Examination of Abiotic Cofactor Assembly in Photosynthetic Biomimetics – Site-Specific Stereoselectivity in the Conjugation of a Ruthenium(II) Tris(Bipyridine) Photosensitizer to a Multi-Heme Protein

Ponomarenko, Nina S.; Kokhan, Oleksandr; Pokkuluri, Phani R.; Mulfort, Karen L.; Tiede, David M.

doi:10.1007/s11120-019-00697-8

Title: Examination of Abiotic Cofactor Assembly in Photosynthetic Biomimetics – Site-Specific Stereoselectivity in the Conjugation of a Ruthenium(II) Tris(Bipyridine) Photosensitizer to a Multi-Heme Protein

Journal Article · 09 January 2020 · Photosynthesis Research

DOI: https://doi.org/10.1007/s11120-019-00697-8 · OSTI ID:1657512

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Argonne National Lab. (ANL), Argonne, IL (United States)
James Madison Univ., Harrisonburg, VA (United States)

To understand design principles for assembling photosynthetic biohybrids that incorporate precisely-controlled sites for electron injection into redox enzyme cofactor arrays, we investigated the influence of chirality in assembly of the photosensitizer ruthenium(II)bis(2,2'-bipyridine)(4-bromomethyl-4'-methyl-2,2'-bipyridine), Ru(bpy)₂(Br-bpy), when covalently conjugated to cysteine residues introduced by site-directed mutagenesis in the triheme periplasmic cytochrome A (PpcA) as a model biohybrid system. For two investigated conjugates that show ultrafast electron transfer, A23C-Ru and K29C-Ru, analysis by circular dichroism spectroscopy, CD, demonstrated site-specific chiral discrimination as a factor emerging from the close association between [Ru(bpy)₃]²⁺ and heme cofactors. CD analysis showed the A23C-Ru and K29C-Ru conjugates to have distinct, but opposite, stereoselectivity for the Λ and Δ-Ru(bpy)₂(Br-bpy) enantiomers, with enantiomeric excesses of 33.1% and 65.6%, respectively. In contrast, Ru(bpy)₂(Br-bpy) conjugation to a protein site with high flexibility, represented by the E39C-Ru construct, exhibited a nearly negligible chiral selectivity, measured by an enantiomeric excess of 4.2% for the Λ enantiomer. Molecular dynamics simulations showed that site-specific stereoselectivity reflects steric constraints at the conjugating sites and that a high degree of chiral selectivity correlates to reduced structural disorder for [Ru(bpy)₃]²⁺ in the linked assembly. This work identifies chiral discrimination as means to achieve site-specific, precise geometric positioning of introduced photosensitizers relative to the heme cofactors in manner that mimics the tuning of cofactors in photosynthesis.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1657512

Journal Information:: Photosynthesis Research, Journal Name: Photosynthesis Research Journal Issue: 2 Vol. 143; ISSN 0166-8595

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (114)

Photobiocatalysis: Activating Redox Enzymes by Direct or Indirect Transfer of Photoinduced Electrons Lee, Sahng Ha; Choi, Da Som; Kuk, Su Keun Angewandte Chemie International Edition, Vol. 57, Issue 27 https://doi.org/10.1002/anie.201710070	journal	May 2018
Theoretical CD studies of polypeptide helices: Examination of important electronic and geometric factors Manning, Mark C.; Woody, Robert W. Biopolymers, Vol. 31, Issue 5 https://doi.org/10.1002/bip.360310511	journal	April 1991
Synthesis, Characterization and Luminescence Properties of Dipyridin-2-ylamine Ligands and Their Bis(2,2′-bipyridyl)ruthenium(II) Complexes and Labelling Studies of Papain from Carica papaya: Luminescent Polypyridyl Ruthenium(II) Complexes Haquette, Pierre; Jacques, Julien; Dagorne, Samuel European Journal of Inorganic Chemistry, Vol. 2010, Issue 32 https://doi.org/10.1002/ejic.201000585	journal	September 2010
Classical force field parameters for the heme prosthetic group of cytochrome c Autenrieth, Felix; Tajkhorshid, Emad; Baudry, Jerome Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20079	journal	October 2004
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
Ratio of ellipticities between 192 and 208 nm ( R ₁ ): An effective electronic circular dichroism parameter for characterization of the helical components of proteins and peptides Banerjee, Raja; Sheet, Tridip Proteins: Structure, Function, and Bioinformatics, Vol. 85, Issue 11 https://doi.org/10.1002/prot.25351	journal	August 2017
Side chain-backbone hydrogen bonding contributes to helix stability in peptides derived from an α-helical region of carboxypeptidase A Bruch, Martha D.; Dhingra, Madan M.; Gierasch, Lila M. Proteins: Structure, Function, and Genetics, Vol. 10, Issue 2 https://doi.org/10.1002/prot.340100206	journal	February 1991
Structure Analysis of Cytochrome c3 From Desulfovibrio vulgaris Hildenborough at 1·9 Å Resolution Matias, Pedro M.; Frazião, Carlos; Morais, José Journal of Molecular Biology, Vol. 234, Issue 3 https://doi.org/10.1006/jmbi.1993.1620	journal	December 1993
A versatile technique based on surface-enhanced Raman spectroscopy for label-free detection of amino acids and peptide formation in body fluids Wang, Xiaoqing; Liu, XiaoLong; Wang, XiaoTong Microchimica Acta, Vol. 189, Issue 2 https://doi.org/10.1007/s00604-022-05191-y	journal	February 2022
The effect of acidic pH on the adsorption and lytic activity of the peptides Polybia-MP1 and its histidine-containing analog in anionic lipid membrane: a biophysical study by molecular dynamics and spectroscopy Martins, Ingrid Bernardes Santana; Viegas, Taisa Giordano; dos Santos Alvares, Dayane Amino Acids, Vol. 53, Issue 5 https://doi.org/10.1007/s00726-021-02982-0	journal	April 2021
An introduction to methods for analyzing thiols and disulfides: Reactions, reagents, and practical considerations Hansen, Rosa E.; Winther, Jakob R. Analytical Biochemistry, Vol. 394, Issue 2 https://doi.org/10.1016/j.ab.2009.07.051	journal	November 2009
Ru(II)-diimine functionalized metalloproteins: From electron transfer studies to light-driven biocatalysis Lam, Quan; Kato, Mallory; Cheruzel, Lionel Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 5 https://doi.org/10.1016/j.bbabio.2015.09.004	journal	May 2016
How to study proteins by circular dichroism Kelly, Sharon M.; Jess, Thomas J.; Price, Nicholas C. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1751, Issue 2 https://doi.org/10.1016/j.bbapap.2005.06.005	journal	August 2005
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity Morgado, Leonor; Bruix, Marta; Pessanha, Miguel Biophysical Journal, Vol. 99, Issue 1 https://doi.org/10.1016/j.bpj.2010.04.017	journal	July 2010
Light-driven hydrogen production from Photosystem I-catalyst hybrids Utschig, Lisa M.; Soltau, Sarah R.; Tiede, David M. Current Opinion in Chemical Biology, Vol. 25 https://doi.org/10.1016/j.cbpa.2014.11.019	journal	April 2015
Ruthenium coordination compounds of biological and biomedical significance. DNA binding agents Brabec, Viktor; Kasparkova, Jana Coordination Chemistry Reviews, Vol. 376 https://doi.org/10.1016/j.ccr.2018.07.012	journal	December 2018
Enantiomeric discrimination of Ru-substrates by cytochrome P450cam Dmochowski, Ivan J.; Winkler, Jay R.; Gray*, Harry B. Journal of Inorganic Biochemistry, Vol. 81, Issue 3 https://doi.org/10.1016/s0162-0134(00)00111-2	journal	August 2000
Still a puzzle: why is haem covalently attached in c-type cytochromes? Barker, Paul D.; Ferguson, Stuart J. Structure, Vol. 7, Issue 12 https://doi.org/10.1016/s0969-2126(00)88334-3	journal	January 1999
Modular Homogeneous Chromophore–Catalyst Assemblies Mulfort, Karen L.; Utschig, Lisa M. Accounts of Chemical Research, Vol. 49, Issue 5 https://doi.org/10.1021/acs.accounts.5b00539	journal	April 2016
