Electron Transfer Interactome of Cytochrome c
Publication Date
December 06, 2012
Journal
PLOS Computational Biology
Authors
Alexander N. Volkov & Nico A. J. Van Nuland
Volume
8
Issue
12
Pages
e1002807
DOI
https://dx.plos.org/10.1371/journal.pcbi.1002807
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1002807
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23236271
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3516563
Europe PMC
http://europepmc.org/abstract/MED/23236271
Web of Science
000312901500014
Scopus
84872012325
Mendeley
http://www.mendeley.com/research/electron-transfer-interactome-cytochrome-c
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Mendeley | Further Information

{"title"=>"Electron Transfer Interactome of Cytochrome c", "type"=>"journal", "authors"=>[{"first_name"=>"Alexander N.", "last_name"=>"Volkov", "scopus_author_id"=>"7402103452"}, {"first_name"=>"Nico A.J.", "last_name"=>"van Nuland", "scopus_author_id"=>"6603837007"}], "year"=>2012, "source"=>"PLoS Computational Biology", "identifiers"=>{"sgr"=>"84872012325", "doi"=>"10.1371/journal.pcbi.1002807", "pui"=>"368067295", "pmid"=>"23236271", "scopus"=>"2-s2.0-84872012325", "issn"=>"1553734X", "isbn"=>"1553-7358"}, "id"=>"bb9b8d19-245d-3fd4-9a63-1dadb3e6966f", "abstract"=>"Lying at the heart of many vital cellular processes such as photosynthesis and respiration, biological electron transfer (ET) is mediated by transient interactions among proteins that recognize multiple binding partners. Accurate description of the ET complexes - necessary for a comprehensive understanding of the cellular signaling and metabolism - is compounded by their short lifetimes and pronounced binding promiscuity. Here, we used a computational approach relying solely on the steric properties of the individual proteins to predict the ET properties of protein complexes constituting the functional interactome of the eukaryotic cytochrome c (Cc). Cc is a small, soluble, highly-conserved electron carrier protein that coordinates the electron flow among different redox partners. In eukaryotes, Cc is a key component of the mitochondrial respiratory chain, where it shuttles electrons between its reductase and oxidase, and an essential electron donor or acceptor in a number of other redox systems. Starting from the structures of individual proteins, we performed extensive conformational sampling of the ET-competent binding geometries, which allowed mapping out functional epitopes in the Cc complexes, estimating the upper limit of the ET rate in a given system, assessing ET properties of different binding stoichiometries, and gauging the effect of domain mobility on the intermolecular ET. The resulting picture of the Cc interactome 1) reveals that most ET-competent binding geometries are located in electrostatically favorable regions, 2) indicates that the ET can take place from more than one protein-protein orientation, and 3) suggests that protein dynamics within redox complexes, and not the electron tunneling event itself, is the rate-limiting step in the intermolecular ET. Further, we show that the functional epitope size correlates with the extent of dynamics in the Cc complexes and thus can be used as a diagnostic tool for protein mobility.", "link"=>"http://www.mendeley.com/research/electron-transfer-interactome-cytochrome-c", "reader_count"=>34, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>14, "Chemistry"=>7, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Chemistry"=>{"Chemistry"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>1, "Japan"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/530652"], "description"=>"<p>(A) Combined binding interface of ferric yeast Cc (PDB entry 2YCC) <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Berghuis1\" target=\"_blank\">[73]</a> in complexes with CcP <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Worrall1\" target=\"_blank\">[74]</a>, Cb<sub>5 </sub><a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Volkov4\" target=\"_blank\">[56]</a> and CCO <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Sakamoto1\" target=\"_blank\">[67]</a> as determined by solution NMR spectroscopy. Residues experiencing binding effects in any of the three, two of the three, and all three complexes are colored light blue, green, and dark blue, respectively. The heme group is indicated by the white rectangle. Several lysine residues affected by the binding are labeled. (B) Absolute counts of Cc CMs with k<sub>ET</sub>>10<sup>6</sup> s<sup>−1</sup> in the ET complexes studied in this work.