Coarse-grained model of coil-to-helix kinetics demonstrates the importance of multiple nucleation sites in helix folding

Journal of Chemical Theory and Computation

Volumn 2, Issue 3, 2006, Pages 674-684

  Van Giessen, Alan E ^a   Straub, John E ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33846207122     PISSN: 15499618     EISSN: None     Source Type: Journal    
DOI: 10.1021/ct0503318     Document Type: Article

References (42)

1. Schellman, J. A. The factors affecting the stability of hydrogen-bonded polypeptide structures in solution. J. Phys. Chem. 1958, 62, 1485-1494.
2. Zimm, B. H.; Bragg, J. K. Theory of the phase transition between helix and random coil in polypeptide chains. J. Chem. Phys. 1959, 31, 526-535.
3. Lifson S.; Roig, A. On the theory of helix-coil transition in polypeptides. J. Chem. Phys. 1960, 34, 1963-1974.
4. Doig, A. J. Recent advances in helix-coil theory. Biophys. Chem. 2002, 101-102, 281-293.
5. Takano, M.; Nagayama, K.; Suyama, A. Investigating a link between all-atom model simulation and the Ising-based theory on the helix-coil transition: Equilibrium statistical mechanics. J. Chem. Phys. 2002, 116, 2219-2228.
6. Zana, R. On the rate-determining step for helix propagation in the helix-coil transition of polypeptides in solution. Biopolymers 1975, 14, 2425-2428.
7. Williams, S.; Causgrove, T. P.; Gihnanshin, R.; Fang, K. S.; Callender, R. H.; Woodruff, W. H.; Dyer, R. B. Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry 1996, 35, 691-697.
8. Thompson, P. A.; Eaton, W. A.; Hofrichter, J. Laser temperature jump study of the helix-coil kinetics of an Alanine peptide interpreted with a 'kinetic zipper' model. Biochemistry 1997, 36, 9200-9210.
9. Lednev, I. K.; Karnoup, A. S.; Sparrow, M. C.; Asher, S. A. α-helix peptide folding and unfolding activation barriers: a nanosecond UV resonance Raman study. J. Am. Chem. Soc. 1999, 121, 8074-8086.
10. Clarke, D. T.; Doig, A. J.; Stapley, B. J.; Jones, G. R. The α-helix folds on the millisecond time scale. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 722-7237.
11. Gilmanshin, R.; Williams, S.; Callender, R.; Woodruff, W.; Dyer, R. Fast events in protein folding: Relaxation dynamics of secondary and tertiary structure in native apomyoglobin. Proc. Natl. Acad. Sci.7 U.S.A. 1997, 94, 3709-3713.
12. Dyer, R.; Gai, F.; Woodruff, W.; Gilmanshin, R.; Callender, R. Infrared Studies of Fast Events in Protein Folding. Acc. Chem. Res. 1998, 31, 709-716.
13. Callender, R.; Dyer, R.; Gilmanshin, R.; Woodruff, W. FAST EVENTS IN PROTEIN FOLDING: The Time Evolution of Primary Processes. Annu. Rev. Phys. Chem. 1998, 49, 173-202.
14. Huang, C.-Y.; Klemke, J. W.; Getahun, Z.; DeGrado, W. F.; Gai F. Temperature-dependent helix-coil transition of an alanine based peptide. J. Am. Chem. Soc. 2001,123, 9235-9238.
15. 13C-labeled helical peptides. J. Am. Chem. Soc. 2001, 123, 12111-12112.
16. Huang, C.-Y.; Getahun, Z.; Zhu, Y.; Klemke, J. W.; DeGrado, W. F.; Gai, F. Helix formation via conformation diffusion search. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2788-2793.
17. Wang, T.; Du, D.; Gai F. Helix-coil kinetics of two 14-residue peptides. Chem. Phys. Lett. 2003, 370, 842-848.
18. Wang, T.; Zhu, Y.; Getahun, Z.; Du, D.; Huang, C.-Y.; DeGrado, W. F.; Gai, F. Length dependent helix-coil transition kinetics of nine alanine-based peptides. J. Phys. Chem. B 2004, 108, 15301-15310.
19. Daggett, V.; Levitt, M. Molecular dynamics simulations of helix denaturation. J. Mol. Biol. 1992, 223, 1121-1138.
20. Klimov, D.; Betancourt, M.; Thirumalai, D. Virtual atom representation of hydrogen bonds in minimal off-lattice models of alpha-helices: Effects on stability, cooperativity and kinetics. Fold. Des. 1998, 3, 481-496.
