Tunable nanomechanics of protein disulfide bonds in redox microenvironments

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 5, Issue 1, 2012, Pages 32-40

  Keten, Sinan ^a,b   Chou, Chia Ching ^a   van Duin, Adri C T ^c   Buehler, Markus J ^a  

^a USA   (United States)

^b Northwestern University   (United States)

^c The Center for Nanotechnology Education and Utilization   (United States)

Author keywords

Cross link; Mechanochemistry; Nanomechanics; Polymer; Protein; Reactive molecular dynamics; ReaxFF; Redox reaction

Indexed keywords

CHEMICAL MICROENVIRONMENT; COMPUTATIONAL APPROACH; COMPUTATIONAL PROTOCOLS; CROSS-LINK; DISULFIDE BONDS; DITHIOTHREITOL; EXPLICIT SOLVENTS; FIBROUS PROTEINS; FRACTURE MECHANISMS; MECHANICAL STRAIN; MECHANOCHEMICALS; MECHANOCHEMISTRY; MICROENVIRONMENTS; REACTIVE FORCE FIELD; REAXFF; REDOX POTENTIALS; RUPTURE MECHANISM; TUNABILITIES;

CHEMICAL STABILITY; COVALENT BONDS; ELASTICITY; MECHANISMS; MOLECULAR DYNAMICS; NANOMECHANICS; POLYMERS; PROTEINS; REACTION KINETICS; REDOX REACTIONS; REDUCING AGENTS;

FRACTURE;

DITHIOTHREITOL; PROTEIN;

ARTICLE; DISULFIDE BOND; MECHANICAL STRESS; MICROENVIRONMENT; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

BIOMECHANICS; CONOTOXINS; DISULFIDES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MECHANICAL PROCESSES; MOLECULAR DYNAMICS SIMULATION; NANOTECHNOLOGY; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SOLVENTS; VISCOSITY;

EID: 80054995363     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2011.08.017     Document Type: Article

References (49)

