Structural characterization of intrinsically disordered proteins by NMR spectroscopy

Molecules

Volumn 18, Issue 9, 2013, Pages 10802-10828

  Kosol, Simone ^a   Contreras Martos, Sara ^a   Cedeño, Cesyen ^a   Tompa, Peter ^a,b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

13C direct detected NMR; IDPs; In cell NMR; NMR spectroscopy

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN PROCESSING; REVIEW;

ANIMALS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84885105947     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules180910802     Document Type: Review

References (135)

1. Pancsa, R.; Tompa, P. Structural disorder in eukaryotes. PLoS one 2012, 7, e34687.
2. Tompa, P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 2005, 579, 3346-3354. (Pubitemid 40804685)
3. Wright, P.E.; Dyson, H.J. Linking folding and binding. Curr. Opin. Struct. Biol. 2009, 19, 31-38.
4. Tompa, P.; Fuxreiter, M. Fuzzy complexes: polymorphism and structural disorder in proteinprotein interactions. Trends Biochem. Sci. 2008, 33, 2-8.
5. Rezaei-Ghaleh, N.; Blackledge, M.; Zweckstetter, M. Intrinsically disordered proteins: From sequence and conformational properties toward drug discovery. ChemBioChem 2012, 13, 930-950.
6. Borcherds, W.; Kashtanov, S.; Wu, H.; Daughdrill, G.W. Structural divergence is more extensive than sequence divergence for a family of intrinsically disordered proteins. Proteins 2013, doi:10.1002/prot.24303.
7. Tompa, P. On the supertertiary structure of proteins. Nat. Chem. Biol. 2012, 8, 597-600.
8. Babu, M.M.; van der Lee, R.; de Groot, N.S.; Gsponer, J. Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 2011, 21, 432-440.
9. Hammoudeh, D.I.; Follis, A.V.; Prochownik, E.V.; Metallo, S.J. Multiple independent binding sites for small-molecule inhibitors on the oncoprotein c-Myc. JACS 2009, 131, 7390-7401.
10. Lamberto, G.R.; Binolfi, A.; Orcellet, M.L.; Bertoncini, C.W.; Zweckstetter, M.; Griesinger, C.; Fernandez, C.O. Structural and mechanistic basis behind the inhibitory interaction of PcTS on alpha-synuclein amyloid fibril formation. PNAS 2009, 106, 21057-21062.
11. Eliezer, D. Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 2009, 19, 23-30.
12. Ozenne, V.; Bauer, F.; Salmon, L.; Huang, J.R.; Jensen, M.R.; Segard, S.; Bernado, P.; Charavay, C.; Blackledge, M. Flexible-meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 2012, 28, 1463-1470.
13. Fisher, C.K.; Stultz, C.M. Constructing ensembles for intrinsically disordered proteins. Curr. Opin. Struct. Biol. 2011, 21, 426-431.
14. Schneider, R.; Huang, J.R.; Yao, M.; Communie, G.; Ozenne, V.; Mollica, L.; Salmon, L.; Jensen, M.R.; Blackledge, M. Towards a robust description of intrinsic protein disorder using nuclear magnetic resonance spectroscopy. Mol. Biosyst. 2012, 8, 58-68.
15. Dyson, H.J.; Wright, P.E. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 2004, 104, 3607-3622.
16. McCann, J.J.; Zheng, L.; Rohrbeck, D.; Felekyan, S.; Kuhnemuth, R.; Sutton, R.B.; Seidel, C.A.; Bowen, M.E. Supertertiary structure of the synaptic MAGuK scaffold proteins is conserved. PNAS 2012, 109, 15775-15780.
17. Zhang, J.; Lewis, S.M.; Kuhlman, B.; Lee, A.L. Supertertiary structure of the MAGUK core from PSD-95. Structure 2013, 21, 402-413.
18. Jensen, M.R.; Ruigrok, R.W.; Blackledge, M. Describing intrinsically disordered proteins at atomic resolution by NMR. Curr. Opin. Struct. Biol. 2013, 23, 426-435.
