Low folding cooperativity of Hp35 revealed by single-molecule force spectroscopy and molecular dynamics simulation

Biophysical Journal

Volumn 102, Issue 8, 2012, Pages 1944-1951

  Lv, Chunmei ^a   Tan, Cheng ^a   Qin, Meng ^a   Zou, Dawei ^a   Cao, Yi ^a   Wang, Wei ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; VILLIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; HUMAN; KINETICS; MECHANICS; MOLECULAR DYNAMICS; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN TERTIARY STRUCTURE;

HUMANS; KINETICS; MECHANICAL PROCESSES; MICROFILAMENT PROTEINS; MICROSCOPY, ATOMIC FORCE; MOLECULAR DYNAMICS SIMULATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84859924251     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.03.028     Document Type: Article

References (73)

1. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nat. Struct. Biol. 4 1997 10 19 (Pubitemid 27020916)
2. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366 (Pubitemid 44118036)
3. V. Muñoz Conformational dynamics and ensembles in protein folding Annu. Rev. Biophys. Biomol. Struct. 36 2007 395 412 (Pubitemid 46998125)
4. J. Kubelka, W.A. Eaton, and J. Hofrichter Experimental tests of villin subdomain folding simulations J. Mol. Biol. 329 2003 625 630 (Pubitemid 36629358)
5. W. Vermeulen, and P. Vanhaesebrouck F.A. Borremans Solution structures of the C-terminal headpiece subdomains of human villin and advillin, evaluation of headpiece F-actin-binding requirements Protein Sci. 13 2004 1276 1287 (Pubitemid 38526092)
6. Y. Duan, and P.A. Kollman Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution Science 282 1998 740 744 (Pubitemid 28489385)
7. H. Lei, and C. Wu Y. Duan Folding free-energy landscape of villin headpiece subdomain from molecular dynamics simulations Proc. Natl. Acad. Sci. USA 104 2007 4925 4930 (Pubitemid 47186153)
8. S. Piana, K. Lindorff-Larsen, and D.E. Shaw How robust are protein folding simulations with respect to force field parameterization? Biophys. J. 100 2011 L47 L49
9. B. Zagrovic, and V.S. Pande Simulated unfolded-state ensemble and the experimental NMR structures of villin headpiece yield similar wide-angle solution x-ray scattering profiles J. Am. Chem. Soc. 128 2006 11742 11743 (Pubitemid 44360195)
10. M.R. Bunagan, and J. Gao F. Gai Probing the folding transition state structure of the villin headpiece subdomain via side chain and backbone mutagenesis J. Am. Chem. Soc. 131 2009 7470 7476
11. K.N. Hu, W.M. Yau, and R. Tycko Detection of a transient intermediate in a rapid protein folding process by solid-state nuclear magnetic resonance J. Am. Chem. Soc. 132 2010 24 25
12. J.K. Chung, M.C. Thielges, and M.D. Fayer Dynamics of the folded and unfolded villin headpiece (HP35) measured with ultrafast 2D IR vibrational echo spectroscopy Proc. Natl. Acad. Sci. USA 108 2011 3578 3583
13. T. Cellmer, and M. Buscaglia W.A. Eaton Making connections between ultrafast protein folding kinetics and molecular dynamics simulations Proc. Natl. Acad. Sci. USA 108 2011 6103 6108
14. M. Rief, and M. Gautel H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112 (Pubitemid 27218118)
15. J.M. Fernandez, and H. Li Force-clamp spectroscopy monitors the folding trajectory of a single protein Science 303 2004 1674 1678 (Pubitemid 38338326)
16. N.C. Harris, Y. Song, and C.H. Kiang Experimental free energy surface reconstruction from single-molecule force spectroscopy using Jarzynski's equality Phys. Rev. Lett. 99 2007 068101
17. A. Borgia, P.M. Williams, and J. Clarke Single-molecule studies of protein folding Annu. Rev. Biochem. 77 2008 101 125
18. I. Schwaiger, and M. Schleicher M. Rief The folding pathway of a fast-folding immunoglobulin domain revealed by single-molecule mechanical experiments EMBO Rep. 6 2005 46 51 (Pubitemid 41710073)
19. M. Schlierf, and M. Rief Surprising simplicity in the single-molecule folding mechanics of proteins Angew. Chem. Int. Ed. Engl. 48 2009 820 822
20. S. Garcia-Manyes, L. Dougan, and J.M. Fernández Osmolyte-induced separation of the mechanical folding phases of ubiquitin Proc. Natl. Acad. Sci. USA 106 2009 10540 10545
