Direct observation of a force-induced switch in the anisotropic mechanical unfolding pathway of a protein

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 44, 2012, Pages 17820-17825

  Jagannathan, Bharat ^a   Elms, Phillip J ^a,b   Bustamante, Carlos ^a,b   Marqusee, Susan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SH3;

ANISOTROPY; ARTICLE; FORCE; GEOMETRY; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN FOLDING; SRC HOMOLOGY DOMAIN;

PROTEIN FOLDING; PROTEINS;

EID: 84868089078     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201800109     Document Type: Article

References (55)

1. Bustamante C, Chemla YR, Forde NR, Izhaky D (2004) Mechanical processes in biochemistry. Annu Rev Biochem 73:705-748.
2. Oberhauser AF, Carrion-Vazquez M (2008) Mechanical biochemistry of proteins one molecule at a time. J Biol Chem 283:6617-6621.
3. Maillard RA, et al. (2011) ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145:459-469.
4. Aubin-Tam ME, Olivares AO, Sauer RT, Baker TA, Lang MJ (2011) Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145:257-267.
5. Best RB, Fowler SB, Toca-Herrera JL, Clarke J (2002) A simple method for probing the mechanical unfolding pathway of proteins in detail. Proc Natl Acad Sci USA 99:12143-12148.
6. Cecconi C, Shank EA, Bustamante C, Marqusee S (2005) Direct observation of the three-state folding of a single protein molecule. Science 309:2057-2060.
7. Stigler J, Ziegler F, Gieseke A, Gebhardt JC, RiefM(2011) The complex folding network of single calmodulin molecules. Science 334:512-516.
8. Tinoco I, Jr, Li PT, Bustamante C (2006) Determination of thermodynamics and kinetics of RNA reactions by force. Q Rev Biophys 39:325-360.
9. Best RB, Paci E, Hummer G, Dudko OK (2008) Pulling direction as a reaction coordinate for the mechanical unfolding of single molecules. J Phys Chem B 112:5968-5976.
10. Dudko OK, Hummer G, Szabo A (2006) Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys Rev Lett 96:108101.
11. Gebhardt JCM, Bornschlögl T, Rief M (2010) Full distance-resolved folding energy landscape of one single protein molecule. Proc Natl Acad Sci USA 107:2013-2018.
12. Crampton N, Brockwell DJ (2010) Unravelling the design principles for single protein mechanical strength. Curr Opin Struct Biol 20:508-517.
13. Dietz H, Berkemeier F, Bertz M, Rief M (2006) Anisotropic deformation response of single protein molecules. Proc Natl Acad Sci USA 103:12724-12728.
14. Li H, Carrion-Vazquez M, Oberhauser AF, Marszalek PE, Fernandez JM (2000) Point mutations alter the mechanical stability of immunoglobulin modules. Nat Struct Biol 7:1117-1120.
15. Best RB, et al. (2003) Mechanical unfolding of a titin Ig domain: Structure of transition state revealed by combining atomic force microscopy, protein engineering and molecular dynamics simulations. J Mol Biol 330:867-877.
16. Brockwell DJ, et al. (2005) Mechanically unfolding the small, topologically simple protein L. Biophys J 89:506-519.
17. Paci E, KarplusM(1999) Forced unfolding of fibronectin type 3 modules: An analysis by biased molecular dynamics simulations. J Mol Biol 288:441-459.
18. Forman JR, et al. (2009) Non-native interactions are critical for mechanical strength in PKD domains. Structure 17:1582-1590.
19. Williams PM, et al. (2003) Hidden complexity in the mechanical properties of titin. Nature 422:446-449.
20. Fowler SB, et al. (2002) Mechanical unfolding of a titin Ig domain: Structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering. J Mol Biol 322:841-849.
21. Lu H, Isralewitz B, Krammer A, Vogel V, Schulten K (1998) Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys J 75:662-671.
22. Marszalek PE, et al. (1999) Mechanical unfolding intermediates in titin modules. Nature 402:100-103.
23. Ng SP, et al. (2005) Mechanical unfolding of TNfn3: The unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. J Mol Biol 350:776-789.
24. Brockwell DJ, et al. (2002) The effect of core destabilization on the mechanical resistance of I27. Biophys J 83:458-472.
25. Best RB, Li B, Steward A, Daggett V, Clarke J (2001) Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys J 81:2344-2356.
26. Graham TG, Best RB (2011) Force-induced change in protein unfolding mechanism: Discrete or continuous switch? J Phys Chem B 115:1546-1561
27. Brockwell DJ, et al. (2003) Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nat Struct Biol 10:731-737.
