Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase

Acheson, Justin F.; Moseson, Hannah; Fox, Brian G.

doi:10.1021/acs.biochem.5b00692

Structure of T4moF, the Toluene 4-Monooxygenase Ferredoxin Oxidoreductase

Journal Article · Wed Aug 26 00:00:00 EDT 2015 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.5b00692· OSTI ID:1497148

Acheson, Justin F. ^[1]; Moseson, Hannah ^[1]; Fox, Brian G. ^[1]

Univ. of Wisconsin, Madison, WI (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Science Foundation; USDOE Office of Science (SC)

Grant/Contract Number:: W-31109-ENG-38

OSTI ID:: 1497148

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 38 Vol. 54; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (46)

A new approach for determining low-frequency normal modes in macromolecules Durand, Philippe; Trinquier, Georges; Sanejouand, Yves-Henri Biopolymers, Vol. 34, Issue 6 https://doi.org/10.1002/bip.360340608	journal	June 1994
Structural prototypes for an extended family of flavoprotein reductases: Comparison of phthalate dioxygenase reductase with ferredoxin reductase and ferredoxin Correll, Carl C.; Ludwig, Martha L.; Bruns, Christopher M. Protein Science, Vol. 2, Issue 12 https://doi.org/10.1002/pro.5560021212	journal	December 1993
HingeProt: Automated prediction of hinges in protein structures Emekli, Ugur; Schneidman-Duhovny, Dina; Wolfson, Haim J. Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 4 https://doi.org/10.1002/prot.21613	journal	September 2007
Refined Crystal Structure of Spinach Ferredoxin Reductase at 1.7 Å Resolution: Oxidized, Reduced and 2′-Phospho-5′-AMP Bound States Bruns, Christopher M.; Karplus, Andrew P. Journal of Molecular Biology, Vol. 247, Issue 1 https://doi.org/10.1006/jmbi.1994.0127	journal	March 1995
The three-dimensional structure of flavodoxin reductase from Escherichia coli at 1.7 å resolution Ingelman, Margareta; Bianchi, Vera; Eklund, Hans Journal of Molecular Biology, Vol. 268, Issue 1 https://doi.org/10.1006/jmbi.1997.0957	journal	April 1997
Flexi Vector Cloning Blommel, Paul G.; Martin, Peter A.; Seder, Kory D. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_4	book	January 2009
Structure-function relations for ferredoxin reductase Karplus, P. Andrew; Bruns, Christopher M. Journal of Bioenergetics and Biomembranes, Vol. 26, Issue 1 https://doi.org/10.1007/BF00763221	journal	February 1994
Protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). A novel regulatory protein of enzyme activity. Green, J.; Dalton, H. Journal of Biological Chemistry, Vol. 260, Issue 29 https://doi.org/10.1016/S0021-9258(17)36328-7	journal	December 1985
Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. Identification of sites of component interaction. Fox, B. G.; Liu, Y.; Dege, J. E. Journal of Biological Chemistry, Vol. 266, Issue 1 https://doi.org/10.1016/S0021-9258(18)52470-4	journal	January 1991
X-ray Crystal Structure of Benzoate 1,2-Dioxygenase Reductase from Acinetobacter sp. Strain ADP1 Karlsson, Andreas; Beharry, Zanna M.; Matthew Eby, D. Journal of Molecular Biology, Vol. 318, Issue 2 https://doi.org/10.1016/S0022-2836(02)00039-6	journal	April 2002
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Evolution of the soluble diiron monooxygenases Leahy, Joseph G.; Batchelor, Patricia J.; Morcomb, Suzanne M. FEMS Microbiology Reviews, Vol. 27, Issue 4 https://doi.org/10.1016/S0168-6445(03)00023-8	journal	October 2003
Redox-dependent Structural Reorganization in Putidaredoxin, a Vertebrate-type [2Fe-2S] Ferredoxin from Pseudomonas putida Sevrioukova, Irina F. Journal of Molecular Biology, Vol. 347, Issue 3 https://doi.org/10.1016/j.jmb.2005.01.047	journal	April 2005
