Temperature-induced transitions in disordered proteins probed by NMR spectroscopy

Methods in Molecular Biology

Volumn 896, Issue , 2012, Pages 233-247

  Kjaergaard, Magnus ^a   Poulsen, Flemming M ^a   Kragelund, Birthe B ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Chemical shift; Polyproline II; Random coil; Residual structure; Transient helicity

Indexed keywords

PROTEIN;

ARTICLE; CHEMISTRY; HUMAN; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; TEMPERATURE;

HUMANS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEINS; TEMPERATURE;

EID: 84865331977     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-3704-8_15     Document Type: Article

References (70)

1. Uversky VN (2009) Intrinsically disordered proteins and their environment: effects of strong denaturants, temperature, pH, counter ions, membranes, binding partners, osmolytes, and macromolecular crowding. Protein J 28 (7-8):305-325
2. Hsu ST, Bertoncini CW, Dobson CM (2009) Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange-broadening. J Am Chem Soc 131 (21):7222-7223
3. Jaenicke R, Bohm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8(6):738-748
4. Jaenicke R (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc Natl Acad Sci USA 97 (7):2962-2964
5. Xue B, Williams RW, Oldfield CJ, Dunker AK, Uversky VN (2010) Archaic chaos: intrinsically disordered proteins in Archaea. BMC Syst Biol 4 Suppl 1:S1
6. Burra PV, Kalmar L, Tompa P (2010) Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes. PLoS One 5(8):e12069
7. Jarvet J, Damberg P, Danielsson J, Johansson I, Eriksson LE, Graslund A (2003) A left-handed 3(1) helical conformation in the Alzheimer Abeta(12-28) peptide. FEBS Lett 555 (2):371-374
8. Uversky VN, Li J, Fink AL (2001) Evidence for a partially folded intermediate in alphasynuclein fibril formation. J Biol Chem 276 (14):10737-10744
9. Dawson R, Muller L, Dehner A, Klein C, Kessler H, Buchner J (2003) The N-terminal domain of p53 is natively unfolded. J Mol Biol 332(5):1131-1141
10. Gast K, Zirwer D, Damaschun G (2003) Are there temperature-dependent structural transitions in the "intrinsically unstructured" protein prothymosin alpha? Eur Biophys J 31 (8):586-594
11. Jeganathan S, von Bergen M, Mandelkow EM, Mandelkow E (2008) The natively unfolded character of tau and its aggregation to Alzheimer-like paired helical filaments. Biochemistry 47(40):10526-10539
12. Sanchez-Puig N, Veprintsev DB, Fersht AR (2005) Human full-length Securin is a natively unfolded protein. Protein Sci 14(6):1410-1418
13. Malm J, Jonsson M, Frohm B, Linse S (2007) Structural properties of semenogelin I. FEBS J 274(17):4503-4510
14. Kjaergaard M, Norholm AB, Hendus-Altenburger R, Pedersen SF, Poulsen FM, Kragelund BB (2010) Temperature-dependent structural changes in intrinsically disordered proteins: formation of alpha-helices or loss of polyproline II? Protein Sci 19(8):1555-1564
15. Yang WY, Larios E, GruebeleM(2003) On the extended beta-conformation propensity of polypeptides at high temperature. J Am Chem Soc 125(52):16220-16227
16. Nettels D, Muller-Spath S, Kuster F, Hofmann H, Haenni D, Ruegger S, Reymond L, Hoffmann A, Kubelka J, Heinz B, Gast K, Best RB, Schuler B (2009) Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proc Natl Acad Sci USA 106(49):20740-20745
17. Shi Z, Olson CA, Rose GD, Baldwin RL, Kallenbach NR (2002) Polyproline II structure in a sequence of seven alanine residues. Proc Natl Acad Sci USA 99(14):9190-9195
18. Dyson HJ, Wright PE (2002) Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv Protein Chem 62:311-340
19. Mittag T, Forman-Kay JD (2007) Atomic-level characterization of disordered protein ensembles. Curr Opin Struct Biol 17(1):3-14
20. Eliezer D (2009) Biophysical characterization of intrinsically disordered proteins. Curr Opin Struct Biol 19(1):23-30
21. Eliezer D (2007) Characterizing residual structure in disordered protein States using nuclear magnetic resonance. Methods Mol Biol 350:49-67
22. Pickford AR, O'Leary JM (2004) Isotopic labeling of recombinant proteins from the methylotrophic yeast Pichia pastoris. Methods Mol Biol 278:17-33
