- Physical Review Journals
All JournalsPhysics Magazine
Access Provided by Xinjiang University

Physical Review E

Export citation

Export citation

Choose format for download:

Download Citation
  • Access by Xinjiang University

Possible role of electrodynamic interactions in long-distance biomolecular recognition

Jordane Preto1,2,3,*, Marco Pettini2,3,†, and Jack A. Tuszynski4,5,‡

  • 1Department of Chemistry, Rice University, Houston, Texas, USA
  • 2Aix-Marseille University, Marseille, France
  • 3CNRS Centre de Physique Théorique UMR7332, 13288 Marseille, France
  • 4Department of Oncology, 3-336, Cross Cancer Institute, Edmonton, Alberta, Canada T6G 1Z2
  • 5Department of Physics, University of Alberta, Edmonton, Alberta, Canada

  • *preto@cpt.univ-mrs.fr
  • †pettini@cpt.univ-mrs.fr
  • ‡jack_BT@ualberta.ca
PDF

Phys. Rev. E 91, 052710 – Published 22 May, 2015

DOI: https://doi.org/10.1103/PhysRevE.91.052710

Abstract

The issue of retarded long-range resonant interactions between two molecules with oscillating dipole moments is revisited within the framework of classical electrodynamics. By taking advantage of a theorem in complex analysis, we present a simple method to calculate the frequencies of the normal modes, which are then used to estimate the interaction potential. The possibility that such interactions play a non-negligible role in ensuring the effective functioning of the biomolecular functions is investigated. On the basis of experimental results reported in the literature and simple numerical estimates, it is found that long-range interactions involving electromagnetic fields of frequencies 0.1–1THz could be temporarily activated despite radiation losses and solvent dissipation. Moreover, the theoretical background used to derive the mentioned interactions sheds light on Fröhlich's theory of selective long-range forces between biomolecules. At variance with a long-standing belief, we show that sizable resonant long-range interactions may exist only if the interacting system is out of thermal equilibrium.

View figure in article

Article Text

References (80)

