Universality in the timescales of internal loop formation in unfolded proteins and single-stranded oligonucleotides

Biophysical Journal

Volumn 99, Issue 12, 2010, Pages 3959-3968

  Cheng, Ryan R ^a   Uzawa, Takanori ^b,d   Plaxco, Kevin W ^c   Makarov, Dmitrii E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78650099766     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.11.017     Document Type: Article

References (72)

1. Bieri, O., J. Wirz,., T. Kiefhaber. 1999. The speed limit for protein folding measured by triplet-triplet energy transfer. Proc. Natl. Acad. Sci. USA. 96:9597-9601.
2. Thirumalai, D. 1999. Time scales for the formation of the most probable tertiary contacts in proteins with applications to cytochrome c. J. Phys. Chem. B. 103:608-610.
3. Hagen, S. J., J. Hofrichter,., W. A. Eaton. 1996. Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding. Proc. Natl. Acad. Sci. USA. 93:11615-11617.
4. Makarov, D. E., and K. W. Plaxco. 2003. The topomer search model: a simple, quantitative theory of two-state protein folding kinetics. Protein Sci. 12:17-26.
5. Uzawa, T., C. Nishimura,., P. E. Wright. 2008. Hierarchical folding mechanism of apomyoglobin revealed by ultra-fast H/D exchange coupled with 2D NMR. Proc. Natl. Acad. Sci. USA. 105:13859-13864.
6. Wright, P. E., and H. J. Dyson. 1999. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293:321-331.
7. Plaxco, K. W., K. T. Simons, and D. Baker. 1998. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277:985-994.
8. Plaxco, K. W., K. T. Simons,., D. Baker. 2000. Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry. 39:11177-11183.
9. Makarov, D. E., C. A. Keller,., H. Metiu. 2002. How the folding rate constant of simple, single-domain proteins depends on the number of native contacts. Proc. Natl. Acad. Sci. USA. 99:3535-3539.
10. Oh, K. J., K. J. Cash, and K. W. Plaxco. 2009. Beyond molecular beacons: optical sensors based on the binding-induced folding of proteins and polypeptides. Chemistry. 15:2244-2251.
11. Lubin, A. A., and K. W. Plaxco. 2010. Folding-based electrochemical biosensors: the case for responsive nucleic acid architectures. Acc. Chem. Res. 43:496-505.
12. Fan, C., K. W. Plaxco, and A. J. Heeger. 2003. Electrochemical interrogation of conformational changes as a reagentless method for the sequence-specific detection of DNA. Proc. Natl. Acad. Sci. USA. 100:9134-9137.
13. Ricci, F., R. Y. Lai, and K. W. Plaxco. 2007. Linear, redox modified DNA probes as electrochemical DNA sensors. Chem. Commun. (Camb.). 36:3768-3770.
14. Jha, A. K., A. Colubri,., T. R. Sosnick. 2005. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc. Natl. Acad. Sci. USA. 102:13099-13104.
15. Shortle, D., and M. S. Ackerman. 2001. Persistence of native-like topology in a denatured protein in 8 M urea. Science. 293:487-489.
16. Andrec, M., A. K. Felts,., R. M. Levy. 2005. Protein folding pathways from replica exchange simulations and a kinetic network model. Proc. Natl. Acad. Sci. USA. 102:6801-6806.
17. Zagrovic, B., and V. S. Pande. 2003. How can proteins be unfolded and yet have native-like properties: structural correspondence between the α-helix and the random-flight chain. Nat. Struct. Biol. 10:955-961.
18. McCarney, E. R., J. H. Werner,., K. W. Plaxco. 2005. Site-specific dimensions across a highly denatured protein; a single molecule study. J. Mol. Biol. 352:672-682.
19. Millett, I. S., S. Doniach, and K. W. Plaxco. 2002. Toward a taxonomy of the denatured state: small angle scattering studies of unfolded proteins. Adv. Protein Chem. 62:241-262.
20. Nettels, D., I. V. Gopich,., B. Schuler. 2007. Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc. Natl. Acad. Sci. USA. 104:2655-2660. (Pubitemid 46327935)
21. Nettels, D., A. Hoffmann, and B. Schuler. 2008. Unfolded protein and peptide dynamics investigated with single-molecule FRETand correlation spectroscopy from picoseconds to seconds. J. Phys. Chem. B. 112:6137-6146.
22. Schuler, B., and W. A. Eaton. 2008. Protein folding studied by singlemolecule FRET. Curr. Opin. Struct. Biol. 18:16-26.