Optical activity of hemoproteins in the Soret region. Circular dichroism of the heme undecapeptide of cytochrome c in aqueous solution Blauer, Gideon; Sreerama, Narasimha; Woody, Robert W. Biochemistry, Vol. 32, Issue 26 https://doi.org/10.1021/bi00077a021	journal	July 1993
Family of Cytochrome c ₇ -Type Proteins from Geobacter sulfurreducens : Structure of One Cytochrome c ₇ at 1.45 Å Resolution ^† ^, ^‡ Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C. Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1021/bi0301439	journal	February 2004
Formation of thin polymeric films by electropolymerization. Reduction of metal complexes containing bromomethyl-substituted derivatives of 2,2'-bipyridine Gould, Sharon.; Strouse, Geoffrey F.; Meyer, Thomas J. Inorganic Chemistry, Vol. 30, Issue 14 https://doi.org/10.1021/ic00014a022	journal	July 1991
Preparation and Characterization of cis-.LAMBDA.-[Ru(bpy)2(py)(O)]2+ Hua, Xiao; Lappin, A. Graham Inorganic Chemistry, Vol. 34, Issue 4 https://doi.org/10.1021/ic00108a036	journal	February 1995
Origin of the heme Cotton effects in myoglobin and hemoglobin Woody, Robert W.; Hsu, Ming-Chu Journal of the American Chemical Society, Vol. 93, Issue 14 https://doi.org/10.1021/ja00743a036	journal	July 1971
Site-Dependent Stereoselective Binding of Ruthenium Aquobipyridine Complexes to Histidine Side Chains in Horse Heart Cytochrome c Luo, Jian; Wishart, James F.; Isied, Stephan S. Journal of the American Chemical Society, Vol. 120, Issue 49 https://doi.org/10.1021/ja9829261	journal	December 1998
Exploiting Chromophore–Protein Interactions through Linker Engineering To Tune Photoinduced Dynamics in a Biomimetic Light-Harvesting Platform Delor, Milan; Dai, Jing; Roberts, Trevor D. Journal of the American Chemical Society, Vol. 140, Issue 20 https://doi.org/10.1021/jacs.7b13598	journal	May 2018
Involvement of Propionate Side Chains of the Heme in Circular Dichroism of Myoglobin: Experimental and Theoretical Analyses Nagai, Masako; Kobayashi, Chika; Nagai, Yukifumi The Journal of Physical Chemistry B, Vol. 119, Issue 4 https://doi.org/10.1021/jp5086203	journal	January 2015
Internal Electric Field in Cytochrome C Explored by Visible Electronic Circular Dichroism Spectroscopy. Schweitzer-Stenner, Reinhard The Journal of Physical Chemistry B, Vol. 112, Issue 33 https://doi.org/10.1021/jp802495q	journal	August 2008
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Sensitivity of circular dichroism to protein tertiary structure class Manavalan, Parthasarathy; Johnson, W. Curtis Nature, Vol. 305, Issue 5937 https://doi.org/10.1038/305831a0	journal	October 1983
Natural engineering principles of electron tunnelling in biological oxidation–reduction Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi Nature, Vol. 402, Issue 6757 https://doi.org/10.1038/46972	journal	November 1999
Using circular dichroism spectra to estimate protein secondary structure Greenfield, Norma J Nature Protocols, Vol. 1, Issue 6, p. 2876-2890 https://doi.org/10.1038/nprot.2006.202	journal	January 2007
Semi-synthetic strategy King, Paul W. Nature Energy, Vol. 3, Issue 11 https://doi.org/10.1038/s41560-018-0274-1	journal	October 2018
Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis Kornienko, Nikolay; Zhang, Jenny Z.; Sakimoto, Kelsey K. Nature Nanotechnology, Vol. 13, Issue 10 https://doi.org/10.1038/s41565-018-0251-7	journal	October 2018
Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62 Itskanov, Samuel; Kuo, Katie M.; Gumbart, James C. Nature Structural & Molecular Biology, Vol. 28, Issue 2 https://doi.org/10.1038/s41594-020-00541-x	journal	January 2021
