Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c

Galinato, Mary Grace I.; Bowman, Sarah E.  J.; Kleingardner, Jesse G.; Martin, Sherri; Zhao, Jiyong; Sturhahn, Wolfgang; Alp, E. Ercan; Bren, Kara L.; Lehnert, Nicolai

doi:10.1021/bi501430z

Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c

Journal Article · Mon Dec 22 00:00:00 EST 2014 · Biochemistry

DOI:https://doi.org/10.1021/bi501430z· OSTI ID:1261133

Galinato, Mary Grace I. ^[1]; Bowman, Sarah E. J. ^[2]; Kleingardner, Jesse G. ^[2]; Martin, Sherri ^[3]; Zhao, Jiyong ^[4]; Sturhahn, Wolfgang ^[4]; Alp, E. Ercan ^[4]; Bren, Kara L. ^[2]; Lehnert, Nicolai ^[3]

Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry; Penn State, Erie, PA (United States). Behrend College
Univ. of Rochester, NY (United States). Dept. of Chemistry
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Cytochrome c (Cyt c) has a heme covalently bound to the polypeptide via a Cys-X-X-Cys-His (CXXCH) linker that is located in the interface region for protein–protein interactions. To determine whether the polypeptide matrix influences iron vibrational dynamics, nuclear resonance vibrational spectroscopy (NRVS) measurements were performed on ⁵⁷Fe-labeled ferric Hydrogenobacter thermophilus cytochrome c-552, and variants M13V, M13V/K22M, and A7F, which have structural modifications that alter the composition or environment of the CXXCH pentapeptide loop. Simulations of the NRVS data indicate that the 150–325 cm^–1 region is dominated by N_His–Fe–S_Met axial ligand and polypeptide motions, while the 325–400 cm^–1 region shows dominant contributions from ν(Fe–N_Pyr) (Pyr = pyrrole) and other heme-based modes. Diagnostic spectral signatures that directly relate to structural features of the heme active site are identified using a quantum chemistry-centered normal coordinate analysis (QCC-NCA). In particular, spectral features that directly correlate with CXXCH loop stiffness, the strength of the Fe–His interaction, and the degree of heme distortion are identified. Cumulative results from our investigation suggest that compared to the wild type (wt), variants M13V and M13V/K22M have a more rigid CXXCH pentapeptide segment, a stronger Fe–N_His interaction, and a more ruffled heme. Conversely, the A7F variant has a more planar heme and a weaker Fe–NHis bond. These results are correlated to the observed changes in reduction potential between wt protein and the variants studied here. Lastly, we discuss the implications of these results for Cyt c biogenesis and electron transfer.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1261133

Alternate ID(s):: OSTI ID: 1362102

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 4 Vol. 54; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (59)

