Nanomechanics of protein unfolding outside a generic nanopore

ACS Nano

Volumn 10, Issue 1, 2016, Pages 317-323

  Luan, Binquan ^a   Huynh, Tien ^a   Li, Jingyuan ^b   Zhou, Ruhong ^a  

^a IBM T J WATSON RESEARCH CENTER   (United States)

^b INSTITUTE OF HIGH ENERGY PHYSICS   (China)

Author keywords

Nanomechanics; Protease; Protein unfolding

Indexed keywords

ATOMIC FORCE MICROSCOPY; FRACTURE; NANOMECHANICS; NANOPORES;

FOLDING AND UNFOLDING; MECHANICAL UNFOLDING; NANOMACHINES; PROTEASE; PROTEASOMES; PROTEIN UNFOLDING; TARGET PROTEINS; UNFOLDING PROCESS;

PROTEINS;

EID: 84989260767     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b04557     Document Type: Article

References (42)

1. Fersht, A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding; Macmillan: New York, 1999.
2. Blanco, F. J.; Rivas, G.; Serrano, L. A Short Linear Peptide That Folds into a Native Stable β-Hairpin in Aqueous Solution. Nat. Struct. Biol. 1994, 1, 584-590.
3. Munoz, V.; Thompson, P. A.; Hofrichter, J.; Eaton, W. A. Folding Dynamics and Mechanism of β-Hairpin Formation. Nature 1997, 390, 196-199.
4. Munoz, V.; Henry, E. R.; Hofrichter, J.; Eaton, W. A. A Statistical Mechanical Model for β-Hairpin Kinetics. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 5872-5879.
5. Zhou, R.; Berne, B. J.; Germain, R. The Energy Landscape for β Hairpin Folding in Explicit Water. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 14931-14936.
6. Carrion-Vazquez, M.; Oberhauser, A.; Fowler, S.; Marszalek, P.; Broedel, S.; Clarke, J.; Fernandez, J. Mechanical and Chemical Unfolding of a Single Protein: A Comparison. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 3694-3699.
7. Li, J.; Fernandez, J. M.; Berne, B. Water's Role in the Force-Induced Unfolding of Ubiquitin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 19284-19289.
8. Schlierf, M.; Li, H.; Fernandez, J. M. The Unfolding Kinetics of Ubiquitin Captured with Single-Molecule Force-Clamp Techniques. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 7299-7304.
9. Stirnemann, G.; Kang, S.-G.; Zhou, R.; Berne, B. J. How Force Unfolding Differs from Chemical Denaturation. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 3413-3418.
10. Sauer, R. T.; Baker, T. A. AAA+ Proteases: ATP-Fueled Machines of Protein Destruction. Annu. Rev. Biochem. 2011, 80, 587-612.
11. Baker, T. A.; Sauer, R. T. ClpXP, an ATP-Powered Unfolding and Protein-Degradation Machine. Biochim. Biophys. Acta, Mol. Cell Res. 2012, 1823, 15-28.
12. Kenniston, J. A.; Baker, T. A.; Sauer, R. T. Partitioning Between Unfolding and Release of Native Domains During ClpXP Degradation Determines Substrate Selectivity and Partial Processing. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 1390-1395.
13. Shin, Y.; Davis, J. H.; Brau, R. R.; Martin, A.; Kenniston, J. A.; Baker, T. A.; Sauer, R. T.; Lang, M. J. Single-Molecule Denaturation and Degradation of Proteins by the AAA+ClpXP Protease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 19340-19345.
14. Gottesman, S. Proteolysis in Bacterial Regulatory Circuits. Annu. Rev. Cell Dev. Biol. 2003, 19, 565-587.
15. Aubin-Tam, M.-E.; Olivares, A. O.; Sauer, R. T.; Baker, T. A.; Lang, M. J. Single-Molecule Protein Unfolding and Translocation by an ATP-Fueled Proteolytic Machine. Cell 2011, 145, 257-267.
16. Maillard, R. A.; Chistol, G.; Sen, M.; Righini, M.; Tan, J.; Kaiser, C. M.; Hodges, C.; Martin, A.; Bustamante, C. ClpX (P) Generates Mechanical Force to Unfold and Translocate Its Protein Substrates. Cell 2011, 145, 459-469.
17. Sen, M.; Maillard, R. A.; Nyquist, K.; Rodriguez-Aliaga, P.; Presse, S.; Martin, A.; Bustamante, C. The ClpXP Protease Unfolds Substrates Using a Constant Rate of Pulling but Different Gears. Cell 2013, 155, 636-646.
18. Glynn, S. E.; Martin, A.; Nager, A. R.; Baker, T. A.; Sauer, R. T. Structures of Asymmetric ClpX Hexamers Reveal Nucleotide-Dependent Motions in a AAA+ Protein-Unfolding Machine. Cell 2009, 139, 744-756.
