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Importance of Atomic Contacts in Vibrational Energy Flow in Proteins

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Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama, Toyonaka, Osaka 560-0043, Japan
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Cite this: J. Phys. Chem. Lett. 2016, 7, 11, 1950–1954
Publication Date (Web):May 10, 2016
https://doi.org/10.1021/acs.jpclett.6b00785
Copyright © 2016 American Chemical Society
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Abstract

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Vibrational energy flow in proteins was studied by monitoring the time-resolved anti-Stokes ultraviolet resonance Raman scattering of three myoglobin mutants in which a Trp residue substitutes a different amino acid residue near heme. The anti-Stokes Raman intensities of the Trp residue in the three mutants increased with similar rates after depositing excess vibrational energy at heme, despite the difference in distance between heme and each substituted Trp residue along the main chain of the protein. This indicates that vibrational energy is not transferred through the main chain of the protein but rather through atomic contacts between heme and the Trp residue. Distinct differences were observed in the amplitude of the band intensity change between the Trp residues at different positions, and the amplitude of the band intensity change exhibits a correlation with the extent of exposure of the Trp residue to solvent water. This correlation indicates that atomic contacts between an amino acid residue and solvent water play an important role in vibrational energy flow in a protein.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.6b00785.

  • Materials and methods (sample preparation, UVRR measurements, and SASA calculations) and supporting results (time-resolved anti-Stokes UVRR spectra of WT Mb, time-resolved Stokes UVRR spectra, evaluation of the heme-Trp contact, relationship between the energy dissipation rate and the SASA value, and temporal profiles of the anti-Stokes W16 band intensity change). (PDF)

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This article is cited by 29 publications.

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  2. Korey M. Reid, Takahisa Yamato, David M. Leitner. Variation of Energy Transfer Rates across Protein–Water Contacts with Equilibrium Structural Fluctuations of a Homodimeric Hemoglobin. The Journal of Physical Chemistry B 2020, 124 (7) , 1148-1159. https://doi.org/10.1021/acs.jpcb.9b11413
  3. David M. Leitner, Hari Datt Pandey, Korey M. Reid. Energy Transport across Interfaces in Biomolecular Systems. The Journal of Physical Chemistry B 2019, 123 (45) , 9507-9524. https://doi.org/10.1021/acs.jpcb.9b07086
  4. L. Maggi, P. Carloni, G. Rossetti. Vibrational Energy in Proteins Correlates with Topology. The Journal of Physical Chemistry Letters 2018, 9 (22) , 6393-6398. https://doi.org/10.1021/acs.jpclett.8b02380
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  14. Takahisa Yamato, David M. Leitner. Structure, dynamics, and energy flow that govern Heme protein functions: theory and experiments. Session 3SBA at the 57th BSJ Annual Meeting. Biophysical Reviews 2020, 12 (2) , 291-292. https://doi.org/10.1007/s12551-020-00625-4
  15. David M. Leitner, Takahisa Yamato. Recent developments in the computational study of protein structural and vibrational energy dynamics. Biophysical Reviews 2020, 12 (2) , 317-322. https://doi.org/10.1007/s12551-020-00661-0
  16. Misao Mizuno, Yasuhisa Mizutani. Role of atomic contacts in vibrational energy transfer in myoglobin. Biophysical Reviews 2020, 12 (2) , 511-518. https://doi.org/10.1007/s12551-020-00681-w
  17. David M. Leitner. Energy Relaxation and Thermal Transport in Molecules. 2020,,, 865-885. https://doi.org/10.1007/978-3-319-44680-6_14
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  19. Andrea Amadei, Massimiliano Aschi. Modelling vibrational relaxation in complex molecular systems. Physical Chemistry Chemical Physics 2019, 21 (36) , 20003-20017. https://doi.org/10.1039/C9CP03379C
  20. Vytautas Balevičius Jr, Tiejun Wei, Devis Di Tommaso, Darius Abramavicius, Jürgen Hauer, Tomas Polívka, Christopher D. P. Duffy. The full dynamics of energy relaxation in large organic molecules: from photo-excitation to solvent heating. Chemical Science 2019, 10 (18) , 4792-4804. https://doi.org/10.1039/C9SC00410F
  21. Saumyak Mukherjee, Sayantan Mondal, Biman Bagchi. Mechanism of Solvent Control of Protein Dynamics. Physical Review Letters 2019, 122 (5) https://doi.org/10.1103/PhysRevLett.122.058101
  22. Bang-Chieh Huang, Lee-Wei Yang. Molecular dynamics simulations and linear response theories jointly describe biphasic responses of myoglobin relaxation and reveal evolutionarily conserved frequent communicators. Biophysics and Physicobiology 2019, 16 (0) , 473-484. https://doi.org/10.2142/biophysico.16.0_473
  23. Tsubasa Okamoto, Hideyuki Takahashi, Eiji Ohmichi, Haruto Ishikawa, Yasuhisa Mizutani, Hitoshi Ohta. Force detection of high-frequency electron paramagnetic resonance spectroscopy of microliter solution sample. Applied Physics Letters 2018, 113 (22) , 223702. https://doi.org/10.1063/1.5055743
  24. David M. Leitner, Takahisa Yamato. MAPPING ENERGY TRANSPORT NETWORKS IN PROTEINS. 2018,,, 63-113. https://doi.org/10.1002/9781119518068.ch2
  25. , . Reviews in Computational Chemistry, Volume 31. 2018,,https://doi.org/10.1002/9781119518068
  26. David M. Leitner. Energy Relaxation and Thermal Transport in Molecules. 2018,,, 1-22. https://doi.org/10.1007/978-3-319-50257-1_14-1
  27. , . Handbook of Materials Modeling. 2018,,https://doi.org/10.1007/978-3-319-50257-1
  28. Yasuhisa Mizutani. Time-Resolved Resonance Raman Spectroscopy and Application to Studies on Ultrafast Protein Dynamics. Bulletin of the Chemical Society of Japan 2017, 90 (12) , 1344-1371. https://doi.org/10.1246/bcsj.20170218
  29. Yijie Yang, Guanhua Liao, Xianglei Kong. Charge-state Resolved Infrared Multiple Photon Dissociation (IRMPD) Spectroscopy of Ubiquitin Ions in the Gas Phase. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/s41598-017-16831-2

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