Forced protein unfolding leads to highly elastic and tough protein hydrogels

Nature Communications

Volumn 4, Issue , 2013, Pages

  Fang, Jie ^a   Mehlich, Alexander ^b   Koga, Nobuyasu ^c   Huang, Jiqing ^a   Koga, Rie ^c   Gao, Xiaoye ^a   Hu, Chunguang ^d   Jin, Chi ^a   Rief, Matthias ^b   Kast, Juergen ^a   Baker, David ^c   Li, Hongbin ^a,d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d TIANJIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FERREDOXIN;

ELASTICITY; ENERGY EFFICIENCY; GEL; PROTEIN; STABILIZATION;

ARTICLE; BIOENGINEERING; BIOMECHANICS; CONTROLLED STUDY; ELASTICITY; ENERGY; HYDROGEL; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN UNFOLDING; TISSUE ENGINEERING;

BIOCOMPATIBLE MATERIALS; CIRCULAR DICHROISM; CYSTEINE; ELASTICITY; FERREDOXINS; HYDROGELS; OPTICAL TWEEZERS; PROTEIN ENGINEERING; PROTEIN UNFOLDING; PROTEINS; STRESS, MECHANICAL; TENSILE STRENGTH; TISSUE ENGINEERING;

EID: 84890933479     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3974     Document Type: Article

References (52)