Electrochemically induced FTIR difference spectroscopy in the mid- to far infrared (200 μm) domain: A new setup for the analysis of metal–ligand interactions in redox proteins Berthomieu, Catherine; Marboutin, Laure; Dupeyrat, François Biopolymers, Vol. 82, Issue 4 https://doi.org/10.1002/bip.20469	journal	January 2006
Conserved nonplanar heme distortions in cytochromesc Hobbs, John David; Shelnutt, John A. Journal of Protein Chemistry, Vol. 14, Issue 1 https://doi.org/10.1007/bf01902840	journal	January 1995
Cytochrome c: Resonance Raman spectra Strekas, Thomas C.; Spiro, Thomas G. Biochimica et Biophysica Acta (BBA) - Protein Structure, Vol. 278, Issue 1 https://doi.org/10.1016/0005-2795(72)90121-3	journal	August 1972
Structure of cytochrome c551 from Pseudomonas aeruginosa refined at 1.6 Å resolution and comparison of the two redox forms Matsuura, Yoshiki; Takano, Tsunehiro; Dickerson, Richard E. Journal of Molecular Biology, Vol. 156, Issue 2 https://doi.org/10.1016/0022-2836(82)90335-7	journal	April 1982
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
Nuclear resonance vibrational spectroscopy ? NRVS Scheidt, W.; Durbin, S.; Sage, J. Journal of Inorganic Biochemistry, Vol. 99, Issue 1 https://doi.org/10.1016/j.jinorgbio.2004.11.004	journal	January 2005
Iron Normal Mode Dynamics in (Nitrosyl)iron(II)tetraphenylporphyrin from X-ray Nuclear Resonance Data Rai, Brajesh K.; Durbin, Stephen M.; Prohofsky, Earl W. Biophysical Journal, Vol. 82, Issue 6 https://doi.org/10.1016/s0006-3495(02)75636-1	journal	June 2002
Conservation of the Conformation of the Porphyrin Macrocycle in Hemoproteins Jentzen, Walter; Ma, Jian-Guo; Shelnutt, John A. Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/s0006-3495(98)74000-7	journal	February 1998
Resonance Raman Investigations of Cytochrome c Conformational Change upon Interaction with the Membranes of Intact and Ca ²⁺ -Exposed Mitochondria ^† Berezhna, Svitlana; Wohlrab, Hartmut; Champion, Paul M. Biochemistry, Vol. 42, Issue 20 https://doi.org/10.1021/bi027387y	journal	May 2003
Mitochondrial and Microsomal Ferric b₅ Cytochromes Exhibit Divergent Conformational Plasticity in the Context of a Common Fold Simeonov, Mario; Altuve, Adriana; Massiah, Michael A. Biochemistry, Vol. 44, Issue 26 https://doi.org/10.1021/bi050564l	journal	June 2005
Protein-Induced Changes in Nonplanarity of the Porphyrin in Nickel Cytochrome c Probed by Resonance Raman Spectroscopy ^† Ma, Jian-Guo; Laberge, Monique; Song, Xing-Zhi Biochemistry, Vol. 37, Issue 15 https://doi.org/10.1021/bi972375b	journal	April 1998
UV Resonance Raman Investigations of Peptide and Protein Structure and Dynamics Oladepo, Sulayman A.; Xiong, Kan; Hong, Zhenmin Chemical Reviews, Vol. 112, Issue 5 https://doi.org/10.1021/cr200198a	journal	February 2012
Spectroscopic Properties and Electronic Structure of Five- and Six-Coordinate Iron(II) Porphyrin NO Complexes: Effect of the Axial N-Donor Ligand Praneeth, V. K. K.; Näther, Christian; Peters, Gerhard Inorganic Chemistry, Vol. 45, Issue 7 https://doi.org/10.1021/ic050865j	journal	April 2006
Quantum Chemistry-Based Analysis of the Vibrational Spectra of Five-Coordinate Metalloporphyrins [M(TPP)Cl] Paulat, Florian; Praneeth, V. K. K.; Näther, Christian Inorganic Chemistry, Vol. 45, Issue 7 https://doi.org/10.1021/ic0510866	journal	April 2006
Variation and Analysis of Second-Sphere Interactions and Axial Histidinate Character in c -type Cytochromes Bowman, Sarah E. J.; Bren, Kara L. Inorganic Chemistry, Vol. 49, Issue 17 https://doi.org/10.1021/ic100899k	journal	September 2010
Oriented Single-Crystal Nuclear Resonance Vibrational Spectroscopy of [Fe(TPP)(MI)(NO)]: Quantitative Assessment of the trans Effect of NO Lehnert, Nicolai; Sage, J. Timothy; Silvernail, Nathan Inorganic Chemistry, Vol. 49, Issue 15 https://doi.org/10.1021/ic1010677	journal	August 2010