Soluble expression and purification of the oxidoreductase component of toluene 4-monooxygenase Bailey, Lucas J.; Elsen, Nathaniel L.; Pierce, Brad S. Protein Expression and Purification, Vol. 57, Issue 1 https://doi.org/10.1016/j.pep.2007.09.007	journal	January 2008
Crystal Structure of NADH-Cytochrome b5 Reductase from Pig Liver at 2.4 .ANG. Resolution Nishida, Hirokazu; Inaka, Koji; Yamanaka, Masaki Biochemistry, Vol. 34, Issue 9 https://doi.org/10.1021/bi00009a004	journal	March 1995
Reaction of Phthalate Dioxygenase Reductase with NADH and NAD: Kinetic and Spectral Characterization of Intermediates Gassner, George; Wang, Lihua; Batie, Christopher Biochemistry, Vol. 33, Issue 40 https://doi.org/10.1021/bi00206a022	journal	October 1994
Crystallization and structure determination of 2.5-.ANG. resolution of the oxidized iron-sulfur [2Fe-2S] ferredoxin isolated from Anabaena 7120 Rypniewski, Wojciech R.; Breiter, Deborah R.; Benning, Matthew M. Biochemistry, Vol. 30, Issue 17 https://doi.org/10.1021/bi00231a003	journal	April 1991
Combined Participation of Hydroxylase Active Site Residues and Effector Protein Binding in a Para to Ortho Modulation of Toluene 4-Monooxygenase Regiospecificity Mitchell, Kevin H.; Studts, Joey M.; Fox, Brian G. Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1021/bi012036p	journal	February 2002
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with Its Hydroxylase † , ‡ Müller, Jens; Lugovskoy, Alexey A.; Wagner, Gerhard Biochemistry, Vol. 41, Issue 1 https://doi.org/10.1021/bi015668k	journal	January 2002
Expression and Characterization of Ferredoxin and Flavin Adenine Dinucleotide Binding Domains of the Reductase Component of Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath) Blazyk, Jessica L.; Lippard, Stephen J. Biochemistry, Vol. 41, Issue 52 https://doi.org/10.1021/bi026757f	journal	December 2002
Crystal Structures and Functional Studies of T4moD, the Toluene 4-Monooxygenase Catalytic Effector Protein^, Lountos, George T.; Mitchell, Kevin H.; Studts, Joey M. Biochemistry, Vol. 44, Issue 19 https://doi.org/10.1021/bi047459g	journal	April 2005
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) † , ‡ Chatwood, Lisa L.; Müller, Jens; Gross, John D. Biochemistry, Vol. 43, Issue 38 https://doi.org/10.1021/bi049066n	journal	September 2004
Redox and Functional Analysis of the Rieske Ferredoxin Component of the Toluene 4-Monooxygenase Elsen, Nathaniel L.; Moe, Luke A.; McMartin, Lea A. Biochemistry, Vol. 46, Issue 4 https://doi.org/10.1021/bi0616145	journal	January 2007
Recombinant Toluene-4-monooxygenase: Catalytic and Mössbauer Studies of the Purified Diiron and Rieske Components of a Four-Protein Complex ^† Pikus, Jeremie D.; Studts, Joey M.; Achim, Catalina Biochemistry, Vol. 35, Issue 28 https://doi.org/10.1021/bi960456m	journal	January 1996
Changes in the Regiospecificity of Aromatic Hydroxylation Produced by Active Site Engineering in the Diiron Enzyme Toluene 4-Monooxygenase Pikus, Jeremie D.; Studts, Joey M.; McClay, Kevin Biochemistry, Vol. 36, Issue 31 https://doi.org/10.1021/bi971049t	journal	August 1997
Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP⁺ reductase Kurisu, Genji; Kusunoki, Masami; Katoh, Etsuko Nature Structural Biology, Vol. 8, Issue 2, p. 117-121 https://doi.org/10.1038/84097	journal	February 2001
Structural basis for biomolecular recognition in overlapping binding sites in a diiron enzyme system Acheson, Justin F.; Bailey, Lucas J.; Elsen, Nathaniel L. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6009	journal	September 2014
