Recent advances in solution NMR studies: 13C direct detection for biomolecular NMR applications

Annual Reports on NMR Spectroscopy

Volumn 80, Issue , 2013, Pages 359-418

  Felli, Isabella C ^a   Piai, Alessandro ^a   Pierattelli, Roberta ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Exclusively heteronuclear NMR; Intrinsically disordered proteins (IDPs); Longitudinal relaxation enhancement (LRE); Multidimensional NMR; Non uniform sampling (NUS); Paramagnetic proteins; Protonless NMR; Very large proteins; Virtual decoupling

Indexed keywords

EID: 84884685221     PISSN: 00664103     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-408097-3.00006-8     Document Type: Chapter

References (189)

1. Sattler M., Schleucher J., Griesinger C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog NMR Spectrosc 1999, 34:93.
2. Bax A., Grzesiek S. Methodological advances in protein NMR. Acc Chem Res 1993, 26:131.
3. Bodenhausen G., Ruben D.J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem Phys Lett 1980, 69:185.
4. 1H chemical shifts in natural-abundance samples via multiple quantum coherence. J Am Chem Soc 1983, 105:7188.
5. Kolczak U., Salgado J., Siegal G., Saraste M., Canters G.W. Paramagnetic NMR studies of blue and purple copper proteins. Biospectroscopy 1999, 5:S19.
6. Serber Z., Richter C., Dötsch V. Carbon-detected NMR experiments to investigate structure and dynamics of biological macromolecules. Chembiochem 2001, 2:247.
7. Bertini I., Lee Y.-M., Luchinat C., Piccioli M., Poggi L. Locating the metal ion in calcium-binding proteins by using cerium(III) as a probe. Chembiochem 2001, 2:550.
8. 2+-containing acireductone dioxygenase. J Am Chem Soc 2002, 124:9054.
9. Arnesano F., Banci L., Bertini I., Felli I.C., Luchinat C., Thompsett A.R. A strategy for the NMR characterization of type II copper(II) proteins: the case of the copper trafficking protein CopC from Pseudomonas syringae. J Am Chem Soc 2003, 125:7200.
10. 13C direct detection experiments on the paramagnetic oxidized monomeric copper, zinc superoxide dismutase. J Am Chem Soc 2003, 125:16423.
11. Bertini I., Duma L., Felli I.C., Fey M., Luchinat C., Pierattelli R., et al. A heteronuclear direct detection NMR experiment for protein backbone assignment. Angew Chem Int Ed 2004, 43:2257.
12. Bermel W., Bertini I., Duma L., Emsley L., Felli I.C., Pierattelli R., et al. Complete assignment of heteronuclear protein resonances by protonless NMR spectroscopy. Angew Chem Int Ed 2005, 44:3089.
13. Serber Z., Richter C., Moskau D., Boehlen J.-M., Gerfin T., Marek D., et al. New carbon-detected protein NMR experiments using cryoprobes. J Am Chem Soc 2000, 122:3554.
14. Kovacs H., Moskau D., Spraul M. Cryogenically cooled probes-a leap in NMR technology. Prog NMR Spectrosc 2005, 46:131.
15. Bertini I., Luchinat C., Parigi G. Solution NMR of paramagnetic molecules 2001, Elsevier, Amsterdam.
16. Bertini I., Luchinat C., Parigi G., Pierattelli R. NMR of paramagnetic metalloproteins. Chembiochem 2005, 6:1536.
17. LeMaster D.M. Isotope labeling in solution protein assignment and structural analysis. Prog NMR Spectrosc 1994, 26:371.
18. 13C'-detected heteronuclear NMR spectroscopy. J Biomol NMR 2006, 36:111.
19. Hsu S.T., Bertoncini C.W., Dobson C.M. Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange-broadening. J Am Chem Soc 2009, 131:7222.
20. Skora L., Becker S., Zweckstetter M. Molten globule precursor states are conformationally correlated to amyloid fibrils of human beta-2-microglobulin. J Am Chem Soc 2010, 132:9223.
21. Gil S, Hosek T, Solyom Z, Kümmerle R, Brutscher B, Pierattelli R, et al. NMR studies of intrinsically disordered proteins near physiological conditions. 2013.
22. Zheng G., Price W.S. Solvent suppression in NMR. Prog NMR Spectrosc 2010, 56:267.
23. 13C direct detection NMR methods. J Biomol NMR 2004, 30:175.
24. Csizmok V., Felli I.C., Tompa P., Banci L., Bertini I. Structural and dynamic characterization of intrinsically disordered human securin by NMR. J Am Chem Soc 2008, 130:16873.
25. 1H NMR spectroscopy by homonuclear semiselective shaped pulse decoupling during acquisition. J Am Chem Soc 1994, 116:8847.
26. 13C-detected experiments with proteins and oligonucleotides. J Biomol NMR 2005, 31:1.
27. Duma L., Hediger S., Brutscher B., Böckmann A., Emsley L. Resolution enhancement in multidimensional solid-state NMR spectroscopy of proteins using spin-state selection. J Am Chem Soc 2003, 125:11816.
28. Duma L., Hediger S., Lesage A., Emsley L. Spin-state selection in solid-state NMR. J Magn Reson 2003, 164:187.
29. 13C spin-diffusion. J Biomol NMR 2004, 30:245.
30. 13C direct detection experiments, including extension to the third dimension, to perform the complete assignment of proteins. J Magn Reson 2006, 178:56.
31. Ottiger M., Delaglio F., Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Reson 1998, 131:373.
32. α direct-detection in protonless NMR. J Magn Reson 2007, 188:301.
33. Lerche M.H., Meissner A., Poulsen F.M., Sørensen O.W. Pulse sequences for measurement of one-bond (15)N-(1)H coupling constants in the protein backbone. J Magn Reson 1999, 140:259.
34. 13C solid-state spectra through spin-state-selection. J Magn Reson 2007, 184:322.
35. 13C direct-detection biomolecular NMR. Concepts Magn Reson 2008, 32A:183.
36. Lee D., Vögeli B., Pervushin K. Detection of C', Ca correlations in proteins using a new time- and sensitivity-optimal experiment. J Biomol NMR 2005, 31:273.
37. 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.
38. Kern T., Schanda P., Brutscher B. Sensitivity-enhanced IPAP-SOFAST-HMQC for fast-pulsing 2D NMR with reduced radiofrequency load. J Magn Reson 2008, 190:333.
39. C-labeled proteins. J Am Chem Soc 2009, 131:10816.
40. Bertini I., Emsley L., Felli I.C., Laage S., Lesage A., Lewandoski D.A., et al. High-resolution and sensitivity through-bond correlations in ultra-fast MAS solid-state NMR. Chem Sci 2011, 2:345.
41. 13C-detected through-bond correlation experiments for protein resonance assignment by ultra-fast MAS NMR. Chemphyschem 2013, Epub ahead of print.
42. 13C residual dipolar coupling in uniformly deuterated proteins. J Am Chem Soc 2004, 126:2414.
43. 15N NMR assignment of human β-parvalbumin. J Biomol NMR 2005, 33:137.
44. Hu K., Eletsky A., Pervushin K. Backbone resonance assignment in large protonated proteins using a combination of new 3D TROSY-HN(CA)HA, 4D TROSY-HACANH and 13C detected HACACO experiments. J Biomol NMR 2003, 26:69.
45. Oh B.-H., Westler W.M., Darba P., Markley J.L. Protein carbon-13 spin systems by a single two-dimensional nuclear magnetic resonance experiment. Science 1988, 240:908.
46. Westler W.M., Kainosho M., Nagao H., Tomonaga M., Markley J.L. Two-dimensional NMR strategies for carbon-carbon correlations and sequence-specific assignments in carbon-13 labeled proteins. J Am Chem Soc 1988, 110:4093.
47. Oh B.-H., Westler W.M., Markley J.L. Carbon-13 spin system directed strategy for assigning cross peaks in the COSY fingerprint region of a protein. J Am Chem Soc 1989, 111:3083.
48. 13C 2D NMR: a novel strategy for the study of paramagnetic proteins with slow electronic relaxation times. J Am Chem Soc 2002, 124:3204.
49. Machonkin T.E., Westler W.M., Markley J.L. Strategy for the study of paramagnetic proteins with slow electronic relaxation rates by NMR spectroscopy application to oxidized human [2Fe-2S] ferredoxin. J Am Chem Soc 2004, 126:5413.
50. 13C-detected protonless NMR spectroscopy of proteins in solution. Prog NMR Spectrosc 2006, 48:25.
51. 13C NOESY: an attractive alternative for studying large macromolecules. J Am Chem Soc 2004, 126:464.
52. 13C NOESY spectra of a 480kDa protein: solution NMR of ferritin. J Biomol NMR 2007, 38:237.
53. 13C spectroscopy. J Biomol NMR 2003, 26:167.
54. Pervushin K., Eletsky A. A new strategy for backbone resonance assignment in large proteins using a MQ-HACACO experiment. J Biomol NMR 2003, 25:147.
55. 13C detected HN(CA)C and HMCMC experiments using a single methyl reprotonated sample for unambiguous methyl-resonance assignment. J Biomol NMR 2006, 36:259.
56. 3-TOCSY using selectively protonated proteins: facile methyl resonance assignment and protein structure determination. J Am Chem Soc 2006, 128:9119.
57. O'Hare B., Benesi A.J., Showalter S.A. Incorporating 1H chemical shift determination into 13C-direct detected spectroscopy of intrinsically disordered proteins in solution. J Magn Reson 2009, 200:354.
58. Bermel W., Bertini I., Felli I.C., Pierattelli R., Vasos P.R. A selective experiment for the sequential protein backbone assignment from 3D heteronuclear spectra. J Magn Reson 2005, 172:324.
59. 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. J Am Chem Soc 2006, 128:3918.
60. 13C direct detection experiments. J Biomol NMR 2009, 43:187.
61. α direct detection. J Am Chem Soc 2010, 132:2945.
62. α direct detection experiment for main chain resonance assignment, dihedral angle information and aminoacid type identification. J Biomol NMR 2010, 47:55.
63. Bermel W., Bruix M., Felli I.C., Kumar V.M.V., Pierattelli R., Serrano S. Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins. J Biomol NMR 2013, 55:231.
64. Castellani F., van Rossum B., Diehl A., Schubert M., Rehbein K., Oschkinat H. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 2002, 420:98.
65. Felli I.C., Brutscher B. Recent advancements in solution NMR: fast methods and heteronuclear direct detection. Chemphyschem 2009, 10:1356.
66. Pervushin K., Vogeli B., Eletsky A. Longitudinal (1)H relaxation optimization in TROSY NMR spectroscopy. J Am Chem Soc 2002, 124:12898.
67. Schanda P., Kupce E., Brutscher B. SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 2005, 33:199.
68. Schanda P., Brutscher B. Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds. J Am Chem Soc 2005, 127:8014.
69. Deschamps M., Campbell I.D. Cooling overall spin temperature: protein NMR experiments optimized for longitudinal relaxation effects. J Magn Reson 2006, 178:206.
70. Schanda P., Van Melckebeke H., Brutscher B. Speeding up three-dimensional protein NMR experiments to a few minutes. J Am Chem Soc 2006, 128:9042.
71. Brutscher B., Schanda P. Rapid multidimensional NMR: fast pulsing techniques and their application to proteins. Encyclopedia of NMR 2009, Wiley. M. Grant, R.K. Harris (Eds.).
72. 13C direct detection biomolecular NMR experiments. J Am Chem Soc 2009, 131:15339.
73. 13C detected NMR experiments to determine key observables. Chembiochem 2011, 12:2347.
74. 13C direct-detection biomolecular NMR spectroscopy in living cells. Angew Chem Int Ed 2011, 50:2339.
75. Hoch J.C. Modern spectrum analysis in nuclear magnetic resonance: alternatives to the Fourier transform. Methods Enzymol 1989, 176:216.
76. Hoch J.C., Stern A.S. NMR data processing 1996, Wiley-Interscience, New York.
77. Hyberts S.G., Frueh D.P., Arthanari H., Wagner G. FM reconstruction of non-uniformly sampled protein NMR data at higher dimensions and optimization by distillation. J Biomol NMR 2009, 45:283.
78. 13C HSQC spectra of metabolite mixtures using nonlinear sampling and forward maximum entropy reconstruction. J Am Chem Soc 2007, 129:5108.
79. Orekhov V.Y., Ibraghimov I., Billeter M. Optimizing resolution in multidimensional NMR by three-way decomposition. J Biomol NMR 2003, 27:165.
80. Orekhov V.Y., Kazimierczuk K. Accelerated NMR spectroscopy by using compressed sensing. Angew Chem Int Ed 2011, 50:5556.
81. Matsuki Y., Eddy M.T., Griffin R.G. Rapid three-dimensional MAS NMR spectroscopy at critical sensitivity. Angew Chem Int Ed 2010, 49:9215.
82. Kazimierczuk K., Zawadzka A., Kozminski W. Narrow peaks and high dimensionalities: exploiting the advantages of random sampling. J Magn Reson 2009, 197:219.
83. Stanek J., Kozminski W. Iterative algorithm of discrete Fourier transform for processing randomly sampled data sets. J Biomol NMR 2010, 47:65.
84. Stanek J., Augustyniak R., Kozminski W. Suppression of sampling artefacts in high-resolution four-dimensional NMR spectra using signal separation algorithm. J Magn Reson 2012, 214:91.
85. Coggins B.E., Zhou P. High resolution 4-D spectroscopy with sparse concentric shell sampling and FFT-CLEAN. J Biomol NMR 2008, 42:225.
86. Kazimierczuk K., Zawadzka A., Kozminski W. Optimization of random time domain sampling in multidimensional NMR. J Magn Reson 2008, 192:123.
87. Bermel W., Bertini I., Gonnelli L., Felli I.C., Kozminski W., Piai A., et al. Speeding up sequence specific assignment of IDPs. J Biomol NMR 2012, 53:293.
88. α)-selective HCBCANCO experiments for the sequential assignment and chemical shift analysis of intrinsically disordered proteins. J Biomol NMR 2012, 53:139.
89. 13C-detected experiments for backbone assignment of unstructured proteins with a very low signal dispersion. J Biomol NMR 2011, 50:1.
90. Olejniczak E.T., Fesik S.W. Two dimensional nuclear magnetic resonance method for identifying the Ha-Ca signals of amino acid residues preceding prolines. J Am Chem Soc 1994, 116:2215.
91. Ghering K., Guittet E. Two-dimensional nuclear magnetic resonance method for identifying the HN/N signals of amino-acid residues following glycine. J Magn Reson B 1995, 109:206.
92. 1H chemical shifts in proteins. J Am Chem Soc 1995, 117:3556.
93. Dötsch V., Oswald R.E., Wagner G. Amino-acid type-selective triple-resonance experiments. J Magn Reson B 1996, 110:107.
94. e{open} protons. J Magn Reson B 1996, 113:272.
95. Dötsch V., Oswald R.E., Wagner G. Selective identification of threonine, valine and isoleucine sequential connectivities with a TVI-CBCACONH experiment. J Magn Reson B 1996, 110:304.
96. Dötsch V., Matsuo H., Wagner G. Amino-acid type identification for deuterated proteins with a β-carbon-edited HNCOCACB experiment. J Magn Reson B 1996, 112:95.
97. 13Cγ coupling. J Magn Reson B 1996, 111:310.
98. 13C-labeled proteins. J Magn Reson 1997, 124:274.
99. Schmieder P., Leidert M., Kelly M., Oschkinat H. Multiplicity-selective coherence transfer steps for the design of amino acid-selective experiments-a triple-resonance experiment selective for ASN and GLN. J Magn Reson 1998, 131:199.
100. 15N correlations. J Magn Reson 1999, 141:34.
101. Bazzo R., Cicero D.O., Barbato G. Selective correlations of amide groups to glycine alpha protons and of arginine guanidine groups to delta protons in proteins by multiple quantum spectroscopy. J Magn Reson 1999, 136:15.
102. 15N correlations to link sequential neighbors of prolines. J Biomol NMR 2000, 17:331.
103. 15N correlations for Arg and Lys. J Biomol NMR 2001, 20:379.
104. 15N correlations, II. J Magn Reson 2001, 148:61.
105. 15N correlations, III. J Magn Reson 2001, 153:186.
106. Brutscher B. DEPT spectral editing in HCCONH-type experiments. Application to fast protein backbone and side chain assignment. J Magn Reson 2004, 167:178.
107. Schubert M., Labudde D., Leitner D., Oschkinat H., Schmieder P. A modified strategy for sequence specific assignment of protein NMR spectra based on amino acid type selective experiments. J Biomol NMR 2005, 31:115.
108. Lescop E., Rasia R., Brutscher B. Hadamard amino-acid-type edited NMR experiment for fast protein resonance assignment. J Am Chem Soc 2008, 130:5014.
109. Kjaergaard M., Poulsen F.M. Disordered proteins studied by chemical shifts. Prog NMR Spectrosc 2012, 60:42.
110. 13C direct-detected exclusively heteronuclear experiments to study intrinsically disordered proteins. Chembiochem 2012, 13:2425.
111. Zhang H., Neal S., Wishart D.S. RefDB: a database of uniformly referenced protein chemical shifts. J Biomol NMR 2003, 25:173.
112. Shen Y., Delaglio F., Cornilescu G., Bax A. TALOS plus: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 2009, 44:213.
113. Cavalli A., Salvatella X., Dobson C.M., Vendruscolo M. Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci USA 2007, 104:9615.
114. 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.
115. 13C-detection for carbonyl relaxation studies of protein dynamics. J Magn Reson 2008, 193:226.
116. 13C direct detected NMR increases the detectability of residual dipolar couplings. J Am Chem Soc 2006, 128:15042.
117. Griesinger C., Sørensen O.W., Ernst R.R. Correlation of connected transitions by two-dimensional NMR spectroscopy. J Chem Phys 1986, 85:6837.
118. α coupling constants in polypeptides using heteronuclear 2D NMR experiments. J Am Chem Soc 1989, 111:5474.
119. Biamonti C., Rios C.B., Lyons B.A., Montelione G.T. Multidimensional NMR experiments and analysis techniques for determining homo-and heteronuclear scalar coupling contents in proteins and nucleic acids. Adv Biophys Chem 1994, 4:51.
120. Wang A.C., Bax A. Determination of the backbone dihedral angles φ in human ubiquitin from reparametrized empirical Karplus equations. J Am Chem Soc 1996, 118:2483.
121. 13C uniformly labeled proteins. J Biomol NMR 1997, 9:409.
122. 13C J couplings in a 20-kDa protein-peptide complex. J Am Chem Soc 1992, 114:6923.
123. 13C three-bond J couplings measured by three-dimensional heteronuclear NMR. How planar is the peptide bond?. J Am Chem Soc 1997, 119:6360.
124. 3J carbon-carbon coupling constants at natural abundance. J Magn Reson B 1996, 112:295.
125. Tjandra N., Grzesiek S., Bax A. Magnetic field dependence of nitrogen-proton J splittings in 15N-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling. J Am Chem Soc 1996, 118:6264.
126. 13C labeled proteins. J Biomol NMR 1998, 12:325.
127. Hu K., Vögeli B., Clore G.M. Spin-state selective carbon-detected HNCO with TROSY optimization in all dimensions and double echo-antiecho sensitivity enhancement in both indirect dimensions. J Am Chem Soc 2007, 129:5484.
128. Mulder F.A.A., Akke M. Carbonyl 13C transverse relaxation measurements to sample protein backbone dynamics. Magn Reson Chem 2003, 41:853.
129. Ishima R., Baber J.L., Louis J.M., Torchia D.A. Carbonyl carbon transverse relaxation dispersion measurements and ms-us timescale motion in a protein hydrogen bond network. J Biomol NMR 2004, 29:187.
130. Fermi E. Z Phys 1930, 60:320.
131. McConnell H.M. Effect of anisotropic hyperfine interactions on paramagnetic relaxation in liquids. J Chem Phys 1956, 25:709.
132. Solomon I. Relaxation processes in a system of two spins. Phys Rev 1955, 99:559.
133. Bloembergen N., Purcell E.M., Pound R.V. Phys Rev 1948, 73:679.
134. 13C direct detected experiments: optimisation to paramagnetic signals. J Magn Reson 2005, 174:125.
135. 13C direct detection NMR methods. J Biomol NMR 2005, 30:175.
136. Babini E., Bertini I., Capozzi F., Felli I.C., Lelli M., Luchinat C. Direct carbon detection in paramagnetic metalloproteins to further exploit pseudocontact shift restraints. J Am Chem Soc 2004, 126:10496.
137. Bertini I., Felli I.C., Luchinat C., Parigi G., Pierattelli R. Towards a protocol for solution structure determination of copper(II) proteins: the case of Cu(II)Zn(II) superoxide dismutase. Chembiochem 2007, 8:1422.
138. Abriata L.A., Ledesma G.N., Pierattelli R., Vila A.J. Electronic structure of the ground and excited states of the Cu(A) site by NMR spectroscopy. J Am Chem Soc 2009, 131:1939.
139. Mainz A., Bardiaux B., Kuppler F., Multhaup G., Felli I.C., Pierattelli R., et al. Structural and mechanistic implications of metal-binding in the small heat-shock protein αB-crystalline. J Biol Chem 2012, 287:1128.
140. 2 ferredoxin. Biochemistry 2001, 40:5602.
141. 13C NMR to investigate the iron(III) hemophore HasA. J Am Chem Soc 2006, 128:150.
142. Caillet-Saguy C., Turano P., Piccioli M., Lukat-Rodgers G., Czjzek M., Guigliarelli B., et al. Decifering the structural role of histidine 83 for heme binding in hemophore HasA. J Biol Chem 2008, 283:5960.
143. Westler W.M., Lin I.J., Perczel A., Weinhold F., Markley J.L. Hyperfine-shifted (13)C resonance assignments in an iron-sulfur protein with quantum chemical verification: aliphatic C-H. . .S 3-center-4-electron interactions. J Am Chem Soc 2011, 133:1310-1316.
144. Pochapsky S.S., Sunshine J., Pochapsky T.C. Completing the circuit: direct-observe 13C,15N double-quantum spectroscopy permits sequential resonance assignments near a paramagnetic center in acireductone dioxygenase. J Am Chem Soc 2008, 130:2156.
145. 9k. J Biomol NMR 2001, 21:85.
146. 13C COSY spectra identifies geometry in paramagnetic proteins. J Am Chem Soc 2005, 127:12216.
147. Gelis I., Katsaros N., Luchinat C., Piccioli M., Poggi L. A simple protocol to study blue copper proteins by NMR. Eur J Biochem 2003, 270:600.
148. 9k. J Biomol NMR 2006, 34:63.
149. 13C direct-detect paramagnetic relaxation enhancements. J Am Chem Soc 2010, 132:7285.
150. Madl T., Guettler T., Gorlich D., Sattler M. Structural analysis of large protein complexes using solvent paramagnetic relaxation enhancements. Angew Chem Int Ed Engl 2011, 50:3993.
151. 13C direct detection NMR: characterization of the 37 kiloDalton trimeric protein CutA1. Proteins Struct Funct Genet 2008, 70:1196.
152. Poget S.F., Girvin M.E. Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochem Biophys Res Commun 2007, 1768:3098.
153. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 1997, 94:12366.
154. 13C-labeled proteins. J Am Chem Soc 1998, 120:6394.
155. Riek R., Pervushin K., Wüthrich K. TROSY and CRINEPT: NMR with large molecular and supramolecular structures in solution. TIBS 2000, 25:462.
156. Tugarinov V., Hwang P.M., Ollerenshaw J.E., Kay L.E. Cross-correlated relaxation enhanced 1H[bond]13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J Am Chem Soc 2003, 125:10420.
157. Ollerenshaw J.E., Tugarinov V., Kay L.E. Magn Reson Chem 2003, 41:843.
158. Cavanagh J., Fairbrother W.J., Palmer A.G., Skelton N.J. Protein NMR spectroscopy. Principles and practice 1996, Academic Press, San Diego.
159. Pintacuda G., Giraud N., Pierattelli R., Böckmann A., Bertini I., Emsley L. Solid-state NMR of a paramagnetic protein: assignment and study of human dimeric oxidized Cu(II), Zn(II) superoxide dismutase. Angew Chem Int Ed 2007, 46:1079.
160. Balayssac S., Bertini I., Falber K., Fragai M., Jehle S., Lelli M., et al. Solid-state NMR of matrix metalloproteinase 12: an approach complementary to solution NMR. Chembiochem 2007, 8:486.
161. Turano P., Lalli D., Felli I.C., Theil E.C., Bertini I. NMR reveals a pathway for iron mineral precursors to the central cavity of ferritin. Proc Natl Acad Sci USA 2010, 107:545.
162. Knight M.J., Felli I.C., Pierattelli R., Emsley L., Pintacuda G. Magic angle spinning NMR of paramagnetic proteins. Acc Chem Res 2013, Epub ahead of print.
163. Bertini I., Luchinat C., Parigi G., Ravera E. SedNMR: on the edge between solution and solid state NMR. Acc Chem Res 2013, Epub ahead of print.
164. Bertini I., Luchinat C., Parigi G., Ravera E., Reif B., Turano P. Solid-state NMR of proteins sedimented by ultracentrifugation. Proc Natl Acad Sci USA 2011, 108:10396.
165. Tompa P. Intrinsically unstructured proteins. Trends Biochem Sci 2002, 27:527.
166. Dyson H.J., Wright P.E. Unfolded proteins and protein folding studied by NMR. Chem Rev 2004, 104:3607.
167. Mittag T., Forman-Kay J. Atomic-level characterization of disordered protein ensembles. Curr Opin Struct Biol 2007, 17:3.
168. Wright P.E., Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 1999, 293:321.
169. Tompa P. Structure and function of intrinsically disordered proteins 2009, CRC Press, Boca Raton, FL.
170. Uversky V., 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.
171. Fink A.L. Natively unfolded proteins. Curr Opin Struct Biol 2005, 15:35.
172. Tompa P. Intrinsically disordered proteins: a 10-year recap. Trends Biochem Sci 2012, 37:509-516.
173. Tompa P., Fuxreiter M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 2008, 33:2.
174. Sickmeier M., Hamilton J.A., LeGall T., Vacic V., Cortese M.S., Tantos A., et al. DisProt: the database of disordered proteins. Nucleic Acids Res 2007, 35:D786.
175. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005, 6:197.
176. Marsh J., Teichmann S.A., Forman-Kay J.D. Probing the diverse landscape of protein flexibility and binding. Curr Opin Struct Biol 2012, 22:643.
177. Mittag T., Marsh J., Grishaev A., Orlicky S., Lin H., Sicheri F., et al. 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.
178. Felli I.C., Pierattelli R., Tompa P. Intrinsically disordered proteins. NMR of biomolecules 2012, Wiley-Blackwell, Weinheim Germany. I. Bertini, K.S. McGreevy, G. Parigi (Eds.).
179. Felli I.C., Pierattelli R. Recent progress in NMR spectroscopy: towards the study of intrinsically disordered proteins of increasing size and complexity. IUBMB Life 2012, 64:473.
180. Eliezer D. Biophysical characterization of intrinsically disordered proteins. Curr Opin Struct Biol 2009, 19:23.
181. 15N) labeled proteins: application to unfolded proteins. J Biomol NMR 2001, 20:135.
182. Narayanan R.L., Duerr H.N., Bilbow S., Biernat J., Mendelkow E., Zweckstetter M. Automatic assignment of the intrinsically disordered protein tau with 441-residues. J Am Chem Soc 2010, 132:11906.
183. Solyom Z., Schwarten M., Geist L., Konrat R., Willbold D., Brutscher B. BEST-TROSY experiments for time-efficient sequential resonance assignment of large disordered proteins. J Biomol NMR 2013, 55:311-321.
184. Motackova V., Novacek J., Zawadzka-Kazimierczuk A., Kazimierczuk K., Zidek L., Sanderová H., et al. Strategy for complete NMR assignment of disordered proteins with highly repetitive sequences based on resolution-enhanced 5D experiments. J Biomol NMR 2010, 48:169.
185. Dyson H.J., Wright P.E. Nuclear magnetic resonance methods for the elucidation of structure and dynamics in disordered states. Meth Enzymol 2001, 339:258.
186. Schwarzinger S., Kroon G.J.A., Foss T.R., Chung J., Wright P.E., Dyson H.J. Sequence-dependent correction of random coil NMR chemical shifts. J Am Chem Soc 2001, 123:2970.
187. Pérez Y., Gairi M., Pons M., Bernadò P. Structural characterization of the natively unfolded N-terminal domain of human c-Src kinase: insights into the role of phosphorylation of the unique domain. J Mol Biol 2009, 391:136.
188. Knoblich K., Whittaker S., Ludwig C., Michiels P., Jiang T., Schafflhausen B., et al. Backbone assignment of the N-terminal polyomavirus large T antigen. Biomol NMR Assign 2009, 3:119.
189. Binolfi A., Theillet F.X., Selenko P. Bacterial in-cell NMR of human alpha-synuclein: a disordered monomer by nature?. Biochem Soc Trans 2012, 40:950.