Circular and linear dichroism of proteins Bulheller, Benjamin M.; Rodger, Alison; Hirst, Jonathan D. Physical Chemistry Chemical Physics, Vol. 9, Issue 17 https://doi.org/10.1039/b615870f	journal	January 2007
Application of electronic circular dichroism in the study of supramolecular systems Pescitelli, Gennaro; Di Bari, Lorenzo; Berova, Nina Chem. Soc. Rev., Vol. 43, Issue 15 https://doi.org/10.1039/c4cs00104d	journal	January 2014
Redox- and pH-linked conformational changes in triheme cytochrome PpcA from Geobacter sulfurreducens Morgado, Leonor; Bruix, Marta; Pokkuluri, P. Raj Biochemical Journal, Vol. 474, Issue 2 https://doi.org/10.1042/bcj20160932	journal	January 2017
A reference database for circular dichroism spectroscopy covering fold and secondary structure space Lees, Jonathan G.; Miles, Andrew J.; Wien, Frank Bioinformatics, Vol. 22, Issue 16 https://doi.org/10.1093/bioinformatics/btl327	journal	June 2006
PCDDB: new developments at the Protein Circular Dichroism Data Bank Whitmore, Lee; Miles, Andrew John; Mavridis, Lazaros Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw796	journal	September 2016
Database of Absorption and Fluorescence Spectra of >300 Common Compounds for use in PhotochemCAD Taniguchi, Masahiko; Lindsey, Jonathan S. Photochemistry and Photobiology, Vol. 94, Issue 2 https://doi.org/10.1111/php.12860	journal	February 2018
Electron-Tunneling Pathways in Oroteins Beratan, David N.; Onuchic, José Nelson; Winkler, Jay R. Science, Vol. 258, Issue 5089, p. 1740-1741 https://doi.org/10.1126/science.1334572	journal	December 1992
Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid Brown, K. A.; Harris, D. F.; Wilker, M. B. Science, Vol. 352, Issue 6284 https://doi.org/10.1126/science.aaf2091	journal	April 2016
Escherichia coli genes required for cytochrome c maturation. Thöny-Meyer, L.; Fischer, F.; Künzler, P. Journal of Bacteriology, Vol. 177, Issue 15 https://doi.org/10.1128/jb.177.15.4321-4326.1995	journal	August 1995
Using spectroscopic tools to probe porphyrin deformation and porphyrin-protein interactions Schweitzer-Stenner, Reinhard Journal of Porphyrins and Phthalocyanines, Vol. 15, Issue 05n06 https://doi.org/10.1142/s1088424611003343	journal	May 2011
The Role of Heme Chirality in the Circular Dichroism of Heme Proteins Woody, Robert W.; Pescitelli, Gennaro Zeitschrift für Naturforschung A, Vol. 69, Issue 7 https://doi.org/10.5560/zna.2014-0004	journal	July 2014
Photobiocatalysis: Activating Redox Enzymes by Direct or Indirect Transfer of Photoinduced Electrons Lee, Sahng Ha; Choi, Da Som; Kuk, Su Keun Angewandte Chemie International Edition, Vol. 57, Issue 27 https://doi.org/10.1002/anie.201710070	journal	May 2018
Theoretical CD studies of polypeptide helices: Examination of important electronic and geometric factors Manning, Mark C.; Woody, Robert W. Biopolymers, Vol. 31, Issue 5 https://doi.org/10.1002/bip.360310511	journal	April 1991
Application of Electronic Circular Dichroism in Configurational and Conformational Analysis of Organic Compounds Berova, Nina; Di Bari, Lorenzo; Pescitelli, Gennaro ChemInform, Vol. 38, Issue 33 https://doi.org/10.1002/chin.200733279	journal	August 2007
Efficient Asymmetric Synthesis ofΔ- andΛ-Enantiomers of (Bipyridyl)ruthenium Complexes and Crystallographic Analysis ofΔ-Bis(2,2′-bipyridine)(2,2′-bipyridine-4,4′-dicarboxylato)ruthenium: Diastereoselective Homo- and Heterochiral Ion Pairing Revisited Caspar, Régis; Amouri, Hani; Gruselle, Michel European Journal of Inorganic Chemistry, Vol. 2003, Issue 16 https://doi.org/10.1002/ejic.200300437	journal	August 2003
