Structural basis of membrane machines that traffick and attach heme to cytochromes

Huynh, Jonathan Q.; Lowder, Ethan P.; Kranz, Robert G.

doi:10.1016/j.jbc.2023.105332

Title: Structural basis of membrane machines that traffick and attach heme to cytochromes

Journal Article · 01 November 2023 · Journal of Biological Chemistry

DOI: https://doi.org/10.1016/j.jbc.2023.105332 · OSTI ID:2205112

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Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0023727

OSTI ID:: 2205112

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 299 Journal Issue: 11; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Cytochrome c biogenesis: the Ccm system Sanders, Carsten; Turkarslan, Serdar; Lee, Dong-Woo Trends in Microbiology, Vol. 18, Issue 6 https://doi.org/10.1016/j.tim.2010.03.006	journal	June 2010
The thioreduction component CcmG confers efficiency and the heme ligation component CcmH ensures stereo-specificity during cytochrome c maturation Verissimo, Andreia F.; Khalfaoui-Hassani, Bahia; Hwang, Josephine Journal of Biological Chemistry, Vol. 292, Issue 32 https://doi.org/10.1074/jbc.M117.794586	journal	June 2017
AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading Trott, Oleg; Olson, Arthur J. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21334	journal	January 2009
Engineered holocytochrome c synthases that biosynthesize new cytochromes c Mendez, Deanna L.; Babbitt, Shalon E.; King, Jeremy D. Proceedings of the National Academy of Sciences, Vol. 114, Issue 9 https://doi.org/10.1073/pnas.1615929114	journal	February 2017
Ion permeation in K+ channels occurs by direct Coulomb knock-on Kopfer, D. A.; Song, C.; Gruene, T. Science, Vol. 346, Issue 6207 https://doi.org/10.1126/science.1254840	journal	October 2014
AF2Complex predicts direct physical interactions in multimeric proteins with deep learning Gao, Mu; Nakajima An, Davi; Parks, Jerry M. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29394-2	journal	April 2022
Mutations in Cytochrome Assembly and Periplasmic Redox Pathways in Bordetella pertussis Feissner, R. E.; Beckett, C. S.; Loughman, J. A. Journal of Bacteriology, Vol. 187, Issue 12 https://doi.org/10.1128/JB.187.12.3941-3949.2005	journal	June 2005
Essential Histidine and Tryptophan Residues in CcsA, a System II Polytopic Cytochrome c Biogenesis Protein Hamel, Patrice P.; Dreyfuss, Beth Welty; Xie, Zhiyi Journal of Biological Chemistry, Vol. 278, Issue 4 https://doi.org/10.1074/jbc.M208651200	journal	November 2002
Mmicular mechanisms of cytochrome c biogenesis: three distinct systems Kranz, Robert; Lill, Roland; Goldman, Barry Molecular Microbiology, Vol. 29, Issue 2 https://doi.org/10.1046/j.1365-2958.1998.00869.x	journal	July 1998
Heme Trafficking and Modifications during System I Cytochrome c Biogenesis: Insights from Heme Redox Potentials of Ccm Proteins Sutherland, Molly C.; Rankin, Joel A.; Kranz, Robert G. Biochemistry, Vol. 55, Issue 22 https://doi.org/10.1021/acs.biochem.6b00427	journal	May 2016
Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB Schulz, H.; Fabianek, R. A.; Pellicioli, E. C. Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.6462	journal	May 1999
A conserved haem redox and trafficking pathway for cofactor attachment Richard-Fogal, Cynthia L.; Frawley, Elaine R.; Bonner, Eric R. The EMBO Journal, Vol. 28, Issue 16 https://doi.org/10.1038/emboj.2009.189	journal	July 2009