</p>", "links"=>[], "tags"=>["binding", "interface", "et", "properties", "redox"], "article_id"=>201153, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cc_binding_interface_and_ET_properties_in_redox_complexes_/201153", "title"=>"Cc binding interface and ET properties in redox complexes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:19:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/530143"], "description"=>"<p>(A) Crystal structure of bovine CCO <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Tsukihara1\" target=\"_blank\">[70]</a>. The intramitochondrial region of the CCO asymmetric unit modeled in this work is shown as a molecular surface. Subunit II is colored yellow, with its dinuclear CuA centre and W104 residue in red. The other CCO redox cofactors are shown in orange. Horizontal lines indicate approximate location of the mitochondrial membrane. (B) The molecular surface of the modeled CCO region coloured by the electrostatic potential (see the scale bar). Protein orientation is the same as in (A). (C) Distribution of Cc CMs around the subunit II colored by the heme-W104 distances and the corresponding ET rates (see the scale bar). Protein orientation is the same as in (A). (D) Distributions of the intermolecular distances (left) and ET rates (right) for heme-W104 (red) and heme-CuA (black). The solid vertical line indicates the fastest experimentally measured intermolecular ET rate in the Cc-CCO system <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Geren1\" target=\"_blank\">[71]</a>. The inset shows the distance distribution in the ternary complex (see text).</p>", "links"=>[], "tags"=>["Computational biology", "biophysics", "Biochemistry"], "article_id"=>200643, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cc_CCO_/200643", "title"=>"Cc-CCO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:10:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/530538"], "description"=>"<p>(A) The hypothetical structural model of Salemme <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Salemme1\" target=\"_blank\">[5]</a>. Cc and Cb<sub>5</sub> are in yellow and blue, respectively, with heme groups shown as red sticks. (B) The molecular surface of Cb<sub>5</sub> colored by the electrostatic potential (see the scale bar). Protein orientation is the same as in (A). (C), (D) Distribution of Cc CMs around Cb<sub>5</sub> in the binary (C) and ternary (D) complexes colored by the heme-heme distances or the corresponding ET rates (see the scale bar). Protein orientation is the same as in (A). Cc in the Salemme model is shown as yellow cartoon (C) or molecular surface (D). See <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807.s020\" target=\"_blank\">Videos S5</a> and <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807.s021\" target=\"_blank\">S6</a> for an expanded view of (C) and (D), respectively. (E) Distributions of the intermolecular heme-heme distances (top) and ET rates (bottom). Red and black traces are the distributions for the binary and ternary complexes, respectively. Solid vertical lines indicate the heme-heme distance (top) and the corresponding ET rate (bottom) in the hypothetical model of Salemme <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Salemme1\" target=\"_blank\">[5]</a>. The dashed line denotes the largest experimentally measured ET rate in the Cc-Cb<sub>5</sub> complex <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Ren1\" target=\"_blank\">[16]</a>.</p>", "links"=>[], "tags"=>["Computational biology", "biophysics", "Biochemistry"], "article_id"=>201033, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g006", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cc_Cb_5_/201033", "title"=>"Cc-Cb<sub>5</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:17:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/530726"], "description"=>"a<p>Shortest separation between redox cofactors;</p>b<p>the values averaged over 10% of the most ET-active protein orientations with k<sub>ET</sub>>10<sup>6</sup> s<sup>−1</sup> are given in parentheses;</p>c<p>number of Cc CMS with k<sub>ET</sub>>10<sup>6</sup> s<sup>−1</sup>;</p>d<p>experimentally measured (pseudo)first order intermolecular electron transfer rate constant (reference given in parentheses);</p>e<p>the range of values reflects the uncertainty in the reorganization energy, λ (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807.s013\" target=\"_blank\">Text S2</a>);</p>f<p>the average and the standard deviation calculated over all members of the simulated ensemble.</p>", "links"=>[], "tags"=>["properties", "cc", "complexes", "modeled"], "article_id"=>201228, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.t001", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ET_properties_of_the_Cc_complexes_modeled_in_this_work_/201228", "title"=>"ET properties of the Cc complexes modeled in this work.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-06 00:20:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/529961"], "description"=>"<p>(A) Crystal structure of the complex <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Pelletier1\" target=\"_blank\">[37]</a>. Cc and CcP are in yellow and blue, respectively; heme groups and CcP residue W191 are shown as red sticks. (B) The molecular surface of CcP colored by the electrostatic potential (see the scale bar) calculated with APBS <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Baker1\" target=\"_blank\">[68]</a>. Low-affinity binding site is located around CcP residue D148, indicated by the arrow. Protein orientation is the same as in (A). (C), (E) Distributions of Cc centers of mass (CM) around CcP colored by the heme-W191 (C) or heme-heme (E) distances and the corresponding ET rates (see the scale bar). The left view is in the same orientation as in (A). The right view is obtained by rotation around the horizontal axis as indicated. Cc in the crystallographic orientation is shown as magenta cartoon. See Supplementary <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807.s016\" target=\"_blank\">Videos S1</a> and <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807.s017\" target=\"_blank\">S2</a> for an expanded view of (C) and (E), respectively. (D), (F) Distributions of the intermolecular heme-W191 (D) or heme-heme (F) distances (top) and the corresponding ET rates (bottom). Red and black traces are the distributions for the binary and ternary complexes, respectively. Solid vertical lines indicate the heme-W191 (D) or heme-heme (F) distance in the X-ray structure of the complex (top) and the corresponding ET rates (bottom). Dashed lines denote the largest experimentally measured ET rate in the Cc-CcP complex <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Wang1\" target=\"_blank\">[41]</a>. All molecular graphics were prepared with PyMOL <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-DeLano1\" target=\"_blank\">[69]</a>.