1. Lutolf, M. P. & Hubbell, J. A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 23, 47-55 (2005). (Pubitemid 41724624)
2. Langer, R. & Tirrell, D. A. Designing materials for biology and medicine. Nature 428, 487-492 (2004). (Pubitemid 38480528)
3. Petka, W. A., Harden, J. L., McGrath, K. P., Wirtz, D. & Tirrell, D. A. Reversible hydrogels from self-assembling artificial proteins. Science 281, 389-392 (1998). (Pubitemid 28340778)
4. Elvin, C. M. et al. Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437, 999-1002 (2005). (Pubitemid 41486978)
5. Kopecek, J. Hydrogel biomaterials: a smart future? Biomaterials 28, 5185-5192 (2007). (Pubitemid 47488492)
6. Urry, D. W. et al. Elastin: a representative ideal protein elastomer. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 169-184 (2002). (Pubitemid 34276208)
7. Vrhovski, B., Jensen, S. & Weiss, A. S. Coacervation characteristics of recombinant human tropoelastin. Eur. J. Biochem. 250, 92-98 (1997). (Pubitemid 27504587)
8. Bellingham, C. M. et al. Recombinant human elastin polypeptides self-assemble into biomaterials with elastin-like properties. Biopolymers 70, 445-455 (2003). (Pubitemid 37531828)
9. Welsh, E. R. & Tirrell, D. A. Engineering the extracellular matrix: a novel approach to polymeric biomaterials. I. Control of the physical properties of artificial protein matrices designed to support adhesion of vascular endothelial cells. Biomacromolecules 1, 23-30 (2000).
10. Nagapudi, K. et al. Protein-based thermoplastic elastomers. Macromolecules 38, 345-354 (2005). (Pubitemid 40184308)
11. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M. & Gaub, H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109-1112 (1997). (Pubitemid 27218118)
12. Oberhauser, A. F., Marszalek, P. E., Erickson, H. P. & Fernandez, J. M. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393, 181-185 (1998). (Pubitemid 28242260)
13. Cao, Y. & Li, H. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat. Mater. 6, 109-114 (2007). (Pubitemid 46197646)
14. Klotzsch, E. et al. Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc. Natl Acad. Sci. USA 106, 18267-18272 (2009).
15. Erickson, H. P. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl Acad. Sci. USA 91, 10114-10118 (1994).
16. Brown, A. E., Litvinov, R. I., Discher, D. E., Purohit, P. K. & Weisel, J. W. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325, 741-744 (2009).
17. Li, H. et al. Reverse engineering of the giant muscle protein titin. Nature 418, 998-1002 (2002). (Pubitemid 34976037)
18. Minajeva, A., Kulke, M., Fernandez, J. M. & Linke, W. A. Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils. Biophys. J. 80, 1442-1451 (2001). (Pubitemid 32182167)
19. Lemmon, C. A., Ohashi, T. & Erickson, H. P. Probing the folded state of fibronectin type III domains in stretched fibrils by measuring buried cysteine accessibility. J. Biol. Chem. 286, 26375-26382 (2011).
20. Doi, M. Introduction to Polymer Physics (Oxford Science Publications, Oxford, 1995).
21. Brockwell, D. J. Force denaturation of proteins-an unfolding story. Curr. Nanosci. 3, 3-15 (2007). (Pubitemid 46322299)
22. Lv, S. et al. Designed biomaterials to mimic the mechanical properties of muscles. Nature 465, 69-73 (2010).
23. Carrion-Vazquez, M. et al. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl Acad. Sci. USA 96, 3694-3699 (1999). (Pubitemid 29168972)
24. Cecconi, C., Shank, E. A., Bustamante, C. & Marqusee, S. Direct observation of the three-state folding of a single protein molecule. Science 309, 2057-2060 (2005). (Pubitemid 41362324)
25. Stigler, J., Ziegler, F., Gieseke, A., Gebhardt, J. C. & Rief, M. The complex folding network of single calmodulin molecules. Science 334, 512-516 (2011).
26. Li, H. Protein Nanomechanics. (eds Andrews, D. S., GD. & Wiederrecht, G. P.) (Academic Press, Oxford, 2011).
27. Koga, N. et al. Principles for designing ideal protein structures. Nature 491, 222-227 (2012).
28. Carrion-Vazquez, M. et al. Mechanical design of proteins studied by singlemolecule force spectroscopy and protein engineering. Prog. Biophys. Mol. Biol. 74, 63-91 (2000). (Pubitemid 32011689)
29. Fancy, D. A. & Kodadek, T. Chemistry for the analysis of protein-protein interactions: rapid and efficient cross-linking triggered by long wavelength light. Proc. Natl Acad. Sci. USA 96, 6020-6024 (1999). (Pubitemid 29256612)
30. Elvin, C. M. et al. The development of photochemically crosslinked native fibrinogen as a rapidly formed and mechanically strong surgical tissue sealant. Biomaterials 30, 2059-2065 (2009).
31. Elvin, C. M. et al. A highly elastic tissue sealant based on photopolymerised gelatin. Biomaterials 31, 8323-8331 (2010).
32. Qin, G. et al. Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials 32, 9231-9243 (2011).
33. Bjork, J. W., Johnson, S. L. & Tranquillo, R. T. Ruthenium-catalyzed photo cross-linking of fibrin-based engineered tissue. Biomaterials 32, 2479-2488 (2011).
34. Sando, L. et al. Photochemical crosslinking of soluble wool keratins produces a mechanically stable biomaterial that supports cell adhesion and proliferation. J. Biomed. Mater. Res. A. 95, 901-911 (2010).
35. Lv, S., Bu, T., Kayser, J., Bausch, A. & Li, H. Towards constructing extracellular matrix-mimetic hydrogels: an elastic hydrogel constructed from tandem modular proteins containing tenascin FnIII domains. Acta. Biomater. 9, 6481-6491 (2013).
36. Li, Y. & Tanaka, T. Phase transitions of gels. Annu Rev. Mater. Sci. 22, 243-277 (1992).
37. Shibayama, M. & Tanaka, T. Volume phase-transition and related phenomena of polymer gels. Adv. Polym. Sci. 109, 1-62 (1993).
38. Johnson, C. P., Tang, H. Y., Carag, C., Speicher, D. W. & Discher, D. E. Forced unfolding of proteins within cells. Science 317, 663-666 (2007). (Pubitemid 47229965)
39. Krieger, C. C. et al. Cysteine shotgun-mass spectrometry (CS-MS) reveals dynamic sequence of protein structure changes within mutant and stressed cells. Proc. Natl Acad. Sci. USA 108, 8269-8274 (2011).
40. Lillie, M. A., Chalmers, G. W. & Gosline, J. M. The effects of heating on the mechanical properties of arterial elastin. Connect. Tissue. Res. 31, 23-35 (1994). (Pubitemid 2159631)
41. Thompson, J. B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773-776 (2001). (Pubitemid 34000777)
42. Smith, B. L. et al. Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761-763 (1999). (Pubitemid 29293167)
43. Gong, J. P. Why are double network hydrogels so tough? Soft Matter 6, 2583-2590 (2010).
44. Gong, J. P., Katsuyama, Y., Kurokawa, T. & Osada, Y. Double-network hydrogels with extremely high mechanical strength. Adv. Mater. 15, 1155-1158 (2003).
45. Sun, J. Y. et al. Highly stretchable and tough hydrogels. Nature 489, 133-136 (2012).
46. Cao, Y. & Li, H. B. Engineered elastomeric proteins with dual elasticity can be controlled by a molecular regulator. Nat. Nanotechnol. 3, 512-516 (2008).
47. von Hansen, Y., Mehlich, A., Pelz, B., Rief, M. & Netz, R. R. Auto-and crosspower spectral analysis of dual trap optical tweezer experiments using Bayesian inference. Rev. Sci. Instrum. 83, 095116 (2012).
48. Moffitt, J. R., Chemla, Y. R., Izhaky, D. & Bustamante, C. Differential detection of dual traps improves the spatial resolution of optical tweezers. Proc. Natl Acad. Sci. USA 103, 9006-9011 (2006). (Pubitemid 43902524)
49. Fang, J. & Li, H. A facile way to tune mechanical properties of artificial elastomeric proteins-based hydrogels. Langmuir. 28, 8260-8265 (2012).
50. Santoro, M. M. & Bolen, D. W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068 (1988).
51. Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906 (2007). (Pubitemid 47308128)
52. Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome. Res. 10, 1794-1805 (2011).