Structurally Mapping Endogenous Heme in the CcmCDE Membrane Complex for Cytochrome c Biogenesis
Open accessAbstract
Although many putative heme transporters have been discovered, it has been challenging to prove that these proteins are directly involved with heme trafficking in vivo and to identify their heme binding domains. The prokaryotic pathways for cytochrome c biogenesis, Systems I and II, transport heme from inside the cell to outside for stereochemical attachment to cytochrome c, making them excellent models to study heme trafficking. System I is composed of eight integral membrane proteins (CcmA-H) and is proposed to transport heme via CcmC to an external "WWD" domain for presentation to the membrane-tethered heme chaperone, CcmE. Herein, we develop a new cysteine/heme crosslinking approach to trap and map endogenous heme in CcmC (WWD domain) and CcmE (defining "2-vinyl" and "4-vinyl" pockets for heme). Crosslinking occurs when either of the two vinyl groups of heme localize near a thiol of an engineered cysteine residue. Double crosslinking, whereby both vinyls crosslink to two engineered cysteines, facilitated a more detailed structural mapping of the heme binding sites, including stereospecificity. Using heme crosslinking results, heme ligand identification, and genomic coevolution data, we model the structure of the CcmCDE complex, including the WWD heme binding domain. We conclude that CcmC trafficks heme via its WWD domain and propose the structural basis for stereochemical attachment of heme.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The best effort to date is a partial model of the CcmCDE complex generated using co-evolutionary analysis.
“To date, the best effort is a partial model of the CcmCDE complex generated using co-evolutionary analysis47.”
From AF2Complex predicts direct physical interactions in multimeric proteins with deep learning (2022) · cites this paper as [47]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The PSIPRED protein structure prediction server
McGuffin, L. J., Bryson, K., & Jones, D. T. (2000) · Bioinformatics · doi:10.1093/bioinformatics/16.4.404 · Cited by 3,841 · see citing works
Protein homology detection by HMM–HMM comparison
Söding, J. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bti125 · Cited by 2,381 · see citing works
A NEW GENERATION OF HOMOLOGY SEARCH TOOLS BASED ON PROBABILISTIC INFERENCE
Eddy, S. R. (2009) · International Conference on Genome Informatics (GIW) · doi:10.1142/9781848165632_0019 · Cited by 1,275 · see citing works
High-Resolution Comparative Modeling with RosettaCM
Song, Y., DiMaio, F., Wang, R. Y., Kim, D. E., Miles, C., Brunette, T., Thompson, J., & Baker, D. A. (2013) · Structure · doi:10.1016/j.str.2013.08.005 · Cited by 1,079 · see citing works
Self-citationSimultaneous determination of hemes a, b, and c from pyridine hemochrome spectra
Berry, E. A., & Trumpower, B. L. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90643-9 · Cited by 918 · see citing works
Kamisetty, H., Ovchinnikov, S., & Baker, D. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314045110 · Cited by 672 · see citing works
Self-citationProtein structure determination using metagenome sequence data
Ovchinnikov, S., Park, H., Varghese, N., Huang, P.-S., Pavlopoulos, G. A., Kim, D. E., Kamisetty, H., Kyrpides, N. C., & Baker, D. (2017) · Science · doi:10.1126/science.aah4043 · Cited by 520 · see citing works
Self-citationHeme in pathophysiology: a matter of scavenging, metabolism and trafficking across cell membranes
Chiabrando, D., Vinchi, F., Fiorito, V., Mercurio, S., & Tolosano, E. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00061 · Cited by 455 · see citing works
Identification of a Human Heme Exporter that Is Essential for Erythropoiesis
