Residue-Resolved Stability of Full-Consensus Ankyrin Repeat Proteins Probed by NMR

Journal of Molecular Biology

Volumn 402, Issue 1, 2010, Pages 241-258

  Wetzel, Svava K ^a   Ewald, Christina ^a   Settanni, Giovanni ^b   Jurt, Simon ^a   Plückthun, Andreas ^a   Zerbe, Oliver ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

Author keywords

Folding; Hydrogen exchange; Ising model; NMR; Repeat proteins

Indexed keywords

ANKYRIN; ANKYRIN REPEAT PROTEIN; DEUTERIUM; PROTON; UNCLASSIFIED DRUG; SPIN LABELING;

AMBIGUITY; AMINO TERMINAL SEQUENCE; ARTICLE; CAPPING PHENOMENON; CARBOXY TERMINAL SEQUENCE; CONSENSUS; DEUTERIUM HYDROGEN EXCHANGE; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; SPIN LABELING; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

ANKYRIN REPEAT; ANKYRINS; CIRCULAR DICHROISM; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPIN LABELS;

EID: 77956176007     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.07.031     Document Type: Article

References (38)

1. Andrade M.A., Perez-Iratxeta C., Ponting C.P. Protein repeats: structures, functions, and evolution. J. Struct. Biol. 2001, 134:117-131.
2. Marcotte E.M., Pellegrini M., Yeates T.O., Eisenberg D. A census of protein repeats. J. Mol. Biol. 1999, 293:151-160.
3. Kobe B., Kajava A.V. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 2000, 25:509-515.
4. Sedgwick S.G., Smerdon S.J. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem. Sci. 1999, 24:311-316.
5. Binz H.K., Amstutz P., Kohl A., Stumpp M.T., Briand C., Forrer P., et al. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 2004, 22:575-582.
6. Binz H.K., Stumpp M.T., Forrer P., Amstutz P., Plückthun A. Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J. Mol. Biol. 2003, 332:489-503.
7. Interlandi G., Wetzel S.K., Settanni G., Plückthun A., Caflisch A. Characterization and further stabilization of designed ankyrin repeat proteins by combining molecular dynamics simulations and experiments. J. Mol. Biol. 2008, 375:837-854.
8. Wetzel S.K., Settanni G., Kenig M., Binz H.K., Plückthun A. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 2008, 376:241-257.
9. Krishna M.M., Hoang L., Lin Y., Englander S.W. Hydrogen exchange methods to study protein folding. Methods 2004, 34:51-64.
10. Zimm B.H., Bragg J.K. Theory of the phase transition between helix and random coil polypeptide chains. J. Chem. Phys. 1959, 31:526-535.
11. Mello C.C., Barrick D. An experimentally determined protein folding energy landscape. Proc. Natl Acad. Sci. USA 2004, 101:14102-14107.
12. Kajander T., Cortajarena A.L., Main E.R., Mochrie S.G., Regan L. A new folding paradigm for repeat proteins. J. Am. Chem. Soc. 2005, 127:10188-10190.
13. Gemmecker G., Jahnke W., Kessler H. Measurements of fast proton-exchange rates in isotopically labeled compounds. J. Am. Chem. Soc. 1993, 115:11620-11621.
14. Palmer A.G. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 2004, 104:3623-3640.
15. Cortajarena A.L., Mochrie S.G., Regan L. Mapping the energy landscape of repeat proteins using NMR-detected hydrogen exchange. J. Mol. Biol. 2008, 379:617-626.
16. Bai Y., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins 1993, 17:75-86.
17. Kohl A., Binz H.K., Forrer P., Stumpp M.T., Plückthun A., Grütter M.G. Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl Acad. Sci. USA 2003, 100:1700-1705.