Modulation of Ligand-Field Parameters by Heme Ruffling in Cytochromes c Revealed by EPR Spectroscopy Can, Mehmet; Zoppellaro, Giorgio; Andersson, K. Kristoffer Inorganic Chemistry, Vol. 50, Issue 23 https://doi.org/10.1021/ic201479q	journal	December 2011
Vibrational Assignments of Six-Coordinate Ferrous Heme Nitrosyls: New Insight from Nuclear Resonance Vibrational Spectroscopy Paulat, Florian; Berto, Timothy C.; DeBeer George, Serena Inorganic Chemistry, Vol. 47, Issue 24 https://doi.org/10.1021/ic801626w	journal	November 2008
NMR and DFT Investigation of Heme Ruffling: Functional Implications for Cytochrome c Liptak, Matthew D.; Wen, Xin; Bren, Kara L. Journal of the American Chemical Society, Vol. 132, Issue 28 https://doi.org/10.1021/ja102098p	journal	July 2010
Crowding Induced Collective Hydration of Biological Macromolecules over Extended Distances King, John T.; Arthur, Evan J.; Brooks, Charles L. Journal of the American Chemical Society, Vol. 136, Issue 1 https://doi.org/10.1021/ja407858c	journal	December 2013
Resonance Raman Optical Activity and Surface Enhanced Resonance Raman Optical Activity Analysis of Cytochrome c Johannessen, Christian; White, Peter C.; Abdali, Salim The Journal of Physical Chemistry A, Vol. 111, Issue 32 https://doi.org/10.1021/jp0705267	journal	July 2007
Vibrational Dynamics of Iron in Cytochrome c Leu, Bogdan M.; Ching, Tom H.; Zhao, Jiyong The Journal of Physical Chemistry B, Vol. 113, Issue 7 https://doi.org/10.1021/jp806574t	journal	February 2009
The chemistry and biochemistry of heme c: functional bases for covalent attachment Bowman, Sarah E. J.; Bren, Kara L. Natural Product Reports, Vol. 25, Issue 6 https://doi.org/10.1039/b717196j	journal	January 2008
Investigations of heme distortion, low-frequency vibrational excitations, and electron transfer in cytochrome c Sun, Y.; Benabbas, A.; Zeng, W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 18 https://doi.org/10.1073/pnas.1322274111	journal	April 2014
Mechanisms of Mitochondrial Holocytochrome c Synthase and the Key Roles Played by Cysteines and Histidine of the Heme Attachment Site, Cys-XX-Cys-His Babbitt, Shalon E.; San Francisco, Brian; Mendez, Deanna L. Journal of Biological Chemistry, Vol. 289, Issue 42 https://doi.org/10.1074/jbc.m114.593509	journal	October 2014
An Obligatory Intermediate in the Folding Pathway of Cytochrome c ₅₅₂ from Hydrogenobacter thermophilus Travaglini-Allocatelli, Carlo; Gianni, Stefano; Dubey, Vikash K. Journal of Biological Chemistry, Vol. 280, Issue 27 https://doi.org/10.1074/jbc.m502628200	journal	May 2005
Unveiling a Hidden Folding Intermediate in c -Type Cytochromes by Protein Engineering Borgia, Alessandro; Bonivento, Daniele; Travaglini-Allocatelli, Carlo Journal of Biological Chemistry, Vol. 281, Issue 14 https://doi.org/10.1074/jbc.m512127200	journal	February 2006
Nuclear resonant spectroscopy Sturhahn, Wolfgang Journal of Physics: Condensed Matter, Vol. 16, Issue 5 https://doi.org/10.1088/0953-8984/16/5/009	journal	January 2004
Density-functional exchange-energy approximation with correct asymptotic behavior Becke, A. D. Physical Review A, Vol. 38, Issue 6 https://doi.org/10.1103/physreva.38.3098	journal	September 1988
Density-functional approximation for the correlation energy of the inhomogeneous electron gas Perdew, John P. Physical Review B, Vol. 33, Issue 12 https://doi.org/10.1103/physrevb.33.8822	journal	June 1986
Conserved nonplanar heme distortions in cytochromesc Hobbs, John David; Shelnutt, John A. Journal of Protein Chemistry, Vol. 14, Issue 1 https://doi.org/10.1007/BF01902840	journal	January 1995
