Diffusion and single molecule dynamics on biomolecular interface binding energy landscape

Abstract We propose a new approach to study the diffusion dynamics on biomolecular interface binding energy landscape. The resulting mean first passage time (MFPT) has ‘U’ curve dependence on the temperature. It is shown that the large specificity ratio of gap to roughness of the underlying binding energy landscape not only guarantees the thermodynamic stability and the specificity [P.A. Rejto, G.M. Verkhivker, in: Proc. Natl. Acad. Sci. 93 (1996) 8945; C.J. Tsai, S. Kumar, B. Ma, R. Nussinov, Protein Sci. 8 (1999) 1181; G.A. Papoian, P.G. Wolynes, Biopolymers 68 (2003) 333; J. Wang, G.M. Verkhivker, Phys. Rev. Lett. 90 (2003) 188101] but also the kinetic accessibility. The complex kinetics and the associated fluctuations reflecting the structures of the binding energy landscape emerge upon temperature changes. The theory suggests a way of connecting the models/simulations with single molecule experiments by analysing the kinetic trajectories.

[1]  P. Wolynes,et al.  Optimal protein-folding codes from spin-glass theory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Peter G. Wolynes,et al.  Analyzing single molecule trajectories on complex energy landscapes using replica correlation functions , 1999 .

[3]  P. Wolynes,et al.  Statistical mechanics of a correlated energy landscape model for protein folding funnels , 1996, cond-mat/9606159.

[4]  E J Ackerman,et al.  Single-molecule conformational dynamics of fluctuating noncovalent DNA-protein interactions in DNA damage recognition. , 2001, Journal of the American Chemical Society.

[5]  P. Wolynes,et al.  Intermediates and barrier crossing in a random energy model , 1989 .

[6]  H. Nguyen,et al.  Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Wolynes,et al.  Statistics of kinetic pathways on biased rough energy landscapes with applications to protein folding. , 1996, Physical review letters.

[8]  R. Nussinov,et al.  Folding funnels, binding funnels, and protein function , 1999, Protein science : a publication of the Protein Society.

[9]  George Stell,et al.  First-passage time distribution and non-Markovian diffusion dynamics of protein folding , 2002, cond-mat/0206395.

[10]  W. Eaton,et al.  Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy , 2002, Nature.

[11]  Gennady M Verkhivker,et al.  Energy landscape theory, funnels, specificity, and optimal criterion of biomolecular binding. , 2003, Physical review letters.

[12]  Y. Jia,et al.  Folding dynamics of single GCN-4 peptides by fluorescence resonant energy transfer confocal microscopy , 1999 .

[13]  P. Wolynes,et al.  Intermittency of activated events in single molecules: The reaction diffusion description , 1999 .

[14]  D. Koshland.  Application of a Theory of Enzyme Specificity to Protein Synthesis. , 1958, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Rebecca C Wade,et al.  Biomolecular diffusional association. , 2002, Current opinion in structural biology.

[16]  B. Kuhlman,et al.  Global analysis of the effects of temperature and denaturant on the folding and unfolding kinetics of the N-terminal domain of the protein L9. , 1998, Journal of molecular biology.

[17]  Gennady M Verkhivker,et al.  Unraveling principles of lead discovery: from unfrustrated energy landscapes to novel molecular anchors. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Wolynes,et al.  Intermittency of single molecule reaction dynamics in fluctuating environments. , 1995, Physical review letters.

[19]  J A McCammon,et al.  Theory of biomolecular recognition. , 1998, Current opinion in structural biology.

[20]  X. Zhuang,et al.  Correlating Structural Dynamics and Function in Single Ribozyme Molecules , 2002, Science.

[21]  Yaoqi Zhou,et al.  Temperature dependence of the distribution of the first passage time: results from discontinuous molecular dynamics simulations of an all-atom model of the second beta-hairpin fragment of protein G. , 2003, Journal of the American Chemical Society.

[22]  R Nussinov,et al.  Protein folding via binding and vice versa. , 1998, Folding & design.

[23]  X. Xie,et al.  Statistical approaches for probing single-molecule dynamics photon-by-photon , 2002 .

[24]  P. Wolynes,et al.  The physics and bioinformatics of binding and folding—an energy landscape perspective , 2003, Biopolymers.

[25]  Wolynes,et al.  Correlated energy landscape model for finite, random heteropolymers. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[26]  Hue Sun Chan,et al.  History-dependent phenomena in the transverse Ising ferroglass: The free-energy landscape , 2000 .

[27]  P. Wolynes,et al.  The energy landscapes and motions of proteins. , 1991, Science.

[28]  T. Clackson,et al.  A hot spot of binding energy in a hormone-receptor interface , 1995, Science.

[29]  Statistics, pathways and dynamics of single molecule protein folding , 2003 .