Substrate specificity of three cytochrome c haem lyase isoenzymes from Wolinella succinogenes : unconventional haem c binding motifs are not sufficient for haem c attachment by NrfI and CcsA1 Kern, Melanie; Eisel, Florian; Scheithauer, Juliane Molecular Microbiology, Vol. 75, Issue 1 https://doi.org/10.1111/j.1365-2958.2009.06965.x	journal	January 2010
The Cytochrome c Maturation Components CcmF, CcmH, and CcmI Form a Membrane-integral Multisubunit Heme Ligation Complex Sanders, Carsten; Turkarslan, Serdar; Lee, Dong-Woo Journal of Biological Chemistry, Vol. 283, Issue 44 https://doi.org/10.1074/jbc.M805413200	journal	August 2008
Heme Mobilization in Animals: A Metallolipid’s Journey Reddi, Amit R.; Hamza, Iqbal Accounts of Chemical Research, Vol. 49, Issue 6 https://doi.org/10.1021/acs.accounts.5b00553	journal	June 2016
Thiol redox requirements and substrate specificities of recombinant cytochrome c assembly systems II and III Richard-Fogal, Cynthia L.; San Francisco, Brian; Frawley, Elaine R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6 https://doi.org/10.1016/j.bbabio.2011.09.008	journal	June 2012
Probing the Heme-Binding Site of the Cytochrome c Maturation Protein CcmE Harvat, Edgar M.; Redfield, Christina; Stevens, Julie M. Biochemistry, Vol. 48, Issue 8 https://doi.org/10.1021/bi801609a	journal	January 2009
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Transmembrane heme delivery systems Goldman, B. S.; Beck, D. L.; Monika, E. M. Proceedings of the National Academy of Sciences, Vol. 95, Issue 9 https://doi.org/10.1073/pnas.95.9.5003	journal	April 1998
Genes required for cytochrome c synthesis inBacillus subtilis: B. subtilis cytochrome c synthesis Le Brun, Nick E.; Bengtsson, Jenny; Hederstedt, Lars Molecular Microbiology, Vol. 36, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.01883.x	journal	May 2000
Cryo-EM structure of mycobacterial cytochrome bd reveals two oxygen access channels Wang, Weiwei; Gao, Yan; Tang, Yanting Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-24924-w	journal	July 2021
ABC transporter-mediated release of a haem chaperone allows cytochrome c biogenesis: New role for ABC transporter is haem release Feissner, Robert E.; Richard-Fogal, Cynthia L.; Frawley, Elaine R. Molecular Microbiology, Vol. 61, Issue 1 https://doi.org/10.1111/j.1365-2958.2006.05221.x	journal	May 2006
NMR Structure of the Heme Chaperone CcmE Reveals a Novel Functional Motif Enggist, Elisabeth; Thöny-Meyer, Linda; Güntert, Peter Structure, Vol. 10, Issue 11 https://doi.org/10.1016/S0969-2126(02)00885-7	journal	November 2002
Architecture of the membrane-bound cytochrome c heme lyase CcmF Brausemann, Anton; Zhang, Lin; Ilcu, Lorena Nature Chemical Biology, Vol. 17, Issue 7 https://doi.org/10.1038/s41589-021-00793-8	journal	May 2021
Structure-function analysis of the heme-binding WWD domain in the bacterial holocytochrome c synthase, CcmFH Grunow, Amber L.; Carroll, Susan C.; Kreiman, Alicia N. mBio https://doi.org/10.1128/mbio.01509-23	journal	November 2023
Structure-Function Analysis of the Bifunctional CcsBA Heme Exporter and Cytochrome c Synthetase Sutherland, Molly C.; Tran, Nathan L.; Tillman, Dustin E. mBio, Vol. 9, Issue 6 https://doi.org/10.1128/mBio.02134-18	journal	December 2018
His protects heme as it crosses the membrane Merchant, Sabeeha S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 25 https://doi.org/10.1073/pnas.0905189106	journal	June 2009
