Recombination of protein fragments: A promising approach toward engineering proteins with novel nanomechanical properties

Protein Science

Volumn 17, Issue 10, 2008, Pages 1815-1826

  Balamurali, M M ^a   Sharma, Deepak ^a   Chang, Anderson ^a   Khor, Dingyue ^a   Chu, Ricky ^a   Li, Hongbin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Elastomeric protein; Mechanical stability; Mechanical unfolding; Recombination; Single molecule force spectroscopy

Indexed keywords

CONNECTIN; HYBRID PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; GENETIC RECOMBINATION; HUMAN; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; DNA SHUFFLING; ELASTICITY; HUMANS; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; NANOSTRUCTURES; PEPTIDES; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN KINASES; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC;

EID: 52949145661     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.036376.108     Document Type: Article

References (50)

1. Arnold, F.H. and Georgiou, G. 2003. Directed enzyme evolution. Humana Press Inc, Clifton, NJ.
2. Ashworth, J., Havranek, J.J., Duarte, C.M., Sussman, D., Monnat Jr., R.J., Stoddard, B.L., and Baker, D. 2006. Computational redesign of endonuclease DNA binding and cleavage specificity. Nature 441: 656-659.
3. Bao, G. and Suresh, S. 2003. Cell and molecular mechanics of biological materials. Nat. Mater. 2: 715-725.
4. Becker, N., Oroudjev, E., Mutz, S., Cleveland, J.P., Hansma, P.K., Hayashi, C.Y., Makarov, D.E., and Hansma, H.G. 2003. Molecular nanosprings in spider capture-silk threads. Nat. Mater. 2: 278-283.
5. Best, R.B., Li, B., Steward, A., Daggett, V., and Clarke, J. 2001. Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys. J. 81: 2344-2356.
6. Bittker, J.A., Le, B.V., Liu, J.M., and Liu, D.R. 2004. Directed evolution of protein enzymes using nonhomologous random recombination. Proc. Natl. Acad. Sci. 101: 7011-7016.
7. Bloom, J.D., Meyer, M.M., Meinhold, P., Otey, C.R., MacMillan, D., and Arnold, F.H. 2005. Evolving strategies for enzyme engineering. Curr. Opin. Struct. Biol. 15: 447-452.
8. Brockwell, D.J., Beddard, G.S., Paci, E., West, D.K., Olmsted, P.D., Smith, D.A., and Radford, S.E. 2005. Mechanically unfolding the small, topologically simple protein L. Biophys. J. 89: 506-519.
9. Cao, Y. and Li, H. 2007. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat. Mater. 6: 109-114.
10. Cao, Y., Lam, C., Wang, M., and Li, H. 2006. Nonmechanical protein can have significant mechanical stability. Angew. Chem. Int. Ed. Engl. 45: 642-645.
11. Carbone, M.N. and Arnold, F.H. 2007. Engineering by homologous recombination: Exploring sequence and function within a conserved fold. Curr. Opin. Struct. Biol. 17: 454-459.
12. Carrion-Vazquez, M., Marszalek, P.E., Oberhauser, A.F., and Fernandez, J.M. 1999a. Atomic force microscopy captures length phenotypes in single proteins. Proc. Natl. Acad. Sci. 96: 11288-11292.
13. Carrion-Vazquez, M., Oberhauser, A.F., Fowler, S.B., Marszalek, P.E., Broedel, S.E., Clarke, J., and Fernandez, J.M. 1999b. Mechanical and chemical unfolding of a single protein: A comparison. Proc. Natl. Acad. Sci. 96: 3694-3699.
14. Cecconi, C., Shank, E.A., Bustamante, C., and Marqusee, S. 2005. Direct observation of the three-state folding of a single protein molecule. Science 309: 2057-2060.
15. Dietz, H. and Rief, M. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. 101: 16192-16197.
16. Elvin, C.M., Carr, A.G., Huson, M.G., Maxwell, J.M., Pearson, R.D., Vuocolo, T., Liyou, N.E., Wong, D.C., Merritt, D.J., and Dixon, N.E. 2005. Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437: 999-1002.
17. Evans, E. 2001. Probing the relation between force-lifetime and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30: 105-128.
18. Fisher, T.E., Oberhauser, A.F., Carrion-Vazquez, M., Marszalek, P.E., and Fernandez, J.M. 1999. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24: 379-384.
19. Fowler, S.B. and Clarke, J. 2001. Mapping the folding pathway of an immunoglobulin domain: Structural detail from φ value analysis and movement of the transition state. Structure 9: 355-366.
20. Goodsell, D.S. 2004. Bionanotechnology. Wiley-Liss, Hoboken, NJ.
21. Gosline, J.M., Guerette, P.A., Ortlepp, C.S., and Savage, K.N. 1999. The mechanical design of spider silks: From fibroin sequence to mechanical function. J. Exp. Biol. 202: 3295-3303.
22. Gosline, J., Lillie, M., Carrington, E., Guerette, P., Ortlepp, C., and Savage, K. 2002. Elastic proteins: Biological roles and mechanical properties. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 121-132.
23. Griswold, K.E., Kawarasaki, Y., Ghoneim, N., Benkovic, S.J., Iverson, B.L., and Georgiou, G. 2005. Evolution of highly active enzymes by homology-independent recombination. Proc. Natl. Acad. Sci. 102: 10082-10087.
