NMR Structure of a Monomeric Intermediate on the Evolutionarily Optimized Assembly Pathway of a Small Trimerization Domain

Journal of Molecular Biology

Volumn 389, Issue 1, 2009, Pages 103-114

  Habazettl, Judith ^a   Reiner, Andreas ^b   Kiefhaber, Thomas ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

fibritin; NMR structure; protein assembly; protein folding; protein protein interaction

Indexed keywords

AMINO ACID; BRIDGED PEPTIDE; FIBRITIN; MONOMER; PROTEIN SUBUNIT; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE T4; CONTROLLED STUDY; HYDROGEN BOND; MOLECULAR INTERACTION; MUTATION; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRIMERIZATION;

EID: 67349164760     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.03.073     Document Type: Article

References (44)

1. Tao Y., Strelkov S.V., Mesyanzhinov V.V., and Rossmann M.G. Structure of bacteriophage T4 fibritin: a segmented coiled coil and the role of the C-terminal domain. Structure 5 (1997) 789-798
2. Letarov A.V., Londer Y.Y., Boudko S.P., and Mesyanzhinov V.V. The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin. Biochemistry (Moscow) 64 (1999) 817-823
3. Boudko S.P., Londer Y.Y., Letarov A.V., Sernova N.V., Engel J., and Mesyanzhinov V.V. Domain organization, folding and stability of bacteriophage T4 fibritin, a segmented coiled-coil protein. Eur. J. Biochem. 269 (2002) 833-841
4. Miroshnikov K.A., Marusich E.I., Cerritelli M.E., Cheng N., Hyde C.C., Steven A.C., and Mesyanzhinov V.V. Engineering trimeric fibrous proteins based on bacteriophage T4 adhesins. Protein Eng. 11 (1998) 329-332
5. Frank S., Kammerer R.A., Mechling D., Schulthess T., Landwehr R.J.B., Guo Y., et al. Stabilization of short collagen-like triple helices by protein engineering. J. Mol. Biol. 308 (2001) 1081-1089
6. Yang X., Lee J., Mahony E.M., Kwong P.D., Wyatt R., and Sodroski J. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76 (2002) 4634-4642
7. Papanikolopoulou K., Teixeira S., Belrhali H., Forsyth V.T., Mitraki A., and van Raaij M.J. Adenovirus fibre shaft sequences fold into the native triple beta-spiral fold when N-terminally fused to the bacteriophage T4 fibritin foldon trimerisation motif. J. Mol. Biol. 342 (2004) 219-227
8. Güthe S., Kapinos L., Möglich A., Meier S., Grzesiek S., and Kiefhaber T. Very fast folding and association of a trimerization domain from bacteriophage T4 fibritin. J. Mol. Biol. 337 (2004) 905-915
9. Milla M.E., and Sauer R.T. P22 arc repressor: folding kinetics of a single-domain, dimeric protein. Biochemistry 33 (1994) 1125-1133
10. Jackson S.E. How do small single-domain proteins fold?. Folding Des. 3 (1998) R81-R91
11. Bachmann A., and Kiefhaber T. Apparent two-state tendamistat folding is a sequential process along a defined route. J. Mol. Biol. 306 (2001) 375-386
12. Sánchez I.E., and Kiefhaber T. Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding. J. Mol. Biol. 325 (2003) 367-376
13. Meier S., Güthe S., Kiefhaber T., and Grzesiek S. Foldon-the natural trimerization domain of T4 fibritin-dissociates into a monomeric A-state form containing a stable beta-hairpin. Atomic details of trimer dissociation and local beta-hairpin stability from residual dipolar couplings. J. Mol. Biol. 344 (2004) 1051-1069
14. Wüthrich K., Billeter M., and Braun W. Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol. 180 (1984) 715-740
15. Evans P.A., Topping K.D., Woolfson D.N., and Dobson C.M. Hydrophobic clustering in nonnative states of a protein: interpretation of chemical shifts in NMR spectra of denatured states of lysozyme. Proteins 9 (1991) 248-266
16. Bundi A., and Wüthrich K. Proton NMR parameters of the common amino acid residues in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH. Biopolymers 18 (1979) 285-296