Quigley, J. G., Yang, Z., Worthington, M., Phillips, J. D., Sabo, K. M., Sabath, D. E., Berg, C. L., Sassa, S., Wood, B. L., & Abkowitz, J. L. (2004) · Cell · doi:10.1016/j.cell.2004.08.014 · Cited by 423 · see citing works
A Heme Export Protein Is Required for Red Blood Cell Differentiation and Iron Homeostasis
Keel, S. B., Doty, R. T., Yang, Z., Quigley, J. G., Chen, J., Knoblaugh, S., Kingsley, P. D., De Domenico, I., Vaughn, M. B., Kaplan, J., et al. (2008) · Science · doi:10.1126/science.1151133 · Cited by 404 · see citing works
Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins
Rajagopal, A., Rao, A. U., Amigo, J., Tian, M., Upadhyay, S. K., Hall, C., Uhm, S., Mathew, M. K., Fleming, M. D., Paw, B. H., et al. (2008) · Nature · doi:10.1038/nature06934 · Cited by 316 · see citing works
Kranz, R. G., Richard-Fogal, C., Taylor, J.-S., & Frawley, E. R. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00001-09 · Cited by 275 · see citing works
Self-citationMmicular mechanisms of cytochrome c biogenesis: three distinct systems
Kranz, R. G., Lill, R., Goldman, B. S., Bonnard, G., & Merchant, S. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00869.x · Cited by 257 · see citing works
Self-citationLack of heme synthesis in a free-living eukaryote
Rao, A. U., Carta, L. K., Lesuisse, E., & Hamza, I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500877102 · Cited by 241 · see citing works
White, C., Yuan, X., Schmidt, P. J., Bresciani, E., Samuel, T. K., Campagna, D. R., Hall, C., Bishop, K. S., Calicchio, M. L., Lapierre, A., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.005 · Cited by 237 · see citing works
One ring to rule them all: Trafficking of heme and heme synthesis intermediates in the metazoans
Hamza, I., & Dailey, H. A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.04.009 · Cited by 237 · see citing works
Sixty-five years of the long march in protein secondary structure prediction: the final stretch?
Yang, Y., Gao, J., Wang, J., Heffernan, R., Hanson, J., Paliwal, K. K., & Zhou, Y. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw129 · Cited by 237 · see citing works
Large-scale determination of previously unsolved protein structures using evolutionary information
Ovchinnikov, S., Kinch, L., Park, H., Liao, Y., Pei, J., Kim, D. E., Kamisetty, H., Grishin, N. V., & Baker, D. (2015) · eLife · doi:10.7554/elife.09248 · Cited by 222 · see citing works
Self-citationThe mitochondrial heme exporter FLVCR1b mediates erythroid differentiation
Chiabrando, D., Marro, S. G., Mercurio, S., Giorgi, C., Petrillo, S., Vinchi, F., Fiorito, V., Fagoonee, S., Camporeale, A., Turco, E., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62422 · Cited by 198 · see citing works
Cytochrome c biogenesis: the Ccm system
Sanders, C., Turkarslan, S., Lee, D.-W., & Daldal, F. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.03.006 · Cited by 197 · see citing works
Heme dynamics and trafficking factors revealed by genetically encoded fluorescent heme sensors
Hanna, D. A., Harvey, R. M., Martinez-Guzman, O., Yuan, X., Chandrasekharan, B. P., Raju, G., Outten, F. W., Hamza, I., & Reddi, A. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523802113 · Cited by 197 · see citing works
Prototype of a Heme Chaperone Essential for Cytochrome c Maturation
Schulz, H., Hennecke, H., & Thöny‐Meyer, L. (1998) · Science · doi:10.1126/science.281.5380.1197 · Cited by 196 · see citing works
Generalized Fragment Picking in Rosetta: Design, Protocols and Applications
Gront, D., Kulp, D. W., Vernon, R. M., Strauss, C. E. M., & Baker, D. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023294 · Cited by 194 · see citing works
Self-citationControl of intracellular heme levels: Heme transporters and heme oxygenases