Efficient Asymmetric Synthesis of Δ‐ and Λ‐Enantiomers of (Bipyridyl)ruthenium Complexes and Crystallographic Analysis of Δ‐Bis(2,2′‐bipyridine)(2,2′‐bipyridine‐4,4′‐dicarboxylato)ruthenium: Diastereoselective Homo‐ and Heterochiral Ion Pairing Revisited Caspar, Régis; Amouri, Hani; Gruselle, Michel European Journal of Inorganic Chemistry, Vol. 2003, Issue 3 https://doi.org/10.1002/ejic.200390071	journal	January 2003
Synthesis, Characterization and Luminescence Properties of Dipyridin-2-ylamine Ligands and Their Bis(2,2′-bipyridyl)ruthenium(II) Complexes and Labelling Studies of Papain from Carica papaya: Luminescent Polypyridyl Ruthenium(II) Complexes Haquette, Pierre; Jacques, Julien; Dagorne, Samuel European Journal of Inorganic Chemistry, Vol. 2010, Issue 32 https://doi.org/10.1002/ejic.201000585	journal	September 2010
Classical force field parameters for the heme prosthetic group of cytochrome c Autenrieth, Felix; Tajkhorshid, Emad; Baudry, Jerome Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20079	journal	October 2004
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
Distinct circular dichroism spectroscopic signatures of polyproline II and unordered secondary structures: Applications in secondary structure analyses: Polyproline II and Disordered CD Spectra Lopes, Jose L. S.; Miles, Andrew J.; Whitmore, Lee Protein Science, Vol. 23, Issue 12 https://doi.org/10.1002/pro.2558	journal	October 2014
Ratio of ellipticities between 192 and 208 nm ( R ₁ ): An effective electronic circular dichroism parameter for characterization of the helical components of proteins and peptides Banerjee, Raja; Sheet, Tridip Proteins: Structure, Function, and Bioinformatics, Vol. 85, Issue 11 https://doi.org/10.1002/prot.25351	journal	August 2017
Side chain-backbone hydrogen bonding contributes to helix stability in peptides derived from an α-helical region of carboxypeptidase A Bruch, Martha D.; Dhingra, Madan M.; Gierasch, Lila M. Proteins: Structure, Function, and Genetics, Vol. 10, Issue 2 https://doi.org/10.1002/prot.340100206	journal	February 1991
Structure Analysis of Cytochrome c3 From Desulfovibrio vulgaris Hildenborough at 1·9 Å Resolution Matias, Pedro M.; Frazião, Carlos; Morais, José Journal of Molecular Biology, Vol. 234, Issue 3 https://doi.org/10.1006/jmbi.1993.1620	journal	December 1993
A role of heme side-chains of human hemoglobin in its function revealed by circular dichroism and resonance Raman spectroscopy Nagai, Masako; Mizusawa, Naoki; Kitagawa, Teizo Biophysical Reviews, Vol. 10, Issue 2 https://doi.org/10.1007/s12551-017-0364-5	journal	December 2017
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
An introduction to methods for analyzing thiols and disulfides: Reactions, reagents, and practical considerations Hansen, Rosa E.; Winther, Jakob R. Analytical Biochemistry, Vol. 394, Issue 2 https://doi.org/10.1016/j.ab.2009.07.051	journal	November 2009
Ru(II)-diimine functionalized metalloproteins: From electron transfer studies to light-driven biocatalysis Lam, Quan; Kato, Mallory; Cheruzel, Lionel Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 5 https://doi.org/10.1016/j.bbabio.2015.09.004	journal	May 2016
How to study proteins by circular dichroism Kelly, Sharon M.; Jess, Thomas J.; Price, Nicholas C. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1751, Issue 2 https://doi.org/10.1016/j.bbapap.2005.06.005	journal	August 2005
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity Morgado, Leonor; Bruix, Marta; Pessanha, Miguel Biophysical Journal, Vol. 99, Issue 1 https://doi.org/10.1016/j.bpj.2010.04.017	journal	July 2010
Light-driven hydrogen production from Photosystem I-catalyst hybrids Utschig, Lisa M.; Soltau, Sarah R.; Tiede, David M. Current Opinion in Chemical Biology, Vol. 25 https://doi.org/10.1016/j.cbpa.2014.11.019	journal	April 2015
Biological applications of Ru(II) polypyridyl complexes Mital, Mariusz; Ziora, Zyta Coordination Chemistry Reviews, Vol. 375 https://doi.org/10.1016/j.ccr.2018.02.013	journal	November 2018
