Structure of the cytochrome aa 3 -600 heme-copper menaquinol oxidase bound to inhibitor HQNO shows TM0 is part of the quinol binding site

Xu, Jingjing; Ding, Ziqiao; Liu, Bing; Yi, Sophia M.; Li, Jiao; Zhang, Zhengguang; Liu, Yuchen; Li, Jin; Liu, Liu; Zhou, Aiwu; Gennis, Robert B.; Zhu, Jiapeng

doi:10.1073/pnas.1915013117

Title: Structure of the cytochrome aa ₃ -600 heme-copper menaquinol oxidase bound to inhibitor HQNO shows TM0 is part of the quinol binding site

Journal Article · 30 December 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1915013117 · OSTI ID:1800648

Xu, Jingjing ^[1]; Ding, Ziqiao ^[2]; Liu, Bing ^[3]; Yi, Sophia M. ^[2]; Li, Jiao ^[3]; Zhang, Zhengguang ^[3]; Liu, Yuchen ^[3]; Li, Jin ^[4]; Liu, Liu ^[4];

^[5]; Gennis, Robert B. ^[2];

^[3]

Nanjing University of Chinese Medicine (China); Nanjing University of Chinese Medicine
Univ. of Illinois at Urbana-Champaign, IL (United States)
Nanjing University of Chinese Medicine (China)
PharmaBlock Sciences, Inc., Nanjing, China
Shanghai Jiao Tong Univ. (China). School of Medicine

Virtually all proton-pumping terminal respiratory oxygen reductases are members of the heme-copper oxidoreductase superfamily. Most of these enzymes use reduced cytochrome c as a source of electrons, but a group of enzymes have evolved to directly oxidize membrane-bound quinols, usually menaquinol or ubiquinol. All of the quinol oxidases have an additional transmembrane helix (TM0) in subunit I that is not present in the related cytochrome c oxidases. The current work reports the 3.6-Å-resolution X-ray structure of the cytochrome aa₃-600 menaquinol oxidase from Bacillus subtilis containing 1 equivalent of menaquinone. The structure shows that TM0 forms part of a cleft to accommodate the menaquinol-7 substrate. Crystals which have been soaked with the quinol-analog inhibitor HQNO (N-oxo-2-heptyl-4-hydroxyquinoline) or 3-iodo-HQNO reveal a single binding site where the inhibitor forms hydrogen bonds to amino acid residues shown previously by spectroscopic methods to interact with the semiquinone state of menaquinone, a catalytic intermediate.

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Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-87ER13716

OSTI ID:: 1800648

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 2 Vol. 117; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (34)

CHARMM-GUI Membrane Builder toward realistic biological membrane simulations Wu, Emilia L.; Cheng, Xi; Jo, Sunhwan Journal of Computational Chemistry, Vol. 35, Issue 27 https://doi.org/10.1002/jcc.23702	journal	August 2014
Diversity of the Heme–Copper Superfamily in Archaea: Insights from Genomics and Structural Modeling Hemp, James; Gennis, Robert B. Bioenergetics https://doi.org/10.1007/400_2007_046	book	January 2008
Cytochrome c oxidase: exciting progress and remaining mysteries Brzezinski, Peter; Gennis, Robert B. Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5 https://doi.org/10.1007/s10863-008-9181-7	journal	October 2008
The sequence of the cyo operon indicates substantial structural similarities between the cytochrome o ubiquinol oxidase of Escherichia coli and the aa3-type family of cytochrome c oxidases. Chepuri, V.; Lemieux, L.; Au, D. C. Journal of Biological Chemistry, Vol. 265, Issue 19 https://doi.org/10.1016/S0021-9258(19)38574-6	journal	July 1990
The quinone-binding sites of the cytochrome bo3 ubiquinol oxidase from Escherichia coli Yap, Lai Lai; Lin, Myat T.; Ouyang, Hanlin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 12 https://doi.org/10.1016/j.bbabio.2010.04.011	journal	December 2010
Characterization of the semiquinone radical stabilized by the cytochrome aa3-600 menaquinol oxidase of Bacillus subtilis Yi, Sophia M.; Narasimhulu, Kuppala V.; Samoilova, Rimma I. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797 https://doi.org/10.1016/j.bbabio.2010.04.284	journal	July 2010
The superfamily of heme–copper oxygen reductases: Types and evolutionary considerations Sousa, Filipa L.; Alves, Renato J.; Ribeiro, Miguel A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 4 https://doi.org/10.1016/j.bbabio.2011.09.020	journal	April 2012
Exploring membrane respiratory chains Marreiros, Bruno C.; Calisto, Filipa; Castro, Paulo J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 8 https://doi.org/10.1016/j.bbabio.2016.03.028	journal	August 2016
Searching for the low affinity ubiquinone binding site in cytochrome bo3 from Escherichia coli Choi, Sylvia K.; Lin, Myat T.; Ouyang, Hanlin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 5 https://doi.org/10.1016/j.bbabio.2017.02.008	journal	May 2017
Single-step production of arabino-xylooligosaccharides by recombinant Bacillus subtilis 3610 cultivated in brewers’ spent grain Amorim, Cláudia; Silvério, Sara C.; Silva, Soraia P. Carbohydrate Polymers, Vol. 199 https://doi.org/10.1016/j.carbpol.2018.07.017	journal	November 2018
Plasticity in the High Affinity Menaquinone Binding Site of the Cytochrome aa ₃ -600 Menaquinol Oxidase from Bacillus subtilis Yi, Sophia M.; Taguchi, Alexander T.; Samoilova, Rimma I. Biochemistry, Vol. 54, Issue 32 https://doi.org/10.1021/acs.biochem.5b00528	journal	August 2015
Q-Band Electron-Nuclear Double Resonance Reveals Out-of-Plane Hydrogen Bonds Stabilize an Anionic Ubisemiquinone in Cytochrome bo ₃ from Escherichia coli Sun, Chang; Taguchi, Alexander T.; Vermaas, Josh V. Biochemistry, Vol. 55, Issue 40 https://doi.org/10.1021/acs.biochem.6b00669	journal	September 2016
Transient-State Reduction and Steady-State Kinetic Studies of Menaquinol Oxidase from Bacillus subtilis , Cytochrome aa ₃ -600 nm. Spectroscopic Characterization of the Steady-State Species ^† Mattatall, Neil R.; Cameron, Linda M.; Hill, Bruce C. Biochemistry, Vol. 40, Issue 44 https://doi.org/10.1021/bi011116q	journal	November 2001
Identification of the Residues Involved in Stabilization of the Semiquinone Radical in the High-Affinity Ubiquinone Binding Site in Cytochrome bo ₃ from Escherichia coli by Site-Directed Mutagenesis and EPR Spectroscopy ^† Hellwig, Petra; Yano, Takahiro; Ohnishi, Tomoko Biochemistry, Vol. 41, Issue 34 https://doi.org/10.1021/bi012146w	journal	August 2002
Interactions of Intermediate Semiquinone with Surrounding Protein Residues at the Q _H Site of Wild-Type and D75H Mutant Cytochrome bo ₃ from Escherichia coli Lin, Myat T.; Baldansuren, Amgalanbaatar; Hart, Richard Biochemistry, Vol. 51, Issue 18 https://doi.org/10.1021/bi300151q	journal	April 2012
Redox-Dependent Conformational Changes in Cytochrome c Oxidase Suggest a Gating Mechanism for Proton Uptake Qin, Ling; Liu, Jian; Mills, Denise A. Biochemistry, Vol. 48, Issue 23 https://doi.org/10.1021/bi9001387	journal	June 2009
Electron Transfer Kinetics during the Reduction and Turnover of the Cytochrome caa ₃ Complex from Bacillus subtilis Assempour, Mahmoud; Lim, Dan; Hill, Bruce C. Biochemistry, Vol. 37, Issue 28 https://doi.org/10.1021/bi980331c	journal	June 1998
Identification of the Nitrogen Donor Hydrogen Bonded with the Semiquinone at the Q _H Site of the Cytochrome bo ₃ from Escherichia coli Lin, Myat T.; Samoilova, Rimma I.; Gennis, Robert B. Journal of the American Chemical Society, Vol. 130, Issue 47 https://doi.org/10.1021/ja805906a	journal	November 2008
Location of the Substrate Binding Site of the Cytochrome bo ₃ Ubiquinol Oxidase from Escherichia coli Choi, Sylvia K.; Schurig-Briccio, Lici; Ding, Ziqiao Journal of the American Chemical Society, Vol. 139, Issue 24 https://doi.org/10.1021/jacs.7b03883	journal	June 2017
Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans Iwata, So; Ostermeier, Christian; Ludwig, Bernd Nature, Vol. 376, Issue 6542 https://doi.org/10.1038/376660a0	journal	August 1995
Structural insights into electron transfer in caa3-type cytochrome oxidase Lyons, Joseph A.; Aragão, David; Slattery, Orla Nature, Vol. 487, Issue 7408 https://doi.org/10.1038/nature11182	journal	July 2012
Crystal structure of heme A synthase from Bacillus subtilis Niwa, Satomi; Takeda, Kazuki; Kosugi, Masayuki Proceedings of the National Academy of Sciences, Vol. 115, Issue 47 https://doi.org/10.1073/pnas.1813346115	journal	November 2018
The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer Konstantinov, A. A.; Siletsky, S.; Mitchell, D. Proceedings of the National Academy of Sciences, Vol. 94, Issue 17 https://doi.org/10.1073/pnas.94.17.9085	journal	August 1997
Characterization of the Semiquinone Radical Stabilized by the Cytochrome aa3-600 Menaquinol Oxidase of Bacillus subtilis Yi, Sophia M.; Narasimhulu, Kuppala V.; Samoilova, Rimma I. Journal of Biological Chemistry, Vol. 285, Issue 24 https://doi.org/10.1074/jbc.M110.116186	journal	June 2010
Exploring by Pulsed EPR the Electronic Structure of Ubisemiquinone Bound at the QH Site of Cytochrome bo3 from Escherichia coli with in Vivo 13C-Labeled Methyl and Methoxy Substituents* Lin, Myat T.; Shubin, Alexander A.; Samoilova, Rimma I. Journal of Biological Chemistry, Vol. 286, Issue 12 https://doi.org/10.1074/jbc.M110.206821	journal	March 2011
Characterization of the Exchangeable Protons in the Immediate Vicinity of the Semiquinone Radical at the QH Site of the Cytochrome bo3 from Escherichia coli Yap, Lai Lai; Samoilova, Rimma I.; Gennis, Robert B. Journal of Biological Chemistry, Vol. 281, Issue 25 https://doi.org/10.1074/jbc.M602544200	journal	June 2006
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
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
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
The Structure of cbb3 Cytochrome Oxidase Provides Insights into Proton Pumping Buschmann, S.; Warkentin, E.; Xie, H. Science, Vol. 329, Issue 5989 https://doi.org/10.1126/science.1187303	journal	June 2010
The Whole Structure of the 13-Subunit Oxidized Cytochrome c Oxidase at 2.8 A Tsukihara, T.; Aoyama, H.; Yamashita, E. Science, Vol. 272, Issue 5265 https://doi.org/10.1126/science.272.5265.1136	journal	May 1996
High Resolution Structure of the ba3 Cytochrome c Oxidase from Thermus thermophilus in a Lipidic Environment Tiefenbrunn, Theresa; Liu, Wei; Chen, Ying PLoS ONE, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pone.0022348	journal	July 2011
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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Title: Structure of the cytochrome aa 3 -600 heme-copper menaquinol oxidase bound to inhibitor HQNO shows TM0 is part of the quinol binding site

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Title: Structure of the cytochrome aa ₃ -600 heme-copper menaquinol oxidase bound to inhibitor HQNO shows TM0 is part of the quinol binding site