Do Vibrational Spectroscopies Uniquely Describe Protein Dynamics? The Case for Myoglobin

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1985 Dec 1

PMID 4092066

Citations 5

Authors

W Bialek

R F Goldstein

Affiliations

Soon will be listed here.

Abstract

We develop a quasi-harmonic description of protein dynamics and apply this description to the anomalous Mössbauer, infrared, x-ray diffraction, and EXAFS (extended x-ray absorption fine structure spectroscopy) data that are available for myoglobin (Mb) and its interactions with carbon monoxide (CO). In the quasi-harmonic approximation the dynamical parameters derived from these spectroscopic data are relevant in the calculation of reaction rates, and we give a quantitative description of the nonexponential kinetics of Mb-CO binding observed at low temperatures. All these data have previously been interpreted in terms of the more complex conformational substates model for protein dynamics. We point out several problems with this model and propose experiments that can provide detailed tests of the quasi-harmonic theory proposed here.

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References

Gavish B . Modelling the unusual temperature dependence of atomic displacements in proteins by local nonharmonic potentials. Proc Natl Acad Sci U S A. 1981; 78(11):6868-72. PMC: 349153. DOI: 10.1073/pnas.78.11.6868. View

Parak F, Frolov E, Mossbauer R, Goldanskii V . Dynamics of metmyoglobin crystals investigated by nuclear gamma resonance absorption. J Mol Biol. 1981; 145(4):825-33. DOI: 10.1016/0022-2836(81)90317-x. View

NOGUTI T, Go N . Collective variable description of small-amplitude conformational fluctuations in a globular protein. Nature. 1982; 296(5859):776-8. DOI: 10.1038/296776a0. View

Tsubaki M, Srivastava R, Yu N . Resonance Raman investigation of carbon monoxide bonding in (carbon monoxy)hemoglobin and -myoglobin: detection of Fe-CO stretching and Fe-C-O bending vibrations and influence of the quaternary structure change. Biochemistry. 1982; 21(6):1132-40. DOI: 10.1021/bi00535a004. View

Alben J, Beece D, Bowne S, Doster W, Eisenstein L, Frauenfelder H . Infrared spectroscopy of photodissociated carboxymyoglobin at low temperatures. Proc Natl Acad Sci U S A. 1982; 79(12):3744-8. PMC: 346503. DOI: 10.1073/pnas.79.12.3744. View

Powers L . X-ray absorption spectroscopy. Application to biological molecules. Biochim Biophys Acta. 1982; 683(1):1-38. DOI: 10.1016/0304-4173(82)90011-8. View

Dauber P, Osguthorpe D, Hagler A . Structure, energetics and dynamics of ligand binding to dihydrofolate reductase. Biochem Soc Trans. 1982; 10(5):312-8. DOI: 10.1042/bst0100312. View

Parak F, Knapp E, Kucheida D . Protein dynamics. Mössbauer spectroscopy on deoxymyoglobin crystals. J Mol Biol. 1982; 161(1):177-94. DOI: 10.1016/0022-2836(82)90285-6. View

Bauminger E, COHEN S, Nowik I, Ofer S, Yariv J . Dynamics of heme iron in crystals of metmyoglobin and deoxymyoglobin. Proc Natl Acad Sci U S A. 1983; 80(3):736-40. PMC: 393454. DOI: 10.1073/pnas.80.3.736. View

10.

Rousseau D, Ondrias M . Resonance Raman scattering studies of the quaternary structure transition in hemoglobin. Annu Rev Biophys Bioeng. 1983; 12:357-80. DOI: 10.1146/annurev.bb.12.060183.002041. View

11.

Blake C, Pulford W, Artymiuk P . X-ray studies of water in crystals of lysozyme. J Mol Biol. 1983; 167(3):693-723. DOI: 10.1016/s0022-2836(83)80105-3. View

12.

Brooks B, Karplus M . Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. Proc Natl Acad Sci U S A. 1983; 80(21):6571-5. PMC: 391211. DOI: 10.1073/pnas.80.21.6571. View

13.

Nakano N, Otsuka J, Tasaki A . Fine structure of iron ion in deoxymyoglobin and deoxyhemoglobin. Biochim Biophys Acta. 1971; 236(1):222-33. DOI: 10.1016/0005-2795(71)90169-3. View

14.

STURTEVANT J . Heat capacity and entropy changes in processes involving proteins. Proc Natl Acad Sci U S A. 1977; 74(6):2236-40. PMC: 432144. DOI: 10.1073/pnas.74.6.2236. View

15.

Desbois A, Lutz M, Banerjee R . Low-frequency vibrations in resonance Raman spectra of horse heart myoglobin. Iron-ligand and iron-nitrogen vibrational modes. Biochemistry. 1979; 18(8):1510-8. DOI: 10.1021/bi00575a019. View

16.

Frauenfelder H, Petsko G, Tsernoglou D . Temperature-dependent X-ray diffraction as a probe of protein structural dynamics. Nature. 1979; 280(5723):558-63. DOI: 10.1038/280558a0. View

17.

Careri G, Fasella P, Gratton E . Enzyme dynamics: the statistical physics approach. Annu Rev Biophys Bioeng. 1979; 8:69-97. DOI: 10.1146/annurev.bb.08.060179.000441. View

18.

Kitagawa T, Nagai K, Tsubaki M . Assignment of the Fe-Nepsilon (His F8) stretching band in the resonance Raman spectra of deoxy myoglobin. FEBS Lett. 1979; 104(2):376-8. DOI: 10.1016/0014-5793(79)80856-x. View

19.

Nagai K, Kitagawa T, Morimoto H . Quaternary structures and low frequency molecular vibrations of haems of deoxy and oxyhaemoglobin studied by resonance raman scattering. J Mol Biol. 1980; 136(3):271-89. DOI: 10.1016/0022-2836(80)90374-5. View

20.

Beece D, Eisenstein L, Frauenfelder H, Good D, Marden M, Reinisch L . Solvent viscosity and protein dynamics. Biochemistry. 1980; 19(23):5147-57. DOI: 10.1021/bi00564a001. View