Lessons from combined experimental and theoretical examination of the FTIR and 2D-IR spectroelectrochemistry of the amide I region of cytochrome c

El Khoury, Youssef; Le Breton, Guillaume; Cunha, Ana. V.; Jansen, Thomas C.; van Wilderen, Luuk W.; Bredenbeck, Jens

doi:10.1063/5.0039969

Title: Lessons from combined experimental and theoretical examination of the FTIR and 2D-IR spectroelectrochemistry of the amide I region of cytochrome c

Journal Article · Mon Mar 29 00:00:00 EDT 2021 · Journal of Chemical Physics

DOI:https://doi.org/10.1063/5.0039969· OSTI ID:1787997

^[1];

^[2]; Cunha, Ana. V. ^[2];

^[2];

^[1];

^[1]

Johann-Wolfgang-Goethe-Universität, Frankfurt am Main (Germany). Institut für Biophysik
Univ. of Groningen (Netherlands). Zernike Inst. for Advanced Materials

Amide I difference spectroscopy is widely used to investigate protein function and structure changes. In this article, we show that the common approach of assigning features in amide I difference signals to distinct secondary structure elements in many cases may not be justified. Evidence comes from Fourier transform infrared (FTIR) and 2D-IR spectroelectrochemistry of the protein cytochrome c in the amide I range, in combination with computational spectroscopy based on molecular dynamics (MD) simulations. This combination reveals that each secondary structure unit, such as an alpha-helix or a beta-sheet, exhibits broad overlapping contributions, usually spanning a large part of the amide I region, which in the case of difference absorption experiments (such as in FTIR spectroelectrochemistry) may lead to intensity-compensating and even sign-changing contributions. We use cytochrome c as the test case, as this small electron-transferring redox-active protein contains different kinds of secondary structure units. Upon switching its redox-state, the protein exhibits a different charge distribution while largely retaining its structural scaffold. Our theoretical analysis suggests that the change in charge distribution contributes to the spectral changes and that structural changes are small. However, in order to confidently interpret FTIR amide I difference signals in cytochrome c and proteins in general, MD simulations in combination with additional experimental approaches such as isotope labeling, the insertion of infrared labels to selectively probe local structural elements will be required. In case these data are not available, a critical assessment of previous interpretations of protein amide I 1D- and 2D-IR difference spectroscopy data is warranted.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

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

Grant/Contract Number:: AC05-00OR22725; INST-161/722-1-FUGG

OSTI ID:: 1787997

Journal Information:: Journal of Chemical Physics, Vol. 154, Issue 12; ISSN 0021-9606

Publisher:: American Institute of Physics (AIP)Copyright Statement

Country of Publication:: United States

Language:: English

References (79)