A stopped-flow kinetic study of soluble methane mono-oxygenase from Methylococcus capsulatus (Bath) Green, J.; Dalton, H. Biochemical Journal, Vol. 259, Issue 1 https://doi.org/10.1042/bj2590167	journal	April 1989
Structural consequences of effector protein complex formation in a diiron hydroxylase Bailey, L. J.; McCoy, J. G.; Phillips, G. N. Proceedings of the National Academy of Sciences, Vol. 105, Issue 49 https://doi.org/10.1073/pnas.0807948105	journal	November 2008
STRAP: editor for STRuctural Alignments of Proteins Gille, C.; Frommel, C. Bioinformatics, Vol. 17, Issue 4 https://doi.org/10.1093/bioinformatics/17.4.377	journal	April 2001
ClusPro: an automated docking and discrimination method for the prediction of protein complexes Comeau, S. R.; Gatchell, D. W.; Vajda, S. Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1093/bioinformatics/btg371	journal	December 2003
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Arnold, Konstantin; Bordoli, Lorenza; Kopp, Jürgen Bioinformatics, Vol. 22, Issue 2 https://doi.org/10.1093/bioinformatics/bti770	journal	November 2005
ClusPro: a fully automated algorithm for protein-protein docking Comeau, S. R.; Gatchell, D. W.; Vajda, S. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh354	journal	July 2004
Crystallographic studies of the interaction between the ferredoxin-NADP ⁺ reductase and ferredoxin from the cyanobacterium Anabaena : looking for the elusive ferredoxin molecule Morales, Renaud; Kachalova, Galina; Vellieux, Frédéric Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 11 https://doi.org/10.1107/S0907444900010052	journal	November 2000
Protein crystallization by rational mutagenesis of surface residues: Lys to Ala mutations promote crystallization of RhoGDI Longenecker, Kenton L.; Garrard, Sarah M.; Sheffield, Peter J. Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 5 https://doi.org/10.1107/S0907444901003122	journal	April 2001
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Structure of T4moC, the Rieske-type ferredoxin component of toluene 4-monooxygenase Moe, Luke A.; Bingman, Craig A.; Wesenberg, Gary E. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 5 https://doi.org/10.1107/S0907444906006056	journal	April 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S] Correll, C.; Batie, C.; Ballou, D. Science, Vol. 258, Issue 5088 https://doi.org/10.1126/science.1280857	journal	December 1992
Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1 Whited, G. M.; Gibson, D. T. Journal of Bacteriology, Vol. 173, Issue 9 https://doi.org/10.1128/jb.173.9.3010-3016.1991	journal	May 1991
Identification of a new gene, tmoF, in the Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase Yen, K. M.; Karl, M. R. Journal of Bacteriology, Vol. 174, Issue 22 https://doi.org/10.1128/jb.174.22.7253-7261.1992	journal	November 1992
Electron Transfer in Proteins Gray, Harry B.; Winkler, Jay R. Annual Review of Biochemistry, Vol. 65, Issue 1 https://doi.org/10.1146/annurev.bi.65.070196.002541	journal	June 1996
Biochemistry of the Soluble Methane Monooxygenase Lipscomb, J. D. Annual Review of Microbiology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.mi.48.100194.002103	journal	October 1994
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with its Hydroxylase Muller, J.; Lugovskoy, A. A.; Wagner, G. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr5148	dataset	January 2002
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) Chatwood, Lisa L.; Mueller, Jens; Gross, John D. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr6295	dataset	January 2004

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