Khan, A., & Quigley, J. G. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.01.008 · Cited by 191 · see citing works
Bacterial cytochromes c biogenesis.Preprint
Beckman, D. L., Trawick, D. R., & Kranz, R. G. (1992) · Genes & Development · doi:10.1101/gad.6.2.268 · Cited by 181 · see citing works
Self-citationThe Plastid-encoded ccsA Gene Is Required for Heme Attachment to Chloroplast c-type Cytochromes
Xie, Z., & Merchant, S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.9.4632 · Cited by 149 · see citing works
Schulz, H., Fabianek, R. A., Pellicioli, E. C., Hennecke, H., & Thöny‐Meyer, L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6462 · Cited by 128 · see citing works
Regulation of intracellular heme trafficking revealed by subcellular reporters
Yuan, X., Rietzschel, N., Kwon, H., Walter‐Nuno, A. B., Hanna, D. A., Phillips, J. D., Raven, E. L., Reddi, A. R., & Hamza, I. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1609865113 · Cited by 123 · see citing works
Heme Mobilization in Animals: A Metallolipid’s Journey
Reddi, A. R., & Hamza, I. (2016) · Accounts of Chemical Research · doi:10.1021/acs.accounts.5b00553 · Cited by 118 · see citing works
Transmembrane heme delivery systems
Goldman, B. S., Beck, D. L., Monika, E. M., & Kranz, R. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5003 · Cited by 106 · see citing works
Self-citationComposition and function of cytochrome c biogenesis System II
Simon, J., & Hederstedt, L. (2011) · FEBS Journal · doi:10.1111/j.1742-4658.2011.08374.x · Cited by 99 · see citing works
Cytochrome c biogenesis System I
Stevens, J. M., Mavridou, D. A. I., Hamer, R., Kritsiligkou, P., Goddard, A. D., & Ferguson, S. J. (2011) · FEBS Journal · doi:10.1111/j.1742-4658.2011.08376.x · Cited by 93 · see citing works
Transmutation of a heme protein.
Barker, P. D., Ferrer, J. C., Mylrajan, M., Loehr, T. M., Feng, R., Konishi, Y., Funk, W. D., MacGillivray, R. T. A., & Mauk, A. G. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.14.6542 · Cited by 90 · see citing works
Chemiluminescent-based methods to detect subpicomole levels of c-type cytochromes
Feissner, R. E., Xiang, Y., & Kranz, R. G. (2003) · Analytical Biochemistry · doi:10.1016/s0003-2697(02)00658-9 · Cited by 86 · see citing works
Self-citationABC transporter‐mediated release of a haem chaperone allows cytochrome <i>c</i> biogenesis
Feissner, R. E., Richard‐Fogal, C. L., Frawley, E. R., & Kranz, R. G. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05221.x · Cited by 85 · see citing works
Self-citationA Genetically Encoded FRET Sensor for Intracellular Heme
Song, Y., Yang, M., Wegner, S. V., Zhao, J., Zhu, R., Wu, Y., He, C., & Chen, P. R. (2015) · ACS Chemical Biology · doi:10.1021/cb5009734 · Cited by 85 · see citing works
Quantification of labile heme in live malaria parasites using a genetically encoded biosensor
Abshire, J. R., Rowlands, C. J., Ganesan, S. M., So, P. T. C., & Niles, J. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615195114 · Cited by 85 · see citing works
Conversion of Cytochrome b562 to c-Type Cytochromes
Barker, P. D., Nerou, E. P., Freund, S. M. V., & Fearnley, I. M. (1995) · Biochemistry · doi:10.1021/bi00046a027 · Cited by 83 · see citing works
CcsBA is a cytochrome c synthetase that also functions in heme transport
Frawley, E. R., & Kranz, R. G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903132106 · Cited by 77 · see citing works
Self-citationGoldman, B. S., Beckman, D. L., Bali, A., Monika, E. M., Gabbert, K. K., & Kranz, R. G. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.0992 · Cited by 75 · see citing works
Self-citationCytochrome c biogenesis System I: An intricate process catalyzed by a maturase supercomplex?