Heme dynamics and trafficking factors revealed by genetically encoded fluorescent heme sensors Hanna, David A.; Harvey, Raven M.; Martinez-Guzman, Osiris Proceedings of the National Academy of Sciences, Vol. 113, Issue 27 https://doi.org/10.1073/pnas.1523802113	journal	May 2016
Haem‐delivery proteins in cytochrome c maturation System II Ahuja, Umesh; Kjelgaard, Peter; Schulz, Benjamin L. Molecular Microbiology, Vol. 73, Issue 6 https://doi.org/10.1111/j.1365-2958.2009.06833.x	journal	September 2009
In vitro reconstitution reveals major differences between human and bacterial cytochrome c synthases Sutherland, Molly C.; Mendez, Deanna L.; Babbitt, Shalon E. eLife, Vol. 10 https://doi.org/10.7554/eLife.64891	journal	May 2021
Unusual Heme−Histidine Bond in the Active Site of a Chaperone Lee, Donghan; Pervushin, Konstantin; Bischof, Daniela Journal of the American Chemical Society, Vol. 127, Issue 11 https://doi.org/10.1021/ja044658e	journal	March 2005
Heme transport and erythropoiesis Yuan, Xiaojing; Fleming, Mark D.; Hamza, Iqbal Current Opinion in Chemical Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.cbpa.2013.01.010	journal	April 2013
The Plastid-encoded ccsA Gene Is Required for Heme Attachment to Chloroplast c-type Cytochromes Merchant, S. Journal of Biological Chemistry, Vol. 271, Issue 9 https://doi.org/10.1074/jbc.271.9.4632	journal	March 1996
Potassium channels MacKinnon, Roderick FEBS Letters, Vol. 555, Issue 1 https://doi.org/10.1016/S0014-5793(03)01104-9	journal	October 2003
Glyceraldehyde-3-phosphate dehydrogenase is a chaperone that allocates labile heme in cells Sweeny, Elizabeth A.; Singh, Anuradha Bharara; Chakravarti, Ritu Journal of Biological Chemistry, Vol. 293, Issue 37 https://doi.org/10.1074/jbc.RA118.004169	journal	July 2018
Oxidation−Reduction Properties of Disulfide-Containing Proteins of the Rhodobacter capsulatus Cytochrome c Biogenesis System ^† Setterdahl, Aaron T.; Goldman, Barry S.; Hirasawa, Masakazu Biochemistry, Vol. 39, Issue 33 https://doi.org/10.1021/bi000663t	journal	August 2000
Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. Dumont, M. E.; Ernst, J. F.; Hampsey, D. M. The EMBO Journal, Vol. 6, Issue 1 https://doi.org/10.1002/j.1460-2075.1987.tb04744.x	journal	January 1987
GAPDH delivers heme to soluble guanylyl cyclase Dai, Yue; Sweeny, Elizabeth A.; Schlanger, Simon Journal of Biological Chemistry, Vol. 295, Issue 24 https://doi.org/10.1074/jbc.RA120.013802	journal	June 2020
Structures of the CcmABCD heme release complex at multiple states Li, Jiao; Zheng, Wan; Gu, Ming Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-34136-5	journal	October 2022
Ccs1 , a Nuclear Gene Required for the Post-translational Assembly of Chloroplast c -Type Cytochromes Inoue, Kaori; Dreyfuss, Beth Welty; Kindle, Karen L. Journal of Biological Chemistry, Vol. 272, Issue 50 https://doi.org/10.1074/jbc.272.50.31747	journal	December 1997
Molecular Basis Behind Inability of Mitochondrial Holocytochrome c Synthase to Mature Bacterial Cytochromes Babbitt, Shalon E.; Hsu, Jennifer; Kranz, Robert G. Journal of Biological Chemistry, Vol. 291, Issue 34 https://doi.org/10.1074/jbc.M116.741231	journal	August 2016
Human mitochondrial holocytochrome c synthase’s heme binding, maturation determinants, and complex formation with cytochrome c San Francisco, Brian; Bretsnyder, Eric C.; Kranz, Robert G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 9 https://doi.org/10.1073/pnas.1213897109	journal	November 2012
Bacterial cytochromes c biogenesis. Beckman, D. L.; Trawick, D. R.; Kranz, R. G. Genes & Development, Vol. 6, Issue 2 https://doi.org/10.1101/gad.6.2.268	journal	February 1992