21. Takada, S.; Luthey-Schulten, Z.; Wolynes, P. G. Folding dynamics with nonadditive forces: a simulation study of a designed helical protein and a random heteropolymer. J. Chem. Phys. 1999, 110, 11616-11629.
22. Margulis, C. J.; Stern, H. A.; Berne, B. J. Helix unfolding and intramolecular hydrogen bond dynamics in small α-helices in explicit solvent. J. Phys. Chem. B 2002, 106, 10748-10752.
23. Dohsi, U. R.; Muñoz, V. The principles of α-helix formation: explaining complex kinetics with nucleation-elongation theory. J. Phys. Chem. B 2004, 108, 8497-8506.
24. Schwartz, G. Kinetics of the helix-coil transition. J. Mol. Biol. 1965, 11, 64-77.
25. Brooks, C. Helix-Coil Kinetics: Folding Time Scales for Helical Peptides from a Sequential Kinetic Model. J. Phys. Chem. 1996, 100, 2546-2549.
26. Buchete, N.-V.; Straub, J. E. Mean first-passage time calculations for the coil-to-helix transition: the active helix Ising model. J. Phys. Chem. 2001, 105, 6684-6697.
27. Voegler Smith, A.; Hall, C. K. Protein refolding versus aggregation: computer simulations on an intermediate-resolution protein model. J. Mol. Biol. 2001, 312, 187-202.
28. Honig, B.; Cohen, F. E. Adding backbone to protein folding: why proteins are polypeptides. Fold. Des. 1996, 1, R17-R20.
29. Cantor, C. R.; Schimmel, P. R. Biophysical Chemistry; Part 1; Freedman: New York, 1980.
30. Veitshans, T.; Klimov, D.; Thirumalai, D. Protein folding kinetics: time scales, pathways and energy landscapes in terms of sequence-dependent properties. Fold. Des. 1996, 2, 1-22.
31. Swenson, R. H.; Wang, J.-S. Replica Monte Carlo simulation of spin-glasses. Phys. Rev. Lett. 1986, 57, 2607-2609.
32. Hukushima, K.; Nemoto, K. Exchange Monte Carlo method and application to spin glass simulations. J. Phys. Soc. Jpn. 1996, 65, 1604-1608.
33. Sugita, Y.; Okamoto, Y. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 1999, 314, 141-151.
34. Sugita, Y.; Okamoto, Y. Replica-exchange multicanonical algorithm and multicanonical replica-exchange method for simulating systems with rough energy landscapes. Chem. Phys. Lett. 2000, 329, 261-270.
35. Press: W. H.; Teukolsky, S. A.; Vetterling, W. T.; Flannery, B. P. Numerical Recipes in C: The Art of Scientific Computing, 2nd ed.; Cambridge University Press: Cambridge, 2002.
36. Ohkubo, Y. Z.; Brooks, C. L., III Exploring Flory's isolated-pair hypothesis: Statistical mechanics of helix-coil transitions in polyalanine and the C-peptide from RNase A. Proc. Natl. Acad. Sci. 2003, 100, 13916-13921.
37. Hansmann, U. H. E.; Okamoto, Y. Finite-size scaling of helix-coil transitions in poly-alanine studied by multicanonical simulations. J. Chem. Phys. 1999, 110, 1267-1276.
38. Mitsutake, A.; Okamoto, Y. Helix-coil transitions of amino-acid homo-oligomers in aqueous solution studied by multi-canonical simulations. J. Chem. Phys. 1999, 122, 10638-10647.
39. van Giessen, A. E.; J. E. Straub, J. E. Monte Carlo simulations of polyalanine using a reduced model and statistics-based interaction potentials. J. Chem. Phys. 2005, 122, 024904.
40. Bredenbeck, J.; Helbing, J.; Kumita, J. R.; Woolley, G. A.; Hamm, P. α-Helix formation in a photoswitchable peptide tracked from picoseconds to microseconds by time-resolved IR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 2379-2384.
41. Goldbeck, R. A.; Thomas, Y. G.; Chen, E.; Esquerra, R. M.; D. S. Kliger, D. S. Multiple pathways on a protein-folding energy landscape: kinetic evidence. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 2782-2787.
42. Nymeyer, H.; Garcia, A. E. Simulation of the folding equilibrium of α-helical peptides: a comparison of the generalized Born approximation with explicit solvent. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13934-13939.