Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts

Biochemistry

Volumn 51, Issue 11, 2012, Pages 2224-2231

  Camilloni, Carlo ^a   De Simone, Alfonso ^a,c   Vranken, Wim F ^b,d   Vendruscolo, Michele ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL PROPERTIES; DISORDERED PROTEINS; DISORDERED REGIONS; DISORDERED STATE; NUCLEAR MAGNETIC RESONANCE CHEMICAL SHIFTS; POLYPROLINE II; QUANTITATIVE INFORMATION; RANDOM COIL; SECONDARY STRUCTURE ELEMENTS; SECONDARY STRUCTURES; SINGLE STRUCTURE; STRUCTURAL BIOLOGY; SYNUCLEIN;

CHEMICAL SHIFT; MAMMALS; MOLECULAR RECOGNITION; OLIGOMERS; PROBABILITY DISTRIBUTIONS;

PROTEINS;

ALPHA CRYSTALLIN; ALPHA SYNUCLEIN; BETA CRYSTALLIN; PEPTIDE; PROTEIN P53;

ARTICLE; CIRCULAR DICHROISM; HUMAN; MAMMAL; MOLECULAR RECOGNITION; PRION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS;

BINDING SITES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEINS;

MAMMALIAN PRION;

EID: 84858634014     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3001825     Document Type: Article

References (57)