Ruthenium coordination compounds of biological and biomedical significance. DNA binding agents Brabec, Viktor; Kasparkova, Jana Coordination Chemistry Reviews, Vol. 376 https://doi.org/10.1016/j.ccr.2018.07.012	journal	December 2018
Orientation of the axial ligands and magnetic properties of the hemes in the triheme ferricytochrome PpcA from G. sulfurreducens determined by paramagnetic NMR Morgado, Leonor; Saraiva, Ivo H.; Louro, Ricardo O. FEBS Letters, Vol. 584, Issue 15 https://doi.org/10.1016/j.febslet.2010.06.043	journal	July 2010
Production and preliminary characterization of a recombinant triheme cytochrome c7 from Geobacter sulfurreducens in Escherichia coli Londer, Yuri Y.; Pokkuluri, P. Raj; Tiede, David M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1554, Issue 3 https://doi.org/10.1016/s0005-2728(02)00244-x	journal	July 2002
Enantiomeric discrimination of Ru-substrates by cytochrome P450cam Dmochowski, Ivan J.; Winkler, Jay R.; Gray*, Harry B. Journal of Inorganic Biochemistry, Vol. 81, Issue 3 https://doi.org/10.1016/s0162-0134(00)00111-2	journal	August 2000
Still a puzzle: why is haem covalently attached in c-type cytochromes? Barker, Paul D.; Ferguson, Stuart J. Structure, Vol. 7, Issue 12 https://doi.org/10.1016/s0969-2126(00)88334-3	journal	January 1999
Modular Homogeneous Chromophore–Catalyst Assemblies Mulfort, Karen L.; Utschig, Lisa M. Accounts of Chemical Research, Vol. 49, Issue 5 https://doi.org/10.1021/acs.accounts.5b00539	journal	April 2016
Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens Ponomarenko, Nina; Niklas, Jens; Pokkuluri, P. Raj Biochemistry, Vol. 57, Issue 11 https://doi.org/10.1021/acs.biochem.7b00917	journal	January 2018
Optical activity of hemoproteins in the Soret region. Circular dichroism of the heme undecapeptide of cytochrome c in aqueous solution Blauer, Gideon; Sreerama, Narasimha; Woody, Robert W. Biochemistry, Vol. 32, Issue 26 https://doi.org/10.1021/bi00077a021	journal	July 1993
Family of Cytochrome c ₇ -Type Proteins from Geobacter sulfurreducens : Structure of One Cytochrome c ₇ at 1.45 Å Resolution ^† ^, ^‡ Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C. Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1021/bi0301439	journal	February 2004
Formation of thin polymeric films by electropolymerization. Reduction of metal complexes containing bromomethyl-substituted derivatives of 2,2'-bipyridine Gould, Sharon.; Strouse, Geoffrey F.; Meyer, Thomas J. Inorganic Chemistry, Vol. 30, Issue 14 https://doi.org/10.1021/ic00014a022	journal	July 1991
Preparation and Characterization of cis-.LAMBDA.-[Ru(bpy)2(py)(O)]2+ Hua, Xiao; Lappin, A. Graham Inorganic Chemistry, Vol. 34, Issue 4 https://doi.org/10.1021/ic00108a036	journal	February 1995
“Chiral-at-Metal” Octahedral Ruthenium(II) Complexes with Achiral Ligands: A New Type of Enantioselective Catalyst Chavarot, Murielle; Ménage, Stéphane; Hamelin, Olivier Inorganic Chemistry, Vol. 42, Issue 16 https://doi.org/10.1021/ic0341338	journal	August 2003
Absorption, Circular Dichroism, and Luminescence Spectroscopy of Electrogenerated Δ-[Ru(bipy) ₃ ] ^+/0/ ^- and Δ-[Os(bipy) ₃ ] ^+/0/ ^- (bipy = 2,2‘-Bipyridine) Noble, Brian; Peacock, Robert D. Inorganic Chemistry, Vol. 35, Issue 6 https://doi.org/10.1021/ic951096e	journal	January 1996
Origin of the heme Cotton effects in myoglobin and hemoglobin Woody, Robert W.; Hsu, Ming-Chu Journal of the American Chemical Society, Vol. 93, Issue 14 https://doi.org/10.1021/ja00743a036	journal	July 1971
Site-Dependent Stereoselective Binding of Ruthenium Aquobipyridine Complexes to Histidine Side Chains in Horse Heart Cytochrome c Luo, Jian; Wishart, James F.; Isied, Stephan S. Journal of the American Chemical Society, Vol. 120, Issue 49 https://doi.org/10.1021/ja9829261	journal	December 1998