23. Camacho, C. J., and D. Thirumalai. 1995. Theoretical predictions of folding pathways by using the proximity rule, with applications to bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. USA. 92: 1277-1281.
24. Doi, M. 1975. Diffusion controlled reaction of polymers. Chem. Phys. 9:455-466.
25. Feige, M. J., and E. Paci. 2008. Rate of loop formation in peptides: a simulation study. J. Mol. Biol. 382:556-565.
26. Guo, Z., and D. Thirumalai. 1995. Kinetics of protein folding: nucleation mechanism, time scales, and pathways. Biopolymers. 36:83-102.
27. Lapidus, L. J., P. J. Steinbach,., J. Hofrichter. 2002. Effects of chain stiffness on the dynamics of loop formation in polypeptides. Appendix: Testing a one-dimensional diffusion model for peptide dynamics. J. Phys. Chem. B. 106:11628-11640.
28. Pastor, R. W., R. Zwanzig, and A. Szabo. 1996. Diffusion limited first contact of the ends of a polymer: comparison of theory with simulation. J. Chem. Phys. 105:3878-3882.
29. Perico, A., and M. Beggiato. 1990. Intramolecular diffusion controlled reactions in polymers in the optimized Rouse-Zimm approach. 1. The effects of chain stiffness, reactive site positions, and site numbers. Macromolecules. 23:797-803.
30. Podtelezhnikov, A., and A. Vologodskii. 1997. Simulations of polymer cyclization by Brownian dynamics. Macromolecules. 30:6668-6673.
31. Portman, J. 2003. Non-Gaussian dynamics from a simulation of a short peptide: loop closure rates and effective diffusion coefficients. J. Chem. Phys. 118:2381-2391.
32. Szabo, A., K. Schulten, and Z. Schulten. 1980. First passage time approach to diffusion controlled reactions. J. Chem. Phys. 72:4350-4357.
33. Toan, N. M., G. Morrison,., D. Thirumalai. 2008. Kinetics of loop formation in polymer chains. J. Phys. Chem. B. 112:6094-6106.
34. Wang, Z. S., and D. E. Makarov. 2002. Rate of intramolecular contact formation in peptides: the loop length dependence. J. Chem. Phys. 117:4591-4593.
35. Wilemski, G., and M. Fixman. 1974. Diffusion-controlled intrachain reactions of polymers. I. Theory. J. Chem. Phys. 60:866-877.
36. Wilemski, G., and M. Fixman. 1974. Diffusion-controlled intrachain reactions of polymers. II. Results for a pair of terminal reactive groups. J. Chem. Phys. 60:878-890.
37. Yeh, I. C., and G. Hummer. 2002. Peptide loop-closure kinetics from microsecond molecular dynamics simulations in explicit solvent. J. Am. Chem. Soc. 124:6563-6568.
38. Lapidus, L. J.,W. A. Eaton, and J. Hofrichter. 2000. Measuring the rate of intramolecular contact formation in polypeptides. Proc. Natl. Acad. Sci. USA. 97:7220-7225.
39. Wang, X. J., and W. M. Nau. 2004. Kinetics of end-to-end collision in short single-stranded nucleic acids. J. Am. Chem. Soc. 126:808-813.
40. Soranno, A., R. Longhi,., M. Buscaglia. 2009. Kinetics of contact formation and end-to-end distance distributions of swollen disordered peptides. Biophys. J. 96:1515-1528.
41. Uzawa, T., R. R. Cheng,., K. W. Plaxco. 2009. The length and viscosity dependence of end-to-end collision rates in single-stranded DNA. Biophys. J. 97:205-210.
42. Daidone, I., H. Neuweiler,., J. C. Smith. 2010. Hydrogen-bond driven loop-closure kinetics in unfolded polypeptide chains. PLOS Comput. Biol. 6:e1000645.
43. Buscaglia, M., L. J. Lapidus,., J. Hofrichter. 2006. Effects of denaturants on the dynamics of loop formation in polypeptides. Biophys. J. 91:276-288.
44. Fierz, B., and T. Kiefhaber. 2007. End-to-end vs interior loop formation kinetics in unfolded polypeptide chains. J. Am. Chem. Soc. 129: 672-679. (Pubitemid 46147768)
45. Qu, P., X. Yang,., X. S. Zhao. 2010. Direct measurement of the rates and barriers on forward and reverse diffusions of intramolecular collision in overhang oligonucleotides. J. Phys. Chem. B. 114:8235-8243.
46. Friedman, B., and B. O'Shaughnessy. 1993. Theory of intramolecular reactions in polymeric liquids. Macromolecules. 26:4888-4898.
47. Ortiz-Repiso, M., J. J. Freire, and A. Rey. 1998. Intramolecular reaction rates of flexible polymers. 1. Simulation results and the classical theory. Macromolecules. 31:8356-8362. (Pubitemid 128563524)
