Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase
Abstract
The 1.6 Å crystal structure of toluene 4-monooxygenase reductase T4moF is reported. The structure includes ferredoxin, flavin, and NADH binding domains. Here, the position of the ferredoxin domain relative to the other two domains represents a new configuration for the iron–sulfur flavoprotein family. Close contacts between the C8 methyl group of FAD and [2Fe-2S] ligand Cys36-O represent a plausible pathway for electron transfer between the redox cofactors. Energy-minimized docking of NADH and calculation of hingelike motions between domains suggest how simple coordinated shifts of residues at the C-terminus of the enzyme could expose the N5 position of FAD for productive interaction with the nicotinamide ring. The domain configuration revealed by the T4moF structure provides an excellent steric and electrostatic match to the obligate electron acceptor, Rieske-type [2Fe-2S] ferredoxin T4moC. Protein–protein docking and energy minimization of the T4moFC complex indicate that T4moF [2Fe-2S] ligand Cys41 and T4moC [2Fe-2S] ligand His67, along with other electrostatic interactions between the protein partners, form the functional electron transfer interface.
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF)
- OSTI Identifier:
- 1497148
- Grant/Contract Number:
- W-31-109-ENG-38; MCB-0843239
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 54; Journal Issue: 38; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; charge transfer; peptides and proteins; crystal structure; chemical structure
Citation Formats
Acheson, Justin F., Moseson, Hannah, and Fox, Brian G. Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase. United States: N. p., 2015.
Web. doi:10.1021/acs.biochem.5b00692.
Acheson, Justin F., Moseson, Hannah, & Fox, Brian G. Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase. United States. https://doi.org/10.1021/acs.biochem.5b00692
Acheson, Justin F., Moseson, Hannah, and Fox, Brian G. Wed .
"Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase". United States. https://doi.org/10.1021/acs.biochem.5b00692. https://www.osti.gov/servlets/purl/1497148.
@article{osti_1497148,
title = {Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase},
author = {Acheson, Justin F. and Moseson, Hannah and Fox, Brian G.},
abstractNote = {The 1.6 Å crystal structure of toluene 4-monooxygenase reductase T4moF is reported. The structure includes ferredoxin, flavin, and NADH binding domains. Here, the position of the ferredoxin domain relative to the other two domains represents a new configuration for the iron–sulfur flavoprotein family. Close contacts between the C8 methyl group of FAD and [2Fe-2S] ligand Cys36-O represent a plausible pathway for electron transfer between the redox cofactors. Energy-minimized docking of NADH and calculation of hingelike motions between domains suggest how simple coordinated shifts of residues at the C-terminus of the enzyme could expose the N5 position of FAD for productive interaction with the nicotinamide ring. The domain configuration revealed by the T4moF structure provides an excellent steric and electrostatic match to the obligate electron acceptor, Rieske-type [2Fe-2S] ferredoxin T4moC. Protein–protein docking and energy minimization of the T4moFC complex indicate that T4moF [2Fe-2S] ligand Cys41 and T4moC [2Fe-2S] ligand His67, along with other electrostatic interactions between the protein partners, form the functional electron transfer interface.},
doi = {10.1021/acs.biochem.5b00692},
journal = {Biochemistry},
number = 38,
volume = 54,
place = {United States},
year = {Wed Aug 26 00:00:00 EDT 2015},
month = {Wed Aug 26 00:00:00 EDT 2015}
}
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Works referenced in this record:
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with its Hydroxylase
dataset, January 2002
- Muller, J.; Lugovskoy, A. A.; Wagner, G.
- Biological Magnetic Resonance Bank
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath)
dataset, January 2004
- Chatwood, Lisa L.; Mueller, Jens; Gross, John D.
- Biological Magnetic Resonance Bank
Biochemistry of the Soluble Methane Monooxygenase
journal, October 1994
- Lipscomb, J. D.
- Annual Review of Microbiology, Vol. 48, Issue 1
Evolution of the soluble diiron monooxygenases
journal, October 2003
- Leahy, Joseph G.; Batchelor, Patricia J.; Morcomb, Suzanne M.
- FEMS Microbiology Reviews, Vol. 27, Issue 4
Protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). A novel regulatory protein of enzyme activity.
journal, December 1985
- Green, J.; Dalton, H.
