Repeat protein engineering: Creating functional nanostructures/biomaterials from modular building blocks

Biochemical Society Transactions

Volumn 41, Issue 5, 2013, Pages 1152-1158

  Main, Ewan R G ^a   Phillips, Jonathan J ^a,b   Millership, Charlotte ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b MEDIMMUNE   (United States)

Author keywords

roll motif; Engineering biomaterial; Protein design; Repeat protein; Tetratricopeptide repeat

Indexed keywords

ANKYRIN; BETA HELICAL BETA ROLL PROTEIN; BIOMATERIAL; LEUCINE RICH REPEAT PROTEIN; NANOMATERIAL; PROTEIN; TETRATRICOPEPTIDE REPEAT PROTEIN; TRANSCRIPTION ACTIVATOR LIKE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; BIOSENSOR; FIBER; HYDROGEL; MORPHOLOGY; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SYNTHESIS;

BIOCOMPATIBLE MATERIALS; BIOSENSING TECHNIQUES; HUMANS; NANOSTRUCTURES; PROTEIN ENGINEERING; PROTEIN INTERACTION MAPS; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84884635701     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130102     Document Type: Article

References (50)

1. Itzhaki, L.S. and Lowe, A.R. (2012) From artificial antibodies to nanosprings: the biophysical properties of repeat proteins. Adv. Exp. Med. Biol. 747, 153-166
2. Main, E.R., Lowe, A.R., Mochrie, S.G., Jackson, S.E. and Regan, L. (2005) A recurring theme in protein engineering: the design, stability and folding of repeat proteins. Curr. Opin. Struct. Biol. 15, 464-471
3. Main, E.R., Jackson, S.E. and Regan, L. (2003) The folding and design of repeat proteins: reaching a consensus. Curr. Opin. Struct. Biol. 13, 482-489
4. Lee, G., Abdi, K., Jiang, Y., Michaely, P., Bennett, V. and Marszalek, P.E. (2006) Nanospring behaviour of ankyrin repeats. Nature 440, 246-249
5. Kobe, B. and Kajava, A.V. (2001) The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11, 725-732
6. Groves, M.R. and Barford, D. (1999) Topological characteristics of helical repeat proteins. Curr. Opin. Struct. Biol. 9, 383-389
7. Crookes, W.J., Ding, L.L., Huang, Q.L., Kimbell, J.R., Horwitz, J. and McFall-Ngai, M.J. (2004) Reflectins: the unusual proteins of squid reflective tissues. Science 303, 235-238
8. Sedgwick, S.G. and Smerdon, S.J. (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem. Sci. 24, 311-316
9. Varadamsetty, G., Tremmel, D., Hansen, S., Parmeggiani, F. and Plückthun, A. (2012) Designed Armadillo repeat proteins: library generation, characterization and selection of peptide binders with high specificity. J. Mol. Biol. 424, 68-87
10. Tamaskovic, R., Simon, M., Stefan, N., Schwill, M. and Plückthun, A. (2012) Designed ankyrin repeat proteins (DARPins) from research to therapy. Methods Enzymol. 503, 101-134
11. Lee, S.C., Park, K., Han, J., Lee, J.J., Kim, H.J., Hong, S., Heu, W., Kim, Y.J., Ha, J.S., Lee, S.G. et al. (2012) Design of a binding scaffold based on variable lymphocyte receptors of jawless vertebrates by module engineering. Proc. Natl. Acad. Sci. U.S.A. 109, 3299-3304
12. Urvoas, A., Guellouz, A., Valerio-Lepiniec, M., Graille, M., Durand, D., Desravines, D.C., van Tilbeurgh, H., Desmadril, M. and Minard, P. (2010) Design, production and molecular structure of a new family of artificial α-helicoidal repeat proteins (αRep) based on thermostable HEAT-like repeats. J. Mol. Biol. 404, 307-327
13. Javadi, Y. and Main, E.R. (2009) Exploring the folding energy landscape of a series of designed consensus tetratricopeptide repeat proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 17383-17388
14. Tripp, K.W. and Barrick, D. (2008) Rerouting the folding pathway of the Notch ankyrin domain by reshaping the energy landscape. J. Am. Chem. Soc. 130, 5681-5688
15. Steiner, D., Forrer, P. and Plückthun, A. (2008) Efficient selection of DARPins with sub-nanomolar affinities using SRP phage display. J. Mol. Biol. 382, 1211-1227
16. Courtemanche, N. and Barrick, D. (2008) The leucine-rich repeat domain of Internalin B folds along a polarized N-terminal pathway. Structure 16, 705-714
17. Lowe, A.R. and Itzhaki, L.S. (2007) Rational redesign of the folding pathway of a modular protein. Proc. Natl. Acad. Sci. U.S.A. 104, 2679-2684
18. Main, E.R., Stott, K., Jackson, S.E. and Regan, L. (2005) Local and long-range stability in tandemly arrayed tetratricopeptide repeats. Proc. Natl. Acad. Sci. U.S.A. 102, 5721-5726
19. Kajander, T., Cortajarena, A.L., Main, E.R., Mochrie, S.G. and Regan, L. (2005) A new folding paradigm for repeat proteins. J. Am. Chem. Soc. 127, 10188-10190
20. Main, E.R., Xiong, Y., Cocco, M.J., D'Andrea, L. and Regan, L. (2003) Design of stable α-helical arrays from an idealized TPR motif. Structure 11, 497-508
21. Kohl, A., Binz, H.K., Forrer, P., Stumpp, M.T., Plückthun, A. and Grutter, M.G. (2003) Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl. Acad. Sci. U.S.A. 100, 1700-1705
