Toward a molecular understanding of the anisotropic response of proteins to external forces: Insights from elastic network models

Biophysical Journal

Volumn 94, Issue 9, 2008, Pages 3424-3435

  Eyal, Eran ^a   Bahar, Ivet ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROLIPOAMIDE ACETYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; PROTEIN; UBIQUITIN;

ANISOTROPY; ARTICLE; CHEMICAL MODEL; CHEMISTRY; ELASTICITY; PROTEIN CONFORMATION; PROTEIN DATABASE; SENSITIVITY AND SPECIFICITY;

ANISOTROPY; DATABASES, PROTEIN; DIHYDROLIPOYLLYSINE-RESIDUE ACETYLTRANSFERASE; ELASTICITY; GREEN FLUORESCENT PROTEINS; MODELS, CHEMICAL; PROTEIN CONFORMATION; PROTEINS; SENSITIVITY AND SPECIFICITY; UBIQUITIN;

EID: 43649085777     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.120733     Document Type: Article

References (78)

1. Kreplak, L., and D. Fudge. 2007. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays. 29:26-35.
2. Nollmann, M., M. D. Stone, Z. Bryant, J. Gore, N. J. Crisona, S. C. Hong, S. Mitelheiser, A. Maxwell, C. Bustamante, and N. R. Cozzarelli. 2007. Multiple modes of Escherichia coli DNA gyrase activity revealed by force and torque. Nat. Struct. Mol. Biol. 14:264-271.
3. Rief, M., and H. Grubmuller. 2002. Force spectroscopy of single biomolecules. ChemPhysChem. 3:255-261.
4. Rounsevell, R., J. R. Forman, and J. Clarke. 2004. Atomic force microscopy: mechanical unfolding of proteins. Methods. 34:100-111.
5. Sotomayor, M., and K. Schulten. 2007. Single-molecule experiments in vitro and in silico. Science. 316:1144-1148.
6. 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.
7. Oberhauser, A. F., P. K. Hansma, M. Carrion-Vazquez, and J. M. Fernandez. 2001. Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. USA. 98:468-472.
8. 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.
9. Tskhovrebova, L., J. Trinick, J. A. Sleep, and R. M. Simmons. 1997. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature. 387:308-312.
10. Kellermayer, M. S., S. B. Smith, H. L. Granzier, and C. Bustamante. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 276:1112-1116.
11. 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.
12. Oberhauser, A. F., C. Badilla-Fernandez, M. Carrion-Vazquez, and J. M. Fernandez. 2002. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319:433-447.
13. Muller, D. J., M. Kessler, F. Oesterhelt, C. Moller, D. Oesterhelt, and H. Gaub. 2002. Stability of bacteriorhodopsin α-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 83:3578-3588.
14. Kessler, M., K. E. Gottschalk, H. Janovjak, D. J. Muller, and H. E. Gaub. 2006. Bacteriorhodopsin folds into the membrane against an external force. J. Mol. Biol. 357:644-654.
15. Kedrov, A., C. Ziegler, H. Janovjak, W. Kuhlbrandt, and D. J. Muller. 2004. Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy. J. Mol. Biol. 340:1143-1152.
16. Sulkowska, J., and M. Cieplak. 2007. Mechanical stretching of proteins-a theoretical survey of the Protein Data Bank. J. Phys. Condens. Matter. 19:doi:283201.
17. Dietz, H., F. Berkemeier, M. Bertz, and M. Rief. 2006. Anisotropic deformation response of single protein molecules. Proc. Natl. Acad. Sci. USA. 103:12724-12728.
18. Carrion-Vazquez, M., H. Li, H. Lu, P. E. Marszalek, A. F. Oberhauser, and J. M. Fernandez. 2003. The mechanical stability of ubiquitin is linkage dependent. Nat. Struct. Biol. 10:738-743.
19. 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 β3-sheet protein. Nat. Struct. Biol. 10:731-737.
20. Pabon, G., and L. M. Amzel. 2006. Mechanism of titin unfolding by force: insight from quasi-equilibrium molecular dynamics calculations. Biophys. J. 91:467-472.
21. Lu, H., and K. Schulten. 2000. The key event in force-induced unfolding of Titin's immunoglobulin domains. Biophys. J. 79:51-65.
22. Lu, H., A. Krammer, B. Isralewitz, V. Vogel, and K. Schulten. 2000. Computer modeling of force-induced titin domain unfolding. Adv. Exp. Med. Biol. 481:143-160 (discussion 161-162).
23. Lee, E. H., M. Gao, N. Pinotsis, M. Wilmanns, and K. Schulten. 2006. Mechanical strength of the titin Z1Z2-telethonin complex. Structure. 14:497-509.
24. Grater, F., J. Shen, H. Jiang, M. Gautel, and H. Grubmuller. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88:790-804.
