2003