28. Carrion-Vazquez M, et al. (2003) The mechanical stability of ubiquitin is linkage dependent. Nat Struct Biol 10:738-743.
29. Junker JP, Rief M (2010) Evidence for a broad transition-state ensemble in calmodulin folding from single-molecule force spectroscopy. Angew Chem Int Ed Engl 49:3306-3309.
30. Shank EA, Cecconi C, Dill JW, Marqusee S, Bustamante C (2010) The folding cooperativity of a protein is controlled by its chain topology. Nature 465:637-640.
31. Grantcharova VP, Baker D (1997) Folding dynamics of the src SH3 domain. Biochemistry 36:15685-15692.
32. Grantcharova VP, Riddle DS, Santiago JV, Baker D (1998) Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat Struct Biol 5:714-720.
33. Rohs R, Etchebest C, Lavery R (1999) Unraveling proteins: A molecular mechanics study. Biophys J 76:2760-2768.
34. Street TO, Courtemanche N, Barrick D (2008) Protein folding and stability using denaturants. Methods Cell Biol 84:295-325.
35. Pace CN, Shaw KL (2000) Linear extrapolation method of analyzing solvent denaturation curves. Proteins 41(Suppl 4):1-7.
36. Smith SB, Cui Y, Bustamante C (2003) Optical-trap force transducer that operates by direct measurement of light momentum. Methods Enzymol 361:134-162.
37. Cecconi C, Shank EA, Dahlquist FW, Marqusee S, Bustamante C (2008) Protein-DNA chimeras for single molecule mechanical folding studies with the optical tweezers. Eur Biophys J 37:729-738.
38. Crooks GE (1999) Entropy production fluctuation theorem and the nonequilibrium work relation for free energy differences. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60:2721-2726.
39. Collin D, et al. (2005) Verification of the Crooks fluctuation theorem and recovery of RNA folding free energies. Nature 437:231-234.
40. Bell GI (1978) Models for the specific adhesion of cells to cells. Science 200:618-627.
41. Hyeon C, Thirumalai D (2007) Measuring the energy landscape roughness and the transition state location of biomolecules using single molecule mechanical unfolding experiments. J Phys Condens Matter 19:1-27.
42. Matthews JM, Fersht AR (1995) Exploring the energy surface of protein folding by structure-reactivity relationships and engineered proteins: Observation of Hammond behavior for the gross structure of the transition state and anti-Hammond behavior for structural elements for unfolding/folding of barnase. Biochemistry 34:6805-6814.
43. Dudko OK, Hummer G, Szabo A (2008) Theory, analysis, and interpretation of singlemolecule force spectroscopy experiments. Proc Natl Acad Sci USA 105:15755-15760.
44. Li PT, Collin D, Smith SB, Bustamante C, Tinoco I, Jr (2006) Probing the mechanical folding kinetics of TAR RNA by hopping, force-jump, and force-ramp methods. Biophys J 90:250-260.
45. Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72:1541-1555.
46. Merkel R, Nassoy P, Leung A, Ritchie K, Evans E (1999) Energy landscapes of receptorligand bonds explored with dynamic force spectroscopy. Nature 397:50-53.
47. Matouschek A, Otzen DE, Itzhaki LS, Jackson SE, Fersht AR (1995) Movement of the position of the transition state in protein folding. Biochemistry 34:13656-13662.
48. Suzuki Y, Dudko OK (2010) Single-molecule rupture dynamics on multidimensional landscapes. Phys Rev Lett 104:048101.
49. Wright CF, Lindorff-Larsen K, Randles LG, Clarke J (2003) Parallel protein-unfolding pathways revealed and mapped. Nat Struct Biol 10:658-662.
50. Fersht AR, Itzhaki LS, elMasry NF, Matthews JM, Otzen DE (1994) Single versus parallel pathways of protein folding and fractional formation of structure in the transition state. Proc Natl Acad Sci USA 91:10426-10429.
51. Schlierf M, Yew ZT, Rief M, Paci E (2010) Complex unfolding kinetics of single-domain proteins in the presence of force. Biophys J 99:1620-1627.
52. Elms P, Chodera J, Bustamante C, Marqusee S (2012) The limitations of constant-forcefeedback experiments. Biophys J, 10.1016/j.bpj.2012.06.051.
53. Best RB, Hummer G (2008) Protein folding kinetics under force from molecular simulation. J Am Chem Soc 130:3706-3707.
54. Fersht AR, Matouschek A, Serrano L (1992) The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol 224:771-782.
55. Liu Z, Reddy G, O'Brien EP, Thirumalai D (2011) Collapse kinetics and chevron plots from simulations of denaturant-dependent folding of globular proteins. Proc Natl Acad Sci USA 108:7787-7792.