1. Cavalli, A., Salvatella, X., Dobson, C. M., and Vendruscolo, M. (2007) Protein structure determination from NMR chemical shifts Proc. Natl. Acad. Sci. U.S.A. 104, 9615-9620 (Pubitemid 47175315)
2. Shen, Y., Lange, O., Delaglio, F., Rossi, P., Aramini, J. M., Liu, G. H., Eletsky, A., Wu, Y. B., Singarapu, K. K., Lemak, A., Ignatchenko, A., Arrowsmith, C. H., Szyperski, T., Montelione, G. T., Baker, D., and Bax, A. (2008) Consistent blind protein structure generation from NMR chemical shift data Proc. Natl. Acad. Sci. U.S.A. 105, 4685-4690 (Pubitemid 351753807)
3. Shen, Y., Vernon, R., Baker, D., and Bax, A. (2009) De novo protein structure generation from incomplete chemical shift assignments J. Biomol. NMR 43, 63-78
4. Berjanskii, M., Tang, P., Liang, J., Cruz, J. A., Zhou, J. J., Zhou, Y., Bassett, E., MacDonell, C., Lu, P., Lin, G. H., and Wishart, D. S. (2009) GENMR: A web server for rapid NMR-based protein structure determination Nucleic Acids Res. 37, W670-W677
5. Shen, Y., Bryan, P. N., He, Y. N., Orban, J., Baker, D., and Bax, A. (2010) De novo structure generation using chemical shifts for proteins with high-sequence identity but different folds Protein Sci. 19, 349-356
6. Raman, S., Lange, O. F., Rossi, P., Tyka, M., Wang, X., Aramini, J., Liu, G. H., Ramelot, T. A., Eletsky, A., Szyperski, T., Kennedy, M. A., Prestegard, J., Montelione, G. T., and Baker, D. (2010) NMR structure determination for larger proteins using backbone-only data Science 327, 1014-1018
7. Korzhnev, D. M., Religa, T. L., Banachewicz, W., Fersht, A. R., and Kay, L. E. (2010) A transient and low-populated protein-folding intermediate at atomic resolution Science 329, 1312-1316
8. Robustelli, P., Cavalli, A., and Vendruscolo, M. (2008) Determination of protein structures in the solid state from NMR chemical shifts Structure 16, 1764-1769
9. Montalvao, R. W., Cavalli, A., Salvatella, X., Blundell, T. L., and Vendruscolo, M. (2008) Structure determination of protein-protein complexes using NMR chemical shifts: Case of an endonuclease colicin-immunity protein complex J. Am. Chem. Soc. 130, 15990-15996
10. Das, R., Andre, I., Shen, Y., Wu, Y. B., Lemak, A., Bansal, S., Arrowsmith, C. H., Szyperski, T., and Baker, D. (2009) Simultaneous prediction of protein folding and docking at high resolution Proc. Natl. Acad. Sci. U.S.A. 106, 18978-18983
11. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223
12. Cheung, M. S., Maguire, M. L., Stevens, T. J., and Broadhurst, R. W. (2010) Dangle: A Bayesian inferential method for predicting protein backbone dihedral angles and secondary structure J. Magn. Reson. 202, 223-233
13. Wishart, D. S. and Sykes, B. D. (1994) Chemical-shifts as a tool for structure determination Methods Enzymol. 239, 363-392
14. Wang, Y. J. and Jardetzky, O. (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data Protein Sci. 11, 852-861 (Pubitemid 34241293)
15. Hung, L. H. and Samudrala, R. (2003) Accurate and automated classification of protein secondary structure with psicsi Protein Sci. 12, 288-295 (Pubitemid 36120341)
16. Marsh, J. A., Singh, V. K., Jia, Z. C., and Forman-Kay, J. D. (2006) Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: Implications for fibrillation Protein Sci. 15, 2795-2804 (Pubitemid 44833760)
17. Cole, C., Barber, J. D., and Barton, G. J. (2008) The JPRED3 secondary structure prediction server Nucleic Acids Res. 36, W197-W201
18. Schwarzinger, S., Kroon, G. J. A., Foss, T. R., Chung, J., Wright, P. E., and Dyson, H. J. (2001) Sequence-dependent correction of random coil NMR chemical shifts J. Am. Chem. Soc. 123, 2970-2978 (Pubitemid 32879567)
19. De Simone, A., Cavalli, A., Hsu, S. T. D., Vranken, W., and Vendruscolo, M. (2009) Accurate random coil chemical shifts from an analysis of loop regions in native states of proteins J. Am. Chem. Soc. 131, 16332-16333
20. Tamiola, K., Acar, B., and Mulder, F. A. A. (2010) Sequence-specific random coil chemical shifts of intrinsically disordered proteins J. Am. Chem. Soc. 132, 18000-18003
21. Dobson, C. M. (2003) Protein folding and misfolding Nature 426, 884-890 (Pubitemid 38056880)
22. Dyson, H. J. and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6, 197-208 (Pubitemid 40314921)
23. Tompa, P. (2005) The interplay between structure and function in intrinsically unstructured proteins FEBS Lett. 579, 3346-3354 (Pubitemid 40804685)
24. Jensen, M. R., Salmon, L., Nodet, G., and Blackledge, M. (2010) Defining conformational ensembles of intrinsically disordered and partially folded proteins directly from chemical shifts J. Am. Chem. Soc. 132, 1270-1271
25. Berisio, R., Loguercio, S., De Simone, A., Zagari, A., and Vitagliano, L. (2006) Polyproline helices in protein structures: A statistical survey Protein Pept. Lett. 13, 847-854 (Pubitemid 44155186)
26. Modig, K., Jurgensen, V. W., Lindorff-Larsen, K., Fieber, W., Bohr, H. G., and Poulsen, F. M. (2007) Detection of initiation sites in protein folding of the four helix bundle ACBP by chemical shift analysis FEBS Lett. 581, 4965-4971 (Pubitemid 47534206)
27. Kuriyan, J., Petsko, G. A., Levy, R. M., and Karplus, M. (1986) Effect of anisotropy and anharmonicity on protein crystallographic refinement: An evaluation by molecular-dynamics J. Mol. Biol. 190, 227-254
28. Richter, B., Gsponer, J., Varnai, P., Salvatella, X., and Vendruscolo, M. (2007) The MUMO (minimal under-restraining minimal over-restraining) method for the determination of native state ensembles of proteins J. Biomol. NMR 37, 117-135 (Pubitemid 46157977)
29. Marsh, J. A. and Forman-Kay, J. D. (2012) Ensemble modeling of protein disordered states: Experimental restraint contributions and validation Proteins 80, 556-572
30. Shen, Y. and Bax, A. (2010) Sparta plus: A modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network J. Biomol. NMR 48, 13-22