22. Forrer, P., Stumpp, M.T., Binz, H.K. and Plückthun, A. (2003) A novel strategy to design binding molecules harnessing the modular nature of repeat proteins. FEBS Lett. 539, 2-6
23. Mosavi, L.K., Minor, D.L. and Peng, Z.Y. (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl. Acad. Sci. U.S.A. 99, 16029-16034
24. Cortajarena, A.L., Liu, T.Y., Hochstrasser, M. and Regan, L. (2010) Designed proteins to modulate cellular networks. ACS Chem. Biol. 5, 545-552
25. Cortajarena, A.L., Yi, F. and Regan, L. (2008) Designed TPR modules as novel anticancer agents. ACS Chem. Biol. 3, 161-166
26. Cermak, T., Doyle, E.L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J.A., Somia, N.V., Bogdanove, A.J. and Voytas, D.F. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82
27. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. and Bonas, U. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512
28. Phillips, J.J., Javadi, Y., Millership, C. and Main, E.R. (2012) Modulation of the multistate folding of designed TPR proteins through intrinsic and extrinsic factors. Protein Sci. 21, 327-338
29. Cortajarena, A.L. and Regan, L. (2011) Calorimetric study of a series of designed repeat proteins: modular structure and modular folding. Protein Sci. 20, 336-340
30. Tripp, K.W. and Barrick, D. (2004) The tolerance of a modular protein to duplication and deletion of internal repeats. J. Mol. Biol. 344, 169-178
31. Kloss, E., Courtemanche, N. and Barrick, D. (2008) Repeat-protein folding: new insights into origins of cooperativity, stability, and topology. Arch. Biochem. Biophys. 469, 83-99
32. Grove, T.Z., Cortajarena, A.L. and Regan, L. (2008) Ligand binding by repeat proteins: natural and designed. Curr. Opin. Struct. Biol. 18, 507-515
33. Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G.M. and Arlotta, P. (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol. 29, 149-153
34. Aksel, T., Majumdar, A. and Barrick, D. (2011) The contribution of entropy, enthalpy, and hydrophobic desolvation to cooperativity in repeat-protein folding. Structure 19, 349-360
35. Aksel, T. and Barrick, D. (2009) Analysis of repeat-protein folding using nearest-neighbor statistical mechanical models. Methods Enzymol. 455, 95-125
36. Cortajarena, A.L., Mochrie, S.G. and Regan, L. (2008) Mapping the energy landscape of repeat proteins using NMR-detected hydrogen exchange. J. Mol. Biol. 379, 617-626
37. Mello, C.C. and Barrick, D. (2004) An experimentally determined protein folding energy landscape. Proc. Natl. Acad. Sci. U.S.A. 101, 14102-14107
38. Grove, T.Z., Osuji, C.O., Forster, J.D., Dufresne, E.R. and Regan, L. (2010) Stimuli-responsive smart gels realized via modular protein design. J. Am. Chem. Soc. 132, 14024-14026
39. Grove, T.Z., Regan, L. and Cortajarena, A.L. (2013) Nanostructured functional films from engineered repeat proteins. J. R. Soc. Interface 10, 20130051
40. Phillips, J.J., Millership, C. and Main, E.R. (2012) Fibrous nanostructures from the self-assembly of designed repeat protein modules. Angew. Chem. Int. Ed. 51, 13132-13135
41. Sawyer, N., Speltz, E.B. and Regan, L. (2013) Next Gen protein design. Biochem. Soc. Trans. 41, 1131-1136
42. Eisenberg, M., Shumacher, I., Cohen-Luria, R. and Ashkenasy, G. (2013) Dynamic combinatorial libraries of artificial repeat proteins. Bioorg. Med. Chem. 21, 3450-3457
43. Krachler, A.M., Sharma, A. and Kleanthous, C. (2010) Self-association of TPR domains: lessons learned from a designed, consensus-based TPR oligomer. Proteins 78, 2131-2143
44. 6 tag-assisted chemical protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 102, 5014-5019
45. Chenal, A., Guijarro, J.I., Raynal, B., Delepierre, M. and Ladant, D. (2009) RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion. J. Biol. Chem. 284, 1781-1789
46. Dooley, K., Kim, Y.H., Lu, H.D., Tu, R. and Banta, S. (2012) Engineering of an environmentally responsive β roll peptide for use as a calcium-dependent cross-linking domain for peptide hydrogel formation. Biomacromolecules 13, 1758-1764
47. Scotter, A.J., Guo, M., Tomczak, M.M., Daley, M.E., Campbell, R.L., Oko, R.J., Bateman, D.A., Chakrabartty, A., Sykes, B.D. and Davies, P.L. (2007) Metal ion-dependent, reversible, protein filament formation by designed β-roll polypeptides. BMC Struct. Biol. 7, 63
48. Simon, M., Zangemeister-Wittke, U. and Plückthun, A. (2012) Facile double-functionalization of designed ankyrin repeat proteins using Click and thiol chemistries. Bioconjugate Chem. 23, 279-286
49. Chang, P.V., Prescher, J.A., Sletten, E.M., Baskin, J.M., Miller, I.A., Agard, N.J., Lo, A. and Bertozzi, C.R. (2010) Copper-free Click chemistry in living animals. Proc. Natl. Acad. Sci. U.S.A. 107, 1821-1826
50. Werbeck, N.D. and Itzhaki, L.S. (2007) Probing a moving target with a plastic unfolding intermediate of an ankyrin-repeat protein. Proc. Natl. Acad. Sci. U.S.A. 104, 7863-7868