Folding simulations of a de Novo designed protein with a βαβ fold

Biophysical Journal

Volumn 98, Issue 2, 2010, Pages 321-329

  Qi, Yifei ^a   Huang, Yongqi ^a   Liang, Huanhuan ^a   Liu, Zhirong ^a   Lai, Luhua ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77049109643     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.10.018     Document Type: Article

References (66)

1. Duan, Y., and P. A. Kollman. 1998. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science. 282:740-744.
2. Kubelka, J., J. Hofrichter, and W. A. Eaton. 2004. The protein folding "speed limit". Curr. Opin. Struct. Biol. 14:76-88.
3. Lei, H., X. Deng, ., Y. Duan. 2008. The fast-folding HP35 double mutant has a substantially reduced primary folding free energy barrier. J. Chem. Phys. 129:155104.
4. Lei, H., and Y. Duan. 2007. Two-stage folding of HP-35 from ab initio simulations. J. Mol. Biol. 370:196-206.
5. Jayachandran, G., V. Vishal, and V. S. Pande. 2006. Using massively parallel simulation and Markovian models to study protein folding: examining the dynamics of the villin headpiece. J. Chem. Phys. 124:164902.
6. Zagrovic, B., C. D. Snow,., V. S. Pande. 2002. Simulation of folding of a small a-helical protein in atomistic detail using worldwide-distributed computing. J. Mol. Biol. 323:927-937.
7. Lei, H., and Y. Duan. 2007. Ab initio folding of albumin binding domain from all-atom molecular dynamics simulation. J. Phys. Chem. B. 111:5458-5463.
8. Jang, S., E. Kim, ., Y. Pak. 2003. Ab initio folding of helix bundle proteins using molecular dynamics simulations. J. Am. Chem. Soc. 125:14841-14846.
9. Vila, J. A., D. R. Ripoll, and H. A. Scheraga. 2003. Atomically detailed folding simulation of the B domain of staphylococcal protein A from random structures. Proc. Natl. Acad. Sci. USA. 100:14812-14816.
10. Lei, H., C. Wu, ., Y. Duan. 2008. Folding processes of the B domain of protein A to the native state observed in all-atom ab initio folding simulations. J. Chem. Phys. 128:235105.
11. Jagielska, A., and H. A. Scheraga. 2007. Influence of temperature, friction, and random forces on folding of the B-domain of staphylococcal protein A: all-atom molecular dynamics in implicit solvent. J. Comput. Chem. 28:1068-1082.
12. Chowdhury, S., M. C. Lee, ., Y. Duan. 2003. Ab initio folding simulation of the Trp-cage mini-protein approaches NMR resolution. J. Mol. Biol. 327:711-717.
13. Paschek, D., H. Nymeyer, and A. E. García. 2007. Replica exchange simulation of reversible folding/unfolding of the Trp-cage miniprotein in explicit solvent: on the structure and possible role of internal water. J. Struct. Biol. 157:524-533.
14. Zhou, R. 2003. Trp-cage: folding free energy landscape in explicit water. Proc. Natl. Acad. Sci. USA. 100:13280-13285.
15. Li, H., R. Helling, ., N. Wingreen. 1996. Emergence of preferred structures in a simple model of protein folding. Science. 273:666-669.
16. Liang, H., H. Chen, ., L. Lai. 2009. De novo design of a βαβ motif. Angew. Chem. Int. Ed. Engl. 48:3301-3303.
17. Butterfoss, G. L., and B. Kuhlman. 2006. Computer-based design of novel protein structures. Annu. Rev. Biophys. Biomol. Struct. 35:49-65.
18. Kuhlman, B., G. Dantas, ., D. Baker. 2003. Design of a novel globular protein fold with atomic-level accuracy. Science. 302: 1364-1368.
19. Dahiyat, B. I., and S. L. Mayo. 1997. De novo protein design: fully automated sequence selection. Science. 278:82-87.
20. Summa, C. M., M. M. Rosenblatt, ., W. F. DeGrado. 2002. Computational de novo design, and characterization of an A(2)B(2) diiron protein. J. Mol. Biol. 321:923-938.
21. Watters, A. L., P. Deka, ., D. Baker. 2007. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell. 128:613-624.