Carbon Dots as Versatile Photosensitizers for Solar-Driven Catalysis with Redox Enzymes Hutton, Georgina A. M.; Reuillard, Bertrand; Martindale, Benjamin C. M. Journal of the American Chemical Society, Vol. 138, Issue 51 https://doi.org/10.1021/jacs.6b10146	journal	December 2016
Exploiting Chromophore–Protein Interactions through Linker Engineering To Tune Photoinduced Dynamics in a Biomimetic Light-Harvesting Platform Delor, Milan; Dai, Jing; Roberts, Trevor D. Journal of the American Chemical Society, Vol. 140, Issue 20 https://doi.org/10.1021/jacs.7b13598	journal	May 2018
Ultrafast Light-Driven Electron Transfer in a Ru(II)tris(bipyridine)-Labeled Multiheme Cytochrome van Wonderen, Jessica H.; Hall, Christopher R.; Jiang, Xiuyun Journal of the American Chemical Society, Vol. 141, Issue 38 https://doi.org/10.1021/jacs.9b06858	journal	August 2019
Involvement of Propionate Side Chains of the Heme in Circular Dichroism of Myoglobin: Experimental and Theoretical Analyses Nagai, Masako; Kobayashi, Chika; Nagai, Yukifumi The Journal of Physical Chemistry B, Vol. 119, Issue 4 https://doi.org/10.1021/jp5086203	journal	January 2015
Bidirectional Photoinduced Electron Transfer in Ruthenium(II)-Tris-bipyridyl-Modified PpcA, a Multi-heme c -Type Cytochrome from Geobacter sulfurreducens Kokhan, Oleksandr; Ponomarenko, Nina S.; Pokkuluri, P. Raj The Journal of Physical Chemistry B, Vol. 119, Issue 24 https://doi.org/10.1021/jp511558f	journal	December 2014
Internal Electric Field in Cytochrome C Explored by Visible Electronic Circular Dichroism Spectroscopy. Schweitzer-Stenner, Reinhard The Journal of Physical Chemistry B, Vol. 112, Issue 33 https://doi.org/10.1021/jp802495q	journal	August 2008
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Sensitivity of circular dichroism to protein tertiary structure class Manavalan, Parthasarathy; Johnson, W. Curtis Nature, Vol. 305, Issue 5937 https://doi.org/10.1038/305831a0	journal	October 1983
Natural engineering principles of electron tunnelling in biological oxidation–reduction Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi Nature, Vol. 402, Issue 6757 https://doi.org/10.1038/46972	journal	November 1999
Using circular dichroism spectra to estimate protein secondary structure Greenfield, Norma J Nature Protocols, Vol. 1, Issue 6, p. 2876-2890 https://doi.org/10.1038/nprot.2006.202	journal	January 2007
Mechanism of pore opening in the calcium-activated chloride channel TMEM16A Lam, Andy K. M.; Dutzler, Raimund Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20788-8	journal	February 2021
Semi-synthetic strategy King, Paul W. Nature Energy, Vol. 3, Issue 11 https://doi.org/10.1038/s41560-018-0274-1	journal	October 2018
Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis Kornienko, Nikolay; Zhang, Jenny Z.; Sakimoto, Kelsey K. Nature Nanotechnology, Vol. 13, Issue 10 https://doi.org/10.1038/s41565-018-0251-7	journal	October 2018
Z-scheme solar water splitting via self-assembly of photosystem I-catalyst hybrids in thylakoid membranes Utschig, Lisa M.; Soltau, Sarah R.; Mulfort, Karen L. Chemical Science, Vol. 9, Issue 45 https://doi.org/10.1039/C8SC02841A	journal	January 2018
Structural and photophysical characterisation of coordination and optical isomers of mononuclear ruthenium(ii) polypyridyl 1,2,4-triazole complexesElectronic supplementary information (ESI) available: analytical and semipreparative HPLC chromatograms, CD and UV/vis spectra. See http://www.rsc.org/suppdata/dt/b3/b301961f/ Browne, Wesley R.; Hesek, Dusan; Gallagher, John F. Dalton Transactions, Issue 12 https://doi.org/10.1039/b301961f	journal	January 2003