19. Sibille, N.; Bernado, P. Structural characterization of intrinsically disordered proteins by the combined use of NMR and SAXS. Biochem. Soc. Trans. 2012, 40, 955-962.
20. Felli, I.C.; Pierattelli, R. Recent progress in NMR spectroscopy: toward the study of intrinsically disordered proteins of increasing size and complexity. IUBMB life 2012, 64, 473-481.
21. Mantylahti, S.; Hellman, M.; Permi, P. Extension of the HA-detection based approach: (HCA)CON(CA)H and (HCA)NCO(CA)H experiments for the main-chain assignment of intrinsically disordered proteins. J. Biomol. NMR 2011, 49, 99-109.
22. Motackova, V.; Novacek, J.; Zawadzka-Kazimierczuk, A.; Kazimierczuk, K.; Zidek, L.; Sanderova, H.; Krasny, L.; Kozminski, W.; Sklenar, V. Strategy for complete NMR assignment of disordered proteins with highly repetitive sequences based on resolution-enhanced 5D experiments. J. Biomol. NMR 2010, 48, 169-177.
23. Zawadzka-Kazimierczuk, A.; Kozminski, W.; Sanderova, H.; Krasny, L. High dimensional and high resolution pulse sequences for backbone resonance assignment of intrinsically disordered proteins. J. Biomol. NMR 2012, 52, 329-337.
24. Bermel, W.; Bertini, I.; Felli, I.C.; Lee, Y.M.; Luchinat, C.; Pierattelli, R. Protonless NMR experiments for sequence-specific assignment of backbone nuclei in unfolded proteins. JACS 2006, 128, 3918-3919.
25. Narayanan, R.L.; Durr, U.H.; Bibow, S.; Biernat, J.; Mandelkow, E.; Zweckstetter, M. Automatic assignment of the intrinsically disordered protein Tau with 441-residues. JACS 2010, 132, 11906-11907.
26. Yao, J.; Dyson, H.J.; Wright, P.E. Chemical shift dispersion and secondary structure prediction in unfolded and partly folded proteins. FEBS Lett. 1997, 419, 285-289. (Pubitemid 28010828)
27. Otten, R.; Wood, K.; Mulder, F.A. Comprehensive determination of 3JHNHα for unfolded proteins using 13C′-resolved spin-echo difference spectroscopy. J. Biomol. NMR 2009, 45, 343-349.
28. Bermel, W.; Bruix, M.; Felli, I.C.; Kumar, M.V.V.; Pierattelli, R.; Serrano, S. Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins. J. Biomol. NMR 2013, 55, 231-237.
29. Mukrasch, M.D.; Bibow, S.; Korukottu, J.; Jeganathan, S.; Biernat, J.; Griesinger, C.; Mandelkow, E.; Zweckstetter, M. Structural polymorphism of 441-residue tau at single residue resolution. PLoS Biol. 2009, 7, e34.
30. Lacy, E.R.; Filippov, I.; Lewis, W.S.; Otieno, S.; Xiao, L.; Weiss, S.; Hengst, L.; Kriwacki, R.W. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol. 2004, 11, 358-364. (Pubitemid 38436801)
31. Wells, M.; Tidow, H.; Rutherford, T.J.; Markwick, P.; Jensen, M.R.; Mylonas, E.; Svergun, D.I.; Blackledge, M.; Fersht, A.R. Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. PNAS 2008, 105, 5762-5767. (Pubitemid 351758446)
32. Mittag, T.; Marsh, J.; Grishaev, A.; Orlicky, S.; Lin, H.; Sicheri, F.; Tyers, M.; Forman-Kay, J.D. Structure/function implications in a dynamic complex of the intrinsically disordered Sic1 with the Cdc4 subunit of an SCF ubiquitin ligase. Structure 2010, 18, 494-506.
33. Allison, J.R.; Varnai, P.; Dobson, C.M.; Vendruscolo, M. Determination of the free energy landscape of alpha-synuclein using spin label nuclear magnetic resonance measurements. JACS 2009, 131, 18314-18326.
34. De Simone, A.; Cavalli, A.; Hsu, S.T.; Vranken, W.; Vendruscolo, M. Accurate random coil chemical shifts from an analysis of loop regions in native states of proteins. JACS 2009, 131, 16332-16333.
35. Tamiola, K.; Acar, B.; Mulder, F.A. Sequence-specific random coil chemical shifts of intrinsically disordered proteins. JACS 2010, 132, 18000-18003.
36. Wishart, D.S.; Sykes, B.D. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 1994, 4, 171-180.
37. Braun, D.; Wider, G.; Wuthrich, K. Sequence-Corrected 15N Random Coil Chemical-Shifts. JACS 1994, 116, 8466-8469.
38. Kjaergaard, M.; Poulsen, F.M. Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution. J. Biomol. NMR 2011, 50, 157-165.
39. Schwarzinger, S.; Kroon, G.J.; Foss, T.R.; Chung, J.; Wright, P.E.; Dyson, H.J. Sequencedependent correction of random coil NMR chemical shifts. JACS 2001, 123, 2970-2978. (Pubitemid 32879567)
40. Wishart, D.S.; Bigam, C.G.; Yao, J.; Abildgaard, F.; Dyson, H.J.; Oldfield, E.; Markley, J.L.; Sykes, B.D. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 1995, 6, 135-140.
41. Wang, L.; Eghbalnia, H.R.; Markley, J.L. Nearest-neighbor effects on backbone alpha and beta carbon chemical shifts in proteins. J. Biomol. NMR 2007, 39, 247-257. (Pubitemid 47617509)
42. Kjaergaard, M.; Norholm, A.B.; Hendus-Altenburger, R.; Pedersen, S.F.; Poulsen, F.M.; Kragelund, B.B. Temperature-dependent structural changes in intrinsically disordered proteins: Formation of alpha-helices or loss of polyproline II? Protein Sci. 2010, 19, 1555-1564.
43. Kjaergaard, M.; Poulsen, F.M. Disordered proteins studied by chemical shifts. Prog. Nucl. Magn. Reson. Spectrosc. 2012, 60, 42-51.
44. Kragelj, J.; Ozenne, V.; Blackledge, M.; Jensen, M.R. Conformational Propensities of Intrinsically Disordered Proteins from NMR Chemical Shifts. Chemphyschem. 2013.
45. Karplus, M. Contact Electron-Spin Coupling of Nuclear Magnetic Moments. J. Chem. Phys. 1959, 30, 11-15.
46. Smith, L.J.; Bolin, K.A.; Schwalbe, H.; MacArthur, M.W.; Thornton, J.M.; Dobson, C.M. Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 1996, 255, 494-506. (Pubitemid 26105572)
47. Permi, P.; Kilpelainen, I.; Annila, A. Determination of backbone angle psi in proteins using a TROSY-based alpha/beta-HN(CO)CA-J experiment. J. Magn. Reson. 2000, 146, 55-59.
48. Permi, P. Determination of three-bond scalar coupling between 13C′ and 1Hα in proteins using an iHN(CA),CO(alpha/beta-J-COHA) experiment. J. Magn. Reson. 2003, 163, 114-120.
49. Petit, A.; Vincent, S.J.; Zwahlen, C. Cosine modulated HSQC: a rapid determination of 3JHNHα scalar couplings in 15N-labeled proteins. J. Magn. Reson. 2002, 156, 313-317.
50. Ponstingl, H.; Otting, G. Rapid measurement of scalar three-bond 1HN-1H alpha spin coupling constants in 15N-labelled proteins. J. Biomol. NMR 1998, 12, 319-324.
51. Lendel, C.; Damberg, P. 3D J-resolved NMR spectroscopy for unstructured polypeptides: fast measurement of 3JHNHα coupling constants with outstanding spectral resolution. J. Biomol. NMR 2009, 44, 35-42.
52. Plaxco, K.W.; Morton, C.J.; Grimshaw, S.B.; Jones, J.A.; Pitkeathly, M.; Campbell, I.D.; Dobson, C.M. The effects of guanidine hydrochloride on the ′random coil′ conformations and NMR chemical shifts of the peptide series GGXGG. J. Biomol. NMR 1997, 10, 221-230. (Pubitemid 127504668)
53. Tjandra, N.; Bax, A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 1997, 278, 1111-1114. (Pubitemid 27517889)
54. Jensen, M.R.; Markwick, P.R.; Meier, S.; Griesinger, C.; Zweckstetter, M.; Grzesiek, S.; Bernado, P.; Blackledge, M. Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings. Structure 2009, 17, 1169-1185.
55. Bouvignies, G.; Markwick, P.R.; Blackledge, M. Simultaneous definition of high resolution protein structure and backbone conformational dynamics using NMR residual dipolar couplings. Chemphyschem. 2007, 8, 1901-1909.
56. Fischer, M.W.; Losonczi, J.A.; Weaver, J.L.; Prestegard, J.H. Domain orientation and dynamics in multidomain proteins from residual dipolar couplings. Biochemistry 1999, 38, 9013-9022.
57. Prestegard, J.H.; Bougault, C.M.; Kishore, A.I. Residual dipolar couplings in structure determination of biomolecules. Chem. Rev. 2004, 104, 3519-3540.
58. Mohana-Borges, R.; Goto, N.K.; Kroon, G.J.; Dyson, H.J.; Wright, P.E. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 2004, 340, 1131-1142. (Pubitemid 38968706)
59. Jensen, M.R.; Houben, K.; Lescop, E.; Blanchard, L.; Ruigrok, R.W.; Blackledge, M. Quantitative conformational analysis of partially folded proteins from residual dipolar couplings: application to the molecular recognition element of Sendai virus nucleoprotein. JACS 2008, 130, 8055-61. (Pubitemid 351875082)
60. Salmon, L.; Nodet, G.; Ozenne, V.; Yin, G.; Jensen, M.R.; Zweckstetter, M.; Blackledge, M. NMR characterization of long-range order in intrinsically disordered proteins. JACS 2010, 132, 8407-8418.
61. Tjandra, N.; Omichinski, J.G.; Gronenborn, A.M.; Clore, G.M.; Bax, A. Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 1997, 4, 732-738. (Pubitemid 27382433)
62. Vendruscolo, M. Determination of conformationally heterogeneous states of proteins. Curr. Opin. Struct. Biol. 2007, 17, 15-20. (Pubitemid 46240813)
63. Vendruscolo, M.; Dobson, C.M. Towards complete descriptions of the free-energy landscapes of proteins. Philos. Trans. R. Soc. London Ser. A 2005, 363, 433-450; Discussion 450-452.
64. Krzeminski, M.; Marsh, J.A.; Neale, C.; Choy, W.Y.; Forman-Kay, J.D. Characterization of disordered proteins with ENSEMBLE. Bioinformatics 2013, 29, 398-399.
65. Eliezer, D.; Barre, P.; Kobaslija, M.; Chan, D.; Li, X.; Heend, L. Residual structure in the repeat domain of tau: echoes of microtubule binding and paired helical filament formation. Biochemistry 2005, 44, 1026-1036. (Pubitemid 40129662)
66. Crowhurst, K.A., Forman-Kay, J.D. Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain. Biochemistry 2003, 42, 8687-8695. (Pubitemid 36899811)
67. Ekiel, I.; Abrahamson, M. Folding-related dimerization of human cystatin C. J. Biol. Chem. 1996, 271, 1314-1321. (Pubitemid 26028611)
68. Wilkins, D.K.; Grimshaw, S.B.; Receveur, V.; Dobson, C.M.; Jones, J.A.; Smith, L.J. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 1999, 38, 16424-16431.
69. Waudby, C.A.; Mantle, M.D.; Cabrita, L.D.; Gladden, L.F.; Dobson, C.M.; Christodoulou, J. Rapid distinction of intracellular and extracellular proteins using NMR diffusion measurements. JACS 2012, 134, 11312-11315.
70. Gillespie, J.R.; Shortle, D. Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J. Mol. Biol. 1997, 268, 158-169. (Pubitemid 27192686)
71. 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.