Energy Transport in Peptide Helices: A Comparison between High- and Low-Energy Excitations Backus, Ellen H. G.; Nguyen, Phuong H.; Botan, Virgiliu The Journal of Physical Chemistry B, Vol. 112, Issue 30 https://doi.org/10.1021/jp711046e	journal	July 2008
Identifying Residual Structure in Intrinsically Disordered Systems: A 2D IR Spectroscopic Study of the GVGXPGVG Peptide Lessing, Joshua; Roy, Santanu; Reppert, Mike Journal of the American Chemical Society, Vol. 134, Issue 11 https://doi.org/10.1021/ja2114135	journal	March 2012
Vibrational dynamics and solvatochromism of the label SCN in various solvents and hemoglobin by time dependent IR and 2D-IR spectroscopy van Wilderen, Luuk J. G. W.; Kern-Michler, Daniela; Müller-Werkmeister, Henrike M. Phys. Chem. Chem. Phys., Vol. 16, Issue 36 https://doi.org/10.1039/c4cp01498g	journal	January 2014
Time-Resolved Fourier Transform Infrared Study on Photoadduct Formation and Secondary Structural Changes within the Phototropin LOV Domain Pfeifer, Anna; Majerus, Teresa; Zikihara, Kazunori Biophysical Journal, Vol. 96, Issue 4 https://doi.org/10.1016/j.bpj.2008.11.016	journal	February 2009
Infrared spectroscopy of proteins Barth, Andreas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 9 https://doi.org/10.1016/j.bbabio.2007.06.004	journal	September 2007
Solution Structure of Horse Heart Ferricytochrome c and Detection of Redox-Related Structural Changes by High-Resolution ¹ H NMR ^† ^, ^‡ Qi, Phoebe Xiurong; Beckman, Robert A.; Wand, A. Joshua Biochemistry, Vol. 35, Issue 38 https://doi.org/10.1021/bi961042w	journal	January 1996
Structural classification of the amide I sites of a β-hairpin with isotope label 2DIR spectroscopy Roy, Santanu; Jansen, Thomas L. C.; Knoester, Jasper Physical Chemistry Chemical Physics, Vol. 12, Issue 32 https://doi.org/10.1039/b925645h	journal	January 2010
Relaxation-Assisted Two-Dimensional Infrared (RA 2DIR) Method: Accessing Distances over 10 Å and Measuring Bond Connectivity Patterns Rubtsov, Igor V. Accounts of Chemical Research, Vol. 42, Issue 9 https://doi.org/10.1021/ar900008p	journal	May 2009
Following local light-induced structure changes and dynamics of the photoreceptor PYP with the thiocyanate IR label Blankenburg, Larissa; Schroeder, Lea; Habenstein, Florian Physical Chemistry Chemical Physics, Vol. 21, Issue 12 https://doi.org/10.1039/c8cp05399e	journal	January 2019
Redox-dependent changes in .beta.-extended chain and turn structures of cytochrome c in water solution determined by second derivative amide I infrared spectra Dong, Aichun; Huang, Ping; Caughey, Winslow S. Biochemistry, Vol. 31, Issue 1 https://doi.org/10.1021/bi00116a027	journal	January 1992
Ultrafast 2D-IR spectroelectrochemistry of flavin mononucleotide El Khoury, Youssef; Van Wilderen, Luuk J. G. W.; Bredenbeck, Jens The Journal of Chemical Physics, Vol. 142, Issue 21 https://doi.org/10.1063/1.4916916	journal	June 2015
Quantification of transition dipole strengths using 1D and 2D spectroscopy for the identification of molecular structures via exciton delocalization: Application to α-helices Grechko, Maksim; Zanni, Martin T. The Journal of Chemical Physics, Vol. 137, Issue 18 https://doi.org/10.1063/1.4764861	journal	November 2012
2DIR Spectroscopy of Human Amylin Fibrils Reflects Stable β-Sheet Structure Wang, Lu; Middleton, Chris T.; Singh, Sadanand Journal of the American Chemical Society, Vol. 133, Issue 40 https://doi.org/10.1021/ja204035k	journal	October 2011
Signatures of Nonequilibrium Solvation Dynamics on Multidimensional Spectra McRobbie, Porscha L.; Hanna, Gabriel; Shi, Qiang Accounts of Chemical Research, Vol. 42, Issue 9 https://doi.org/10.1021/ar800280s	journal	June 2009
OH-Stretching in Synthetic Hydrogen-Bonded Chains van der Vegte, C. P.; Knop, S.; Vöhringer, P. The Journal of Physical Chemistry B, Vol. 118, Issue 23 https://doi.org/10.1021/jp504267h	journal	May 2014
Site-Specific Spectroscopic Reporters of the Local Electric Field, Hydration, Structure, and Dynamics of Biomolecules Waegele, Matthias M.; Culik, Robert M.; Gai, Feng The Journal of Physical Chemistry Letters, Vol. 2, Issue 20 https://doi.org/10.1021/jz201161b	journal	September 2011