  1. S. Zhao and R. Iyengar, Systems pharmacology: Network analysis to identify multiscale mechanisms of drug action, Annu. Rev. Pharmacol. Toxicol. 52, 505 (2012).
  2. J. R. de Xammar Oro, G. Ruderman, J. R. Grigera, and F. Vericat, Threshold frequency for the ionic screening of electric fields in electrolyte solutions, J. Chem. Soc., Faraday Trans. 88, 699 (1992); J. R. de Xammar Oro, G. Ruderman, and J. R. Grigera, Electrodynamics of interactions in electrolyte media. Possible consequences in biological functions, Biophysics 53, 195 (2008).
  3. J. C. Maxwell, A Treatise on Electricity and Magnetism (Dover, New York, 1954).
  4. See, for example, M. J. Stephen, First-order dispersion forces, J. Chem. Phys. 40, 669 (1964); A. D. McLachlan, Resonance transfer of molecular excitation energy, Mol. Phys. 8, 409 (1964), in the case of two identical atoms; D. P. Craig and T. Thirunamachandran, Molecular Quantum Electrodynamics (Academic, London, 1984).
  5. J. Preto, E. Floriani, I. Nardecchia, P. Ferrier, and M. Pettini, Experimental assessment of the contribution of electrodynamic interactions to long-distance recruitment of biomolecular partners: Theoretical basis, Phys. Rev. E 85, 041904 (2012).
  6. J. Preto, Long-range interactions in biological systems, Ph.D. thesis, Aix-Marseille University, 2012.
  7. I. Nardecchia, Feasibility study of the experimental detection of long-range selective resonant recruitment forces between biomolecules, Ph.D. thesis, Aix-Marseille University, 2012.
  8. H. Fröhlich, Selective long range dispersion forces between large systems, Phys. Lett. A 39, 153 (1972).
  9. H. Fröhlich, The extraordinary dielectric properties of biological materials and the action of enzymes, Proc. Natl. Acad. Sci. U.S.A. 72, 4211 (1975).
  10. H. Fröhlich, Coherent electric vibrations in biological systems and the cancer problem, IEEE Trans. Microwave Theory & Tech. 26, 613 (1978).
  11. H. Fröhlich, The biological effects of microwaves and related questions, Adv. Electron. Electron Phys. 53, 85 (1980).
  12. J. Preto and M. Pettini, Resonant long-range interactions between polar macromolecules, Phys. Lett. A 377, 587 (2013).
  13. L. D. Landau and E. M. Lifshitz, Statistical Physics (Pergamon Press, New York, 1980).
  14. P. C. Painter, L. E. Mosher, and C. Rhoads, Low-frequency modes in the Raman spectra of proteins, Biopolymers 21, 1469 (1982); K. C. Chou, Low-frequency motions in protein molecules. Beta-sheet and beta-barrel, Biophys. J. 48, 289 (1985).
  15. J. B. Hasted, Liquid water: Dielectric properties, in Water: A Comprehensive Treatise, edited by F. Franks (Plenum Press, New York, 1972), Vol. 1, pp. 255–309.
  16. M. Cifra, J. Pokorný, D. Havelka, and O. Kučera, Electric field generated by axial longitudinal vibration modes of microtubule, BioSystems 100, 122 (2010).
  17. F. Jelínek, M. Cifra, J. Pokorný, J. Vaniš, J. Šimša, J. Hašek, and I. Frýdlová, Measurement of electrical oscillations and mechanical vibrations of yeast cells membrane around 1 kHz, Electromagn. Biol. Med. 28, 223 (2009).
  18. I. Nardecchia, L. Spinelli, J. Preto, M. Gori, E. Floriani, S. Jaeger, P. Ferrier, and M. Pettini, Experimental detection of long-distance interactions between biomolecules through their diffusion behavior: Numerical study, Phys. Rev. E 90, 022703 (2014).
  19. S. Takashima, Measurement and computation of the dipole moment of globular proteins III: chymotrypsin, Biophys. Chem. 58, 13 (1996).
  20. S. Takashima, Electric dipole moments of globular proteins: Measurement and calculation with NMR and X-ray databases, J. Non-Cryst. Solids 305, 303 (2002).
  21. S. R. Kabir, K. Yokoyama, K. Mihashi, T. Kodama, and M. Suzuki, Hyper-mobile water is induced around actin filaments, Biophys. J. 85, 3154 (2003).
  22. G. H. Pollack, The Fourth Phase of Water: Beyond Solid, Liquid, and Vapor (Ebner & Sons, Seattle, 2013).
  23. G. M. Giambasu, T. Luchko, D. Herschlag, D. M. York, and D. A. Case, Ion counting from explicit-solvent simulations and 3D-RISM, Biophys. J. 106, 883 (2014).
  24. J. A. Tuszyński, E. J. Carpenter, J. M. Dixon, and Y. Engelborghs, Non-Gaussian statistics of the vibrational fluctuations of myoglobin, Eur. Biophys. J. 33, 159 (2004).
  25. A. Ben-Naim, Water and Aqueous Solutions (Plenum, New York, 1974).
  26. J. A. Tuszyński, J. A. Brown, E. Crawford, E. J. Carpenter, M. L. A. Nip, J. M. Dixon, and M. V. Satarić, Molecular dynamics simulations of tubulin structure and calculations of electrostatic properties of microtubules, Math. Comput. Model. 41, 1055 (2005).