Axial histidyl imidazole non-exchangeable proton resonances as indicators of imidazole hydrogen bonding in ferric cyanide complexes of heme peroxidases La Mar, Gerd N.; De Ropp, Jeffrey S.; Chacko, V. P. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 708, Issue 3 https://doi.org/10.1016/0167-4838(82)90443-5	journal	November 1982
Electron transfers in chemistry and biology Marcus, R. A.; Sutin, Norman Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 3 https://doi.org/10.1016/0304-4173(85)90014-X	journal	August 1985
Iron Normal Mode Dynamics in (Nitrosyl)iron(II)tetraphenylporphyrin from X-ray Nuclear Resonance Data Rai, Brajesh K.; Durbin, Stephen M.; Prohofsky, Earl W. Biophysical Journal, Vol. 82, Issue 6 https://doi.org/10.1016/S0006-3495(02)75636-1	journal	June 2002
Conservation of the Conformation of the Porphyrin Macrocycle in Hemoproteins Jentzen, Walter; Ma, Jian-Guo; Shelnutt, John A. Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/S0006-3495(98)74000-7	journal	February 1998
Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c Liu, Xuesong; Kim, Caryn Naekyung; Yang, Jie Cell, Vol. 86, Issue 1 https://doi.org/10.1016/S0092-8674(00)80085-9	journal	July 1996
Substrate recognition of holocytochromecsynthase: N-terminal region and CXXCH motif of mitochondrial cytochromec Zhang, Yulin; Stevens, Julie M.; Ferguson, Stuart J. FEBS Letters, Vol. 588, Issue 18 https://doi.org/10.1016/j.febslet.2014.07.026	journal	July 2014
Protein Dynamics Studied with Ultrafast Two-Dimensional Infrared Vibrational Echo Spectroscopy Thielges, Megan C.; Fayer, Michael D. Accounts of Chemical Research, Vol. 45, Issue 11 https://doi.org/10.1021/ar200275k	journal	March 2012
Heme Attachment Motif Mobility Tunes Cytochrome c Redox Potential ^† Michel, Lea V.; Ye, Tao; Bowman, Sarah E. J. Biochemistry, Vol. 46, Issue 42 https://doi.org/10.1021/bi701177j	journal	October 2007
Resonance Raman Investigation of Nickel Microperoxidase-11 Ma, Jian-Guo; Vanderkooi, Jane M.; Zhang, Jun Biochemistry, Vol. 38, Issue 9 https://doi.org/10.1021/bi982332a	journal	February 1999
Effect on redox potentials of hydrogen bonding from coordinated imidazole in metalloporphyrin complexes O'Brien, P.; Sweigart, D. A. Inorganic Chemistry, Vol. 24, Issue 9 https://doi.org/10.1021/ic00203a028	journal	April 1985
Nuclear Resonance Vibrational Spectroscopy Applied to [Fe(OEP)(NO)]: The Vibrational Assignments of Five-Coordinate Ferrous Heme−Nitrosyls and Implications for Electronic Structure Lehnert, Nicolai; Galinato, Mary Grace I.; Paulat, Florian Inorganic Chemistry, Vol. 49, Issue 9 https://doi.org/10.1021/ic902181e	journal	March 2010
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
Influence of hydrogen bonding on the properties of iron porphyrin imidazole complexes. An internally hydrogen bonded imidazole ligand Quinn, Robert; Mercer-Smith, Janet; Burstyn, Judith N. Journal of the American Chemical Society, Vol. 106, Issue 15 https://doi.org/10.1021/ja00327a012	journal	July 1984
Direct Determination of the Complete Set of Iron Normal Modes in a Porphyrin-Imidazole Model for Carbonmonoxy-heme Proteins: [Fe(TPP)(CO)(1-MeIm)] Rai, Brajesh K.; Durbin, Stephen M.; Prohofsky, Earl W. Journal of the American Chemical Society, Vol. 125, Issue 23 https://doi.org/10.1021/ja028219w	journal	June 2003
Resonance Raman Studies of Heme Axial Ligation in H93G Myoglobin Franzen, Stefan; Boxer, Steven G.; Dyer, R. Brian The Journal of Physical Chemistry B, Vol. 104, Issue 44 https://doi.org/10.1021/jp001231v	journal	October 2000
Carbon−Deuterium Bonds as Site-Specific and Nonperturbative Probes for Time-Resolved Studies of Protein Dynamics and Folding Zimmermann, Jörg; Thielges, Megan C.; Yu, Wayne The Journal of Physical Chemistry Letters, Vol. 2, Issue 5 https://doi.org/10.1021/jz200012h	journal	February 2011
