Single molecule force spectroscopy reveals critical roles of hydrophobic core packing in determining the mechanical stability of protein GB1

Langmuir

Volumn 28, Issue 33, 2012, Pages 12319-12325

  Bu, Tianjia ^a,b   Wang, Hui Chuan Eileen ^b   Li, Hongbin ^b  

^a Jilin University   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BUILDING BLOCKES; ELASTOMERIC PROTEINS; HYDROPHOBIC CORE; HYDROPHOBIC INTERACTIONS; MECHANICAL UNFOLDING; MOLECULAR DETERMINANTS; NANOMECHANICAL PROPERTY; PROTEIN ENGINEERING; SIDE-CHAINS; SINGLE MOLECULE; SINGLE MOLECULE FORCE SPECTROSCOPY; STRETCHING FORCE; SUB-DOMAINS; WILD TYPES;

ATOMIC FORCE MICROSCOPY; BIOLOGICAL MATERIALS; GENETIC ENGINEERING; HYDROPHOBICITY; PROTEINS;

MECHANICAL STABILITY;

BACTERIAL PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; MECHANICS; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN UNFOLDING; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; BIOMECHANICS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MECHANICAL PROCESSES; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN UNFOLDING;

EID: 84865514087     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la301940g     Document Type: Article

References (48)

1. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton; Sinauer Associates Publishers: Sunderland, MA, 2001; p xvi, 367 p.
2. Bustamante, C.; Chemla, Y. R.; Forde, N. R.; Izhaky, D. Mechanical processes in biochemistry Annu. Rev. Biochem. 2004, 73, 705-48 (Pubitemid 39050384)
3. Rief, M.; Gautel, M.; Oesterhelt, F.; Fernandez, J. M.; Gaub, H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM Science 1997, 276, 1109-12 (Pubitemid 27218118)
4. Carrion-Vazquez, M.; Oberhauser, A. F.; Fisher, T. E.; Marszalek, P. E.; Li, H.; Fernandez, J. M. Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering Prog. Biophys. Mol. Biol. 2000, 74, 63-91 (Pubitemid 32011689)
5. Brockwell, D. J. Probing the mechanical stability of proteins using the atomic force microscope Biochem. Soc. Trans. 2007, 35, 1564-8
6. Borgia, A.; Williams, P. M.; Clarke, J. Single-molecule studies of protein folding Annu. Rev. Biochem. 2008, 77, 101-25
7. Lee, G.; Abdi, K.; Jiang, Y.; Michaely, P.; Bennett, V.; Marszalek, P. E. Nanospring behaviour of ankyrin repeats Nature 2006, 440, 246-9 (Pubitemid 43372106)
8. Oberhauser, A. F.; Marszalek, P. E.; Erickson, H. P.; Fernandez, J. M. The molecular elasticity of the extracellular matrix protein tenascin Nature 1998, 393, 181-5 (Pubitemid 28242260)
9. Lu, H.; Isralewitz, B.; Krammer, A.; Vogel, V.; Schulten, K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation Biophys. J. 1998, 75, 662-71 (Pubitemid 28357508)
10. Sotomayor, M.; Schulten, K. Single-molecule experiments in vitro and in silico Science 2007, 316, 1144-8 (Pubitemid 46877468)
11. Li, H. B. "Mechanical Engineering" of Elastomeric Proteins: Toward Designing New Protein Building Blocks for Biomaterials Adv. Funct. Mater. 2008, 18, 2643-2657
12. Brockwell, D. J.; Beddard, G. S.; Paci, E.; West, D. K.; Olmsted, P. D.; Smith, D. A.; Radford, S. E. Mechanically unfolding the small, topologically simple protein L Biophys. J. 2005, 89, 506-19 (Pubitemid 41098304)
13. Sikora, M.; Sulkowska, J. I.; Cieplak, M. Mechanical strength of 17,134 model proteins and cysteine slipknots PLoS Comput. Biol. 2009, 5, e1000547
14. Brockwell, D. J. Force denaturation of proteins-an unfolding story Curr. Nanosci. 2007, 3, 3-15 (Pubitemid 46322299)
15. Sharma, D.; Perisic, O.; Peng, Q.; Cao, Y.; Lam, C.; Lu, H.; Li, H. Single-molecule force spectroscopy reveals a mechanically stable protein fold and the rational tuning of its mechanical stability Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 9278-83 (Pubitemid 47185770)
16. Lu, H.; Schulten, K. The key event in force-induced unfolding of Titin's immunoglobulin domains Biophys. J. 2000, 79, 51-65 (Pubitemid 30436727)
17. Best, R. B.; Fowler, S. B.; Herrera, J. L.; Steward, A.; Paci, E.; Clarke, J. 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. 2003, 330, 867-77
18. Garcia, T. I.; Oberhauser, A. F.; Braun, W. Mechanical stability and differentially conserved physical-chemical properties of titin Ig-domains Proteins 2009, 75, 706-18
19. Oberhauser, A. F.; Badilla-Fernandez, C.; Carrion-Vazquez, M.; Fernandez, J. M. The mechanical hierarchies of fibronectin observed with single-molecule AFM J. Mol. Biol. 2002, 319, 433-47 (Pubitemid 34729470)
20. Li, H.; Linke, W. A.; Oberhauser, A. F.; Carrion-Vazquez, M.; Kerkvliet, J. G.; Lu, H.; Marszalek, P. E.; Fernandez, J. M. Reverse engineering of the giant muscle protein titin Nature 2002, 418, 998-1002 (Pubitemid 34976037)
21. Fersht, A. R.; Matouschek, A.; Serrano, L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding J. Mol. Biol. 1992, 224, 771-82
22. Matouschek, A.; Kellis, J. T., Jr.; Serrano, L.; Fersht, A. R. Mapping the transition state and pathway of protein folding by protein engineering Nature 1989, 340, 122-6 (Pubitemid 19175363)
23. Fersht, A. R.; Daggett, V. Protein folding and unfolding at atomic resolution Cell 2002, 108, 573-82 (Pubitemid 34260881)
24. Fowler, S. B.; Best, R. B.; Toca Herrera, J. L.; Rutherford, T. J.; Steward, A.; Paci, E.; Karplus, M.; Clarke, J. 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. 2002, 322, 841-9
25. Ng, S. P.; Rounsevell, R. W.; Steward, A.; Geierhaas, C. D.; Williams, P. M.; Paci, E.; Clarke, J. Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation J. Mol. Biol. 2005, 350, 776-89 (Pubitemid 40848674)