72. Iwahara, J.; Tang, C.; Marius Clore, G. Practical aspects of 1H transverse paramagnetic relaxation enhancement measurements on macromolecules. J. Magn. Reson. 2007, 184, 185-195. (Pubitemid 46177665)
73. Clore, G.M.; Tang, C.; Iwahara, J. Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement. Curr. Opin. Struct. Biol. 2007, 17, 603-616. (Pubitemid 350019011)
74. Pintacuda, G.; Otting, G. Identification of protein surfaces by NMR measurements with a pramagnetic Gd(III) chelate. JACS 2002, 124, 372-373. (Pubitemid 34084122)
75. Su, X.C.; Otting, G. Paramagnetic labelling of proteins and oligonucleotides for NMR. J. Biomol. NMR 2010, 46, 101-112.
76. Akoury, E.; Gajda, M.; Pickhardt, M.; Biernat, J.; Soraya, P.; Griesinger, C.; Mandelkow, E.; Zweckstetter, M. Inhibition of tau filament formation by conformational modulation. JACS 2013, 135, 2853-28562.
77. Bibow, S.; Ozenne, V.; Biernat, J.; Blackledge, M.; Mandelkow, E.; Zweckstetter, M. Structural impact of proline-directed pseudophosphorylation at AT8, AT100, and PHF1 epitopes on 441-residue tau. JACS 2011, 133, 15842-15845.
78. Dedmon, M.M.; Lindorff-Larsen, K.; Christodoulou, J.; Vendruscolo, M.; Dobson, C.M. Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. JACS 2005, 127, 476-477. (Pubitemid 40174345)
79. Zangger, K.; Respondek, M.; Gobl, C.; Hohlweg, W.; Rasmussen, K.; Grampp, G.; Madl, T. Positioning of micelle-bound peptides by paramagnetic relaxation enhancements. J. Phys. Chem. B 2009, 113, 4400-4406.
80. Grossauer, J.; Kosol, S.; Schrank, E.; Zangger, K. The peptide hormone ghrelin binds to membrane-mimetics via its octanoyl chain and an adjacent phenylalanine. Bioorg. Med. Chem. 2010, 18, 5483-5488.
81. Csermely, P.; Palotai, R.; Nussinov, R. Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem. Sci. 2010, 35, 539-546.
82. Palmer, A.G. 3rd. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 2004, 104, 3623-3640.
83. Kim, S.; Wu, K.P.; Baum, J. Fast hydrogen exchange affects 15N relaxation measurements in intrinsically disordered proteins. J. Biomol. NMR 2013, 55, 249-256.
84. Rezaei-Ghaleh, N.; Giller, K.; Becker, S.; Zweckstetter, M. Effect of zinc binding on beta-amyloid structure and dynamics: implications for Abeta aggregation. Biophys. J. 2011, 101, 1202-1211.
85. Farrow, N.A.; Muhandiram, R.; Singer, A.U.; Pascal, S.M.; Kay, C.M.; Gish, G.; Shoelson, S.E.; Pawson, T.; Forman-Kay, J.D.; Kay, L.E. Backbone dynamics of a free and phosphopeptidecomplexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 1994, 33, 5984-6003. (Pubitemid 24184605)
86. Korzhnev, D.M.; Religa, T.L.; Banachewicz, W.; Fersht, A.R.; Kay, L.E. A transient and low-populated protein-folding intermediate at atomic resolution. Science 2010, 329, 1312-1316.
87. Sugase, K.; Dyson, H.J.; Wright, P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 2007, 447, 1021-1025. (Pubitemid 46975749)
88. Palmer, A.G., 3rd; Kroenke, C.D.; Loria, J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Meth. Enzymol. 2001, 339, 204-238. (Pubitemid 32666562)
89. Baldwin, A.J.; Kay, L.E. NMR spectroscopy brings invisible protein states into focus. Nat. Chem. Biol. 2009, 5, 808-814.
90. Bermel, W.; Felli, I.C.; Kummerle, R.; Pierattelli, R. 13C direct-detection biomolecular NMR. Concept. Magn. Reson. A 2008, 32A, 183-200.
91. Bax, A.; Griffey, R.H.; Hawkins, B.L. Correlation of Proton and 15N Chemical-Shifts by Multiple Quantum Nmr. J. Magn. Reson. 1983, 55, 301-315.
92. Kovacs, H.; Moskau, D.; Spraul, M. Cryogenically cooled probes - a leap in NMR technology. Prog. Nucl. Mag. Res. Sp. 2005, 46, 131-155. (Pubitemid 40749327)
93. Serber, Z.; Richter, C.; Moskau, D.; Bohlen, J.M.; Gerfin, T.; Marek, D.; Haberli, M.; Baselgia, L.; Laukien, F.; Stern, A.S.; Hoch, J.C.; Dotsch, V. New carbon-detected protein NMR experiments using CryoProbes. JACS 2000, 122, 3554-3555. (Pubitemid 30211144)
94. Bertini, I.; Duma, L.; Felli, I.C.; Fey, M.; Luchinat, C.; Pierattelli, R.; Vasos, P.R. A heteronuclear direct-detection NMR spectroscopy experiment for protein-backbone assignment. Angew. Chem. Int. Edit. 2004, 43, 2257-2259. (Pubitemid 39257766)
95. Bermel, W.; Bertini, I.; Duma, L.; Felli, I.C.; Emsley, L.; Pierattelli, R.; Vasos, P.R. Complete assignment of heteronuclear protein resonances by protonless NMR spectroscopy. Angewandte Chemie 2005, 44, 3089-3092. (Pubitemid 40689850)
96. Bermel, W.; Bertini, I.; Felli, I.C.; Matzapetakis, M.; Pierattelli, R.; Theil, E.C.; Turano, P. A method for C(alpha) direct-detection in protonless NMR. J. Magn. Reson. 2007, 188, 301-310. (Pubitemid 47562807)
97. Bermel, W.; Bertini, I.; Csizmok, V.; Felli, I.C.; Pierattelli, R.; Tompa, P. H-start for exclusively heteronuclear NMR spectroscopy: the case of intrinsically disordered proteins. J. Magn. Reson. 2009, 198, 275-281.
98. Bermel, W.; Bertini, I.; Chill, J.; Felli, I.C.; Haba, N.; Kumar, M.V.V.; Pierattelli, R. Exclusively heteronuclear 13C-detected amino-acid-selective NMR experiments for the study of intrinsically disordered proteins (IDPs). Chembiochem. 2012, 13, 2425-2432.
99. Werbeck, N.D.; Kirkpatrick, J.; Hansen, D.F. Probing arginine side-chains and their dynamics with carbon-detected NMR spectroscopy: Application to the 42 kDa human histone deacetylase 8 at high pH. Angewandte Chemie 2013, 52, 3145-3147.
100. Andre, I.; Linse, S.; Mulder, F.A. Residue-specific pKa determination of lysine and arginine side chains by indirect 15N and 13C NMR spectroscopy: application to apo calmodulin. JACS 2007, 129, 15805-15813.
101. Uversky, V.N.; Dunker, A.K. The case for intrinsically disordered proteins playing contributory roles in molecular recognition without a stable 3D structure. F1000 Biol. Rep. 2013, 5, 1.
102. Lawrence, C.W.; Showalter, S.A. Carbon-Detected 15N NMR Spin Relaxation of an Intrinsically Disordered Protein: FCP1 Dynamics Unbound and in Complex with RAP74. J. Phys. Chem. Lett. 2012, 3, 1409-1413.
103. Balayssac, S.; Bertini, I.; Luchinat, C.; Parigi, G.; Piccioli, M. 13C direct detected NMR increases the detectability of residual dipolar couplings. JACS 2006, 128, 15042-15043. (Pubitemid 44853490)
104. Bermel, W.; Bertini, I.; Felli, I.C.; Peruzzini, R.; Pierattelli, R. Exclusively heteronuclear NMR experiments to obtain structural and dynamic information on proteins. Chemphyschem. 2010, 11, 689-695.
105. Bertini, I.; Felli, I.C.; Gonnelli, L.; Vasantha Kumar, M.V.; Pierattelli, R. High-resolution characterization of intrinsic disorder in proteins: expanding the suite of 13C-detected NMR spectroscopy experiments to determine key observables. Chembiochem. 2011, 12, 2347-2352.
106. Cino, E.A.; Karttunen, M.; Choy, W.Y. Effects of molecular crowding on the dynamics of intrinsically disordered proteins. PloS One 2012, 7, e49876.
107. Li, C.; Charlton, L.M.; Lakkavaram, A.; Seagle, C.; Wang, G.; Young, G.B.; Macdonald, J.M.; Pielak, G.J. Differential dynamical effects of macromolecular crowding on an intrinsically disordered protein and a globular protein: implications for in-cell NMR spectroscopy. JACS 2008, 130, 6310-6311. (Pubitemid 351706077)
108. Szasz, C.S.; Alexa, A.; Toth, K.; Rakacs, M.; Langowski, J.; Tompa, P. Protein disorder prevails under crowded conditions. Biochemistry 2011, 50, 5834-5844.
109. Johansen, D.; Jeffries, C.M.; Hammouda, B.; Trewhella, J.; Goldenberg, D.P. Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-angle neutron scattering with contrast matching. Biophys. J. 2011, 100, 1120-1108.
110. Flaugh, S.L.; Lumb, K.J. Effects of macromolecular crowding on the intrinsically disordered proteins c-Fos and p27(Kip1). Biomacromolecules 2001, 2, 538-540. (Pubitemid 32707535)
111. Amata, I.; Maffei, M.; Igea, A.; Gay, M.; Vilaseca, M.; Nebreda, A.R.; Pons, M. Multi-phosphorylation of the Intrinsically Disordered Unique Domain of c-Src Studied by In-Cell and Real-Time NMR Spectroscopy. ChemBioChem 2013, doi:10.1002/cbic.201300139.
112. Bodart, J.F.; Wieruszeski, J.M.; Amniai, L.; Leroy, A.; Landrieu, I.; Rousseau-Lescuyer, A.; Vilain, J.P.; Lippens, G. NMR observation of Tau in Xenopus oocytes. J. Magn. Reson. 2008, 192, 252-257.
113. Burz, D.S.; Dutta, K.; Cowburn, D.; Shekhtman, A. In-cell NMR for protein-protein interactions (STINT-NMR). Nat. Protoc. 2006, 1, 146-152.
114. Li, C.; Liu, M. Protein dynamics in living cells studied by in-cell NMR spectroscopy. FEBS Lett. 2013, 587, 1008-1011.
115. Sakakibara, D.; Sasaki, A.; Ikeya, T.; Hamatsu, J.; Hanashima, T.; Mishima, M.; Yoshimasu, M.; Hayashi, N.; Mikawa, T.; Walchli, M.; Smith, B.O.; Shirakawa, M.; Guntert, P.; Ito, Y. Protein structure determination in living cells by in-cell NMR spectroscopy. Nature 2009, 458, 102-105.
116. Maldonado, A.Y.; Burz, D.S.; Shekhtman, A. In-cell NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc 2011, 59, 197-212.
117. Inomata, K.; Ohno, A.; Tochio, H.; Isogai, S.; Tenno, T.; Nakase, I.; Takeuchi, T.; Futaki, S.; Ito, Y.; Hiroaki, H.; Shirakawa, M. High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 2009, 458, 106-109.
118. Ogino, S.; Kubo, S.; Umemoto, R.; Huang, S.; Nishida, N.; Shimada, I. Observation of NMR signals from proteins introduced into living mammalian cells by reversible membrane permeabilization using a pore-forming toxin, streptolysin O. JACS 2009, 131, 10834-10835.
119. Bekei, B.; Rose, H.M.; Herzig, M.; Selenko, P. In-cell NMR in mammalian cells: part 2. Methods Mol. Biol. 2012, 895, 55-66.
