The effect of temperature on mechanical resistance of the native and intermediate states of I27

Biophysical Journal

Volumn 95, Issue 11, 2008, Pages 5296-5305

  Taniguchi, Yukinori ^a   Brockwell, David J ^b   Kawakami, Masaru ^a,c  

^a JAPAN ADVANCED INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; MUSCLE PROTEIN; PROTEIN KINASE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; MECHANICAL STRESS; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; THERMODYNAMICS;

MICROSCOPY, ATOMIC FORCE; MUSCLE PROTEINS; PROTEIN DENATURATION; PROTEIN KINASES; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; STRESS, MECHANICAL; TEMPERATURE; THERMODYNAMICS;

EID: 58149356274     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.141275     Document Type: Article

References (50)

1. Best, R. B., and J. Clarke. 2002. What can atomic force microscopy tell us about protein folding? Chem. Commun. 3:183-192.
2. Forman, J. R., and J. Clarke. 2007. Mechanical unfolding of proteins: insights into biology, structure and folding. Curr. Opin. Struct. Biol. 17:58-66.
3. Sotomayor, M., and K. Schulten. 2007. Single-molecule experiments in vitro and in silico. Science. 316:1144-1148.
4. Sulkowska, J. I., and M. Cieplak. 2007. Mechanical stretching of proteins - a theoretical survey of the Protein Data Bank. J. Phys. Condens. Matter. 19:283201.
5. Yang, G., C. Cecconi, W. A. Baase, I. R. Vetter, W. A. Breyer, J. A. Haack, B. W. Matthews, F. W. Dahlquist, and C. Bustamante. 2000. Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme. Proc. Natl. Acad. Sci. USA. 97:139-144.
6. Cao, Y., and H. Li. 2008. How do chemical denaturants affect the mechanical folding and unfolding of proteins? J. Mol. Biol. 375:316-324.
7. Dougan, L., and J. M. Fernandez. 2007. Tandem repeating modular proteins avoid aggregation in single molecule force spectroscopy experiments. J. Phys. Chem. A. 111:12402-12408.
8. Dougan, L., G. Feng, H. Lu, and J. M. Fernandez. 2008. Solvent molecules bridge the mechanical unfolding transition state of a protein. Proc. Natl. Acad. Sci. USA. 105:3185-3190.
9. Chyan, C. L., F. C. Lin, H. Peng, J. M. Yuan, C. H. Chang, S. H. Lin, and G. Yang. 2004. Reversible mechanical unfolding of single ubiquitin molecules. Biophys. J. 87:3995-4006.
10. Janovjak, H., M. Kessler, D. Oesterhelt, H. Gaub, and D. J. Müller. 2003. Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 22:5220-5229.
11. Law, R., G. Liao, S. Harper, G. Yang, D. W. Speicher, and D. E. Discher. 2003. Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains. Biophys. J. 85:3286-3293.
12. Schlierf, M., and M. Rief. 2005. Temperature softening of a protein in single-molecule experiments. J. Mol. Biol. 354:497-503.
13. Yang, Y., F. C. Lin, and G. Yang. 2006. Temperature control device for single molecule measurements using the atomic force microscope. Rev. Sci. Instrum. 77:063701.
14. Carrion-Vazquez, M., A. F. Oberhauser, S. B. Fowler, P. E. Marszalek, S. E. Broedel, J. Clarke, and J. M. Fernandez. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96:3694-3699.
15. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, K. Schulten, and J. M. Fernandez. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
16. Brockwell, D. J., G. S. Beddard, J. Clarkson, R. C. Zinober, A. W. Blake, J. Trinick, P. D. Olmsted, D. A. Smith, and S. E. Radford. 2002. The effect of core destabilization on the mechanical resistance of I27. Biophys. J. 83:458-472.
17. Williams, P. M., S. B. Fowler, R. B. Best, J. L. Toca-Herrera, K. A. Scott, A. Steward, and J. Clarke. 2003. Hidden complexity in the mechanical properties of titin. Nature. 422:446-449.
18. Kawakami, M., K. Byrne, D. J. Brockwell, S. E. Radford, and D. A. Smith. 2006. Viscoelastic study of the mechanical unfolding of a protein by AFM. Biophys. J. 91:L16-L18.
19. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671.
20. Li, P. C., and D. E. Makarov. 2003. Theoretical studies of the mechanical unfolding of the muscle protein titin: bridging the time-scale gap between simulation and experiment. J. Chem. Phys. 119:9260-9268.
21. Cieplak, M., T. X. Hoang, and M. O. Robbins. 2004. Thermal effects in stretching of Go-like models of titin and secondary structures. Proteins. 56:285-297.
22. Bang, M. L., T. Centner, F. Fornoff, A. J. Geach, M. Gotthardt, M. McNabb, C. C. Witt, D. Labeit, C. C. Gregorio, H. Granzier, and S. Labeit. 2001. The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89:1065-1072.
23. Linke, W. A., and A. Grützner. 2008. Pulling single molecules of titin by AFM-recent advances and physiological implications. Pflugers Arch. 456:101-115.
24. Fowler, S. B., R. B. Best, J. L. Toca Herrera, T. J. Rutherford, A. Steward, E. Paci, M. Karplus, and J. Clarke. 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.
25. Li, H., M. Carrion-Vazquez, A. F. Oberhauser, P. E. Marszalek, and J. M. Fernandez. 2000. Point mutations alter the mechanical stability of immunoglobulin modules. Nat. Struct. Biol. 7:1117-1120.
26. Zinober, R. C., D. J. Brockwell, G. S. Beddard, A. W. Blake, P. D. Olmsted, S. E. Radford, and D. A. Smith. 2002. Mechanically unfolding proteins: the effect of unfolding history and the supramolecular scaffold. Protein Sci. 11:2759-2765.
27. Haverkamp, R. G., A. T. Marshall, and M. A. Williams. 2007. Entropic and enthalpic contributions to the chair-boat conformational transformation in dextran under single molecule stretching. J. Phys. Chem. B. 111:13653-13657.
28. Hutter, J. L., and J. Bechhoefer. 1993. Calibration of atomic-force microscope tip. Rev. Sci. Instrum. 64:1868-1873.
29. Schwaiger, I., C. Sattler, D. R. Hostetter, and M. Rief. 2002. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 1:232-235.
30. Kawakami, M., K. Byrne, B. S. Khatri, T. C. McLeish, and D. A. Smith. 2006. Viscoelastic properties of single poly(ethylene glycol) molecules. ChemPhysChem. 7:1710-1716.
31. Haverkamp, R. G., A. T. Marshall, and M. A. Williams. 2007. Model for stretching elastic biopolymers which exhibit conformational transformations. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75:021907.
32. Brockwell, D. J., G. S. Beddard, E. Paci, D. K. West, P. D. Olmsted, D. A. Smith, and S. E. Radford. 2005. Mechanically unfolding the small, topologically simple protein L. Biophys. J. 89:506-519.
33. Nevo, R., V. Brumfeld, R. Kapon, P. Hinterdorfer, and Z. Reich. 2005. Direct measurement of protein energy landscape roughness. EMBO Rep. 6:482-486.
34. Brockwell, D. J., E. Paci, R. C. Zinober, G. S. Beddard, P. D. Olmsted, D. A. Smith, R. N. Perham, and S. E. Radford. 2003. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nat. Struct. Biol. 10:731-737.
35. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
36. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes. 1991. The energy landscapes and motions of proteins. Science. 254:1598-1603.
37. Onuchic, J. N., and P. G. Wolynes. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70-75.
38. Hyeon, C., and D. Thirumalai. 2003. Can energy landscape roughness of proteins and RNA be measured by using mechanical unfolding experiments? Proc. Natl. Acad. Sci. USA. 100:10249-10253.
39. Janovjak, H., H. Knaus, and D. J. Müller. 2007. Transmembrane helices have rough energy surfaces. J. Am. Chem. Soc. 129:246-247.
40. Rico, F., and V. T. Moy. 2007. Energy landscape roughness of the streptavidin-biotin interaction. J. Mol. Recognit. 20:495-501.
41. Khatri, B. S., M. Kawakami, K. Byrne, D. A. Smith, and T. C. McLeish. 2007. Entropy and barrier-controlled fluctuations determine conformational viscoelasticity of single biomolecules. Biophys. J. 92:1825-1835.
42. Winzor, D. J., and C. M. Jackson. 2006. Interpretation of the temperature dependence of equilibrium and rate constants. J. Mol. Recognit. 19:389-407.
43. Pabón, G., and L. M. Amzel. 2006. Mechanism of titin unfolding by force: insight from quasi-equilibrium molecular dynamics calculations. Biophys. J. 91:467-472.
44. Best, R. B., S. B. Fowler, J. L. Herrera, A. Steward, E. Paci, and J. Clarke. 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.
45. Ng, S. P., K. S. Billings, T. Ohashi, M. D. Allen, R. B. Best, L. G. Randles, H. P. Erickson, and J. Clarke. 2007. Designing an extracellular matrix protein with enhanced mechanical stability. Proc. Natl. Acad. Sci. USA. 104:9633-9637.
46. Preiner, J., H. Janovjak, C. Rankl, H. Knaus, D. A. Cisneros, A. Kedrov, F. Kienberger, D. J. Muller, and P. Hinterdorfer. 2007. Free energy of membrane protein unfolding derived from single-molecule force measurements. Biophys. J. 93:930-937.
47. Bullard, B., T. Garcia, V. Benes, M. C. Leake, W. A. Linke, and A. F. Oberhauser. 2006. The molecular elasticity of the insect flight muscle proteins projectin and kettin. Proc. Natl. Acad. Sci. USA. 103:4451-4456.
48. Schwaiger, I., A. Kardinal, M. Schleicher, A. A. Noegel, and M. Rief. 2004. A mechanical unfolding intermediate in an actin-crosslinking protein. Nat. Struct. Mol. Biol. 11:81-85.
49. Improta, S., A. S. Politou, and A. Pastore. 1996. Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity. Structure. 4:323-337.
50. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-PDB Viewer: an environment for comparative protein modeling. Electrophoresis. 18:2714-2723.