22. Zhang, Z., and H. S. Chan. 2009. Native topology of the designed protein Top7 is not conducive to cooperative folding. Biophys. J. 96:L25-L27.
23. Case, D. A., T. E. Cheatham, 3rd, ., R. J. Woods. 2005. The Amber biomolecular simulation programs. J. Comput. Chem. 26:1668-1688.
24. Duan, Y., C. Wu, ., P. Kollman. 2003. A point-charge force field for molecular mechanics simulations of proteins based on condensedphase quantum mechanical calculations. J. Comput. Chem. 24: 1999-2012.
25. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of Cartesian equations of motion of a system with constraints: molecular dynamics of N-alkanes. J. Comput. Phys. 23:327-341.
26. Legrand, S. M., and K. M. Merz. 1993. Rapid approximation to molecular surface area via the use of Boolean logic and look-up tables. J. Comput. Chem. 14:349-352.
27. Go, N. 1983. Theoretical studies of protein folding. Annu. Rev. Biophys. Bioeng. 12:183-210.
28. Clementi, C., H. Nymeyer, and J. N. Onuchic. 2000. Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 298:937-953.
29. Liu, Z. R., and H. S. Chan. 2005. Solvation and desolvation effects in protein folding: native flexibility, kinetic cooperativity and enthalpic barriers under isostability conditions. Phys. Biol. 2:S75-S85.
30. Badasyan, A., Z. Liu, and H. S. Chan. 2009. Interplaying roles of native topology and chain length in marginally cooperative and noncooperative folding of small protein fragments. Int. J. Quantum Chem. 109:3482-3499.
31. Onufriev, A., D. Bashford, and D. A. Case. 2004. Exploring protein native states and large-scale conformational changes with a modified generalized Born model. Proteins. 55:383-394.
32. Lee, I. H., S. Y. Kim, and J. Lee. 2009. Dynamic folding pathway models of the villin headpiece subdomain (HP-36) structure. J. Comput. Chem. 31:57-65.
33. Mukherjee, S., P. Chowdhury, ., F. Gai. 2008. Folding kinetics of a naturally occurring helical peptide: implication of the folding speed limit of helical proteins. J. Phys. Chem. B. 112:9146-9150.
34. Dill, K. A., and H. S. Chan. 1997. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4:10-19.
35. Bryngelson, J. D., J. N. Onuchic, ., P. G. Wolynes. 1995. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins. 21:167-195.
36. Ueda, Y., H. Taketomi, and N. Go. 1978. Studies on protein folding, unfolding, and fluctuations by computer simulation. 2. 3-Dimensional lattice model of lysozyme. Biopolymers. 17:1531-1548.
37. Koga, N., and S. Takada. 2001. Roles of native topology and chainlength scaling in protein folding: a simulation study with a Go-like model. J. Mol. Biol. 313:171-180.
38. Badasyan, A., Z. Liu, and H. S. Chan. 2008. Probing possible downhill folding: native contact topology likely places a significant constraint on the folding cooperativity of proteins with approximately 40 residues. J. Mol. Biol. 384:512-530.
39. Kaya, H., and H. S. Chan. 2003. Solvation effects and driving forces for protein thermodynamic and kinetic cooperativity: how adequate is native-centric topological modeling? J. Mol. Biol. 326:911-931.
40. Cho, S. S., P. Weinkam, and P. G. Wolynes. 2008. Origins of barriers and barrierless folding in BBL. Proc. Natl. Acad. Sci. USA. 105: 118-123.
41. Ferguson, A., Z. Liu, and H. S. Chan. 2009. Desolvation barrier effects are a likely contributor to the remarkable diversity in the folding rates of small proteins. J. Mol. Biol. 389:619-636.
42. Turjanski, A. G., J. S. Gutkind,., G. Hummer. 2008. Binding-induced folding of a natively unstructured transcription factor. PLOS Comput. Biol. 4:e1000060.