120. Selenko, P.; Frueh, D.P.; Elsaesser, S.J.; Haas, W.; Gygi, S.P.; Wagner, G. In situ observation of protein phosphorylation by high-resolution NMR spectroscopy. Nat. Struct. Mol. Biol. 2008, 15, 321-329. (Pubitemid 351654049)
121. Selenko, P.; Serber, Z.; Gadea, B.; Ruderman, J.; Wagner, G. Quantitative NMR analysis of the protein G B1 domain in Xenopus laevis egg extracts and intact oocytes. PNAS 2006, 103, 11904-11909. (Pubitemid 44215784)
122. Banci, L.; Barbieri, L.; Bertini, I.; Luchinat, E.; Secci, E.; Zhao, Y.; Aricescu, A.R. Atomic-resolution monitoring of protein maturation in live human cells by NMR. Nat. Chem. Biol. 2013, 9, 297-299.
123. Hamatsu, J.; O′Donovan, D.; Tanaka, T.; Shirai, T.; Hourai, Y.; Mikawa, T.; Ikeya, T.; Mishima, M.; Boucher, W.; Smith, B.O.; et al. High-resolution heteronuclear multidimensional NMR of proteins in living insect cells using a baculovirus protein expression system. JACS 2013, 135, 1688-1691.
124. Bertrand, K.; Reverdatto, S.; Burz, D.S.; Zitomer, R.; Shekhtman, A. Structure of proteins in eukaryotic compartments. JACS 2012, 134, 12798-12806.
125. Serber, Z.; Ledwidge, R.; Miller, S.M.; Dotsch, V. Evaluation of parameters critical to observing proteins inside living Escherichia coli by in-cell NMR spectroscopy. JACS 2001, 123, 8895-8901. (Pubitemid 32884710)
126. Arnesano, F.; Banci, L.; Bertini, I.; Felli, I.C.; Losacco, M.; Natile, G. Probing the interaction of cisplatin with the human copper chaperone Atox1 by solution and in-cell NMR spectroscopy. JACS 2011, 133, 18361-18369.
127. Burz, D.S.; Shekhtman, A. The STINT-NMR method for studying in-cell protein-protein interactions. Curr. Protoc. Protein Sci. 2010, doi:10.1002/0471140864.ps1711s61.
128. Banci, L.; Barbieri, L.; Bertini, I.; Cantini, F.; Luchinat, E. In-cell NMR in E. coli to monitor maturation steps of hSOD1. PLoS one 2011, 6, e23561.
129. Schlesinger, A.P.; Wang, Y.; Tadeo, X.; Millet, O.; Pielak, G.J. Macromolecular crowding fails to fold a globular protein in cells. JACS 2011, 133, 8082-8085.
130. Bertini, I.; Felli, I.C.; Gonnelli, L.; Kumar, M.V. V.; Pierattelli, R. 13C direct-detection biomolecular NMR spectroscopy in living cells. Angewandte Chemie 2011, 50, 2339-2341.
131. Bekei, B.; Rose, H.M.; Herzig, M.; Dose, A.; Schwarzer, D.; Selenko, P. In-cell NMR in mammalian cells: part 1. Methods Mol. Biol. 2012, 895, 43-54.
132. Theillet, F.X.; Smet-Nocca, C.; Liokatis, S.; Thongwichian, R.; Kosten, J.; Yoon, M.K.; Kriwacki, R.W.; Landrieu, I.; Lippens, G.; Selenko, P. Cell signaling, post-translational protein modifications and NMR spectroscopy. J. Biomol. NMR 2012, 54, 217-236.
133. Liokatis, S.; Dose, A.; Schwarzer, D.; Selenko, P. Simultaneous detection of protein phosphorylation and acetylation by high-resolution NMR spectroscopy. JACS 2010, 132, 14704-14705.
134. Theillet, F.X.; Liokatis, S.; Jost, J.O.; Bekei, B.; Rose, H.M.; Binolfi, A.; Schwarzer, D.; Selenko, P. Site-specific mapping and time-resolved monitoring of lysine methylation by high-resolution NMR spectroscopy. JACS 2012, 134, 7616-7619.
135. Jensen, M.R.; Communie, G.; Ribeiro, E.A., Jr.; Martinez, N.; Desfosses, A.; Salmon, L.; Mollica, L.; Gabel, F.; Jamin, M.; Longhi, S.; et al. Intrinsic disorder in measles virus nucleocapsids. PNAS 2011, 108, 9839-9844.