Veríssimo, A. F., & Daldal, F. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.03.003 · Cited by 72 · see citing works
Hamel, P. P., Dreyfuss, B. W., Xie, Z., Gabilly, S. T., & Merchant, S. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208651200 · Cited by 70 · see citing works
A conserved haem redox and trafficking pathway for cofactor attachment
Richard‐Fogal, C. L., Frawley, E. R., Bonner, E. R., Zhu, H., Francisco, B. S., & Kranz, R. G. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.189 · Cited by 66 · see citing works
Self-citationDo Mammalian Cells Really Need to Export and Import Heme?
Ponka, P., Sheftel, A. D., English, A. M., Bohle, D. S., & Garcia‐Santos, D. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.01.006 · Cited by 64 · see citing works
Daltrop, O., Stevens, J. M., Higham, C. W., & Ferguson, S. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152120699 · Cited by 63 · see citing works
The Interaction of Covalently Bound Heme with the Cytochrome c Maturation Protein CcmE
Uchida, T., Stevens, J. M., Daltrop, O., Harvat, E. M., Lin, H., Ferguson, S. J., & Kitagawa, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408963200 · Cited by 61 · see citing works
NMR Structure of the Heme Chaperone CcmE Reveals a Novel Functional Motif
Enggist, E., Thöny‐Meyer, L., Güntert, P., & Pervushin, K. V. (2002) · Structure · doi:10.1016/s0969-2126(02)00885-7 · Cited by 60 · see citing works
Unusual Heme−Histidine Bond in the Active Site of a Chaperone
Lee, D., Pervushin, K. V., Bischof, D., Braun, M., & Thöny‐Meyer, L. (2005) · Journal of the American Chemical Society · doi:10.1021/ja044658e · Cited by 57 · see citing works
The CcmC:Heme:CcmE Complex in Heme Trafficking and Cytochrome c Biosynthesis
Richard-Fogal, C., & Kranz, R. G. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.06.041 · Cited by 53 · see citing works
Self-citationHeme transport and erythropoiesis
Yuan, X., Fleming, M. D., & Hamza, I. (2013) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2013.01.010 · Cited by 52 · see citing works
Lee, J., Harvat, E. M., Stevens, J. M., Ferguson, S. J., & Saier, M. H. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.04.022 · Cited by 48 · see citing works
Biochemical and Mutational Characterization of the Heme Chaperone CcmE Reveals a Heme Binding Site
Enggist, E., Schneider, M. J., Schulz, H., & Thöny‐Meyer, L. (2002) · Journal of Bacteriology · doi:10.1128/jb.185.1.175-183.2003 · Cited by 41 · see citing works
Haem‐delivery proteins in cytochrome c maturation System II
Ahuja, U., Kjelgaard, P., Schulz, B. L., Thöny‐Meyer, L., & Hederstedt, L. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06833.x · Cited by 37 · see citing works
Redox Processes Controlling the Biogenesis of c -Type Cytochromes
Bonnard, G., Corvest, V., Meyer, E. H., & Hamel, P. P. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3161 · Cited by 36 · see citing works
Probing the Heme-Binding Site of the Cytochrome c Maturation Protein CcmE
Harvat, E. M., Redfield, C., Stevens, J. M., & Ferguson, S. J. (2009) · Biochemistry · doi:10.1021/bi801609a · Cited by 33 · see citing works
San Francisco, B., Sutherland, M. C., & Kranz, R. G. (2014) · Molecular Microbiology · doi:10.1111/mmi.12510 · Cited by 29 · see citing works
Self-citationDynamic Features of a Heme Delivery System for Cytochrome c Maturation
Ahuja, U., & Thöny‐Meyer, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m310077200 · Cited by 28 · see citing works
Topology and Function of CcmD in Cytochrome c Maturation