23. Dawson RMC, Elliot DC, Elliot WH, Jones KM (1986) Data for biochemical research, 3rd edn. Oxford University Press, Oxford, UK.
24. Voehler MW, Collier G, Young JK, Stone MP, Germann MW (2006) Performance of cryogenic probes as a function of ionic strength and sample tube geometry. J Magn Reson 183(1):102-109
25. Kelly AE, Ou HD,Withers R, Dotsch V (2002) Low-conductivity buffers for high-sensitivity NMR measurements. J Am Chem Soc 124 (40):12013-12019
26. Teilum K, Kragelund BB, Poulsen FM (2005) Application of hydrogen exchange kinetics to studies of protein folding. Protein folding handbook. Wiley-VCH Verlag GmbH. doi:10.1002/9783527619498.ch18
27. Kjaergaard M, Iesmantavicius V, Poulsen FM (in press) The interplay between transient a-helix formation and side chain rotamer distributions in disordered proteins probed by methyl chemical shifts. Protein Sci 20(12):2023-34.
28. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6(2):135-140
29. Zhang H, Neal S, Wishart DS (2003) RefDB: a database of uniformly referenced protein chemical shifts. J Biomol NMR25(3):173-195
30. Wang Y, Wishart DS (2005) A simple method to adjust inconsistently referenced 13C and 15N chemical shift assignments of proteins. J Biomol NMR 31(2):143-148
31. Findeisen M, Brand T, Berger S (2007) A 1HNMR thermometer suitable for cryoprobes. Magn Reson Chem 45(2):175-178
32. Grzesiek S, Bax A (1992) Improved 3D tripleresonance NMR techniques applied to a 31-kDa protein. J Magn Reson 96(2):432-440
33. Ikura M, Kay LE, Bax A (1990) A novel approach for sequential assignment of 1H, 13C, and 15N spectra of proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29(19):4659-4667
34. Wittekind M, Mueller L (1993) Hncacb, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-carbon and beta-carbon resonances in proteins. J Magn Reson B 101 (2):201-205
35. Kay LE, Xu GY, Yamazaki T (1994) Enhancedsensitivity triple-resonance spectroscopy with minimal H2O saturation. J Magn Reson A 109(1):129-133
36. Grzesiek S, Bax A (1992) Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114(16):6291-6293
37. Panchal SC, Bhavesh NS, Hosur RV (2001) Improved 3D triple resonance experiments, HNN and HN(C)N, for HN and 15N sequential correlations in (13C, 15N) labeled proteins: application to unfolded proteins. J Biomol NMR 20(2):135-147
38. Ikura M, Kay LE, Bax A (1990) A novelapproach for sequential assignment of H-1, C-13, and N-15 spectra of larger proteins-heteronuclear triple-resonance 3-dimensional NMR-spectroscopy-application to calmodulin. Biochemistry 29(19):4659-4667
39. Yamazaki T, Muhandiram R, Kay LE (1994) NMR experiments for the measurement of carbon relaxation properties in highly enriched, uniformly C-13, N-15-labeled proteins-application to C-13(alpha) carbons. J AmChem Soc 116(18):8266-8278
40. Kjaergaard M, Brander S, Poulsen FM (2011) Random coil chemical shift for intrinsically disordered proteins: effects of temperature and pH. J Biomol NMR 49(2):139-149
41. Mantylahti S, Aitio O, Hellman M, Permi P (2010) HA-detected experiments for the backbone assignment of intrinsically disordered proteins. J Biomol NMR 47(3):171-181
42. Bermel W, Bertini I, Felli IC, Lee YM, Luchinat C, Pierattelli R (2006) Protonless NMR experiments for sequence-specific assignment of backbone nuclei in unfolded proteins. J Am Chem Soc 128(12):3918-3919
43. Ebert MO, Bae SH, Dyson HJ, Wright PE (2008) NMR relaxation study of the complex formed between CBP and the activation domain of the nuclear hormone receptor coactivator ACTR. Biochemistry 47 (5):1299-1308
44. Danielsson J, Liljedahl L, Barany-Wallje E, Sonderby P, Kristensen LH, Martinez-Yamout MA, Dyson HJ, Wright PE, Poulsen FM, Maler L, Graslund A, Kragelund BB (2008) The intrinsically disordered RNR inhibitor Sml1 is a dynamic dimer. Biochemistry 47 (50):13428-13437
45. Wishart DS, Sykes BD, Richards FM (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222(2):311-333
46. Spera S, Bax A (1991) Empirical correlation between protein backbone conformation and C.alpha. and C.beta. 13C nuclear magnetic resonance chemical shifts. J Am Chem Soc 113(14):5490-5492