  27. J. D. Jackson, Classical Electrodynamics, 6th printing (John Wiley & Sons, Inc., New York, 1967).
  28. W. K. H. Panofsky and M. Phillips, Classical Electricity and Magnetism (Addison-Wesley, New York, 1962).
  29. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell, 2nd ed. (Garland Publishing, Inc., New York, 1989), pp. 93–94, pp. 354–355.
  30. P. Debye, Reaction rates in ionic solutions, Trans. Electrochem. Soc. 82, 265 (1942).
  31. R. M. Noyes, Effects of diffusion rates on chemical kinetics in Progress in Reaction Kinetics, Vol. 1, edited by G. Porter (Pergamon Press, New York, 1961), p. 128.
  32. J. Howard, Mechanics of Motor Proteins and the Cytoskeleton (Sinauer Associates, Inc., Sunderland, 2001), pp. 41–45.
  33. J. J. Chang, Physical properties of biophotons and their biological functions, Indian J. Exp. Biol. 46, 371 (2008).
  34. S. Cohen and F. A. Popp, Biophoton emission of the human body, J. Photochem. Photobiol. B 40, 187 (1997).
  35. B. Devaraj, R. Q. Scott, P. Roschger, and H. Inaba, Ultraweak light emission from rat liver nuclei, Photochem. Photobiol. 54, 289 (1991).
  36. M. Kobayashi, D. Kikuchi, and H. Okamura, Imaging of ultraweak spontaneous photon emission from human body displaying diurnal rhythm, PLoS One 4, e6256 (2009).
  37. M. Kobayashi, M. Takeda, K.-I. Ito, H. Kato, and H. Inaba, Two-dimensional photon counting imaging and spatiotemporal characterization of ultraweak photon emission from a rat's brain in vivo, J. Neurosci. Methods 93, 163 (1999).
  38. T. I. Quickenden and S. S. Que Hee, Weak luminescence from the yeast saccharomyces cerevisiae and the existence of mitogenetic radiation, Biochem. Biophys. Res. Commun. 60, 764 (1974).
  39. M. Takeda, M. Kobayashi, M. Takayama, S. Suzuki, T. Ishida, K. Ohnuki, T. Moriya, and N. Ohuchi, Biophoton detection as a novel technique for cancer imaging, Cancer Sci. 95, 656 (2004).
  40. R. van Wijk, J. M. Ackerman, and E. P. van Wijk, Effects of a color filter used in auriculomedicine on ultraweak photon emission of the human body, J. Altern. Complement. Med. 12, 955 (2006).
  41. Y. Z. Yoon, J. Kim, B. C. Lee, Y. U. Kim, S. K. Lee, and K. S. Soh, Changes in ultraweak photon emission and heart rate variability of epinephrine-injected rats, Gen. Physiol. Biophys. 24, 147 (2005).
  42. R. Thar and M. Kuhl, Propagation of electromagnetic radiation in mitochondria? J. Theor. Biol. 230, 261 (2004).
  43. M. Nakano, Low-level chemiluminescence during lipid peroxidations and enzymatic reactions, J. Biolumin. Chemilum. 4, 231 (2005).
  44. Y. Isojima, T. Isoshima, K. Nagai, K. Kikuchi, and H. Nakagawa, Ultraweak biochemiluminescence detected from rat hippocampal slices, Neuro. Rep. 6, 658 (1995).
  45. Y. Kataoka, Y. Cui, A. Yamagata, M. Niigaki, T. Hirohata, N. Oishi, and Y. Watanabe, Activity-dependent neural tissue oxidation emits intrinsic ultraweak photons, Biochem. Biophys. Res. Commun. 285, 1007 (2001).
  46. M. Kobayashi, M. Takeda, T. Sato, Y. Yamazaki, K. Kaneko, K. I. Ito, H. Kato, and H. Inaba, In vivo imaging of spontaneous ultraweak photon emission from a rats brain correlated with cerebral energy metabolism and oxidative stress, Neurosci. Res. 34, 103 (1999).
  47. Y. Sun, C. H. Wang, and J. Dai, Biophotons as neural communication signals demonstrated by in situ biophoton autography, Photochem. Photobiol. Sci. 9, 315 (2010).
  48. V. Voeikov, Reactive oxygen species, water, photons and life, Rivista di Biologia/Biology Forum 94, 237 (2001).
  49. J. T. Kindt and C. A. Schmuttenmaer, Far-infrared dielectric properties of polar liquids probed by femtosecond terahertz pulse spectroscopy, J. Phys. Chem. 100, 10373 (1996).
  50. J. B. Hasted, S. K. Husain, F. A. M. Frescura, and J. R. Birch, Far-infrared absorption in liquid water, Chem. Phys. Lett. 118, 622 (1985).
  51. G. J. Wilmink, B. D. Rivest, B. L. Ibey, L. X. Cundin, E. C. Haywood, and W. P. Roach, The optical properties of biological tissues in the terahertz wavelength range, Proc. SPIE 7175, 717507 (2009).
  52. C. T. Tai and R. E. Collin, Radiation of a Hertzian dipole immersed in a dissipative medium, IEEE Trans. Antennas Propag. 48, 1501 (2000).
  53. K. G. Brown, S. C. Erfurth, E. W. Small, and W. L. Peticolas, Conformationally dependent low-frequency motions of proteins by laser Raman spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 69, 1467 (1972).
  54. L. Genzel, F. Keilmann, T. P. Martin, G. Wintreling, Y. Yacoby, H. Fröhlich, and M. W. Makinen, Low-frequency Raman spectra of lysozyme, Biopolymers 15, 219 (1976).