</p>", "links"=>[], "tags"=>["Computational biology", "biophysics", "Biochemistry"], "article_id"=>200462, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cc_CcP_/200462", "title"=>"Cc-CcP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:07:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/530368"], "description"=>"<p>(A) Crystal structure of yeast Fcb<sub>2 </sub><a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Cunane1\" target=\"_blank\">[51]</a>. Two of the four Cb<sub>5</sub> heme domains (yellow), not observed in the crystal structure, were modeled in. The heme groups and FMN co-factors are colored red. The dimer modeled in this work is shown as a molecular surface. (B) Simulated ensemble of Fcb<sub>2</sub> domain-domain orientations with residues 99–100 as a mobile linker. The green mesh is a reweighted atomic probability density map <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002807#pcbi.1002807-Schwieters2\" target=\"_blank\">[72]</a>, plotted at a threshold of 10% maximum, for the overall distribution of the Cb<sub>5</sub> domains among 100 generated structures. Two representative, low-energy solutions are shown in cyan and dark blue, with heme groups as red sticks. The crystallographic dimer is colored as in (A). (C)–(D) Distribution of Cc CMs around the Cb<sub>5</sub> domain in (C) the crystallographic orientation or (D) a modeled domain-domain conformation (cyan structure in (B)), colored by the heme-heme distances and the corresponding ET rates (see the scale bar). (E) Distributions of the intermolecular heme-heme distances (left) and ET rates (right) for the crystallographic (red) and the simulated domain-domain orientations (black). Black open and filled symbols refer to the simulated ensemble members shown in (B) in cyan and dark blue, respectively.</p>", "links"=>[], "tags"=>["Computational biology", "biophysics", "Biochemistry"], "article_id"=>200861, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cc_Fcb_2_/200861", "title"=>"Cc-Fcb<sub>2</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:14:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/529641"], "description"=>"<p>(A) Definition of the search space in the spherical coordinates. Proteins' CMs are shown as grey spheres, one of which is at the origin of the coordinate system. The moving protein (typically Cc) possesses three translational (θ, φ, <i>r</i>) and three rotational (χ, ψ, ξ) degrees of freedom. For the definition of the rotational axes see text. (B, C) Conformational search in the reduced rotational space. (B) Cc in the starting structure (black circles) is rotated to obtain the shortest separation between the ET cofactors (arrows). This ensures the frontal orientation of the Cc heme during subsequent θ and φ rotations (grey circle). (C) The reduced rotational space −45°≤χ, ψ≤45° traced by a point on the surface of a sphere (bold shape). Location of the other rotation axis, ξ, is indicated.</p>", "links"=>[], "tags"=>["conformational"], "article_id"=>200144, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Illustration_of_the_conformational_search_used_in_this_work_/200144", "title"=>"Illustration of the conformational search used in this work.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:02:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/529750"], "description"=>"<p>(A) Distribution of the heme-heme distances in the simulation runs with the full vdW potential and side-chain optimization (black); full vdW potential without side-chain optimization (vdW cut-off values of 300 kcal/mol and 10 kcal/mol; red and orange, respectively); and reduced vdW term, set to zero for all atoms extending beyond C<sub>β</sub> (vdW cut-off values 300 kcal/mol and 10 kcal/mol; blue and green, respectively). In these runs, only translational degrees of freedom of Cc were simulated. (B) Correlation plots of heme-heme distance occurrences in the side-chain optimization run (horizontal axis) and the other control runs (vertical axis), color-coded as in (A). Pearson correlation coefficients are indicated in the plots. (C) Distribution of the heme-heme distances in the runs with the reduced vdW term (vdW cut-off 10 kcal/mol, green dataset in A) and a given rotational increment (δχ = δψ = δξ, 0°≤χ, ψ<360°, 0°≤ξ<180°). For the composite run, δχ = δψ = 5°, δξ = 15°; −45°≤χ, ψ≤45°, 0°≤ξ<360°. (D) Number of rotamers for each Cc CM, the total number of structures sampled per run, and the total run time (for 1 CPU).