24. Jiang, L., Althoff, E.A., Clemente, F.R., Doyle, L., Rothlisberger, D., Zanghellini, A., Gallaher, J.L., Betker, J.L., Tanaka, F., Barbas III., C.F., et al. 2008. De novo computational design of retro-aldol enzymes. Science 319: 1387-1391.
25. Kellermayer, M.S., Smith, S.B., Granzier, H.L., and Bustamante, C. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276: 1112-1116.
26. Kortemme, T. and Baker, D. 2004. Computational design of protein-protein interactions. Curr. Opin. Chem. Biol. 8: 91-97.
27. Labeit, S. and Kolmerer, B. 1995. Titins: Giant proteins in charge of muscle ultrastructure and elasticity. Science 270: 293-296.
28. Li, H. 2007. Engineering proteins with tailored nanomechanical properties: A single molecule approach. Org. Biomol. Chem. 5: 3399-3406.
29. Li, H., Carrion-Vazquez, M., Oberhauser, A.F., Marszalek, P.E., and Fernandez, J.M. 2000a. Point mutations alter the mechanical stability of immunoglobulin modules. Nat. Struct. Biol. 7: 1117-1120.
30. Li, H., Oberhauser, A.F., Fowler, S.B., Clarke, J., and Fernandez, J.M. 2000b. Atomic force microscopy reveals the mechanical design of a modular protein. Proc. Natl. Acad. Sci. 97: 6527-6531.
31. Li, H., Oberhauser, A.F., Redick, S.D., Carrion-Vazquez, M., Erickson, H.P., and Fernandez, J.M. 2001. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. 98: 10682-10686.
32. Li, H., Linke, W.A., Oberhauser, A.F., Carrion-Vazquez, M., Kerkvliet, J.G., Lu, H., Marszalek, P.E., and Fernandez, J.M. 2002. Reverse engineering of the giant muscle protein titin. Nature 418: 998-1002.
33. Li, Y., Drummond, D.A., Sawayama, A.M., Snow, C.D., Bloom, J.D., and Arnold, F.H. 2007.Adiverse family of thermostable cytochrome P450s created by recombination of stabilizing fragments. Nat. Biotechnol. 25: 1051-1056.
34. Lu, H., Isralewitz, B., Krammer, A., Vogel, V., and Schulten, K. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75: 662-671.
35. Lu, H. and Schulten, K. 2000. The key event in force-induced unfolding of Titin's immunoglobulin domains. Biophys. J. 79: 51-65.
36. Meyer, M.M., Silberg, J.J., Voigt, C.A., Endelman, J.B., Mayo, S.L., Wang, Z.G., and Arnold, F.H. 2003. Library analysis of SCHEMA-guided protein recombination. Protein Sci. 12: 1686-1693.
37. Meyer, M.M., Hochrein, L., and Arnold, F.H. 2006. Structure-guided SCHEMA recombination of distantly related β-lactamases. Protein Eng. Des. Sel. 19: 563-570.
38. Minor Jr., D.L. and Kim, P.S. 1996. Context-dependent secondary structure formation of a designed protein sequence. Nature 380: 730-734.
39. Oberhauser, A.F., Marszalek, P.E., Erickson, H.P., and Fernandez, J.M. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393: 181-185.
40. Otey, C.R., Silberg, J.J., Voigt, C.A., Endelman, J.B., Bandara, G., and Arnold, F.H. 2004. Functional evolution and structural conservation in chimeric cytochromes p450: Calibrating a structure-guided approach. Chem. Biol. 11: 309-318.
41. Pfuhl, M. and Pastore, A. 1995. Tertiary structure of an immunoglobulin-like domain from the giant muscle protein titin: A new member of the I set. Structure 3: 391-401.
42. Politou, A.S., Thomas, D.J., and Pastore, A. 1995. The folding and stability of titin immunoglobulin-like modules, with implications for the mechanism of elasticity. Biophys. J. 69: 2601-2610.
43. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J.M., and Gaub, H.E. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
44. Scott, K.A., Steward, A., Fowler, S.B., and Clarke, J. 2002. Titin; a multi-domain protein that behaves as the sum of its parts. J. Mol. Biol. 315: 819-829.
45. Sharma, D., Cao, Y., and Li, H. 2006. Engineering proteins with novel mechanical properties by recombination of protein fragments. Angew. Chem. Int. Ed. Engl. 45: 5633-5638.
46. Sharma, D., Perisic, O., Peng, Q., Cao, Y., Lam, C., Lu, H., and Li, H. 2007. Single-molecule force spectroscopy reveals a mechanically stable protein fold and the rational tuning of its mechanical stability. Proc. Natl. Acad. Sci. 104: 9278-9283.
47. Tatham, A.S. and Shewry, P.R. 2000. Elastomeric proteins: Biological roles, structures and mechanisms. Trends Biochem. Sci. 25: 567-571.
48. Tskhovrebova, L., Trinick, J., Sleep, J.A., and Simmons, R.M. 1997. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387: 308-312.
49. Voigt, C.A., Martinez, C., Wang, Z.G., Mayo, S.L., and Arnold, F.H. 2002. Protein building blocks preserved by recombination. Nat. Struct. Biol. 9: 553-558.
50. Yang, G., Cecconi, C., Baase, W.A., Vetter, I.R., Breyer, W.A., Haack, J.A., Matthews, B.W., Dahlquist, F.W., and Bustamante, C. 2000. Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme. Proc. Natl. Acad. Sci. 97: 139-144.