Application of electronic circular dichroism in configurational and conformational analysis of organic compounds Berova, Nina; Bari, Lorenzo Di; Pescitelli, Gennaro Chemical Society Reviews, Vol. 36, Issue 6 https://doi.org/10.1039/b515476f	journal	January 2007
Circular and linear dichroism of proteins Bulheller, Benjamin M.; Rodger, Alison; Hirst, Jonathan D. Physical Chemistry Chemical Physics, Vol. 9, Issue 17 https://doi.org/10.1039/b615870f	journal	January 2007
Application of electronic circular dichroism in the study of supramolecular systems Pescitelli, Gennaro; Di Bari, Lorenzo; Berova, Nina Chem. Soc. Rev., Vol. 43, Issue 15 https://doi.org/10.1039/c4cs00104d	journal	January 2014
Redox- and pH-linked conformational changes in triheme cytochrome PpcA from Geobacter sulfurreducens Morgado, Leonor; Bruix, Marta; Pokkuluri, P. Raj Biochemical Journal, Vol. 474, Issue 2 https://doi.org/10.1042/bcj20160932	journal	January 2017
Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens Morgado, Leonor; Paixão, Vítor B.; Schiffer, Marianne Biochemical Journal, Vol. 441, Issue 1 https://doi.org/10.1042/bj20111103	journal	December 2011
A reference database for circular dichroism spectroscopy covering fold and secondary structure space Lees, Jonathan G.; Miles, Andrew J.; Wien, Frank Bioinformatics, Vol. 22, Issue 16 https://doi.org/10.1093/bioinformatics/btl327	journal	June 2006
PCDDB: new developments at the Protein Circular Dichroism Data Bank Whitmore, Lee; Miles, Andrew John; Mavridis, Lazaros Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw796	journal	September 2016
Database of Absorption and Fluorescence Spectra of >300 Common Compounds for use in PhotochemCAD Taniguchi, Masahiko; Lindsey, Jonathan S. Photochemistry and Photobiology, Vol. 94, Issue 2 https://doi.org/10.1111/php.12860	journal	February 2018
Electron-Tunneling Pathways in Oroteins Beratan, David N.; Onuchic, José Nelson; Winkler, Jay R. Science, Vol. 258, Issue 5089, p. 1740-1741 https://doi.org/10.1126/science.1334572	journal	December 1992
Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid Brown, K. A.; Harris, D. F.; Wilker, M. B. Science, Vol. 352, Issue 6284 https://doi.org/10.1126/science.aaf2091	journal	April 2016
Escherichia coli genes required for cytochrome c maturation. Thöny-Meyer, L.; Fischer, F.; Künzler, P. Journal of Bacteriology, Vol. 177, Issue 15 https://doi.org/10.1128/JB.177.15.4321-4326.1995	journal	August 1995
Using spectroscopic tools to probe porphyrin deformation and porphyrin-protein interactions Schweitzer-Stenner, Reinhard Journal of Porphyrins and Phthalocyanines, Vol. 15, Issue 05n06 https://doi.org/10.1142/s1088424611003343	journal	May 2011
Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis. Kornienko, Nikolay; Zhang, Jenny; Sakimoto, Kelsey K. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.38298	text	January 2018
Research data supporting "Carbon Dots as Versatile Photosensitizers for Solar-Driven Catalysis with Redox Enzymes" Hutton, Gma; Reuillard, B.; Martindale, Cm Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.6573	dataset	January 2016
Carbon Dots as Versatile Photosensitizers for Solar-Driven Catalysis with Redox Enzymes Hutton, Gam; Reuillard, Bertrand; Martindale, Benjamin Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.7975	text	January 2016
CHARMM: the biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Wiley-Blackwell https://doi.org/10.5167/uzh-19245	text	January 2009
The Role of Heme Chirality in the Circular Dichroism of Heme Proteins Woody, Robert W.; Pescitelli, Gennaro Zeitschrift für Naturforschung A, Vol. 69, Issue 7 https://doi.org/10.5560/zna.2014-0004	journal	July 2014

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