17. Perkins S.J., and Wüthrich K. Ring current effects in the conformation dependent NMR chemical shifts of aliphatic protons in the basic pancreatic trypsin inhibitor. Biochim. Biophys. Acta 576 (1979) 409-423
18. Schwarzinger S., Kroon G.J.A., Foss T.R., Chung J., Wright P.E., and Dyson H.J. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123 (2001) 2970-2978
19. 13C chemical shift data. J. Biomol. NMR 4 (1994) 171-180
20. Pardi A., Wagner G., and Wüthrich K. Protein conformation and proton nuclear-magnetic-resonance chemical shifts. Eur. J. Biochem. 137 (1983) 445-454
21. 1H chemical shifts in proteins. J. Biomol. NMR 9 (1997) 359-369
22. Goto Y., and Nishikiori S. Role of electrostatic repulsion in the acidic molten globule of cytochrome c. J. Mol. Biol. 222 (1991) 679-686
23. Klein-Seetharaman J., Oikawa M., Grimshaw S.B., Wirmer J., Duchardt E., Ueda T., et al. Long-range interactions within a nonnative protein. Science 295 (2002) 1719-1722
24. Peng J.W., and Wagner G. Mapping of the spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry 31 (1992) 8571-8586
25. Schreiber G., and Fersht A.R. Rapid, electrostatically assisted association of proteins. Nat. Struct. Biol. 3 (1996) 427-431
26. Wendt H., Berger C., Baici A., Thomas R.M., and Bosshard H.R. Kinetics of folding of leucine zipper domains. Biochemistry 34 (1995) 4097-4107
27. Bosshard H.R. Concurrent association and folding of small oligomeric proteins. In: Buchner J., and Kiefhaber T. (Eds). Protein Folding Handbook vol. 2 (2005), Wiley/VCH, Weinheim, Germany 965-997 5 vols
28. Wagner C., and Kiefhaber T. Intermediates can accelerate protein folding. Proc. Natl Acad. Sci. USA 96 (1999) 6716-6721
29. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
30. Bax A., and Drobny G. Optimization of two-dimensional homonuclear relayed coherence transfer NMR spectroscopy. J. Magn. Reson. 61 (1985) 306-320
31. Piotto M., Saudek V., and Sklenář V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2 (1992) 661-666
32. Raiford D.S., Fisk C.L., and Becker E.D. Calibration of methanol and ethylene glycol nuclear magnetic resonance thermometers. Anal. Chem. 51 (1979) 2050-2051
33. Grzesiek S., Bax A., Hu J.S., Kaufman J., Palmer I., Stahl S.J., et al. Refined solution structure and backbone dynamics of HIV-1 Nef. Protein Sci. 6 (1997) 1248-1263
34. Holland D.R., Tronrud D.E., Pley H.W., Flaherty K.M., Stark W., Jansonius J.N., et al. Structural comparison suggests that thermolysin and related neutral proteases undergo hinge-bending motion during catalysis. Biochemistry 31 (1992) 11310-11316
35. Ishima R., and Torchia D.A. Estimating the time scale of chemical exchange of proteins from measurements of transverse relaxation rates in solution. J. Biomol. NMR 14 (1999) 369-372
36. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
37. Goddard, T. D. & Kneller, D. G. SPARKY 3, University of California, San Francisco, CA.
38. Güntert P., Braun W., and Wüthrich K. Efficient computation of 3D protein structures. J. Mol. Biol. 217 (1991) 517-530
39. Wüthrich K., Billeter M., and Braun W. Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. J. Mol. Biol. 169 (1983) 949-961
40. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160 (2003) 66-74
41. Linge J.P., Williams M.A., Spronk C.A., Bonvin A.M., and Nilges M. Refinement of protein structures in explicit solvent. Proteins 50 (2003) 496-506
42. Beglov D., and Roux B. Dominant solvation effects from the primary shell of hydration: approximation for molecular dynamics simulations. Biopolymers 35 (1995) 171-178
43. Jorgensen W.L., and Tirado-Rives J. The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110 (1988) 1657-1666
44. Koradi R., Billeter M., and Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14 (1996) 51-55