21. S. Garcia-Manyes, and L. Dougan J.M. Fernández Direct observation of an ensemble of stable collapsed states in the mechanical folding of ubiquitin Proc. Natl. Acad. Sci. USA 106 2009 10534 10539
22. J.M. Nunes, and U. Hensen D.J. Muller A "force buffer" protecting immunoglobulin titin Angew. Chem. Int. Ed. Engl. 49 2010 3528 3531
23. E.M. Puchner, and H.E. Gaub Force and function: probing proteins with AFM-based force spectroscopy Curr. Opin. Struct. Biol. 19 2009 605 614
24. M. Carrion-Vazquez, and A.F. Oberhauser J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl. Acad. Sci. USA 96 1999 3694 3699 (Pubitemid 29168972)
25. H.B. Li Mechanical engineering of elastomeric proteins: toward designing new protein building blocks for biomaterials Adv. Funct. Mater. 18 2008 2643 2657
26. E. Paci, and M. Karplus Unfolding proteins by external forces and temperature: the importance of topology and energetics Proc. Natl. Acad. Sci. USA 97 2000 6521 6526 (Pubitemid 30412746)
27. M. Sotomayor, and K. Schulten Single-molecule experiments in vitro and in silico Science 316 2007 1144 1148 (Pubitemid 46877468)
28. M. Bertz, and M. Rief Mechanical unfoldons as building blocks of maltose-binding protein J. Mol. Biol. 378 2008 447 458
29. L. Li, and H.H. Huang J.M. Fernandez Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module J. Mol. Biol. 345 2005 817 826 (Pubitemid 39600935)
30. M. Damaghi, and S. Köster D.J. Müller One β hairpin follows the other: exploring refolding pathways and kinetics of the transmembrane β-barrel protein OmpG Angew. Chem. Int. Ed. Engl. 50 2011 7422 7424
31. Q. Peng, and J. Fang H. Li Kinetic partitioning mechanism governs the folding of the third FnIII domain of tenascin-C: evidence at the single-molecule level J. Mol. Biol. 412 2011 698 709
32. M. Mickler, and R.I. Dima M. Rief Revealing the bifurcation in the unfolding pathways of GFP by using single-molecule experiments and simulations Proc. Natl. Acad. Sci. USA 104 2007 20268 20273
33. H. Dietz, and F. Berkemeier M. Rief Anisotropic deformation response of single protein molecules Proc. Natl. Acad. Sci. USA 103 2006 12724 12728 (Pubitemid 44298628)
34. E.A. Shank, and C. Cecconi C. Bustamante The folding cooperativity of a protein is controlled by its chain topology Nature 465 2010 637 640
35. C. Hyeon, and G. Morrison D. Thirumalai Refolding dynamics of stretched biopolymers upon force quench Proc. Natl. Acad. Sci. USA 106 2009 20288 20293
36. G. Yang, and C. Cecconi C. Bustamante Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme Proc. Natl. Acad. Sci. USA 97 2000 139 144 (Pubitemid 30055797)
37. M. Schlierf, and M. Rief Temperature softening of a protein in single-molecule experiments J. Mol. Biol. 354 2005 497 503 (Pubitemid 41579861)
38. Y. Taniguchi, D.J. Brockwell, and M. Kawakami The effect of temperature on mechanical resistance of the native and intermediate states of I27 Biophys. J. 95 2008 5296 5305
39. L. Ma, M. Xu, and A.F. Oberhauser Naturally occurring osmolytes modulate the nanomechanical properties of polycystic kidney disease domains J. Biol. Chem. 285 2010 38438 38443
40. Y. Cao, and H. Li How do chemical denaturants affect the mechanical folding and unfolding of proteins? J. Mol. Biol. 375 2008 316 324 (Pubitemid 350160691)
41. A.F. Oberhauser, and P.E. Marszalek J.M. Fernandez Single protein misfolding events captured by atomic force microscopy Nat. Struct. Biol. 6 1999 1025 1028 (Pubitemid 29519595)
42. Y. Cao, and H. Li Polyprotein of GB1 is an ideal artificial elastomeric protein Nat. Mater. 6 2007 109 114 (Pubitemid 46197646)
43. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
44. Y. Cao, and C. Lam H. Li Nonmechanical protein can have significant mechanical stability Angew. Chem. Int. Ed. Engl. 45 2006 642 645 (Pubitemid 43121465)
45. H. Li, and A.F. Oberhauser J.M. Fernandez Atomic force microscopy reveals the mechanical design of a modular protein Proc. Natl. Acad. Sci. USA 97 2000 6527 6531 (Pubitemid 30412747)
46. Y. Cao, and H. Li Engineered elastomeric proteins with dual elasticity can be controlled by a molecular regulator Nat. Nanotechnol. 3 2008 512 516
