Structural basis and mechanism for metallochaperone-assisted assembly of the CuA center in cytochrome oxidase

Science Advances
Fabia CanonicaRudi Glockshuber

Abstract

The mechanisms underlying the biogenesis of the structurally unique, binuclear Cu1.5+•Cu1.5+ redox center (CuA) on subunit II (CoxB) of cytochrome oxidases have been a long-standing mystery. Here, we reconstituted the CoxB•CuA center in vitro from apo-CoxB and the holo-forms of the copper transfer chaperones ScoI and PcuC. A previously unknown, highly stable ScoI•Cu2+•CoxB complex was shown to be rapidly formed as the first intermediate in the pathway. Moreover, our structural data revealed that PcuC has two copper-binding sites, one each for Cu1+ and Cu2+, and that only PcuC•Cu1+•Cu2+ can release CoxB•Cu2+ from the ScoI•Cu2+•CoxB complex. The CoxB•CuA center was then formed quantitatively by transfer of Cu1+ from a second equivalent of PcuC•Cu1+•Cu2+ to CoxB•Cu2+. This metalation pathway is consistent with all available in vivo data and identifies the sources of the Cu ions required for CuA center formation and the order of their delivery to CoxB.

References

Aug 1, 1983·Archives of Microbiology·B Regensburger, H Hennecke
Aug 1, 1996·Current Opinion in Structural Biology·C OstermeierH Michel
Jun 12, 1998·Journal of Bioenergetics and Biomembranes·S YoshikawaT Tsukihara
Jun 9, 1999·Nature Structural Biology·P A WilliamsD E McRee
Jan 29, 2000·Journal of Magnetic Resonance·M PannierH W Spiess
May 9, 2001·Biochimica Et Biophysica Acta·J AbramsonS Iwata
Nov 7, 2002·Advances in Protein Chemistry·Shinya Yoshikawa
Dec 2, 2004·Acta Crystallographica. Section D, Biological Crystallography·Alexei A VaginGarib N Murshudov
Mar 2, 2005·Proceedings of the National Academy of Sciences of the United States of America·Harry B Gray, Jay R Winkler
Mar 9, 2005·Proceedings of the National Academy of Sciences of the United States of America·Lucia BanciStefano Mangani
Aug 11, 2005·The Journal of Biological Chemistry·Yih-Chern HorngDennis R Winge
Sep 29, 2005·Journal of Magnetic Resonance·Stefan Stoll, Arthur Schweiger
Mar 30, 2006·Journal of Biological Inorganic Chemistry : JBIC : a Publication of the Society of Biological Inorganic Chemistry·Carnie Abajian, Amy C Rosenzweig
Jun 1, 2006·Proceedings of the National Academy of Sciences of the United States of America·Lucia BanciShenlin Wang
Sep 14, 2007·Structure·Lucia BanciShenlin Wang
Apr 19, 2008·The Biochemical Journal·Liang ZhouNick E Le Brun
May 7, 2008·Proceedings of the National Academy of Sciences of the United States of America·Lucia BanciPeep Palumaa
Sep 2, 2008·Nature Chemical Biology·Luciano A AbriataShenlin Wang
Nov 7, 2008·Methods in Molecular Biology·Joseph E TropeaDavid S Waugh
Nov 26, 2008·Advances in Applied Microbiology·Deenah Osman, Jennifer S Cavet
Apr 2, 2009·Human Molecular Genetics·Scot C LearyEric A Shoubridge
May 7, 2009·Proceedings of the National Academy of Sciences of the United States of America·Lee Macomber, James A Imlay
Feb 4, 2010·Acta Crystallographica. Section D, Biological Crystallography·Wolfgang Kabsch
Mar 9, 2010·Annual Review of Biochemistry·Nigel J Robinson, Dennis R Winge
Mar 26, 2010·The Journal of Biological Chemistry·Doris BühlerHauke Hennecke
Apr 13, 2010·Acta Crystallographica. Section D, Biological Crystallography·P EmsleyK Cowtan
Nov 9, 2010·Chemical Reviews·Ville R I KailaMårten Wikström
Apr 27, 2011·The FEBS Journal·Lucia BanciSimone Ciofi-Baffoni
Sep 6, 2012·Journal of the American Chemical Society·Kelly N Chacón, Ninian J Blackburn
Sep 27, 2012·The Journal of Biological Chemistry·Fabio ServentiHauke Hennecke
Dec 12, 2012·Molecular Microbiology·Dietrich H Nies, Martin Herzberg

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Citations

Sep 24, 2020·Membranes·Andreea AndreiHans-Georg Koch
Sep 19, 2019·The Journal of Biological Chemistry·Oriana S FisherAmy C Rosenzweig
Feb 17, 2021·Molecular Microbiology·Claes von WachenfeldtLars Hederstedt
May 1, 2021·Journal of Biological Inorganic Chemistry : JBIC : a Publication of the Society of Biological Inorganic Chemistry·Dwaipayan Dutta GuptaShyamalava Mazumdar
Dec 31, 2020·Journal of the American Chemical Society·Lin ZhangOliver Einsle
Oct 1, 2021·Frontiers in Microbiology·Andreea AndreiHans-Georg Koch

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Methods Mentioned

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electron paramagnetic resonance
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x-ray diffraction

Software Mentioned

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