1. Ackbarow T., Chen X., et al. Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proceedings of the National Academy of Sciences 2007, 104(42):16410-16415.
2. Albrecht K., Bernkop-Schnurch A. Thiomers: forms, functions and applications to nanomedicine. Nanomedicine 2007, 2(1):41-50.
3. Aslund F., Beckwith J. Bridge over troubled waters: sensing stress by disulfide bond formation. Cell 1999, 96(6):751-753.
4. Becke A.D. Density-functional thermochemistry. III. The role of exact exchange. Journal of Chemical and Physics 1993, 98:5648.
5. Bell G.I. Models for specific adhesion of cells to cells. Science 1978, 200(4342):618-627.
6. Bernkop-Schnürch A., Schwarz V., et al. Polymers with thiol groups: a new generation of mucoadhesive polymers?. Pharmaceutical Research 1999, 16(6):876-881.
7. Bernstein F.C., Koetzle T.F., et al. Protein data bank-computer-based archival file for macromolecular structures. Journal of Molecular Biology 1977, 112(3):535-542.
8. Bonomi M., Branduardi D., et al. PLUMED: a portable plugin for free-energy calculations with molecular dynamics. Computer Physics Communications 2009, 180(10):1961-1972.
9. Bonomi M., Parrinello M. Enhanced sampling in the well-tempered ensemble. Physical Review Letters 2010, 104(19):190601.
10. Brändén C.-I., Tooze J. Introduction to Protein Structure 1999, Garland Pub., New York.
11. Brockwell D.J., Paci E., et al. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nature Structural Biology 2003, 10(9):731-737.
12. Buehler M.J., van Duin A.C.T., et al. Multiparadigm modeling of dynamical crack propagation in silicon using a reactive force field. Physical Review Letters 2006, 96(9):095505-4.
13. Buehler M.J., Yung Y.C. Deformation and failure of protein materials in physiologically extreme conditions and disease. Nature Materials 2009, 8(3):175-188.
14. Cerritelli S., Velluto D., et al. PEG-SS-PPS: reduction-sensitive disulfide block copolymer vesicles for intracellular drug delivery. Biomacromolecules 2007, 8(6):1966-1972.
15. Cheek S., Krishna S.S., et al. Structural classification of small, disulfide-rich protein domains. Journal of Molecular Biology 2006, 359(1):215-237.
16. Chenoweth K., van Duin A.C.T., et al. ReaxFF reactive force field for molecular dynamics simulations of hydrocarbon oxidation. The Journal of Physical Chemistry A 2008, 112(5):1040-1053.
17. Cumming R.C., Andon N.L., et al. Protein disulfide bond formation in the cytoplasm during oxidative stress. The Journal of Biological Chemistry 2004, 279(21):21749-21758.
18. Dietz H., Rief M. Elastic bond network model for protein unfolding mechanics. Physical Review Letters 2008, 100(9):098101.
19. Fernandes P.A., Ramos M.J. Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry-A European Journal 2004, 10(1):257-266.
20. Flory P.J. Principles of Polymer Chemistry 1953, Cornell University Press, Ithaca.
21. Fratzl P., Weinkamer R. Nature's hierarchical materials. Progress in Materials Science 2007, 52(8):1263-1334.
22. Garcia-Manyes S., Liang J., et al. Force-activated reactivity switch in a bimolecular chemical reaction. Nature Chemistry 2009, 1(3):236-242.
23. Grossfield, A., 2008. WHAM: the weighted histogram analysis method. http://membrane.urmc.rochester.edu/content/wham.
24. Hofbauer F., Frank I. Disulfide bond cleavage: a redox reaction without electron transfer. Chemistry-A European Journal 2010, 16(17):5097-5101.
25. Hogg P.J. Disulfide bonds as switches for protein function. Trends in Biochemical Sciences 2003, 28(4):210-214.
26. Humphrey W., Dalke A., et al. VMD: visual molecular dynamics. Journal of Molecular Graphics 1996, 14(1):33.
27. Isralewitz B., Gao M., et al. Steered molecular dynamics and mechanical functions of proteins. Current Opinion in Structural Biology 2001, 11(2):224-230.
28. Keten S., Buehler M.J. Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Letters 2008, 8(2):743-748.
29. Krishnan R., Binkley J.S., et al. Self-consistent molecular orbital methods. XX. A basis set for correlated wave functions. Journal of Chemical and Physics 1980, 72:650.
30. Laioa A., Parrinello M. Escaping free-energy minima. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:12562-12566.
31. Leitner V.M., Walker G.F., et al. Thiolated polymers: evidence for the formation of disulphide bonds with mucus glycoproteins. European Journal of Pharmaceutics and Biopharmaceutics 2003, 56(2):207-214.
32. Li W., Grater F. Atomistic evidence of how force dynamically regulates thiol/disulfide exchange. Journal of the American Chemical Society 2010, 132(47):16790-16795.
33. Lv L.-P., Xu J.-P., et al. Disulfide-crosslinked biomimetic micelles: formation, thiol reactivity and cytotoxicity behavior. Macromolecular Chemistry and Physics 2010, 211(21):2292-2300.
34. MacKerell A.D., Bashford D., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. The Journal of Physical Chemistry B 1998, 102(18):3586-3616.
35. Mayans O., Wuerges J., et al. Structural evidence for a possible role of reversible disulphide bridge formation in the elasticity of the muscle protein titin. Structure 2001, 9(4):331-340.
36. Mucke N., Kreplak L., et al. Assessing the flexibility of intermediate filaments by atomic force microscopy. Journal of Molecular Biology 2004, 335(5):1241-1250.
37. Napoli A., Valentini M., et al. Oxidation-responsive polymeric vesicles. Nature Materials 2004, 3(3):183-189.
38. Nielson K.D., van Duin A.C.T., et al. Development of the ReaxFF reactive force field for describing transition metal catalyzed reactions, with application to the initial stages of the catalytic formation of carbon nanotubes. The Journal of Physical Chemistry A 2005, 109(3):493-499.
39. Parbhu A.N., Bryson W.G., et al. Disulfide bonds in the outer layer of keratin fibers confer higher mechanical rigidity: correlative nano-indentation and elasticity measurement with an AFM. Biochemistry 1999, 38(36):11755-11761.
40. Perez-Jimenez R., Li J.Y., et al. Diversity of chemical mechanisms in thioredoxin catalysis revealed by single-molecule force spectroscopy. Nature Structural & Molecular Biology 2009, 16(8). 890-U120.
41. Plimpton S. Fast parallel algorithms for short-range molecular dynamics. Journal of Computational Physics 1995, 117(1):1-19.
42. Ponder J.W., Case D.A., et al. Force fields for protein simulations. Advances in Protein Chemistry 2003, vol. 66:27-85. Academic Press.
43. Rahaman O., van Duin A.C.T., et al. Development of a ReaxFF reactive force field for glycine and application to solvent effect and tautomerization. The Journal of Physical Chemistry A 2011, 115(2):249-261.
44. Shewry P.R., Tatham A.S. Disulphide bonds in wheat gluten proteins. Journal of Cereal Science 1997, 25(3):207-227.
45. van Duin A.C.T., Dasgupta S., et al. ReaxFF: a reactive force field for hydrocarbons. The Journal of Physical Chemistry A 2001, 105(41):9396-9409.
46. Voet D., Voet J.G. Biochemistry 2004, J. Wiley & Sons, New York.
47. Wang H., Parry D.A.D., et al. In vitro assembly and structure of trichocyte keratin intermediate filaments: a novel role for stabilization by disulfide bonding. The Journal of Cell Biology 2000, 151(7):1459-1468.
48. Wiita A.P., Ainavarapu S.R.K., et al. Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(19):7222-7227.
49. Wiita A.P., Perez-Jimenez R., et al. Probing the chemistry of thioredoxin catalysis with force. Nature 2007, 450(7166):124-127.