48. Sheng, Y.-J., P.-H. Hsu,., H.-K. Tsao. 2004. Loop formation of a flexible polymer with two random reactive sites. Macromolecules. 37:9257-9263.
49. Doucet, D., A. Roitberg, and S. J. Hagen. 2007. Kinetics of internalloop formation in polypeptide chains: a simulation study. Biophys. J. 92:2281-2289.
50. Reiner, A., P. Henklein, and T. Kiefhaber. 2010. An unlocking/relocking barrier in conformational fluctuations of villin headpiece subdomain. Proc. Natl. Acad. Sci. USA. 107:4955-4960.
51. Waldauer, S. A., O. Bakajin, and L. J. Lapidus. 2010. Extremely slow intramolecular diffusion in unfolded protein L. Proc. Natl. Acad. Sci. USA. 107:13713-13717.
52. Hyeon, C., and D. Thirumalai. 2006. Kinetics of interior loop formation in semiflexible chains. J. Chem. Phys. 124:104905.
53. Doi, M., and S. F. Edwards. 1986. The Theory of Polymer Dynamics. Oxford Press, New York; Clarendon Press, New York; Oxford University Press, Oxford, UK, 391.
54. Chan, H. S., and K. Dill. 1988. Intrachain loops in polymers: effects of excluded volume. J. Chem. Phys. 90:492-509.
55. Gaines, G. L. 1979. Coulombic effects in the quenching of photoexcited tris(2,2′-bipyridine)ruthenium(II) and related complexes by methyl viologen. J. Phys. Chem. 83:3088-3091.
56. Yonemoto, E. H., G. B. Saupe,., T. E. Mallouk. 1994. Electron-transfer reactions of ruthenium trisbipyridyl-viologen donor-acceptor molecules: comparison of the distance dependence of electron transfer-rates in the normal and Marcus inverted regions. J. Am. Chem. Soc. 116:4786-4795.
57. Flechsig, G.-U., J. Peter,., P. Gründler. 2005. Electrochemical DNA hybridization detection using the fluorescence quenching label DABCYL. Electrochem. Comm. 7:1059-1065.
58. Monk, P. M. S. 1999. The viologens: physicochemical properties. In Synthesis and Applications of the Salts of 4,4′-Bipyridine. John Wiley and Sons, Chichester, UK.
59. Cheng, R. R., and D. E. Makarov. 2010. End-to-surface reaction dynamics of a single surface-attached DNA or polypeptide. J. Phys. Chem. B. 114:3321-3329.
60. Cheng, R. R., T. Uzawa,., D. E. Makarov. 2009. The rate of intramolecular loop formation in DNA and polypeptides: the absence of the diffusion-controlled limit and fractional power-law viscosity dependence. J. Phys. Chem. B. 113:14026-14034.
61. Ermak, D. L., and J. A. McCammon. 1978. Brownian dynamics with hydrodynamic interactions. J. Chem. Phys. 69:1352-1360.
62. Rotne, J., and S. Prager. 1969. Variational treatment of hydrodynamic interaction in polymers. J. Chem. Phys. 50:4831-4837.
63. Reference deleted in proof.
64. Ortiz-Repiso, M., and A. Rey. 1998. Intramolecular reaction rates of flexible polymers. 2. Comparison with the renormalization group theory. Macromolecules. 31:8363-8369. (Pubitemid 128563525)
65. Makarov, D. E. 2010. Spatiotemporal correlations in denatured proteins: the dependence of fluorescence resonance energy transfer (FRET)-derived protein reconfiguration times on the location of the FRET probes. J. Chem. Phys. 132:035104.
66. De Gennes, P. G. 1979. Scaling Concepts in Polymer Physics. Cornell University Press, Ithaca, NY.
67. Oono, Y., and T. Ohta. 1981. The distribution function for internal distances in a self-avoiding polymer chain. Phys. Lett. A. 85:480-482.
68. Friedman, B., and B. O'Shaughnessy. 1991. Short-time behavior and universal relations in polymer cyclization. J. Phys. II. 1:471-486.
69. Kim, J. H., W. Lee,., S. Lee. 2008. Excluded volume effects on the intrachain reaction kinetics. J. Phys. Chem. B. 112:6250-6258.
70. Fierz, B., A. Reiner, and T. Kiefhaber. 2009. Local conformational dynamics in α-helices measured by fast triplet transfer. Proc. Natl. Acad. Sci. USA. 106:1057-1062.
71. Fitzkee, N. C., and G. D. Rose. 2004. Reassessing random-coil statistics in unfolded proteins. Proc. Natl. Acad. Sci. USA. 101:12497-12502.
72. Wang, Z., K. W. Plaxco, and D. E. Makarov. 2007. Influence of local and residual structures on the scaling behavior and dimensions of unfolded proteins. Biopolymers. 86:321-328.