19. Kravats, A.; Jayasinghe, M.; Stan, G. Unfolding and Translocation Pathway of Substrate Protein Controlled by Structure in Repetitive Allosteric Cycles of the ClpY ATPase. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 2234-2239.
20. Kravats, A. N.; Tonddast-Navaei, S.; Bucher, R. J.; Stan, G. Asymmetric Processing of a Substrate Protein in Sequential Allosteric Cycles of AAA+ Nanomachines. J. Chem. Phys. 2013, 139, 121921.
21. Koga, N.; Kameda, T.; Okazaki, K.-I.; Takada, S. Paddling Mechanism for the Substrate Translocation by AAA+ Motor Revealed by Multiscale Molecular Simulations. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 18237-18242.
22. Tonddast-Navaei, S.; Stan, G. Mechanism of Transient Binding and Release of Substrate Protein During the Allosteric Cycle of the P97 Nanomachine. J. Am. Chem. Soc. 2013, 135, 14627-14636.
23. Huang, L.; Kirmizialtin, S.; Makarov, D. E. Computer Simulations of the Translocation and Unfolding of a Protein Pulled Mechanically Through a Pore. J. Chem. Phys. 2005, 123, 124903.
24. West, D. K.; Brockwell, D. J.; Paci, E. Prediction of the Translocation Kinetics of a Protein from Its Mechanical Properties. Biophys. J. 2006, 91, L51-L53.
25. Wojciechowski, M.; Szymczak, P.; Carrion-Vazquez, M.; Cieplak, M. Protein Unfolding by Biological Unfoldases: Insights from Modeling. Biophys. J. 2014, 107, 1661-1668.
26. Zhou, R.; Eleftheriou, M.; Royyuru, A. K.; Berne, B. J. Destruction of Long-Range Interactions by a Single Mutation in Lysozyme. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 5824-5829.
27. Schleicher, E.; Kowalczyk, R. M.; Kay, C. W. M.; Hegemann, P.; Bacher, A.; Fischer, M.; Bittl, R.; Richter, G.; Weber, S. On the Reaction Mechanism of Adduct Formation in LOV Domains of the Plant Blue-Light Receptor Phototropin. J. Am. Chem. Soc. 2004, 126, 11067-76.
28. 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.
29. Luan, B.; Zhou, B.; Huynh, T.; Zhou, R. Controlled Transport of DNa Through a Y-Shaped Carbon Nanotube in a Solid Membrane. Nanoscale 2014, 6, 11479-11483.
30. Isralewitz, B.; Gao, M.; Schulten, K. Steered Molecular Dynamics and Mechanical Functions of Proteins. Curr. Opin. Struct. Biol. 2001, 11, 224-230.
31. MacKerell, A., Jr.; et al. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J. Phys. Chem. B 1998, 102, 3586-3616.
32. Beglov, D.; Roux, B. Finite Representation of an Infinite Bulk System: Solvent Boundary Potential for Computer Simulations. J. Chem. Phys. 1994, 100, 9050-9063.
33. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 1983, 79, 926-935.
34. Neria, E.; Fischer, S.; Karplus, M. Simulation of Activation Free Energies in Molecular Systems. J. Chem. Phys. 1996, 105, 1902.
35. Maity, H.; Maity, M.; Krishna, M. M.; Mayne, L.; Englander, S. W. Protein Folding: The Stepwise Assembly of Foldon Units. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 4741-4746.
36. Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids; Oxford University Press: New York, 1987.
37. Luan, B.; Robbins, M. O. The Breakdown of Continuum Models for Mechanical Contacts. Nature 2005, 435, 929-932.
38. Kanninen, M. F.; Popelar, C. L. Advanced Fracture Mechanics; Oxford University Press: New York, 1985.
39. Bell, G. I. Models for the Specific Adhesion of Cells to Cells. Science 1978, 200, 618-627.
40. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with NAMD. J. Comput. Chem. 2005, 26, 1781-1802.
41. Tu, Y.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z.; Huang, Q.; Fan, C.; Fang, H.; Zhou, R. Destructive Extraction of Phospholipids from Escherichia Coli Membranes by Graphene Nanosheets. Nat. Nanotechnol. 2013, 8, 594-601.
42. Martyna, G. J.; Tobias, D. J.; Klein, M. L. Constant Pressure Molecular Dynamics Algorithms. J. Chem. Phys. 1994, 101, 4177-4189.