47. Kim HY, Heise H, Fernandez CO, Baldus M, Zweckstetter M(2007) Correlation of amyloid fibril beta-structure with the unfolded state of alpha-synuclein. Chembiochem 8 (14):1671-1674
48. Wu KP, Kim S, Fela DA, Baum J (2008) Characterization of conformational and dynamic properties of natively unfolded human and mouse alpha-synuclein ensembles by NMR: implication for aggregation. J Mol Biol 378 (5):1104-1115
49. Marsh JA, Singh VK, Jia Z, Forman-Kay JD (2006) Sensitivity of secondary structure propensities to sequence differences between alpha-and gamma-synuclein: implications for fibrillation. Protein Sci 15(12):2795-2804
50. Lam SL, Hsu VL (2003) NMR identification of left-handed polyproline type II helices. Biopolymers 69(2):270-281
51. Iwadate M, Asakura T, Williamson MP (1999) C alpha and C beta carbon-13 chemical shifts in proteins from an empirical database. J Biomol NMR 13(3):199-211
52. Schwarzinger S, Kroon GJ, Foss TR, Wright PE, Dyson HJ (2000) Random coil chemical shifts in acidic 8 M urea: implementation of random coil shift data in NMR view. J Biomol NMR 18(1):43-48
53. Wishart DS, Bigam CG, Holm A, Hodges RS, Sykes BD (1995) 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearestneighbor effects. J Biomol NMR 5(1):67-81
54. De Simone A, Cavalli A, Hsu ST, Vranken W, Vendruscolo M (2009) Accurate random coil chemical shifts from an analysis of loop regions in native states of proteins. J AmChem Soc 131 (45):16332-16333
55. Tamiola K, Acar B, Mulder FA (2010) Sequence-specific random coil chemical shifts of intrinsically disordered proteins. J Am Chem Soc 132(51):18000-18003
56. Schwarzinger S, Kroon GJ, Foss TR, Chung J, Wright PE, Dyson HJ (2001) Sequencedependent correction of random coil NMR chemical shifts. J Am Chem Soc 123 (13):2970-2978
57. Merutka G, Dyson HJ, Wright PE (1995) 'Random coil' 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J Biomol NMR 5(1):14-24
58. Modig K, Jurgensen VW, Lindorff-Larsen K, Fieber W, Bohr HG, Poulsen FM (2007) Detection of initiation sites in protein folding of the four helix bundle ACBP by chemical shift analysis. FEBS Lett 581(25):4965-4971
59. Munoz V, Serrano L (1995) Elucidating the folding problem of helical peptides using empirical parameters. III. Temperature and pH dependence. J Mol Biol 245(3):297-308
60. Gillespie JR, Shortle D (1997) Characterization of long-range structure in the denatured state of staphylococcal nuclease. 1. Paramagnetic relaxation enhancement by nitroxide spin labels. J Mol Biol 268(1):158-169
61. Gillespie JR, Shortle D (1997) Characterization of long-range structure in the denatured state of staphylococcal nuclease. 2. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. J Mol Biol 268(1):170-184
62. Teilum K, Kragelund BB, Poulsen FM (2002) Transient structure formation in unfolded acylcoenzyme A-binding protein observed by sitedirected spin labelling. J Mol Biol 324 (2):349-357
63. Lietzow MA, Jamin M, Dyson HJ, Wright PE (2002) Mapping long-range contacts in a highly unfolded protein. J Mol Biol 322 (4):655-662
64. Jensen MR, Markwick PR, Meier S, Griesinger C, Zweckstetter M, Grzesiek S, Bernado P, Blackledge M (2009) Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings. Structure 17(9):1169-1185
65. Gebel EB, Shortle D (2007) Characterization of denatured proteins using residual dipolar couplings. Methods Mol Biol 350:39-48
66. Rückert M, Otting G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc 122(32):7793-7797
67. Fleming K, Matthews S (2004) Media for studies of partially aligned states. Methods Mol Biol 278:79-88
68. Tycko R, Blanco FJ, Ishii Y (2000) Alignment of biopolymers in strained gels: a new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR. J Am Chem Soc 122(38):9340-9341
69. Demarest SJ, Martinez-Yamout M, Chung J, Chen H, Xu W, Dyson HJ, Evans RM, Wright PE (2002) Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415 (6871):549-553
70. Demarest SJ, Chung J, Dyson HJ, Wright PE (2002) Assignment of a 15 kDa protein complex formed between the p160 coactivator ACTR and CREB binding protein. J Biomol NMR 22(4):377-378