Composition and function of cytochrome c biogenesis System II: Cytochrome c biogenesis System II Simon, Jörg; Hederstedt, Lars FEBS Journal, Vol. 278, Issue 22 https://doi.org/10.1111/j.1742-4658.2011.08374.x	journal	October 2011
Cytochrome c biogenesis System I: Cytochrome c biogenesis System I Stevens, Julie M.; Mavridou, Despoina A. I.; Hamer, Rebecca FEBS Journal, Vol. 278, Issue 22 https://doi.org/10.1111/j.1742-4658.2011.08376.x	journal	October 2011
Insights into the Mechanisms of K ⁺ Permeation in K ⁺ Channels from Computer Simulations Oakes, Victoria; Furini, Simone; Domene, Carmen Journal of Chemical Theory and Computation, Vol. 16, Issue 1 https://doi.org/10.1021/acs.jctc.9b00971	journal	November 2019
Oxidized or Reduced Cytochrome c and Axial Ligand Variants All Form the Apoptosome in Vitro Mendez, Deanna L.; Akey, Ildikó V.; Akey, Christopher W. Biochemistry, Vol. 56, Issue 22 https://doi.org/10.1021/acs.biochem.7b00309	journal	May 2017
Evolutionary origins of members of a superfamily of integral membrane cytochrome c biogenesis proteins Lee, Jong-Hoon; Harvat, Edgar M.; Stevens, Julie M. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 9 https://doi.org/10.1016/j.bbamem.2007.04.022	journal	September 2007
Handling heme with care Brown, Breann L.; Iverson, T. M. Nature Chemical Biology, Vol. 17, Issue 7 https://doi.org/10.1038/s41589-021-00821-7	journal	June 2021
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
The CcmE protein of the c-type cytochrome biogenesis system: Unusual in vitro heme incorporation into apo-CcmE and transfer from holo-CcmE to apocytochrome Daltrop, O.; Stevens, J. M.; Higham, C. W. Proceedings of the National Academy of Sciences, Vol. 99, Issue 15 https://doi.org/10.1073/pnas.152120699	journal	July 2002
Mitochondrial cytochrome c biogenesis: no longer an enigma Babbitt, Shalon E.; Sutherland, Molly C.; Francisco, Brian San Trends in Biochemical Sciences, Vol. 40, Issue 8 https://doi.org/10.1016/j.tibs.2015.05.006	journal	August 2015
Cryo-EM of CcsBA reveals the basis for cytochrome c biogenesis and heme transport Mendez, Deanna L.; Lowder, Ethan P.; Tillman, Dustin E. Nature Chemical Biology, Vol. 18, Issue 1 https://doi.org/10.1038/s41589-021-00935-y	journal	December 2021
Prototype of a Heme Chaperone Essential for Cytochrome c Maturation Schulz, H. Science, Vol. 281, Issue 5380 https://doi.org/10.1126/science.281.5380.1197	journal	August 1998
Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis , a unique bacterial model : A bacterial model for system II cytochrome Beckett, Caroline S.; Loughman, Jennifer A.; Karberg, Katherine A. Molecular Microbiology, Vol. 38, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.02174.x	journal	November 2000
Recombinant cytochromes c biogenesis systems I and II and analysis of haem delivery pathways in Escherichia coli Feissner, Robert E.; Richard-Fogal, Cynthia L.; Frawley, Elaine R. Molecular Microbiology, Vol. 60, Issue 3 https://doi.org/10.1111/j.1365-2958.2006.05132.x	journal	May 2006
CcsBA is a cytochrome c synthetase that also functions in heme transport Frawley, E. R.; Kranz, R. G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 25 https://doi.org/10.1073/pnas.0903132106	journal	June 2009
Essential histidine pairs indicate conserved haem binding in epsilonproteobacterial cytochrome c haem lyases Kern, Melanie; Scheithauer, Juliane; Kranz, Robert G. Microbiology, Vol. 156, Issue 12 https://doi.org/10.1099/mic.0.042838-0	journal	December 2010
