Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c
Abstract
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 Fe-57-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 nu(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 planarmore »
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1261133
- Alternate Identifier(s):
- OSTI ID: 1362102
- Grant/Contract Number:
- R01-GM63170; AC02-06CH11357
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 54; Journal Issue: 4; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Galinato, Mary Grace I., Bowman, Sarah E. J., Kleingardner, Jesse G., Martin, Sherri, Zhao, Jiyong, Sturhahn, Wolfgang, Alp, E. Ercan, Bren, Kara L., and Lehnert, Nicolai. Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c. United States: N. p., 2014.
Web. doi:10.1021/bi501430z.
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. Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c. United States. https://doi.org/10.1021/bi501430z
Galinato, Mary Grace I., Bowman, Sarah E. J., Kleingardner, Jesse G., Martin, Sherri, Zhao, Jiyong, Sturhahn, Wolfgang, Alp, E. Ercan, Bren, Kara L., and Lehnert, Nicolai. 2014.
"Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c". United States. https://doi.org/10.1021/bi501430z. https://www.osti.gov/servlets/purl/1261133.
@article{osti_1261133,
title = {Effects of Protein Structure on Iron–Polypeptide Vibrational Dynamic Coupling in Cytochrome c},
author = {Galinato, Mary Grace I. and Bowman, Sarah E. J. and Kleingardner, Jesse G. and Martin, Sherri and Zhao, Jiyong and Sturhahn, Wolfgang and Alp, E. Ercan and Bren, Kara L. and Lehnert, Nicolai},
abstractNote = {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 Fe-57-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 nu(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-N-His bond. These results are correlated to the observed changes in reduction potential between wt protein and the variants studied here. Implications of these results for Cyt c biogenesis and electron transfer are also discussed.},
doi = {10.1021/bi501430z},
url = {https://www.osti.gov/biblio/1261133},
journal = {Biochemistry},
issn = {0006-2960},
number = 4,
volume = 54,
place = {United States},
year = {Mon Dec 22 00:00:00 EST 2014},
month = {Mon Dec 22 00:00:00 EST 2014}
}
Web of Science
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Works referencing / citing this record:
What Can Be Learned from Nuclear Resonance Vibrational Spectroscopy: Vibrational Dynamics and Hemes
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