</p>", "links"=>[], "tags"=>["sampling"], "article_id"=>200250, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002807.g002", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conformational_sampling_in_the_Cc_Cb_5_complex_/200250", "title"=>"Conformational sampling in the Cc-Cb<sub>5</sub> complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-06 00:04:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/286445", "https://ndownloader.figshare.com/files/286456", "https://ndownloader.figshare.com/files/286501", "https://ndownloader.figshare.com/files/286532", "https://ndownloader.figshare.com/files/286584", "https://ndownloader.figshare.com/files/286616", "https://ndownloader.figshare.com/files/286666", "https://ndownloader.figshare.com/files/286703", "https://ndownloader.figshare.com/files/286736", "https://ndownloader.figshare.com/files/286785", "https://ndownloader.figshare.com/files/286830", "https://ndownloader.figshare.com/files/286876", "https://ndownloader.figshare.com/files/286931", "https://ndownloader.figshare.com/files/286965", "https://ndownloader.figshare.com/files/287011", "https://ndownloader.figshare.com/files/287052", "https://ndownloader.figshare.com/files/287263", "https://ndownloader.figshare.com/files/287353", "https://ndownloader.figshare.com/files/287441", "https://ndownloader.figshare.com/files/287539", "https://ndownloader.figshare.com/files/287586", "https://ndownloader.figshare.com/files/287638", "https://ndownloader.figshare.com/files/287821"], "description"=>"<div><p>Lying at the heart of many vital cellular processes such as photosynthesis and respiration, biological electron transfer (ET) is mediated by transient interactions among proteins that recognize multiple binding partners. Accurate description of the ET complexes – necessary for a comprehensive understanding of the cellular signaling and metabolism – is compounded by their short lifetimes and pronounced binding promiscuity. Here, we used a computational approach relying solely on the steric properties of the individual proteins to predict the ET properties of protein complexes constituting the functional interactome of the eukaryotic cytochrome <em>c</em> (Cc). Cc is a small, soluble, highly-conserved electron carrier protein that coordinates the electron flow among different redox partners. In eukaryotes, Cc is a key component of the mitochondrial respiratory chain, where it shuttles electrons between its reductase and oxidase, and an essential electron donor or acceptor in a number of other redox systems. Starting from the structures of individual proteins, we performed extensive conformational sampling of the ET-competent binding geometries, which allowed mapping out functional epitopes in the Cc complexes, estimating the upper limit of the ET rate in a given system, assessing ET properties of different binding stoichiometries, and gauging the effect of domain mobility on the intermolecular ET. The resulting picture of the Cc interactome 1) reveals that most ET-competent binding geometries are located in electrostatically favorable regions, 2) indicates that the ET can take place from more than one protein-protein orientation, and 3) suggests that protein dynamics within redox complexes, and not the electron tunneling event itself, is the rate-limiting step in the intermolecular ET. Further, we show that the functional epitope size correlates with the extent of dynamics in the Cc complexes and thus can be used as a diagnostic tool for protein mobility.</p> </div>", "links"=>[], "tags"=>["electron", "interactome", "cytochrome"], "article_id"=>116474, "categories"=>["Biological Sciences", "Biochemistry", "Biophysics"], "users"=>["Alexander N. Volkov", "Nico A. J. van Nuland"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002807.s001", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s002", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s003", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s004", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s005", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s006", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s007", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s008", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s009", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s010", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s011", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s012", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s013", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s014", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s015", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s016", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s017", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s018", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s019", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s020", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s021", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s022", "https://dx.doi.org/10.1371/journal.pcbi.1002807.s023"], "stats"=>{"downloads"=>42, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Electron_Transfer_Interactome_of_Cytochrome_c__/116474", "title"=>"Electron Transfer Interactome of Cytochrome <em>c</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-12-06 01:47:54"}

PMC Usage Stats | Further Information

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Relative Metric

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