Richard‐Fogal, C. L., Frawley, E. R., & Kranz, R. G. (2008) · Journal of Bacteriology · doi:10.1128/jb.00146-08 · Cited by 28 · see citing works
Self-citationMaturation of Plastid c-type Cytochromes
Gabilly, S. T., & Hamel, P. P. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01313 · Cited by 27 · see citing works
Interaction of HoloCcmE with CcmF in Heme Trafficking and Cytochrome c Biosynthesis
San Francisco, B., & Kranz, R. G. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.10.025 · Cited by 24 · see citing works
Self-citationConverting Cytochrome b5 into Cytochrome c‐Like Protein
Lin, Y., Wang, W., Zhang, Q., Lu, H., Yang, P., Xie, Y., Huang, Z., & Wu, H. (2005) · ChemBioChem · doi:10.1002/cbic.200500030 · Cited by 24 · see citing works
Sutherland, M. C., Rankin, J. A., & Kranz, R. G. (2016) · Biochemistry · doi:10.1021/acs.biochem.6b00427 · Cited by 19 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
AF2Complex predicts direct physical interactions in multimeric proteins with deep learning
Gao, M., Nakajima An, D., Parks, J. M., & Skolnick, J. (2022) · Nature Communications · doi:10.1038/s41467-022-29394-2 · Cited by 252 · see citing works
Cryo-EM of CcsBA reveals the basis for cytochrome c biogenesis and heme transport
Mendez, D. L., Lowder, E. P., Tillman, D. E., Sutherland, M. C., Collier, A. L., Rau, M., Fitzpatrick, J. A. J., & Kranz, R. G. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00935-y · Cited by 31 · see citing works
Self-citationStructures of the CcmABCD heme release complex at multiple states
Li, J., Zheng, W., Gu, M., Han, L., Luo, Y., Yu, K., Sun, M., Zong, Y., Ma, X., Liu, B., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34136-5 · Cited by 26 · see citing works
Self-citationA brief survey of the “cytochromome”
Paquete, C. M., Rusconi, G., Silva, A. V., Soares, R., & Louro, R. O. (2019) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2019.07.005 · Cited by 23 · see citing works
Structure-Function Analysis of the Bifunctional CcsBA Heme Exporter and Cytochrome c Synthetase
Sutherland, M. C., Tran, N. L., Tillman, D. E., Jarodsky, J. M., Yuan, J. X. ‐., & Kranz, R. G. (2018) · mBio · doi:10.1128/mbio.02134-18 · Cited by 22 · see citing works
Self-citationState-of-the-art web services for de novo protein structure prediction
Abriata, L. A., & Peraro, M. D. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa139 · Cited by 21 · see citing works
In vitro reconstitution reveals major differences between human and bacterial cytochrome c synthases
Sutherland, M. C., Mendez, D. L., Babbitt, S. E., Tillman, D. E., Melnikov, O., Tran, N. L., Prizant, N. T., Collier, A. L., & Kranz, R. G. (2021) · eLife · doi:10.7554/elife.64891 · Cited by 15 · see citing works
Self-citationEller, J., Hein, S., & Simon, J. (2019) · Biochimica et Biophysica Acta - Bioenergetics · doi:10.1016/j.bbabio.2018.10.002 · Cited by 7 · see citing works
Shevket, S. H., González, D., CARTWRIGHT, J. L., Kleanthous, C., Ferguson, S. J., Redfield, C., & Mavridou, D. A. I. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005024 · Cited by 10 · see citing works
Yeasmin, T., Carroll, S. C., Hawtof, D. J., & Sutherland, M. C. (2024) · Communications Biology · doi:10.1038/s42003-024-06688-3 · Cited by 8 · see citing works
Self-citationHird, K., Campeciño, J., & Hegg, E. (2025) · Applied and Environmental Microbiology · doi:10.1128/aem.00292-25 · Cited by 7 · see citing works
The OXA2a Insertase of Arabidopsis Is Required for Cytochrome c Maturation