26. Sadler, D. P.; Petrik, E.; Taniguchi, Y.; Pullen, J. R.; Kawakami, M.; Radford, S. E.; Brockwell, D. J. Identification of a mechanical rheostat in the hydrophobic core of protein L J. Mol. Biol. 2009, 393, 237-48
27. Brockwell, D. J.; Beddard, G. S.; Clarkson, J.; Zinober, R. C.; Blake, A. W.; Trinick, J.; Olmsted, P. D.; Smith, D. A.; Radford, S. E. The effect of core destabilization on the mechanical resistance of I27 Biophys. J. 2002, 83, 458-72 (Pubitemid 34694749)
28. Gronenborn, A. M.; Filpula, D. R.; Essig, N. Z.; Achari, A.; Whitlow, M.; Wingfield, P. T.; Clore, G. M. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G Science 1991, 253, 657-61 (Pubitemid 21917198)
29. McCallister, E. L.; Alm, E.; Baker, D. Critical role of beta-hairpin formation in protein G folding Nat. Struct. Biol. 2000, 7, 669-73 (Pubitemid 30636679)
30. Cao, Y.; Lam, C.; Wang, M.; Li, H. Nonmechanical protein can have significant mechanical stability Angew. Chem., Int. Ed. 2006, 45, 642-5 (Pubitemid 43121465)
31. Cao, Y.; Li, H. Polyprotein of GB1 is an ideal artificial elastomeric protein Nat. Mater. 2007, 6, 109-14 (Pubitemid 46197646)
32. Cao, Y.; Yoo, T.; Li, H. Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 11152-7
33. Cao, Y.; Yoo, T.; Zhuang, S.; Li, H. Protein-protein interaction regulates proteins' mechanical stability J. Mol. Biol. 2008, 378, 1132-41
34. Carrion-Vazquez, M.; Oberhauser, A. F.; Fowler, S. B.; Marszalek, P. E.; Broedel, S. E.; Clarke, J.; Fernandez, J. M. Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 3694-9 (Pubitemid 29168972)
35. Fernandez, J. M.; Li, H. Force-clamp spectroscopy monitors the folding trajectory of a single protein Science 2004, 303, 1674-8 (Pubitemid 38338326)
36. Rief, M.; Fernandez, J. M.; Gaub, H. E. Elastically coupled two-level systems as a model for biopolymer extensibility Phys. Rev. Lett. 1998, 81, 4764-4767 (Pubitemid 128626983)
37. Carrion-Vazquez, M.; Marszalek, P. E.; Oberhauser, A. F.; Fernandez, J. M. Atomic force microscopy captures length phenotypes in single proteins Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 11288-92 (Pubitemid 29487373)
38. Li, H.; Oberhauser, A. F.; Fowler, S. B.; Clarke, J.; Fernandez, J. M. Atomic force microscopy reveals the mechanical design of a modular protein Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 6527-31 (Pubitemid 30412747)
39. Bell, G. I. Models for the specific adhesion of cells to cells Science 1978, 200, 618-27
40. Evans, E. Probing the relation between force - lifetime - and chemistry in single molecular bonds Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 105-28 (Pubitemid 32566158)
41. Best, R. B.; Fowler, S. B.; Toca-Herrera, J. L.; Clarke, J. A simple method for probing the mechanical unfolding pathway of proteins in detail Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12143-8
42. Li, H.; Oberhauser, A. F.; Redick, S. D.; Carrion-Vazquez, M.; Erickson, H. P.; Fernandez, J. M. Multiple conformations of PEVK proteins detected by single-molecule techniques Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 10682-6 (Pubitemid 32878681)
43. Glyakina, A. V.; Balabaev, N. K.; Galzitskaya, O. V. Mechanical unfolding of proteins L and G with constant force: similarities and differences J. Chem. Phys. 2009, 131, 045102
44. Peng, Q.; Zhuang, S.; Wang, M.; Cao, Y.; Khor, Y.; Li, H. Mechanical design of the third FnIII domain of tenascin-C J. Mol. Biol. 2009, 386, 1327-42
45. Li, P. C.; Makarov, D. E. Simulation of the mechanical unfolding of ubiquitin: Probing different unfolding reaction coordinates by changing the pulling geometry J. Chem. Phys. 2004, 121, 4826-4832
46. Malakauskas, S. M.; Mayo, S. L. Design, structure and stability of a hyperthermophilic protein variant Nat. Struct. Biol. 1998, 5, 470-5 (Pubitemid 28265030)
47. Carrion-Vazquez, M.; Li, H.; Lu, H.; Marszalek, P. E.; Oberhauser, A. F.; Fernandez, J. M. The mechanical stability of ubiquitin is linkage dependent Nat. Struct. Biol. 2003, 10, 738-43 (Pubitemid 37052413)
48. Chyan, C. L.; Lin, F. C.; Peng, H.; Yuan, J. M.; Chang, C. H.; Lin, S. H.; Yang, G. Reversible mechanical unfolding of single ubiquitin molecules Biophys. J. 2004, 87, 3995-4006 (Pubitemid 39602904)