31. Han, B., Liu, Y. F., Ginzinger, S. W., and Wishart, D. S. (2011) SHIFTX2: Significantly improved protein chemical shift prediction J. Biomol. NMR 50, 43-57
32. Heinig, M. and Frishman, D. (2004) Stride: A web server for secondary structure assignment from known atomic coordinates of proteins Nucleic Acids Res. 32, W500-W502
33. Stapley, B. J. and Creamer, T. P. (1999) A survey of left-handed polyproline II helices Protein Sci. 8, 587-595 (Pubitemid 29117973)
34. Gsponer, J., Hopearuoho, H., Whittaker, S. B. M., Spence, G. R., Moore, G. R., Paci, E., Radford, S. E., and Vendruscolo, M. (2006) Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein im7 Proc. Natl. Acad. Sci. U.S.A. 103, 99-104 (Pubitemid 43076111)
35. Jensen, M. R., Houben, K., Lescop, E., Blanchard, L., Ruigrok, R. W. H., and Blackledge, M. (2008) Quantitative conformational analysis of partially folded proteins from residual dipolar couplings: Application to the molecular recognition element of sendai virus nucleoprotein J. Am. Chem. Soc. 130, 8055-8061 (Pubitemid 351875082)
36. Lawrence, C. W., Bonny, A., and Showalter, S. A. (2011) The disordered C-terminus of the RNA polymerase II phosphatase FCP1 is partially helical in the unbound state Biochem. Biophys. Res. Commun. 410, 461-465
37. Vousden, K. H. and Lane, D. P. (2007) P53 in health and disease Nat. Rev. Mol. Cell Biol. 8, 275-283 (Pubitemid 46474662)
38. Teufel, D. P., Freund, S. M., Bycroft, M., and Fersht, A. R. (2007) Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53 Proc. Natl. Acad. Sci. U.S.A. 104, 7009-7014 (Pubitemid 47186000)
39. Wells, M., Tidow, H., Rutherford, T. J., Markwick, P., Jensen, M. R., Mylonas, E., Svergun, D. I., Blackledge, M., and Fersht, A. R. (2008) Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain Proc. Natl. Acad. Sci. U.S.A. 105, 5762-5767 (Pubitemid 351758446)
40. Hardy, J. and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimers disease: Progress and problems on the road to therapeutics Science 297, 353-356 (Pubitemid 34790756)
41. Hou, L. M., Shao, H. Y., Zhang, Y. B., Li, H., Menon, N. K., Neuhaus, E. B., Brewer, J. M., Byeon, I. J. L., Ray, D. G., Vitek, M. P., Iwashita, T., Makula, R. A., Przybyla, A. B., and Zagorski, M. G. (2004) Solution NMR studies of the Aβ(1-40) and Aβ(1-42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation J. Am. Chem. Soc. 126, 1992-2005 (Pubitemid 38228879)
42. Spillantini, M. G., Schmidt, M. L., Lee, V. M. Y., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) α-Synuclein in Lewy bodies Nature 388, 839-840
43. Uversky, V. N., Li, J., Souillac, P., Millett, I. S., Doniach, S., Jakes, R., Goedert, M., and Fink, A. L. (2002) Biophysical properties of the synucleins and their propensities to fibrillate: Inhibition of α-synuclein assembly by β- and γ-synucleins J. Biol. Chem. 277, 11970-11978 (Pubitemid 34952757)
44. Bertoncini, C. W., Rasia, R. M., Lamberto, G. R., Binolfi, A., Zweckstetter, M., Griesinger, C., and Fernandez, C. O. (2007) Structural characterization of the intrinsically unfolded protein β-synuclein, a natural negative regulator of α-synuclein aggregation J. Mol. Biol. 372, 708-722 (Pubitemid 47313489)
45. Rao, J. N., Kim, Y. E., Park, L. S., and Ulmer, T. S. (2009) Effect of pseudorepeat rearrangement on α-synuclein misfolding, vesicle binding, and micelle binding J. Mol. Biol. 390, 516-529
46. Ninkina, N., Peters, O., Millership, S., Salem, H., van der Putten, H., and Buchman, V. L. (2009) γ-Synucleinopathy: Neurodegeneration associated with overexpression of the mouse protein Hum. Mol. Genet. 18, 1779-1794
47. Chandra, S., Chen, X. C., Rizo, J., Jahn, R., and Sudhof, T. C. (2003) A broken α-helix in folded α-synuclein J. Biol. Chem. 278, 15313-15318
48. Prusiner, S. B. (1998) Prions Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383 (Pubitemid 28525623)
49. Zahn, R., Liu, A. Z., Luhrs, T., Riek, R., von Schroetter, C., Garcia, F. L., Billeter, M., Calzolai, L., Wider, G., and Wuthrich, K. (2000) NMR solution structure of the human prion protein Proc. Natl. Acad. Sci. U.S.A. 97, 145-150 (Pubitemid 30055798)
50. Tartaglia, G. G., Pawar, A. P., Campioni, S., Dobson, C. M., Chiti, F., and Vendruscolo, M. (2008) Prediction of aggregation-prone regions in structured proteins J. Mol. Biol. 380, 425-436
51. Blanch, E. W., Gill, A. C., Rhie, A. G. O., Hope, J., Hecht, L., Nielsen, K., and Barron, L. D. (2004) Raman optical activity demonstrates poly(l -proline) II helix in the N-terminal region of the ovine prion protein: Implications for function and misfunction J. Mol. Biol. 343, 467-476 (Pubitemid 39296879)
52. Lysek, D. A. and Wuthrich, K. (2004) Prion protein interaction with the C-terminal SH3 domain of GRB2 studied using NMR and optical spectroscopy Biochemistry 43, 10393-10399 (Pubitemid 39079313)
53. Gerum, C., Schlepckow, K., and Schwalbe, H. (2010) The unfolded state of the murine prion protein and properties of single-point mutants related to human prion diseases J. Mol. Biol. 401, 7-12
54. Shi, Z. S., Chen, K., Liu, Z. G., and Kallenbach, N. R. (2006) Conformation of the backbone in unfolded proteins Chem. Rev. 106, 1877-1897 (Pubitemid 43792784)
55. Horwitz, J. (1992) α-Crystallin can function as a molecular chaperone Proc. Natl. Acad. Sci. U.S.A. 89, 10449-10453
56. Jehle, S., Rajagopal, P., Bardiaux, B., Markovic, S., Kuhne, R., Stout, J. R., Higman, V. A., Klevit, R. E., van Rossum, B. J., and Oschkinat, H. (2010) Solid-state NMR and saxs studies provide a structural basis for the activation of αβ-crystallin oligomers Nat. Struct. Mol. Biol. 17, 1037-1043
57. Whitmore, L. and Wallace, B. A. (2008) Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 89, 392-400