25. Li, P. C., and D. E. Makarov. 2004. Simulation of the mechanical unfolding of ubiquitin: probing different unfolding reaction coordinates by changing the pulling geometry. J. Chem. Phys. 121:4826-4832.
26. Paci, E., and M. Karplus. 2000. Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc. Natl. Acad. Sci. USA. 97:6521-6526.
27. West, D. K., D. J. Brockwell, P. D. Olmsted, S. E. Radford, and E. Paci. 2006. Mechanical resistance of proteins explained using simple molecular models. Biophys. J. 90:287-297.
28. Kleiner, A., and E. Shakhnovich. 2007. The mechanical unfolding of ubiquitin through all-atom Monte Carlo simulation with a Go-type potential. Biophys. J. 92:2054-2061.
29. Atilgan, A. R., S. R. Durell, R. L. Jernigan, M. C. Demirel, O. Keskin, and I. Bahar. 2001. Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys. J. 80:505-515.
30. Doruker, P., A. R. Atilgan, and I. Bahar. 2000. Dynamics of proteins predicted by molecular dynamics simulations and analytical approaches: application to α-amylase inhibitor. Proteins. 40:512-524.
31. Eyal, E., L. W. Yang, and I. Bahar. 2006. Anisotropic network model: systematic evaluation and a new web interface. Bioinformatics. 22:2619-2627.
32. Bahar, I., A. R. Atilgan, and B. Erman. 1997. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold. Des. 2:173-181.
33. Eyal, E., C. Chennubhotla, L.-W. Yang, and I. Bahar. 2007. Aniso-tropic fluctuations of amino acids in protein structures: insights from x-ray crystallography and elastic network models. Bioinformatics. 23:i175-i184.
34. Bahar, I., A. R. Atilgan, M. C. Demirel, and B. Erman. 1998. Vibrational dynamics of folded proteins: significance of slow and fast motions in relation to function and stability. Phys. Rev. Lett. 80:2733-2736.
35. Qiang, C., and I. Bahar. 2006. Normal Mode Analysis. Theory and Applications to Biological and Chemical Systems. Chapman & Hall/CRC, Boca Raton, FL.
36. Kundu, S., J. S. Melton, D. C. Sorensen, and G. N. Phillips Jr. 2002. Dynamics of proteins in crystals: comparison of experiment with simple models. Biophys. J. 83:723-732.
37. Kondrashov, D. A., Q. Cui, and G. N. Phillips Jr. 2006. Optimization and evaluation of a coarse-grained model of protein motion using x-ray crystal data. Biophys. J. 91:2760-2767.
38. Dietz, H., and M. Rief. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. USA. 101:16192-16197.
39. Dietz, H., and M. Rief. 2006. Protein structure by mechanical trian-gulation. Proc. Natl. Acad. Sci. USA. 103:1244-1247.
40. Perez-Jimenez, R., S. Garcia-Manyes, S. R. Ainavarapu, and J. M. Fernandez. 2006. Mechanical unfolding pathways of the enhanced yellow fluorescent protein revealed by single molecule force spectroscopy. J. Biol. Chem. 281:40010-40014.
41. 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.
42. 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.
43. Elsasser, S., and D. Finley. 2005. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7:742-749.
44. Alexeev, D., S. M. Bury, M. A. Turner, O. M. Ogunjobi, T. W. Muir, R. Ramage, and L. Sawyer. 1994. Synthetic, structural and biological studies of the ubiquitin system: chemically synthesized and native ubiquitin fold into identical three-dimensional structures. Biochem. J. 299:159-163.
45. Pickart, C. M., and D. Fushman. 2004. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8:610-616.
46. Navon, A., and A. L. Goldberg. 2001. Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol. Cell. 8:1339-1349.
47. Lee, C., M. P. Schwartz, S. Prakash, M. Iwakura, and A. Matouschek. 2001. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell. 7:627-637.
48. Hochstrasser, M., and J. Wang. 2001. Unraveling the means to the end in ATP-dependent proteases. Nat. Struct. Biol. 8:294-296.
49. 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 β3-sheet protein. Nat. Struct. Biol. 10:731-737. (Erratum in Nat. Struct. Biol. 2003. 10:872. Comment in Nat. Struct. Biol. 2003. 10:674-676).
50. Klimov, D. K., and D. Thirumalai. 2000. Native topology determines force-induced unfolding pathways in globular proteins. Proc. Natl. Acad. Sci. USA. 97:7254-7259.
51. Oberdorfer, H., H. Fuchs, and A. Janshoff. 2000. Conformational analysis of native fibronectin by means of force spectroscopy. Langmuir. 16:9955-9958.
52. Leahy, D. J., H. P. Erickson, I. Aukhil, P. Joshi, and W. A. Hendrickson. 1994. Crystallization of a fragment of human fibronectin: introduction of methionine by site-directed mutagenesis to allow phasing via selenomethionine. Proteins. 19:48-54.