47. J.P. Junker, F. Ziegler, and M. Rief Ligand-dependent equilibrium fluctuations of single calmodulin molecules Science 323 2009 633 637
48. M. Kim, and K. Abdi P.E. Marszalek Fast and forceful refolding of stretched alpha-helical solenoid proteins Biophys. J. 98 2010 3086 3092
49. G. Lee, and K. Abdi P.E. Marszalek Nanospring behaviour of ankyrin repeats Nature 440 2006 246 249 (Pubitemid 43372106)
50. M. Schlierf, F. Berkemeier, and M. Rief Direct observation of active protein folding using lock-in force spectroscopy Biophys. J. 93 2007 3989 3998 (Pubitemid 350223814)
51. J.F. Marko, and E.D. Siggia Stretching DNA Macromolecules 28 1995 8759 8770
52. H. Li, and A.F. Oberhauser J.M. Fernandez Multiple conformations of PEVK proteins detected by single-molecule techniques Proc. Natl. Acad. Sci. USA 98 2001 10682 10686 (Pubitemid 32878681)
53. J.H. Cho, and N. O'Connell A.G. Palmer 3rd Phi-value analysis for ultrafast folding proteins by NMR relaxation dispersion J. Am. Chem. Soc. 132 2010 450 451
54. E. Evans, and K. Ritchie Strength of a weak bond connecting flexible polymer chains Biophys. J. 76 1999 2439 2447 (Pubitemid 29264606)
55. H. Lu, and K. Schulten The key event in force-induced unfolding of Titin's immunoglobulin domains Biophys. J. 79 2000 51 65 (Pubitemid 30436727)
56. D.J. Brockwell, and G.S. Beddard S.E. Radford Mechanically unfolding the small, topologically simple protein L Biophys. J. 89 2005 506 519 (Pubitemid 41098304)
57. R.B. Best, and B. Li J. Clarke Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation Biophys. J. 81 2001 2344 2356 (Pubitemid 32917181)
58. S.P. Ng, and R.W. Rounsevell J. Clarke Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation J. Mol. Biol. 350 2005 776 789 (Pubitemid 40848674)
59. D. Sharma, and G. Feng H. Li Stabilization provided by neighboring strands is critical for the mechanical stability of proteins Biophys. J. 95 2008 3935 3942
60. Y. Tang, M.J. Goger, and D.P. Raleigh NMR characterization of a peptide model provides evidence for significant structure in the unfolded state of the villin headpiece helical subdomain Biochemistry 45 2006 6940 6946 (Pubitemid 43856678)
61. W. Meng, and B. Shan D.P. Raleigh Native like structure in the unfolded state of the villin headpiece helical subdomain, an ultrafast folding protein Protein Sci. 18 2009 1692 1701
62. J.K. Myers, and T.G. Oas Preorganized secondary structure as an important determinant of fast protein folding Nat. Struct. Biol. 8 2001 552 558 (Pubitemid 32525017)
63. N. Ferguson, and T.D. Sharpe A.R. Fersht Ultra-fast barrier-limited folding in the peripheral subunit-binding domain family J. Mol. Biol. 353 2005 427 446 (Pubitemid 41356622)
64. S. Chowdhury, H. Lei, and Y. Duan Denatured-state ensemble and the early-stage folding of the G29A mutant of the B-domain of protein A J. Phys. Chem. B 109 2005 9073 9081 (Pubitemid 40750944)
65. V. Daggett, and A.R. Fersht Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28 2003 18 25 (Pubitemid 36051002)
66. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208 (Pubitemid 40314921)
67. N. Crampton, and K. Alzahrani D.J. Brockwell Mechanically unfolding protein L using a laser-feedback-controlled cantilever Biophys. J. 100 2011 1800 1809
68. H. Dietz, and M. Rief Exploring the energy landscape of GFP by single-molecule mechanical experiments Proc. Natl. Acad. Sci. USA 101 2004 16192 16197 (Pubitemid 39552821)
69. K. Arnold, and L. Bordoli T. Schwede The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201 (Pubitemid 43205406)
70. T. Schwede, and J. Kopp M.C. Peitsch SWISS-MODEL: an automated protein homology-modeling server Nucleic Acids Res. 31 2003 3381 3385 (Pubitemid 37442164)
71. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723 (Pubitemid 28059943)
72. C. Bustamante, and J.F. Marko S. Smith Entropic elasticity of lambda-phage DNA Science 265 1994 1599 1600
73. R.B. Best, and G. Hummer Protein folding kinetics under force from molecular simulation J. Am. Chem. Soc. 130 2008 3706 3707 (Pubitemid 351429809)