43. Huang, Y., and Z. Liu. 2009. Kinetic advantage of intrinsically disordered proteins in coupled folding-binding process: a critical assessment of the "fly-casting" mechanism. J. Mol. Biol. 393:1143-1159.
44. Baker, D. 2000. A surprising simplicity to protein folding. Nature. 405:39-42.
45. 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.
46. Knott, M., and H. S. Chan. 2006. Criteria for downhill protein folding: calorimetry, chevron plot, kinetic relaxation, and single-molecule radius of gyration in chain models with subdued degrees of cooperativity. Proteins. 65:373-391.
47. Kaya, H., and H. S. Chan. 2000. Polymer principles of protein calorimetric two-state cooperativity. Proteins. 40:637-661.
48. Sadqi, M., D. Fushman, and V. Muñoz. 2006. Atom-by-atom analysis of global downhill protein folding. Nature. 442:317-321.
49. Gruebele, M. 2005. Downhill protein folding: evolution meets physics. C. R. Biol. 328:701-712.
50. Liu, F., D. G. Du,., M. Gruebele. 2008. An experimental survey of the transition between two-state and downhill protein folding scenarios. Proc. Natl. Acad. Sci. USA. 105:2369-2374.
51. Garcia-Mira, M. M., M. Sadqi,., V. Muñoz. 2002. Experimental identification of downhill protein folding. Science. 298:2191-2195.
52. Chavez, L. L., J. N. Onuchic, and C. Clementi. 2004. Quantifying the roughness on the free energy landscape: entropic bottlenecks and protein folding rates. J. Am. Chem. Soc. 126:8426-8432.
53. Jackson, S. E., and A. R. Fersht. 1991. Folding of chymotrypsin inhibitor-2. 1. Evidence for a 2-state transition. Biochemistry. 30:10428-10435.
54. Scalley, M. L., and D. Baker. 1997. Protein folding kinetics exhibit an Arrhenius temperature dependence when corrected for the temperature dependence of protein stability. Proc. Natl. Acad. Sci. USA. 94:10636-10640.
55. Spector, S., and D. P. Raleigh. 1999. Submillisecond folding of the peripheral subunit-binding domain. J. Mol. Biol. 293:763-768.
56. Cobos, E. S., V. V. Filimonov, ., J. C. Martínez. 2003. A thermodynamic and kinetic analysis of the folding pathway of an SH3 domain entropically stabilised by a redesigned hydrophobic core. J. Mol. Biol. 328:221-233.
57. Horng, J. C., V. Moroz, and D. P. Raleigh. 2003. Rapid cooperative two-state folding of a miniature α-β protein and design of a thermostable variant. J. Mol. Biol. 326:1261-1270.
58. Ferguson, N., T. D. Sharpe, ., A. R. Fersht. 2005. Ultra-fast barrierlimited folding in the peripheral subunit-binding domain family. J. Mol. Biol. 353:427-446.
59. Wallin, S., and H. S. Chan. 2006. Conformational entropic barriers in topology-dependent protein folding: perspectives from a simple nativecentric polymer model. J. Phys. Condens. Matter. 18:S307-S328.
60. Zhu, Y., D. O. Alonso, ., F. Gai. 2003. Ultrafast folding of α3D: a de novo designed three-helix bundle protein. Proc. Natl. Acad. Sci. USA. 100:15486-15491.
61. Sadqi, M., E. de Alba, ., V. Muñoz. 2009. A designed protein as experimental model of primordial folding. Proc. Natl. Acad. Sci. USA. 106:4127-4132.
62. Gutin, A. M., V. I. Abkevich, VI, and E. I. Shakhnovich. 1996. Chain length scaling of protein folding time. Phys. Rev. Lett. 77:5433-5436.
63. Wolynes, P. G. 1997. Folding funnels and energy landscapes of larger proteins within the capillarity approximation. Proc. Natl. Acad. Sci. USA. 94:6170-6175.
64. Li, M. S., D. K. Klimov, and D. Thirumalai. 2004. Thermal denaturation and folding rates of single domain proteins: size matters. Polymer (Guildf.). 45:573-579.
65. Naganathan, A. N., and V. Muñoz. 2005. Scaling of folding times with protein size. J. Am. Chem. Soc. 127:480-481.
66. Zhu, Y., X. Fu, T. Wang, A. Tamura, S. Takada., 2004. Guiding the search for a protein's maximum rate of folding. Chem. Phys. 307: 99-109.