Control of intracellular heme levels: Heme transporters and heme oxygenases Khan, Anwar A.; Quigley, John G. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1813, Issue 5 https://doi.org/10.1016/j.bbamcr.2011.01.008	journal	May 2011
Genetic Analysis of Chloroplast c-Type Cytochrome Assembly in Chlamydomonas reinhardtii: One Chloroplast Locus and at Least Four Nuclear Loci Are Required for Heme Attachment Xie, Zhiyi; Culler, Duane; Dreyfuss, Beth Welty Genetics, Vol. 148, Issue 2 https://doi.org/10.1093/genetics/148.2.681	journal	February 1998
Functional Characterization of the C-terminal Domain of the Cytochrome c Maturation Protein CcmE Harvat, Edgar M.; Stevens, Julie M.; Redfield, Christina Journal of Biological Chemistry, Vol. 280, Issue 44 https://doi.org/10.1074/jbc.M508355200	journal	November 2005
Mechanisms of Mitochondrial Holocytochrome c Synthase and the Key Roles Played by Cysteines and Histidine of the Heme Attachment Site, Cys-XX-Cys-His Babbitt, Shalon E.; San Francisco, Brian; Mendez, Deanna L. Journal of Biological Chemistry, Vol. 289, Issue 42 https://doi.org/10.1074/jbc.M114.593509	journal	October 2014
Genomic analyses of bacterial respiratory and cytochrome c assembly systems: Bordetella as a model for the System II cytochrome c biogenesis pathway Kranz, Robert G.; Beckett, Caroline S.; Goldman, Barry S. Research in Microbiology, Vol. 153, Issue 1 https://doi.org/10.1016/S0923-2508(01)01278-5	journal	January 2002
The chemistry and biochemistry of heme c: functional bases for covalent attachment Bowman, Sarah E. J.; Bren, Kara L. Natural Product Reports, Vol. 25, Issue 6 https://doi.org/10.1039/b717196j	journal	January 2008
The CcmC:Heme:CcmE Complex in Heme Trafficking and Cytochrome c Biosynthesis Richard-Fogal, Cynthia; Kranz, Robert G. Journal of Molecular Biology, Vol. 401, Issue 3 https://doi.org/10.1016/j.jmb.2010.06.041	journal	August 2010
Compensatory thio-redox interactions between DsbA, CcdA and CcmG unveil the apocytochrome c holdase role of CcmG during cytochrome c maturation Turkarslan, Serdar; Sanders, Carsten; Ekici, Seda Molecular Microbiology, Vol. 70, Issue 3 https://doi.org/10.1111/j.1365-2958.2008.06441.x	journal	November 2008
The mitochondrial heme metabolon: Insights into the complex(ity) of heme synthesis and distribution Piel, Robert B.; Dailey, Harry A.; Medlock, Amy E. Molecular Genetics and Metabolism, Vol. 128, Issue 3 https://doi.org/10.1016/j.ymgme.2019.01.006	journal	November 2019
Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c -Type Cytochrome Biogenesis Dreyfuss, Beth Welty; Hamel, Patrice P.; Nakamoto, Stacie S. Journal of Biological Chemistry, Vol. 278, Issue 4 https://doi.org/10.1074/jbc.M208652200	journal	November 2002
Computed structures of core eukaryotic protein complexes Humphreys, Ian R.; Pei, Jimin; Baek, Minkyung Science, Vol. 374, Issue 6573 https://doi.org/10.1126/science.abm4805	journal	December 2021
Interaction of HoloCcmE with CcmF in Heme Trafficking and Cytochrome c Biosynthesis San Francisco, Brian; Kranz, Robert G. Journal of Molecular Biology, Vol. 426, Issue 3 https://doi.org/10.1016/j.jmb.2013.10.025	journal	February 2014
Structurally Mapping Endogenous Heme in the CcmCDE Membrane Complex for Cytochrome c Biogenesis Sutherland, Molly C.; Jarodsky, Joshua M.; Ovchinnikov, Sergey Journal of Molecular Biology, Vol. 430, Issue 8 https://doi.org/10.1016/j.jmb.2018.01.022	journal	April 2018

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