Kolli, R., Engstler, C., Akbaş, Ş., Mower, J. P., Soll, J., & Carrie, C. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.01248 · Cited by 8 · see citing works
Structural basis of membrane machines that traffick and attach heme to cytochromes
Huynh, J. Q., Lowder, E. P., & Kranz, R. G. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105332 · Cited by 8 · see citing works
Self-citationMechanisms and Control of Heme Transport and Incorporation into Cytochrome c
Kranz, R. G., & Sutherland, M. C. (2025) · Annual Review of Microbiology · doi:10.1146/annurev-micro-050624-031631 · Cited by 6 · see citing works
Self-citationGrunow, A. L., Carroll, S. C., Kreiman, A. N., & Sutherland, M. C. (2023) · mBio · doi:10.1128/mbio.01509-23 · Cited by 6 · see citing works
Self-citationWang, W., Huang, S., Li, S., Li, X., Ling, Y., Wang, X., Zhang, S., Zhou, D., & Yin, W. (2024) · Nutrients · doi:10.3390/nu16162784 · Cited by 4 · see citing works
Assembly of Protein Complexes in and on the Membrane with Predicted Spatial Arrangement Constraints
Christoffer, C., Harini, K., Archit, G., & Kihara, D. (2024) · Journal of Molecular Biology · doi:10.1016/j.jmb.2024.168486 · Cited by 4 · see citing works
Recombinant Biogenesis and Analysis of Cytochrome c Species
Kreiman, A. N., Yeasmin, T., & Sutherland, M. C. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-4043-2_10 · Cited by 4 · see citing works
Self-citationKreiman, A. N., Garner, S. E., Carroll, S. C., & Sutherland, M. C. (2025) · mBio · doi:10.1128/mbio.03515-24 · Cited by 2 · see citing works
Self-citationPredicting direct physical interactions in multimeric proteins with deep learningPreprint
Gao, M., An, D. N., Parks, J. M., & Skolnick, J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.09.467949 · Cited by 2 · see citing works
Bioenergetics Theory and Components | Cytochrome c Assembly
Das, A., & Hamel, P. P. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819460-7.00219-x · Cited by 2 · see citing works
Structural Insights into Mechanisms Underlying Mitochondrial and Bacterial Cytochrome c Synthases
Childs, P. L., Lowder, E. P., Mendez, D. L., Babbitt, S. E., Martinie, A., Huynh, J. Q., & Kranz, R. G. (2024) · Biomolecules · doi:10.3390/biom14121483 · Cited by 1 · see citing works
Self-citationKreiman, A. N., Carroll, S. C., Varde, N. P., Garner, S. E., Price, D. R., & Sutherland, M. C. (2026) · Microbiology Spectrum · doi:10.1128/spectrum.03266-25
Self-citation
- Authors
- Sutherland, M. C., Jarodsky, J. M., Ovchinnikov, S., Baker, D., & Kranz, R. G.
- Affiliations
- Washington University in St. Louis (US)
- University of Washington (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Kranz, Robert G.
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 430
- Issue
- 8
- Pages
- 1065-1080
- ISSN
- 0022-2836 (ISSN-L)
- PMC
- PMC5889519
- OpenAlex
- W2793251203
- Cited by
- 23
- References
- 62
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 2 · 2019: 1 · 2018: 3
- FWCI
- 0.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (R01 GM47909, F32GM115020)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
- Keywords
- heme transport, cytochrome c biogenesis, CCMC, heme binding site, heme trafficking
- MeSH terms
- Bacterial Outer Membrane Proteins, Bacterial Proteins, Binding Sites, Cysteine, Escherichia coli, Heme, Hemeproteins, Membrane Proteins, Models, Molecular, Mutation, Protein Binding, Protein Transport, Escherichia coli Proteins, Cytochromes c, Multiprotein Complexes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