53. Sharma, A., J. A. Askari, M. J. Humphries, E. Y. Jones, and D. I. Stuart. 1999. Crystal structure of a heparin- and integrin-binding segment of human fibronectin. EMBO J. 18:1468-1479.
54. Xu, C., D. Tobi, and I. Bahar. 2003. Allosteric changes in protein structure computed by a simple mechanical model: hemoglobin T↔R2 transition. J. Mol. Biol. 333:153-168.
55. Mouawad, L., and D. Perahia. 1996. Motions in hemoglobin studied by normal mode analysis and energy minimization: evidence for the existence of tertiary T-like, quaternary R-like intermediate structures. J. Mol. Biol. 258:393-410.
56. Thomas, A., M. J. Field, L. Mouawad, and D. Perahia. 1996. Analysis of the low frequency normal modes of the T-state of aspartate trans- carbamylase. J. Mol. Biol. 257:1070-1087.
57. Thomas, A., K. Hinsen, M. J. Field, and D. Perahia. 1999. Tertiary and quaternary conformational changes in aspartate transcarbamylase: a normal mode study. Proteins. 34:96-112.
58. Hinsen, K. 1998. Analysis of domain motions by approximate normal mode calculations. Proteins. 33:417-429.
59. Petrone, P., and V. S. Pande. 2006. Can conformational change be described by only a few normal modes? Biophys. J. 90:1583-1593.
60. Tama, F., and Y. H. Sanejouand. 2001. Conformational change of proteins arising from normal mode calculations. Protein Eng. 14:1-6.
61. Tobi, D., and I. Bahar. 2005. Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Proc. Natl. Acad. Sci. USA. 102:18908-18913.
62. Bahar, I., A. Wallqvist, D. G. Covell, and R. L. Jernigan. 1998. Correlation between native-state hydrogen exchange and cooperative residue fluctuations from a simple model. Biochemistry. 37:1067-1075.
63. Cieplak, M., T. X. Hoang, and M. O. Robbins. 2002. Folding and stretching in a Go-like model of titin. Proteins. 49:114-124.
64. Cieplak, M., and P. E. Marszalek. 2005. Mechanical unfolding of ubiquitin molecules. J. Chem. Phys. 123:194903.
65. Cieplak, M., A. Pastore, and T. X. Hoang. 2005. Mechanical properties of the domains of titin in a Go-like model. J. Chem. Phys. 122:54906.
66. Plaxco, K. W., S. Larson, I. Ruczinski, D. S. Riddle, E. C. Thayer, B. Buchwitz, A. R. Davidson, and D. Baker. 2000. Evolutionary conservation in protein folding kinetics. J. Mol. Biol. 298:303-312.
67. Sharma, D., Y. Cao, and H. Li. 2006. Engineering proteins with novel mechanical properties by recombination of protein fragments. Angew. Chem. Int. Ed. Engl. 45:5633-5638.
68. Jmol: an open-source Java viewer for chemical structures in 3D. http://jmol.sourceforge.net/.
69. Schlierf, M., and M. Rief. 2006. Single-molecule unfolding force distributions reveal a funnel-shaped energy landscape. Biophys. J. 90:L33-L35.
70. Law, R., P. Carl, S. Harper, P. Dalhaimer, D. W. Speicher, and D. E. Discher. 2003. Cooperativity in forced unfolding of tandem spectrin repeats. Biophys. J. 84:533-544.
71. Rief, M., J. Pascual, M. Saraste, and H. E. Gaub. 1999. Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J. Mol. Biol. 286:553-561.
72. 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.
73. Li, H., and J. M. Fernandez. 2003. Mechanical design of the first proximal Ig domain of human cardiac titin revealed by single molecule force spectroscopy. J. Mol. Biol. 334:75-86.
74. Yang, F., L. G. Moss, and G. N. Phillips Jr. 1996. The molecular structure of green fluorescent protein. Nat. Biotechnol. 14:1246-1251.
75. Jones, D. D., K. M. Stott, M. J. Howard, and R. N. Perham. 2000. Restricted motion of the lipoyl-lysine swinging arm in the pyruvate de- hydrogenase complex of Escherichia coli. Biochemistry. 39:8448-8459.
76. O'Neill, J. W., D. E. Kim, D. Baker, and K. Y. Zhang. 2001. Structures of the B1 domain of protein L from Peptostreptococcus magnus with a tyrosine to tryptophan substitution. Acta Crystallogr. D Biol. Crystal-logr. 57:480-487.
77. Mayans, O., J. Wuerges, S. Canela, M. Gautel, and M. Wilmanns. 2001. Structural evidence for a possible role of reversible disulphide bridge formation in the elasticity of the muscle protein titin. Structure. 9:331-340.
78. Kusunoki, H., G. Minasov, R. I. Macdonald, and A. Mondragon. 2004. Independent movement, dimerization and stability of tandem repeats of chicken brain a-spectrin. J. Mol. Biol. 344:495-511.