Principles and patterns in the interaction between mono-heme cytochrome c and its partners in electron transfer processes Bertini, Ivano; Cavallaro, Gabriele; Rosato, Antonio Metallomics, Vol. 3, Issue 4 https://doi.org/10.1039/c0mt00108b	journal	January 2011
Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg Hay, P. Jeffrey; Wadt, Willard R. The Journal of Chemical Physics, Vol. 82, Issue 1 https://doi.org/10.1063/1.448799	journal	January 1985
Ab initio effective core potentials for molecular calculations. Potentials for main group elements Na to Bi Wadt, Willard R.; Hay, P. Jeffrey The Journal of Chemical Physics, Vol. 82, Issue 1 https://doi.org/10.1063/1.448800	journal	January 1985
Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals Hay, P. Jeffrey; Wadt, Willard R. The Journal of Chemical Physics, Vol. 82, Issue 1, p. 299-310 https://doi.org/10.1063/1.448975	journal	January 1985
Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface Galinato, M. G. I.; Kleingardner, J. G.; Bowman, S. E. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 23 https://doi.org/10.1073/pnas.1200345109	journal	May 2012
Mechanisms of Mitochondrial Holocytochrome c Synthase and the Key Roles Played by Cysteines and Histidine of the Heme Attachment Site, Cys-XX-Cys-His Babbitt, Shalon E.; San Francisco, Brian; Mendez, Deanna L. Journal of Biological Chemistry, Vol. 289, Issue 42 https://doi.org/10.1074/jbc.M114.593509	journal	October 2014
Effect of Cytochrome c on the Generation and Elimination of O 2 ⨪ and H2O2 in Mitochondria Zhao, Yungang; Wang, Zhi-Bo; Xu, Jian-Xing Journal of Biological Chemistry, Vol. 278, Issue 4 https://doi.org/10.1074/jbc.M209681200	journal	January 2003
An Obligatory Intermediate in the Folding Pathway of Cytochrome c ₅₅₂ from Hydrogenobacter thermophilus Travaglini-Allocatelli, Carlo; Gianni, Stefano; Dubey, Vikash K. Journal of Biological Chemistry, Vol. 280, Issue 27 https://doi.org/10.1074/jbc.M502628200	journal	May 2005
Unveiling a Hidden Folding Intermediate in c -Type Cytochromes by Protein Engineering Borgia, Alessandro; Bonivento, Daniele; Travaglini-Allocatelli, Carlo Journal of Biological Chemistry, Vol. 281, Issue 14 https://doi.org/10.1074/jbc.M512127200	journal	February 2006
Density-functional exchange-energy approximation with correct asymptotic behavior Becke, A. D. Physical Review A, Vol. 38, Issue 6 https://doi.org/10.1103/PhysRevA.38.3098	journal	September 1988
Density-functional approximation for the correlation energy of the inhomogeneous electron gas Perdew, John P. Physical Review B, Vol. 33, Issue 12 https://doi.org/10.1103/PhysRevB.33.8822	journal	June 1986
Hydrogen Tunneling Links Protein Dynamics to Enzyme Catalysis Klinman, Judith P.; Kohen, Amnon Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-051710-133623	journal	June 2013

Cited By (1)

What Can Be Learned from Nuclear Resonance Vibrational Spectroscopy: Vibrational Dynamics and Hemes Scheidt, W. Robert; Li, Jianfeng; Sage, J. Timothy Chemical Reviews, Vol. 117, Issue 19 https://doi.org/10.1021/acs.chemrev.7b00295	journal	September 2017

Similar Records

Stabilization of a Heme-HNO Model Complex Using a Bulky Bis-Picket Fence Porphyrin and Reactivity Studies with NO

Journal Article · Wed Oct 11 20:00:00 EDT 2023 · Journal of the American Chemical Society · OSTI ID:2557458

Nuclear resonance vibrational spectroscopy applied to [Fe(OEP)(NO)] : the vibrational assignments of five-coordinate ferrous heme-nitrosyls and implications for electronic structure.

Journal Article · Thu Dec 31 23:00:00 EST 2009 · Inorg. Chem. · OSTI ID:1011311

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c

Citation Formats

References (59)

Cited By (1)

Similar Records

Related Subjects