18. Parmeggiani F., Pellarin R., Larsen A.P., Varadamsetty G., Stumpp M.T., Zerbe O., et al. Designed armadillo repeat proteins as general peptide-binding scaffolds: consensus design and computational optimization of the hydrophobic core. J. Mol. Biol. 2008, 376:1282-1304.
19. Mosavi L.K., Minor D.L.J., Peng Z.Y. Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl Acad. Sci. USA 2002, 99:16029-16034.
20. Merz T., Wetzel S.K., Firbank S., Plückthun A., Grütter M.G., Mittl P.R. Stabilizing ionic interactions in a full-consensus ankyrin repeat protein. J. Mol. Biol. 2008, 376:232-240.
21. Munoz V., Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. Nat. Struct. Biol. 1994, 1:399-409.
22. Pace C.N., Shaw K.L. Linear extrapolation method of analyzing solvent denaturation curves. Proteins 2000, 1-7.
23. Tang K.S., Fersht A.R., Itzhaki L.S. Sequential unfolding of ankyrin repeats in tumor suppressor p16. Structure 2003, 11:67-73.
24. Boice J.A., Fairman R. Structural characterization of the tumor suppressor p16, an ankyrin-like repeat protein. Protein Sci. 1996, 5:1776-1784.
25. Main E.R., Stott K., Jackson S.E., Regan L. Local and long-range stability in tandemly arrayed tetratricopeptide repeats. Proc. Natl Acad. Sci. USA 2005, 102:5721-5726.
26. Lietzow M.A., Jamin M., Dyson H.J., Wright P.E. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 2002, 322:655-662.
27. Hornung T., Volkov O.A., Zaida T.M., Delannoy S., Wise J.G., Vogel P.D. Structure of the cytosolic part of the subunit β-dimer of Escherichia coli F0F1-ATP synthase. Biophys. J. 2008, 94:5053-5064.
28. Kay L.E., Keifer P., Saarien T. Pure absorption gradient enhanced heteronuclear single-quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 1992, 114:10663-10665.
29. Keeler J., Clowes R.T., Davis A.L., Laue E.D. Pulsed-field gradients: theory and practice. Methods Enzymol. 1994, 239:145-207.
30. Shan X., Gardner K.H., Muhandiram D.R., Rao N.S., Arrowsmith C.H., Kay L.E. Assignment of N-15, C-13(alpha), C-13(beta), and HN resonances in an N-15, C-13, H-2 labeled 64 kDa trp repressor-operator complex using triple-resonance NMR spectroscopy and H-2-decoupling. J. Am. Chem. Soc. 1996, 118:6570-6579.
31. McCallum S.A., Hitchens T.K., Rule G.S. Unambiguous correlations of backbone amide and aliphatic gamma resonances in deuterated proteins. J. Magn. Reson. 1998, 134:350-354.
32. Yamazaki T., Lee W., Arrowsmith C.H., Muhandiram D.R., Kay L.E. A suite of triple-resonance NMR experiments for the backbone assignment of N-15,C-13,H2-labeled proteins with high sensitivity. J. Am. Chem. Soc. 1994, 116:11655-11666.
33. 13C-labelled proteins. J. Biomol. NMR 1993, 3:113-120.
34. Noggle J.H., Schirmer R.E. The Nuclear Overhauser Effect-Chemical Applications 1971, Academic Press, New York, NY.
35. Keller R. The Computer Aided Resonance Assignment 2004, CANTINA Verlag, Goldau, Switzerland.
36. Bartels C., Xia T.H., Billeter M., Güntert P., Wüthrich K. The program XEASY for computer-supported spectral analysis of biological macromolecules. J. Biomol. NMR 1995, 6:1-10.
37. Hofmann H., Weininger U., Low C., Golbik R.P., Balbach J., Ulbrich-Hofmann R. Fast amide proton exchange reveals close relation between native-state dynamics and unfolding kinetics. J. Am. Chem. Soc. 2009, 131:140-146.
38. Loftus D., Gbenle G.O., Kim P.S., Baldwin R.L. Effects of denaturants on amide proton exchange rates: a test for structure in protein fragments and folding intermediates. Biochemistry 1986, 25:1428-1436.