Quantitative IR spectrophotometry of peptide compounds in water (H2O) solutions. II. Amide absorption bands of polypeptides and fibrous proteins in ?-, ?-, and random coil conformations Venyaminov, S. Yu.; Kalnin, N. N. Biopolymers, Vol. 30, Issue 13-14 https://doi.org/10.1002/bip.360301310	journal	January 1990
Site-Specific Protein Dynamics Probed by Ultrafast Infrared Spectroscopy of a Noncanonical Amino Acid Hall, Christopher R.; Tolentino Collado, Jinnette; Iuliano, James N. The Journal of Physical Chemistry B, Vol. 123, Issue 45 https://doi.org/10.1021/acs.jpcb.9b09425	journal	October 2019
Cytochrome c: functions beyond respiration Ow, Yong-Ling P.; Green, Douglas R.; Hao, Zhenyue Nature Reviews Molecular Cell Biology, Vol. 9, Issue 7 https://doi.org/10.1038/nrm2434	journal	July 2008
Multiscale modeling of molecular structure and optical properties of complex supramolecular aggregates Bondarenko, Anna S.; Patmanidis, Ilias; Alessandri, Riccardo Chemical Science, Vol. 11, Issue 42 https://doi.org/10.1039/d0sc03110k	journal	January 2020
Comparison of redox and ligand binding behaviour of yeast and bovine cytochrome c oxidases using FTIR spectroscopy Maréchal, Amandine; Hartley, Andrew M.; Warelow, Thomas P. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 9 https://doi.org/10.1016/j.bbabio.2018.05.018	journal	September 2018
Coherent two-dimensional infrared spectroscopy: Quantitative analysis of protein secondary structure in solution Baiz, Carlos R.; Peng, Chunte Sam; Reppert, Mike E. The Analyst, Vol. 137, Issue 8 https://doi.org/10.1039/c2an16031e	journal	January 2012
Redox-dependent conformational changes in eukaryotic cytochromes revealed by paramagnetic NMR spectroscopy Volkov, Alexander N.; Vanwetswinkel, Sophie; Van de Water, Karen Journal of Biomolecular NMR, Vol. 52, Issue 3 https://doi.org/10.1007/s10858-012-9607-8	journal	February 2012
Two-dimensional IR spectroscopy and segmental 13C labeling reveals the domain structure of human D-crystallin amyloid fibrils Moran, S. D.; Woys, A. M.; Buchanan, L. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 9 https://doi.org/10.1073/pnas.1117704109	journal	February 2012
Temperature-Induced Collapse of Elastin-like Peptides Studied by 2DIR Spectroscopy Selig, Oleg; Cunha, Ana V.; van Eldijk, Mark B. The Journal of Physical Chemistry B, Vol. 122, Issue 34 https://doi.org/10.1021/acs.jpcb.8b05221	journal	August 2018
Computing infrared spectra of proteins using the exciton model Husseini, Fouad S.; Robinson, David; Hunt, Neil T. Journal of Computational Chemistry, Vol. 38, Issue 16 https://doi.org/10.1002/jcc.24674	journal	November 2016
Site-Specific 1D and 2D IR Spectroscopy to Characterize the Conformations and Dynamics of Protein Molecular Recognition Ramos, Sashary; Thielges, Megan C. The Journal of Physical Chemistry B, Vol. 123, Issue 17 https://doi.org/10.1021/acs.jpcb.9b00969	journal	March 2019
Observation of Ultrafast Coherence Transfer and Degenerate States with Polarization-Controlled Two-Dimensional Electronic Spectroscopy Sardjan, Andy S.; Westerman, Floris P.; Ogilvie, Jennifer P. The Journal of Physical Chemistry B, Vol. 124, Issue 42 https://doi.org/10.1021/acs.jpcb.0c08126	journal	September 2020
Concepts and Methods of 2D Infrared Spectroscopy Hamm, Peter; Zanni, Martin Cambridge University Press https://doi.org/10.1017/CBO9780511675935	book	January 2011
Application of two-dimensional infrared spectroscopy to benchmark models for the amide I band of proteins Bondarenko, Anna S.; Jansen, Thomas L. C. The Journal of Chemical Physics, Vol. 142, Issue 21 https://doi.org/10.1063/1.4919716	journal	June 2015
Light-Induced Infrared Difference Spectroscopy in the Investigation of Light Harvesting Complexes Mezzetti, Alberto Molecules, Vol. 20, Issue 7 https://doi.org/10.3390/molecules200712229	journal	July 2015
Assignment of Protoheme Resonance Raman Spectrum by Heme Labeling in Myoglobin Hu, Songzhou; Smith, Kevin M.; Spiro, Thomas G. Journal of the American Chemical Society, Vol. 118, Issue 50 https://doi.org/10.1021/ja962239e	journal	January 1996
Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution Shim, S. -H.; Gupta, R.; Ling, Y. L. Proceedings of the National Academy of Sciences, Vol. 106, Issue 16 https://doi.org/10.1073/pnas.0805957106	journal	April 2009
Picosecond conformational transition and equilibration of a cyclic peptide Bredenbeck, J.; Helbing, J.; Sieg, A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 11, p. 6452-6457 https://doi.org/10.1073/pnas.1036583100	journal	May 2003
A spectroelectrochemical cell for ultrafast two-dimensional infrared spectroscopy El Khoury, Youssef; Van Wilderen, Luuk J. G. W.; Vogt, Tim Review of Scientific Instruments, Vol. 86, Issue 8 https://doi.org/10.1063/1.4927533	journal	August 2015
Cyano-tryptophans as dual infrared and fluorescence spectroscopic labels to assess structural dynamics in proteins van Wilderen, L. J. G. W.; Brunst, H.; Gustmann, H. Physical Chemistry Chemical Physics, Vol. 20, Issue 30 https://doi.org/10.1039/c8cp00846a	journal	January 2018
Direct knock-on of desolvated ions governs strict ion selectivity in K+ channels Kopec, Wojciech; Köpfer, David A.; Vickery, Owen N. Nature Chemistry, Vol. 10, Issue 8 https://doi.org/10.1038/s41557-018-0105-9	journal	July 2018
Structure of rice ferricytochrome c at 2·0 Å resolution Ochi, Hiroshi; Hata, Yasuo; Tanaka, Nobuo Journal of Molecular Biology, Vol. 166, Issue 3 https://doi.org/10.1016/s0022-2836(83)80092-8	journal	May 1983
Structure and dynamics of membrane proteins as studied by infrared spectroscopy Arrondo, José Luis R.; Goñi, Félix M. Progress in Biophysics and Molecular Biology, Vol. 72, Issue 4 https://doi.org/10.1016/s0079-6107(99)00007-3	journal	November 1999
Vibrational Lifetime of the SCN Protein Label in H ₂ O and D ₂ O Reports Site-Specific Solvation and Structure Changes During PYP’s Photocycle Schmidt-Engler, Julian M.; Blankenburg, Larissa; Błasiak, Bartosz Analytical Chemistry, Vol. 92, Issue 1 https://doi.org/10.1021/acs.analchem.9b03997	journal	November 2019
Electrochemically induced conformational changes in cytochrome c monitored by Fourier transform infrared difference spectroscopy: Influence of temperature, pH, and electrode surfaces Schlereth, Daniela D.; Maentele, Werner Biochemistry, Vol. 32, Issue 4 https://doi.org/10.1021/bi00055a018	journal	February 1993
Amide I′−II′ 2D IR Spectroscopy Provides Enhanced Protein Secondary Structural Sensitivity DeFlores, Lauren P.; Ganim, Ziad; Nicodemus, Rebecca A. Journal of the American Chemical Society, Vol. 131, Issue 9 https://doi.org/10.1021/ja8094922	journal	February 2009
Tracking Fiber Formation in Human Islet Amyloid Polypeptide with Automated 2D-IR Spectroscopy Strasfeld, David B.; Ling, Yun L.; Shim, Sang-Hee Journal of the American Chemical Society, Vol. 130, Issue 21 https://doi.org/10.1021/ja801483n	journal	May 2008
Structure of the Amide I Band of Peptides Measured by Femtosecond Nonlinear-Infrared Spectroscopy Hamm, Peter; Lim, Manho; Hochstrasser, Robin M. The Journal of Physical Chemistry B, Vol. 102, Issue 31 https://doi.org/10.1021/jp9813286	journal	July 1998
High-resolution three-dimensional structure of horse heart cytochrome c Bushnell, Gordon W.; Louie, Gordon V.; Brayer, Gary D. Journal of Molecular Biology, Vol. 214, Issue 2 https://doi.org/10.1016/0022-2836(90)90200-6	journal	July 1990
Site-specific detection of protein secondary structure using 2D IR dihedral indexing: a proposed assembly mechanism of oligomeric hIAPP Maj, Michał; Lomont, Justin P.; Rich, Kacie L. Chemical Science, Vol. 9, Issue 2 https://doi.org/10.1039/c7sc03789a	journal	January 2018
Differentiation of β-Sheet-Forming Structures: Ab Initio-Based Simulations of IR Absorption and Vibrational CD for Model Peptide and Protein β-Sheets Kubelka, Jan; Keiderling, Timothy A. Journal of the American Chemical Society, Vol. 123, Issue 48 https://doi.org/10.1021/ja0116627	journal	December 2001
Recent advances in the electrochemistry and spectroelectrochemistry of membrane proteins Melin, Frederic; Hellwig, Petra Biological Chemistry, Vol. 394, Issue 5 https://doi.org/10.1515/hsz-2012-0344	journal	May 2013
Assessing Spectral Simulation Protocols for the Amide I Band of Proteins Cunha, Ana V.; Bondarenko, Anna S.; Jansen, Thomas L. C. Journal of Chemical Theory and Computation, Vol. 12, Issue 8 https://doi.org/10.1021/acs.jctc.6b00420	journal	July 2016
Complete assignment of cytochrome c resonance Raman spectra via enzymic reconstitution with isotopically labeled hemes Hu, Songzhou; Morris, Ian K.; Singh, Jai P. Journal of the American Chemical Society, Vol. 115, Issue 26 https://doi.org/10.1021/ja00079a028	journal	December 1993
Applications of 2D IR Spectroscopy to Peptides, Proteins, and Hydrogen-Bond Dynamics ^† Kim, Yung Sam; Hochstrasser, Robin M. The Journal of Physical Chemistry B, Vol. 113, Issue 24 https://doi.org/10.1021/jp8113978	journal	June 2009
Nitrate as a probe of cytochrome c surface: Crystallographic identification of crucial “hot spots” for protein–protein recognition De March, Matteo; Demitri, Nicola; De Zorzi, Rita Journal of Inorganic Biochemistry, Vol. 135 https://doi.org/10.1016/j.jinorgbio.2014.02.015	journal	June 2014
Instantaneous ion configurations in the K ⁺ ion channel selectivity filter revealed by 2D IR spectroscopy Kratochvil, Huong T.; Carr, Joshua K.; Matulef, Kimberly Science, Vol. 353, Issue 6303 https://doi.org/10.1126/science.aag1447	journal	September 2016
A relaxation-assisted 2D IR spectroscopy method Kurochkin, D. V.; Naraharisetty, S. R. G.; Rubtsov, I. V. Proceedings of the National Academy of Sciences, Vol. 104, Issue 36 https://doi.org/10.1073/pnas.0700560104	journal	June 2007
Redox-linked conformational changes in proteins detected by a combination of infrared spectroscopy and protein electrochemistry. Evaluation of the technique with cytochrome c Moss, David; Nabedryk, Eliane; Breton, Jacques European Journal of Biochemistry, Vol. 187, Issue 3 https://doi.org/10.1111/j.1432-1033.1990.tb15338.x	journal	February 1990
Functional Vibrational Spectroscopy of a Cytochrome c Monolayer: SEIDAS Probes the Interaction with Different Surface-Modified Electrodes Ataka, Kenichi; Heberle, Joachim Journal of the American Chemical Society, Vol. 126, Issue 30 https://doi.org/10.1021/ja048346n	journal	August 2004
Determinants of the Vinyl Stretching Frequency in Protoporphyrins. Implications for Cofactor-Protein Interactions in Heme Proteins Kalsbeck, William A.; Ghosh, Abhik; Pandey, Ravindra K. Journal of the American Chemical Society, Vol. 117, Issue 44 https://doi.org/10.1021/ja00149a019	journal	November 1995
Two-Step Structural Changes in Orange Carotenoid Protein Photoactivation Revealed by Time-Resolved Fourier Transform Infrared Spectroscopy Mezzetti, Alberto; Alexandre, Maxime; Thurotte, Adrien The Journal of Physical Chemistry B, Vol. 123, Issue 15 https://doi.org/10.1021/acs.jpcb.9b01242	journal	March 2019
Comparison of the solution and crystal structures of mitochondrial cytochrome c Williams, Glyn; Clayden, Nigel J.; Moore, Geoffrey R. Journal of Molecular Biology, Vol. 183, Issue 3 https://doi.org/10.1016/0022-2836(85)90013-0	journal	June 1985
Two-Dimensional Heterospectral Correlation Analysis of the Redox-Induced Conformational Transition in Cytochrome c Using Surface-Enhanced Raman and Infrared Absorption Spectroscopies on a Two-Layer Gold Surface Zou, Changji; Larisika, Melanie; Nagy, Gabor The Journal of Physical Chemistry B, Vol. 117, Issue 33 https://doi.org/10.1021/jp404573q	journal	August 2013
Redox infrared markers of the heme and axial ligands in microperoxidase: bases for the analysis of c-type cytochromes Marboutin, Laure; Boussac, Alain; Berthomieu, Catherine JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 7 https://doi.org/10.1007/s00775-006-0119-4	journal	June 2006
Transient 2D IR spectroscopy of ubiquitin unfolding dynamics Chung, H. S.; Ganim, Z.; Jones, K. C. Proceedings of the National Academy of Sciences, Vol. 104, Issue 36 https://doi.org/10.1073/pnas.0700959104	journal	June 2007
The Grateful Infrared: Sequential Protein Structural Changes Resolved by Infrared Difference Spectroscopy Kottke, Tilman; Lórenz-Fonfría, Víctor A.; Heberle, Joachim The Journal of Physical Chemistry B, Vol. 121, Issue 2 https://doi.org/10.1021/acs.jpcb.6b09222	journal	December 2016
Correction: Vibrational dynamics and solvatochromism of the label SCN in various solvents and hemoglobin by time dependent IR and 2D-IR spectroscopy van Wilderen, Luuk J. G. W.; Kern-Michler, Daniela; Müller-Werkmeister, Henrike M. Physical Chemistry Chemical Physics, Vol. 19, Issue 14 https://doi.org/10.1039/c7cp90063e	journal	January 2017
Redox-Dependent Changes in β-Sheet and Loop Structures of Cu,Zn Superoxide Dismutase in Solution Observed by Infrared Spectroscopy Dong, A. C.; Huang, P.; Caughey, W. S. Archives of Biochemistry and Biophysics, Vol. 320, Issue 1 https://doi.org/10.1006/abbi.1995.1342	journal	June 1995
ATR–FTIR Detection of Metal-Sensitive Structural Changes in the Light-Harvesting 1 Reaction Center Complex from the Thermophilic Purple Sulfur Bacterium Thermochromatium tepidum Li, Yong; Kimura, Yukihiro; Arikawa, Teruhisa Biochemistry, Vol. 52, Issue 50 https://doi.org/10.1021/bi401033y	journal	November 2013
Two-Dimensional Infrared Spectroscopy of Antiparallel β-Sheet Secondary Structure Demirdöven, Nurettin; Cheatum, Christopher M.; Chung, Hoi Sung Journal of the American Chemical Society, Vol. 126, Issue 25 https://doi.org/10.1021/ja049811j	journal	June 2004
Isotope-edited two-dimensional vibrational spectroscopy of trialanine in aqueous solution Woutersen, S.; Hamm, P. The Journal of Chemical Physics, Vol. 114, Issue 6 https://doi.org/10.1063/1.1336807	journal	February 2001
Transparent Window Vibrational Probes for the Characterization of Proteins With High Structural and Temporal Resolution Adhikary, Ramkrishna; Zimmermann, Jörg; Romesberg, Floyd E. Chemical Reviews, Vol. 117, Issue 3 https://doi.org/10.1021/acs.chemrev.6b00625	journal	January 2017
Replica-exchange molecular dynamics method for protein folding Sugita, Yuji; Okamoto, Yuko Chemical Physics Letters, Vol. 314, Issue 1-2 https://doi.org/10.1016/s0009-2614(99)01123-9	journal	November 1999
Studying Protein–Protein Binding through T-Jump Induced Dissociation: Transient 2D IR Spectroscopy of Insulin Dimer Zhang, Xin-Xing; Jones, Kevin C.; Fitzpatrick, Ann The Journal of Physical Chemistry B, Vol. 120, Issue 23 https://doi.org/10.1021/acs.jpcb.6b03246	journal	May 2016
Vibrational analysis of peptides, polypeptides, and proteins: Characteristic amide bands of -turns Bandekar, J.; Krimm, S. Proceedings of the National Academy of Sciences, Vol. 76, Issue 2 https://doi.org/10.1073/pnas.76.2.774	journal	February 1979
Infrared Spectroscopic Discrimination between the Loop and α-Helices and Determination of the Loop Diffusion Kinetics by Temperature-Jump Time-Resolved Infrared Spectroscopy for Cytochrome c Ye, Manping; Zhang, Qing-Li; Li, Heng Biophysical Journal, Vol. 93, Issue 8 https://doi.org/10.1529/biophysj.107.106799	journal	October 2007
Measuring proteins in H ₂ O with 2D-IR spectroscopy Hume, Samantha; Hithell, Gordon; Greetham, Gregory M. Chemical Science, Vol. 10, Issue 26 https://doi.org/10.1039/c9sc01590f	journal	January 2019
Melting of a β-Hairpin Peptide Using Isotope-Edited 2D IR Spectroscopy and Simulations Smith, Adam W.; Lessing, Joshua; Ganim, Ziad The Journal of Physical Chemistry B, Vol. 114, Issue 34 https://doi.org/10.1021/jp104017h	journal	August 2010
Solution Structure of Horse Heart Ferrocytochrome c Determined by High-Resolution NMR and Restrained Simulated Annealing Qi, Phoebe Xiurong; Di Stefano, Deena L.; Wand, A. Joshua Biochemistry, Vol. 33, Issue 21 https://doi.org/10.1021/bi00187a004	journal	May 1994
Computational Amide I 2D IR Spectroscopy as a Probe of Protein Structure and Dynamics Reppert, Mike; Tokmakoff, Andrei Annual Review of Physical Chemistry, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-physchem-040215-112055	journal	May 2016
Master equation model to predict energy transport pathways in proteins Valiño Borau, Luis; Gulzar, Adnan; Stock, Gerhard The Journal of Chemical Physics, Vol. 152, Issue 4 https://doi.org/10.1063/1.5140070	journal	January 2020
Amide I Two-Dimensional Infrared Spectroscopy of Proteins Ganim, Ziad; Chung, Hoi Sung; Smith, Adam W. Accounts of Chemical Research, Vol. 41, Issue 3 https://doi.org/10.1021/ar700188n	journal	March 2008

Similar Records

In Situ Attenuated Total Reflectance Infrared Spectroelectrochemistry (ATR-IR-SEC) for the Characterization of Molecular Redox Processes on Surface-Proximal Doped Silicon ATR Crystal Working Electrodes

Journal Article · Wed Mar 15 00:00:00 EDT 2023 · Journal of Physical Chemistry. C · OSTI ID:1787997

Bottum, Samuel R.; Teitsworth, Taylor S.; Han, Qi; +12 more

Comparison of various molecular forms of bovine trypsin: Correlation of infrared spectra with X-ray crystal structures

Journal Article · Tue Jan 01 00:00:00 EST 1991 · Biochemistry; (United States) · OSTI ID:1787997

Prestrelski, S J; Byler, D M; Liebman, M N

Efficient Total Chemical Synthesis of ¹³C= ¹⁸O Isotopomers of Human Insulin for Isotope-Edited FTIR

Journal Article · Wed Dec 30 00:00:00 EST 2015 · ChemBioChem: a European journal of chemical biology · OSTI ID:1787997

Dhayalan, Balamurugan; Fitzpatrick, Ann; Mandal, Kalyaneswar; +4 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
71 CLASSICAL AND QUANTUM MECHANICS
GENERAL PHYSICS
coherent multidimensional spectroscopy
protein structure
molecular dynamics
spectroelectrochemistry
femtosecond lasers
Heme group
Fourier transform spectroscopy
infrared spectroscopy
cytochrome

Title: Lessons from combined experimental and theoretical examination of the FTIR and 2D-IR spectroelectrochemistry of the amide I region of cytochrome c

Citation Formats

References (79)

Similar Records

Related Subjects