Low-frequency Collective Motion

Low-frequency collective motion in proteins and DNA

The concept of low-frequency phonons (or internal motion) in proteins was originally proposed by Professor Kuo-Chen Chou and Professor Nian-Yi Chen in order to solve a perplexing “free-energy deficit” problem [1], which was encountered in studying the binding interaction between insulin and insulin receptor [2]. According to the inference elaborated in [1], the wave numbers of the low-frequency phonons were in the range of 10~100 cm^-1 , corresponding to the range of terahertz frequency (3×10¹¹ to 3×10¹² Hz). In the mean time, the possible biological functions of low-frequency phonons in proteins were also discussed [1].

Subsequently, the aforementioned low-frequency modes have been indeed observed by Raman spectroscopy for a number of protein molecules [3,4] and different types of DNA [5-8]. These observed results have also been further confirmed by neutron scattering experiments [9]. To identify and analyze this kind of low-frequency motions in protein and DNA molecules, the quasi-continuum model was developed [10-16]. It has been successfully used to simulate various low-frequency collective motions in protein and DNA molecules, such as accordion-like motion, pulsation or breathing motion, as reflected by the fact that the low-frequency wave numbers thus derived were quite close to the experimental observations [10,11,13,15,16]. It was also revealed through the quasicontinuum model that the low-frequency motions in biomacromolecules originate from their two common and intrinsic characteristics; i.e., they usually contain (1) a series of weak bonds, such as hydrogen bonds, and (2) a substantial mass distributed over the region of these weak bonds [17]. The most interesting is that many marvelous biological functions and their profound dynamic mechanisms, such as cooperative effects [18,19], allosteric transition [20,21], and intercalation of drugs into DNA [22,23], can be revealed through the low-frequency collective motion or resonance in protein and DNA molecules. In this regard, some phenomenological theories [20,21,23,24] were established. Meanwhile, the solitary wave motion was also used to address the internal motion during microtubule growth [25]. A soliton is a self-reinforcing solitary wave (a wave packet or pulse) that maintains its shape while it travels at constant speed. The relationship between the solitons and the low-frequency phonons in proteins have been discussed in a recent paper [26]. As stated on the web-page of Vermont Photonics Technologies Corp. at Vermont (http://www.sover.net/~bell/newFrontierpics.htm), “Study of low-frequency (or Terahertz frequency) motions in biomacromolecules holds a very exciting potential that could lead to revolutionize biophysics, molecular biology, and biomedicine.” For a systematic introduction of the low-frequency collective motion in biomacromolecules and its biological functions, refer to a comprehensive review article [27].

References

1. Chou, K.C. and Chen, N.Y. (1977) The biological functions of low-frequency phonons. Scientia Sinica, 20, 447-457.
2. Chothia, C. and Janin, J. (1975) Principles of protein-protein recognition. Nature, 256, 705-708.
3. Painter, P.C. and Mosher, L.E. (1979) The low-frequency Raman spectrum of an antibody molecule: bovine IgG. Biopolymers, 18, 3121-3123.
4. Painter, P.C., Mosher, L.E. and Rhoads, C. (1982) Low-frequency modes in the Raman spectra of proteins. Biopolymers, 21, 1469-1472.
5. Painter, P.C., Mosher, L.E. and Rhoads, C. (1981) Low-frequency modes in the Raman spectrum of DNA. Biopolymers, 20, 243-247.
6. Urabe, H. and Tominaga, Y. (1982) Low-frequency collective modes of DNA double helix by Raman spectroscopy. Biopolymers, 21, 2477-2481.
7. Urabe, H., Tominaga, Y. and Kubota, K. (1983) Experimental evidence of collective vibrations in DNA double helix Raman spectroscopy. Journal of Chemical Physics, 78, 5937-5939.
8. Urabe, H., Sugawara, Y., Ataka, M. and Rupprecht, A. (1998) Low-frequency Raman spectra of lysozyme crystals and oriented DNA films: dynamics of crystal water. Biophys J, 74, 1533-1540.
9. Martel, P. (1992) Biophysical aspects of neutron scattering from vibrational modes of proteins. Prog Biophys Mol Biol, 57, 129-179.
10. Chou, K.C. (1983) Low-frequency vibrations of helical structures in protein molecules. Biochemical Journal, 209, 573-580.
11. Chou, K.C. (1983) Identification of low-frequency modes in protein molecules. Biochemical Journal, 215, 465-469.
12. Chou, K.C. (1984) The biological functions of low-frequency phonons: 3. Helical structures and microenvironment. Biophysical Journal, 45, 881-890.
13. Chou, K.C. (1984) Low-frequency vibration of DNA molecules. Biochemical Journal, 221, 27-31.
14. Chou, K.C. (1985) Prediction of a low-frequency mode in BPTI. International Journal of Biological Macromolecules, 7, 77-80.
15. Chou, K.C. (1985) Low-frequency motions in protein molecules: beta-sheet and beta-barrel. Biophysical Journal, 48, 289-297.
16. Chou, K.C., Maggiora, G.M. and Mao, B. (1989) Quasi-continuum models of twist-like and accordion-like low-frequency motions in DNA. Biophysical Journal, 56, 295-305.
17. Chou, K.C. (1986) Origin of low-frequency motion in biological macromolecules: A view of recent progress of quasi-continuity model. Biophysical Chemistry, 25, 105-116.
18. Chou, K.C., Chen, N.Y. and Forsen, S. (1981) The biological functions of lowfrequency phonons: 2. Cooperative effects. Chemica Scripta, 18, 126-132.
19. Chou, K.C. (1989) Low-frequency resonance and cooperativity of hemoglobin. Trends in Biochemical Sciences, 14, 212.
20. Chou, K.C. (1984) The biological functions of low-frequency phonons: 4. Resonance effects and allosteric transition. Biophysical Chemistry, 20, 61-71.
21. Chou, K.C. (1987) The biological functions of low-frequency phonons: 6. A possible dynamic mechanism of allosteric transition in antibody molecules. Biopolymers, 26, 285-295.
22. Chou, K.C. and Maggiora, G.M. (1988) The biological functions of lowfrequency phonons: 7. The impetus for DNA to accommodate intercalators. British Polymer Journal, 20, 143-148.
23. Chou, K.C. and Mao, B. (1988) Collective motion in DNA and its role in [...] intercalation. Biopolymers, 27, 1795-1815.
24. Chou, K.C. and Kiang, Y.S. (1985) The biological functions of low-frequency phonons: 5. A phenomenological theory. Biophysical Chemistry, 22, 219-235.
25. Chou, K.C., Zhang, C.T. and Maggiora, G.M. (1994) Solitary wave dynamics as a mechanism for explaining the internal motion during microtubule growth. Biopolymers, 34, 143-153.
26. Sinkala, Z. (2006) Soliton/exciton transport in proteins. J Theor Biol, 241, 919- 927.
27. Chou, K.C. (1988) Review: Low-frequency collective motion in biomacromolecules and its biological functions. Biophysical Chemistry, 30, 3-48.