- Journal of Biological Chemistry, Vol. 260, Issue 29
Recombinant Toluene-4-monooxygenase: Catalytic and Mössbauer Studies of the Purified Diiron and Rieske Components of a Four-Protein Complex †
journal, January 1996
- Pikus, Jeremie D.; Studts, Joey M.; Achim, Catalina
- Biochemistry, Vol. 35, Issue 28
Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1
journal, May 1991
- Whited, G. M.; Gibson, D. T.
- Journal of Bacteriology, Vol. 173, Issue 9
Changes in the Regiospecificity of Aromatic Hydroxylation Produced by Active Site Engineering in the Diiron Enzyme Toluene 4-Monooxygenase
journal, August 1997
- Pikus, Jeremie D.; Studts, Joey M.; McClay, Kevin
- Biochemistry, Vol. 36, Issue 31
Structure of T4moC, the Rieske-type ferredoxin component of toluene 4-monooxygenase
journal, April 2006
- Moe, Luke A.; Bingman, Craig A.; Wesenberg, Gary E.
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 5
Crystal Structures and Functional Studies of T4moD, the Toluene 4-Monooxygenase Catalytic Effector Protein,
journal, April 2005
- Lountos, George T.; Mitchell, Kevin H.; Studts, Joey M.
- Biochemistry, Vol. 44, Issue 19
Structural consequences of effector protein complex formation in a diiron hydroxylase
journal, November 2008
- Bailey, L. J.; McCoy, J. G.; Phillips, G. N.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 49
Structural basis for biomolecular recognition in overlapping binding sites in a diiron enzyme system
journal, September 2014
- Acheson, Justin F.; Bailey, Lucas J.; Elsen, Nathaniel L.
- Nature Communications, Vol. 5, Issue 1
X-ray Crystal Structure of Benzoate 1,2-Dioxygenase Reductase from Acinetobacter sp. Strain ADP1
journal, April 2002
- Karlsson, Andreas; Beharry, Zanna M.; Matthew Eby, D.
- Journal of Molecular Biology, Vol. 318, Issue 2
Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S]
journal, December 1992
- Correll, C.; Batie, C.; Ballou, D.
- Science, Vol. 258, Issue 5088
Soluble expression and purification of the oxidoreductase component of toluene 4-monooxygenase
journal, January 2008
- Bailey, Lucas J.; Elsen, Nathaniel L.; Pierce, Brad S.
- Protein Expression and Purification, Vol. 57, Issue 1
Flexi Vector Cloning
book, January 2009
- Blommel, Paul G.; Martin, Peter A.; Seder, Kory D.
- Methods in Molecular Biology
Combined Participation of Hydroxylase Active Site Residues and Effector Protein Binding in a Para to Ortho Modulation of Toluene 4-Monooxygenase Regiospecificity
journal, February 2002
- Mitchell, Kevin H.; Studts, Joey M.; Fox, Brian G.
- Biochemistry, Vol. 41, Issue 9
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
journal, November 2005
- Arnold, Konstantin; Bordoli, Lorenza; Kopp, Jürgen
- Bioinformatics, Vol. 22, Issue 2
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009
- Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
ClusPro: a fully automated algorithm for protein-protein docking
journal, July 2004
- Comeau, S. R.; Gatchell, D. W.; Vajda, S.
- Nucleic Acids Research, Vol. 32, Issue Web Server
ClusPro: an automated docking and discrimination method for the prediction of protein complexes
journal, December 2003
- Comeau, S. R.; Gatchell, D. W.; Vajda, S.
- Bioinformatics, Vol. 20, Issue 1
Identification of a new gene, tmoF, in the Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase
journal, November 1992
- Yen, K. M.; Karl, M. R.
- Journal of Bacteriology, Vol. 174, Issue 22
Protein crystallization by rational mutagenesis of surface residues: Lys to Ala mutations promote crystallization of RhoGDI
journal, April 2001
- Longenecker, Kenton L.; Garrard, Sarah M.; Sheffield, Peter J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 5
Structure-function relations for ferredoxin reductase
journal, February 1994
- Karplus, P. Andrew; Bruns, Christopher M.
- Journal of Bioenergetics and Biomembranes, Vol. 26, Issue 1
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with Its Hydroxylase † , ‡
journal, January 2002
- Müller, Jens; Lugovskoy, Alexey A.; Wagner, Gerhard
- Biochemistry, Vol. 41, Issue 1
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) † , ‡
journal, September 2004
- Chatwood, Lisa L.; Müller, Jens; Gross, John D.
- Biochemistry, Vol. 43, Issue 38
STRAP: editor for STRuctural Alignments of Proteins
journal, April 2001
- Gille, C.; Frommel, C.
- Bioinformatics, Vol. 17, Issue 4
Refined Crystal Structure of Spinach Ferredoxin Reductase at 1.7 Å Resolution: Oxidized, Reduced and 2′-Phospho-5′-AMP Bound States
journal, March 1995
- Bruns, Christopher M.; Karplus, Andrew P.
- Journal of Molecular Biology, Vol. 247, Issue 1
Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase
journal, February 2001
- Kurisu, Genji; Kusunoki, Masami; Katoh, Etsuko
- Nature Structural Biology, Vol. 8, Issue 2, p. 117-121
Crystal Structure of NADH-Cytochrome b5 Reductase from Pig Liver at 2.4 .ANG. Resolution
journal, March 1995
- Nishida, Hirokazu; Inaka, Koji; Yamanaka, Masaki
- Biochemistry, Vol. 34, Issue 9
Crystallization and structure determination of 2.5-.ANG. resolution of the oxidized iron-sulfur [2Fe-2S] ferredoxin isolated from Anabaena 7120
journal, April 1991
- Rypniewski, Wojciech R.; Breiter, Deborah R.; Benning, Matthew M.
- Biochemistry, Vol. 30, Issue 17
Redox-dependent Structural Reorganization in Putidaredoxin, a Vertebrate-type [2Fe-2S] Ferredoxin from Pseudomonas putida
journal, April 2005
- Sevrioukova, Irina F.
- Journal of Molecular Biology, Vol. 347, Issue 3
The three-dimensional structure of flavodoxin reductase from Escherichia coli at 1.7 å resolution
journal, April 1997
- Ingelman, Margareta; Bianchi, Vera; Eklund, Hans
- Journal of Molecular Biology, Vol. 268, Issue 1
Structural prototypes for an extended family of flavoprotein reductases: Comparison of phthalate dioxygenase reductase with ferredoxin reductase and ferredoxin
journal, December 1993
- Correll, Carl C.; Ludwig, Martha L.; Bruns, Christopher M.
- Protein Science, Vol. 2, Issue 12
HingeProt: Automated prediction of hinges in protein structures
journal, September 2007
- Emekli, Ugur; Schneidman-Duhovny, Dina; Wolfson, Haim J.
- Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 4
A new approach for determining low-frequency normal modes in macromolecules
journal, June 1994
- Durand, Philippe; Trinquier, Georges; Sanejouand, Yves-Henri
- Biopolymers, Vol. 34, Issue 6
Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. Identification of sites of component interaction.
journal, January 1991
- Fox, B. G.; Liu, Y.; Dege, J. E.
- Journal of Biological Chemistry, Vol. 266, Issue 1
Electron Transfer in Proteins
journal, June 1996
- Gray, Harry B.; Winkler, Jay R.
- Annual Review of Biochemistry, Vol. 65, Issue 1
Redox and Functional Analysis of the Rieske Ferredoxin Component of the Toluene 4-Monooxygenase
journal, January 2007
- Elsen, Nathaniel L.; Moe, Luke A.; McMartin, Lea A.
- Biochemistry, Vol. 46, Issue 4
Reaction of Phthalate Dioxygenase Reductase with NADH and NAD: Kinetic and Spectral Characterization of Intermediates
journal, October 1994
- Gassner, George; Wang, Lihua; Batie, Christopher
- Biochemistry, Vol. 33, Issue 40
A stopped-flow kinetic study of soluble methane mono-oxygenase from Methylococcus capsulatus (Bath)
journal, April 1989
- Green, J.; Dalton, H.
- Biochemical Journal, Vol. 259, Issue 1
Expression and Characterization of Ferredoxin and Flavin Adenine Dinucleotide Binding Domains of the Reductase Component of Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath)
journal, December 2002
- Blazyk, Jessica L.; Lippard, Stephen J.
- Biochemistry, Vol. 41, Issue 52
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journal, April 2017
- Karmi, Ola; Holt, Sarah H.; Song, Luhua
- PLOS ONE, Vol. 12, Issue 4