  55. H. Urabe, Y. Sugawara, M. Ataka, and A. Rupprecht, Low-frequency Raman spectra of lysozyme crystals and oriented DNA films: Dynamics of crystal water, Biophys. J. 74, 1533 (1998).
  56. Y. M. Romanovsky, A. V. Netrebko, and A. Y. Chikishev, Are the subglobular oscillations of protein molecules in water overdamped?, in Saratov Fall Meeting 2001 (International Society for Optics and Photonics): Optical Technologies in Biophysics and Medicine III, pp. 16–29 (2002).
  57. K. R. Foster and J. W. Baish, Viscous damping of vibrations in microtubules, J. Biol. Phys. 26, 255 (2000).
  58. R. K. Adair, Vibrational resonances in biological systems at microwave frequencies, Biophys. J. 82, 1147 (2002).
  59. V. Conti Nibali and M. Havenith, New insights into the role of water in biological function: Studying solvated biomolecules using terahertz absorption spectroscopy in conjunction with molecular dynamics simulations, J. Am. Chem. Soc. 136, 12800 (2014).
  60. J. Pokorný, Excitation of vibrations in microtubules in living cells, Bioelectrochemistry 63, 321 (2004).
  61. G. S. Edwards, C. C. Davis, J. D. Saffer, and M. L. Swicord, Resonant microwave absorption of selected DNA molecules, Phys. Rev. Lett. 53, 1284 (1984).
  62. L. L. Van Zandt, Resonant microwave absorption by dissolved DNA, Phys. Rev. Lett. 57, 2085 (1986).
  63. L. L. Van Zandt, Why structured water causes sharp absorption by DNA at microwave frequencies, J. Biomol. Struct. Dyn. 4, 569 (1987).
  64. F. Gruia, M. Kubo, X. Ye, and P. M. Champion, Investigations of vibrational coherence in the low-frequency region of ferric heme proteins, Biophys. J. 94, 2252 (2008).
  65. T. Cimei, A. R. Bizzarri, S. Cannistraro, G. Cerullo, and S. De Silvestri, Vibrational coherence in Azurin with impulsive excitation of the LMCT absorption band, Chem. Phys. Lett. 362, 497 (2002).
  66. D. A. Turton, H. M. Senn, T. Harwood, A. J. Lapthorn, E. M. Ellis, and K. Wynne, Terahertz underdamped vibrational motion governs protein-ligand binding in solution, Nat. Commun. 5, 3999 (2014).
  67. A. Xie, A. F. G. van der Meer, and R. H. Austin, Excited-state lifetimes of far-infrared collective modes in proteins, Phys. Rev. Lett. 88, 018102 (2001).
  68. V. V. Mitrofanov, Y. M. Romanovsky, and A. V. Netrebko, On the structure and dynamics of hydrogen bonds in liquid water, in Saratov Fall Meeting 2003 (International Society for Optics and Photonics): Optical Technologies in Biophysics and Medicine V, pp. 42-48 (2004).
  69. L. Gomberoff, R. R. McLone, and E. A. Power, Long-range retarded potentials between molecules, J. Chem. Phys. 44, 4148 (1966).
  70. R. R. McLone and E. A. Power, The long range van der Waals forces between non-identical systems, Proc. R. Soc. London, Ser. A 286, 573 (1965); G.-I. Kweon and N. M. Lawandy, Dispersion interactions between excited atoms, Phys. Rev. A 47, 4513 (1993); Erratum: Dispersion interactions between excited atoms, ibid. 49, 2205 (1994).
  71. E. A. Power and T. Thirunamachandran, Casimir-Polder potential as an interaction between induced dipoles, Phys. Rev. A 48, 4761 (1993).
  72. H. B. G. Casimir and D. Polder, The influence of retardation on the London-van der Waals forces, Phys. Rev. 73, 360 (1948).
  73. H. Fröhlich, Long-range coherence in biological systems, Riv. Nuovo Cimento 7, 399 (1977).
  74. M. J. Kennedy, R. M. Hughes, L. A. Peteya, J. W. Schwartz, M. D. Ehlers, and C. L. Tucker, Rapid blue-light-mediated induction of protein interactions in living cells, Nat. Methods 7, 973 (2010).
  75. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, and H. J. C. Berendsen, GROMACS: fast, flexible, and free, J. Comput. Chem. 26, 1701 (2005).
  76. D. A. Pearlman, D. A. Case, J. W. Caldwell, W. S. Ross, T. E. Cheatham, S. DeBolt, D. Ferguson, G. Seibel, and P. Kollman, AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules, Comput. Phys. Commun. 91, 1 (1995).
  77. J. A. Tuszyński and E. K. Strong, Application of the Fröhlich theory to the modelling of rouleau formation in human erythrocytes, J. Biol. Phys. 17, 19 (1989).
  78. M. Pettini, Geometry and Topology in Hamiltonian Dynamics and Statistical Mechanics (Springer, New York, 2007).
  79. H. Fröhlich, Long-range coherence and energy storage in biological systems, Int. J. Quantum Chem. 2, 641 (1968).
  80. E. T. Whittaker and G. N. Watson, A Course of Modern Analysis, 4th ed. (Cambridge University Press, Cambridge, England, 1927), pp. 131–133.

Outline

Information

Phys. Rev. E 91, 052710– Published 22 May, 2015
  • Received 28 February 2014
  • Revised 31 August 2014

©2015 American Physical Society

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation