The dynamic duo: Combining NMR and small angle scattering in structural biology

Protein Science

Volumn 23, Issue 6, 2014, Pages 669-682

  Hennig, Janosch ^a,b   Sattler, Michael ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

Author keywords

Multidomain proteins; Nuclear magnetic resonance spectroscopy; Protein complexes; Small angle neutron scattering; Small angle X Ray scattering; Structural biology

Indexed keywords

MULTIPROTEIN COMPLEX; RNA; PROTEIN; SOLUTION AND SOLUBILITY;

CRYSTAL STRUCTURE; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN RNA BINDING; REVIEW; SMALL ANGLE SCATTERING; X RAY CRYSTALLOGRAPHY; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; SOLUTION AND SOLUBILITY;

CRYSTALLOGRAPHY, X-RAY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEINS; SCATTERING, SMALL ANGLE; SOLUTIONS;

EID: 84904170133     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2467     Document Type: Review

References (155)

1. Levitt M (2009) Nature of the protein universe. Proc Natl Acad Sci USA 106:11079-11084.
2. Selmer M, Dunham CM, Murphy FV, IV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935-1942.
3. Steitz TA (2008) A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol 9: 242-253.
4. Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-Bound 11-Subunit eukaryotic exosome complex. Nature 495:70-75.
5. Maier T, Jenni S, Ban N (2006) Architecture of mammalian fatty acid synthase at 4.5 A resolution. Science 311:1258-1262.
6. Kornberg RD (2007) The molecular basis of eukaryotic transcription. Proc Natl Acad Sci USA 104:12955-12961.
7. Liu X, Bushnell DA, Kornberg RD (2013) RNA polymerase II transcription: Structure and mechanism. Biochim Biophys Acta 1829:2-8.
8. Sainsbury S, Niesser J, Cramer P (2013) Structure and function of the initially transcribing RNA polymerase II-TFIIB complex. Nature 493:437-440.
9. Lariviere L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P (2012) Structure of the mediator head module. Nature 492:448-451.
10. Schirle NT, MacRae IJ (2012) The crystal structure of human Argonaute2. Science 336:1037-1040.
11. Nakanishi K, Weinberg DE, Bartel DP, Patel DJ (2012) Structure of yeast Argonaute with guide RNA. Nature 486:368-374.
12. Elkayam E, Kuhn CD, Tocilj A, Haase AD, Greene EM, Hannon GJ, Joshua-Tor L (2012) The structure of human argonaute-2 in complex with miR-20a. Cell 150:100-110.
13. Tomko RJ, Jr, Hochstrasser M (2013) Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 82:415-445.
14. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386: 463-471.
15. Lasker K, Forster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P, Beck F, Aebersold R, Sali A, Baumeister W (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109:1380-1387.
16. Golas MM, Sander B, Bessonov S, Grote M, Wolf E, Kastner B, Stark H, Luhrmann R (2010) 3D cryo-EM structure of an active step I spliceosome and localization of its catalytic core. Mol Cell 40:927-938.
17. Diebolder CA, Koster AJ, Koning RI (2012) Pushing the resolution limits in cryo electron tomography of biological structures. J Microsc 248:1-5.
18. Grigorieff N (2013) Direct detection pays off for electron cryo-Microscopy. Elife 2:e00573.
19. Bai XC, Fernandez IS, McMullan G, Scheres SH (2013) Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife 2:e00461.
20. Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H (2010) Ribosome dynamics and tRNA movement by time-Resolved electron cryomicroscopy. Nature 466:329-333.
21. Religa TL, Sprangers R, Kay LE (2010) Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 328:98-102.
22. Rosenzweig R, Moradi S, Zarrine-Afsar A, Glover JR, Kay LE (2013) Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339:1080-1083.
23. Sprangers R, Kay LE (2007) Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445:618-622.
24. Sattler M, Fesik SW (1996) Use of deuterium labeling in NMR: Overcoming a sizeable problem. Structure 4: 1245-1249.
25. Gardner KH, Rosen MK, Kay LE (1997) Global folds of highly deuterated, methyl-Protonated proteins by multidimensional NMR. Biochemistry 36:1389-1401.
26. Tugarinov V, Kanelis V, Kay LE (2006) Isotope labeling strategies for the study of high-Molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 1: 749-754.
27. Pervushin K, Riek R, Wider G, Wuthrich K (1997) Attenuated T2 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 94:12366-12371.
28. Neudecker P, Lundstrom P, Kay LE (2009) Relaxation dispersion NMR spectroscopy as a tool for detailed studies of protein folding. Biophys J 96:2045-2054.
29. Sprangers R, Velyvis A, Kay LE (2007) Solution NMR of supramolecular complexes: Providing new insights into function. Nat Methods 4:697-703.
30. Lundstrom P, Vallurupalli P, Hansen DF, Kay LE (2009) Isotope labeling methods for studies of excited protein states by relaxation dispersion NMR spectroscopy. Nat Protoc 4:1641-1648.
31. Tugarinov V, Hwang PM, Ollerenshaw JE, Kay LE (2003) Cross-Correlated relaxation enhanced 1HA13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J Am Chem Soc 125:10420-10428.
32. Tugarinov V, Kay LE (2005) Methyl groups as probes of structure and dynamics in NMR studies of highmolecular- weight proteins. Chembiochem 6:1567-1577.
33. Riek R, Fiaux J, Bertelsen EB, Horwich AL, Wüthrich K (2002) Solution NMR techniques for large molecular and supramolecular structures. J Am Chem Soc 124: 12144-12153.
34. Zhang Q, Sun X, Watt ED, Al-Hashimi HM (2006) Resolving the motional modes that code for RNA adaptation. Science 311:653-656.
35. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121.
36. Bibow S, Mukrasch MD, Chinnathambi S, Biernat J, Griesinger C, Mandelkow E, Zweckstetter M (2011) The dynamic structure of filamentous tau. Angew Chem Int Ed Engl 50:11520-11524.
37. Jensen MR, Ruigrok RW, Blackledge M (2013) Describing intrinsically disordered proteins at atomic resolution by NMR. Curr Opin Struct Biol 23:426-435.
38. Ozenne V, Schneider R, Yao M, Huang JR, Salmon L, Zweckstetter M, Jensen MR, Blackledge M (2012) Mapping the potential energy landscape of intrinsically disordered proteins at amino acid resolution. J Am Chem Soc 134:15138-15148.
39. Bhabha G, Lee J, Ekiert DC, Gam J, Wilson IA, Dyson HJ, Benkovic SJ, Wright PE (2011) A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332:234-238.
40. Mackereth CD, Madl T, Bonnal S, Simon B, Zanier K, Gasch A, Rybin V, Valcarcel J, Sattler M (2011) Multidomain conformational selection underlies pre-MRNA splicing regulation by U2AF. Nature 475:408-411.
41. Barrett PJ, Chen J, Cho MK, Kim JH, Lu Z, Mathew S, Peng D, Song Y, Van Horn WD, Zhuang T, Sönnichsen FD, Sanders CR (2013) The quiet renaissance of protein nuclear magnetic resonance. Biochemistry 52:1303-1320.
42. Jacques DA, Trewhella J (2010) Small-Angle scattering for structural biology-expanding the frontier while avoiding the pitfalls. Protein Sci 19:642-657.
43. Mertens HD, Svergun DI (2010) Structural characterization of proteins and complexes using small-Angle X-Ray solution scattering. J Struct Biol 172:128-141.
44. Putnam CD, Hammel M, Hura GL, Tainer JA (2007) X-Ray solution scattering (SAXS) combined with crystallography and computation: Defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 40:191-285.
45. Madl T, Gabel F, Sattler M (2011) NMR and smallangle scattering-Based structural analysis of protein complexes in solution. J Struct Biol 173:472-482.
46. Dominguez C, Schubert M, Duss O, Ravindranathan S, Allain FH (2011) Structure determination and dynamics of protein-RNA complexes by NMR spectroscopy. Prog Nucl Magn Reson Spectrosc 58:1-61.
47. Mackereth CD, Simon B, Sattler M (2005) Extending the size of protein-RNA complexes studied by nuclear magnetic resonance spectroscopy. Chembiochem 6: 1578-1584.
48. Tugarinov V, Hwang PM, Kay LE (2004) Nuclear magnetic resonance spectroscopy of high-Molecularweight proteins. Annu Rev Biochem 73:107-146.
49. Fernandez C, Wider G (2003) TROSY in NMR studies of the structure and function of large biological macromolecules. Curr Opin Struct Biol 13:570-580.
50. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114.
51. Blackledge M (2005) Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings. Prog Nucl Magn Reson Spectrosc 46:23-61.
52. Prestegard JH, Bougault CM, Kishore AI (2004) Residual dipolar couplings in structure determination of biomolecules. Chem Rev 104:3519-3540.
53. Battiste JL, Wagner G (2000) Utilization of sitedirected spin labeling and high-Resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39:5355-5365.
54. Madl T, Felli IC, Bertini I, Sattler M (2010) Structural analysis of protein interfaces from 13C directdetected paramagnetic relaxation enhancements. J Am Chem Soc 132:7285-7287.
55. Madl T, Guttler T, Gorlich D, Sattler M (2011) Structural analysis of large protein complexes using solvent paramagnetic relaxation enhancements. Angew Chem Int Ed Engl 50:3993-3997.
56. Pintacuda G, John M, Su XC, Otting G (2007) NMR structure determination of protein-ligand complexes by lanthanide labeling. Acc Chem Res 40:206-212.
57. Simon B, Madl T, Mackereth CD, Nilges M, Sattler M (2010) An efficient protocol for NMR-Spectroscopybased structure determination of protein complexes in solution. Angew Chem Int Ed Engl 49:1967-1970.
58. Clore GM, Iwahara J (2009) Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-Population states of biological macromolecules and their complexes. Chem Rev 109:4108-4139.
59. Clore GM, Schwieters CD (2003) Docking of proteinprotein complexes on the basis of highly ambiguous intermolecular distance restraints derived from 1H/15N chemical shift mapping and backbone 15N-1H residual dipolar couplings using conjoined rigid body/torsion angle dynamics. J Am Chem Soc 125:2902-2912.
60. Rieping W, Habeck M, Nilges M (2005) Inferential structure determination. Science 309:303-306.
61. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: A protein-Protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125:1731-1737.
62. de Vries SJ, van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-Driven biomolecular docking. Nat Protoc 5:883-897.
63. Lange OF, Rossi P, Sgourakis NG, Song Y, Lee HW, Aramini JM, Ertekin A, Xiao R, Acton TB, Montelione GT, Baker D (2012) Determination of solution structures of proteins up to 40 kDa using CS-Rosetta with sparse NMR data from deuterated samples. Proc Natl Acad Sci USA 109:10873-10878.
64. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, Liu G, Eletsky A, Wu Y, Singarapu KK, Lemak A Ignatchenko A, Arrowsmith CH, Szyperski T, Montelione GT, Baker D, Bax A (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 105:4685-4690.
65. Cusack S, Jacrot B, Leberman R, May R, Timmins P, Zaccai G (1989) Neutron scattering. Nature 339:330.
66. Jacrot B (1976) The study of biological structures by neutron scattering from solution. Rep Prog Phys 39: 911-953.
67. Capel MS, Engelman DM, Freeborn BR, Kjeldgaard M, Langer JA, Ramakrishnan V, Schindler DG, Schneider DK, Schoenborn BP, Sillers IY et al (1987) A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science 238:1403-1406.
68. Ramakrishnan V (1986) Distribution of protein and RNA in the 30S ribosomal subunit. Science 231:1562-1564.
69. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HDT, Konarev PV, Svergun DI (2012) New developments in the ATSAS program package for small-Angle scattering data analysis. J Appl Crystallogr 45:342-350.
70. Round AR, Franke D, Moritz S, Huchler R, Fritsche M, Malthan D, Klaering R, Svergun DI, Roessle M (2008) Automated sample-Changing robot for solution scattering experiments at the EMBL Hamburg SAXS station X33. J Appl Crystallogr 41:913-917.
71. Jacques DA, Guss JM, Svergun DI, Trewhella J (2012) Publication guidelines for structural modelling of small-Angle scattering data from biomolecules in solution. Acta Crystallogr D68:620-626.
72. Rambo RP, Tainer JA (2013) Accurate assessment of mass, models and resolution by small-Angle scattering. Nature 496:477-481.
73. Trewhella J, Hendrickson WA, Kleywegt GJ, Sali A, Sato M, Schwede T, Svergun DI, Tainer JA, Westbrook J, Berman HM (2013) Report of the wwPDB small-Angle scattering task force: Data requirements for biomolecular modeling and the PDB. Structure 21:875-881.
74. Spill YG, Kim SJ, Schneidman-Duhovny D, Russel D, Webb B, Sali A, Nilges M (2014) SAXS Merge: An automated statistical method to merge SAXS profiles using Gaussian processes. J Synchrotron Radiat 21: 203-208.
75. Pieper U, Webb BM, Dong GQ, Schneidman-Duhovny D, Fan H, Kim SJ, Khuri N, Spill YG, Weinkam P, Hammel M, Tainer JA, Nilges M, Sali A (2014) Mod- Base, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Res 42:D336-D346.
76. Madl T, Bermel W, Zangger K (2009) Use of relaxation enhancements in a paramagnetic environment for the structure determination of proteins using NMR spectroscopy. Angew Chem Int Ed Engl 48:8259-8262.
77. Guttler T, Madl T, Neumann P, Deichsel D, Corsini L, Monecke T, Ficner R, Sattler M, Gorlich D (2010) NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat Struct Mol Biol 17:1367-1376.
78. Dominguez C, Bonvin AM, Winkler GS, van Schaik FM, Timmers HT, Boelens R (2004) Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches. Structure 12:633-644.
79. Grishaev A, Anthis NJ, Clore GM (2012) Contrastmatched small-Angle X-Ray scattering from a heavyatom- labeled protein in structure determination: Application to a lead-Substituted calmodulin-Peptide complex. J Am Chem Soc 134:14686-14689.
80. Bax A, Kontaxis G, Tjandra N (2001) Dipolar couplings in macromolecular structure determination. Methods Enzymol 339:127-174.
81. de Alba E, Tjandra, N (2002) NMR dipolar couplings for the structure determination of biopolymers in solution. Prog Nucl Magn Res Spectrosc 40:175-197.
82. Rückert M, Otting, G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc 122: 7793-7797.
83. Bloembergen N (1957) Proton relaxation times in paramagnetic solutions. J Chem Phys 27:572-573.
84. Bloembergen N, Morgan LO (1961) Proton relaxation times in paramagnetic solutions effects of electron spin relaxation. J Chem Phys 34:842.
85. Solomon I (1955) Relaxation processes in a system of 2 spins. Phys Rev 99:559-565.
86. Solomon I, Bloembergen N (1956) Nuclear magnetic interactions in the HF molecule. J Chem Phys 25:261-266.
87. Bertini I, Luchinat C, Parigi G (2002) Magnetic susceptibility in paramagnetic NMR. Prog Nucl Magn Reson Spectrosc 40:249-273.
88. Bernado P (2010) Effect of interdomain dynamics on the structure determination of modular proteins by small-Angle scattering. Eur Biophys J 39:769-780.
89. Gaponenko V, Howarth JW, Columbus L, Gasmi- Seabrook G, Yuan J, Hubbell WL, Rosevear PR (2000) Protein global fold determination using site-Directed spin and isotope labeling. Protein Sci 9:302-309.
90. Ollerenshaw JE, Tugarinov V, Kay LE (2003) Methyl TROSY: Explanation and experimental verification. Mag Reson Chem 41:843-852.
91. Bertini I, Felli IC, Luchinat C (2000) Lanthanide induced residual dipolar couplings for the conformational investigation of peripheral 15NH2 moieties. J Biomol NMR 18:347-355.
92. Bertini I, Luchinat C, Parigi G, Pierattelli R (2005) NMR spectroscopy of paramagnetic metalloproteins. Chembiochem 6:1536-1549.
93. Lu Y, Berry SM, Pfister TD (2001) Engineering novel metalloproteins: Design of metal-Binding sites into native protein scaffolds. Chem Rev 101:3047-3080.
94. Wohnert J, Franz KJ, Nitz M, Imperiali B, Schwalbe H (2003) Protein alignment by a coexpressed lanthanide-Binding tag for the measurement of residual dipolar couplings. J Am Chem Soc 125:13338-13339.
95. Barthelmes K, Reynolds AM, Peisach E, Jonker HR, DeNunzio NJ, Allen KN, Imperiali B, Schwalbe H (2011) Engineering encodable lanthanide-Binding tags into loop regions of proteins. J Am Chem Soc 133: 808-819.
96. Keizers PH, Saragliadis A, Hiruma Y, Overhand M, Ubbink M (2008) Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment. J Am Chem Soc 130:14802-14812.
97. Shimada I (2005) NMR techniques for identifying the interface of a larger protein-Protein complex: Crosssaturation and transferred cross-Saturation experiments. Methods Enzymol 394:483-506.
98. Falb M, Amata I, Gabel F, Simon B, Carlomagno T (2010) Structure of the K-turn U4 RNA: A combined NMR and SANS study. Nucleic Acids Res 38:6274-6285.
99. Lapinaite A, Simon B, Skjaerven L, Rakwalska-Bange M, Gabel F, Carlomagno T (2013) The structure of the box C/D enzyme reveals regulation of RNA methylation. Nature 502:519-523.
100. Hennig J, Wang I, Sonntag M, Gabel F, Sattler M (2013) Combining NMR and small angle X-Ray and neutron scattering in the structural analysis of a ternary protein-RNA complex. J Biomol NMR 56:17-30.
101. Svergun DI, Barberato C, Koch MHJ (1995) CRYSOL- a program to evaluate X-Ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28:768-773.
102. Cierpicki T, Bielnicki J, Zheng M, Gruszczyk J, Kasterka M, Petoukhov M, Zhang A, Fernandez EJ, Svergun DI, Derewenda U, Bushweller JH, Derewenda ZS (2009) The solution structure and dynamics of the DH-PH module of PDZRhoGEF in isolation and in complex with nucleotide-Free RhoA. Protein Sci 18:2067-2079.
103. Wang J, Zuo X, Yu P, Byeon IJ, Jung J, Wang X, Dyba M, Seifert S, Schwieters CD, Qin J, Gronenborn AM, Wang YX (2009) Determination of multicomponent protein structures in solution using global orientation and shape restraints. J Am Chem Soc 131: 10507-10515.
104. Zuo X, Wang J, Yu P, Eyler D, Xu H, Starich MR, Tiede DM, Simon AE, Kasprzak W, Schwieters CD, Shapiro BA, Wang YX (2010) Solution structure of the cap-independent translational enhancer and ribosome-Binding element in the 3' UTR of turnip crinkle virus. Proc Natl Acad Sci USA 107:1385-1390.
105. Grishaev A, Wu J, Trewhella J, Bax A (2005) Refinement of multidomain protein structures by combination of solution small-Angle X-Ray scattering and NMR data. J Am Chem Soc 127:16621-16628.
106. Grishaev A, Tugarinov V, Kay LE, Trewhella J, Bax A (2008) Refined solution structure of the 82-KDa enzyme malate synthase G from joint NMR and synchrotron SAXS restraints. J Biomol NMR 40:95-106.
107. Schwieters CD, Suh JY, Grishaev A, Ghirlando R, Takayama Y, Clore GM (2010) Solution structure of the 128 kDa enzyme I dimer from Escherichia coli and its 146 kDa complex with HPr using residual dipolar couplings and small- and wide-Angle X-Ray scattering. J Am Chem Soc 132:13026-13045.
108. Takayama Y, Schwieters CD, Grishaev A, Ghirlando R, Clore GM (2011) Combined use of residual dipolar couplings and solution X-Ray scattering to rapidly probe rigid-Body conformational transitions in a nonphosphorylatable active-Site mutant of the 128 kDa enzyme I dimer. J Am Chem Soc 133:424-427.
109. Gabel F, Simon B, Sattler M (2006) A target function for quaternary structural refinement from small angle scattering and NMR orientational restraints. Eur Biophys J 35:313-327.
110. Gabel F, Simon B, Nilges M, Petoukhov M, Svergun D, Sattler M (2008) A structure refinement protocol combining NMR residual dipolar couplings and small angle scattering restraints. J Biomol NMR 41:199-208
111. Gabel F (2012) A simple procedure to evaluate the efficiency of bio-Macromolecular rigid-Body refinement by small-Angle scattering. Eur Biophys J 41:1-11.
112. Mackereth CD, Sattler M (2012) Dynamics in multidomain protein recognition of RNA. Curr Opin Struct Biol 22:287-296.
113. Morgan HP, Schmidt CQ, Guariento M, Blaum BS, Gillespie D, Herbert AP, Kavanagh D, Mertens HD, Svergun DI, Johansson CM, Uhrin D, Barlow PN, Hannan JP (2011) Structural basis for engagement by complement factor H of C3b on a self surface. Nat Struct Mol Biol 18:463-470.
114. Sickmier EA, Frato KE, Shen H, Paranawithana SR, Green MR, Kielkopf CL (2006) Structural basis for polypyrimidine tract recognition by the essential premRNA splicing factor U2AF65. Mol Cell 23:49-59.
115. Bernado P, Modig K, Grela P, Svergun DI, Tchorzewski M, Pons M, Akke M (2010) Structure and dynamics of ribosomal protein L12: An ensemble model based on SAXS and NMR relaxation. Biophys J 98:2374-2382.
116. Bernado P, Mylonas E, Petoukhov MV, Blackledge M, Svergun DI (2007) Structural characterization of flexible proteins using small-Angle X-Ray scattering. J Am Chem Soc 129:5656-5664.
117. Bertini I, Giachetti A, Luchinat C, Parigi G, Petoukhov MV, Pierattelli R, Ravera E, Svergun DI (2010) Conformational space of flexible biological macromolecules from average data. J Am Chem Soc 132: 13553-13558.
118. Bertini I, Ferella L, Luchinat C, Parigi G, Petoukhov MV, Ravera E, Rosato A, Svergun DI (2012) MaxOcc: A web portal for maximum occurrence analysis. J Biomol NMR 53:271-280.
119. Ozenne V, Bauer F, Salmon L, Huang JR, Jensen MR, Segard S, Bernado P, Charavay C, Blackledge M (2012) Flexible-Meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 28:1463-1470.
120. Bertini I, Calderone V, Fragai M, Jaiswal R, Luchinat C, Melikian M, Mylonas E, Svergun DI (2008) Evidence of reciprocal reorientation of the catalytic and hemopexin-like domains of full-Length MMP-12. J Am Chem Soc 130:7011-7021.
121. Bertini I, Fragai M, Luchinat C, Melikian M, Mylonas E, Sarti N, Svergun DI (2009) Interdomain flexibility in full-Length matrix metalloproteinase-1 (MMP-1). J Biol Chem 284:12821-12828.
122. Grela P, Helgstrand M, Krokowski D, Boguszewska A, Svergun D, Liljas A, Bernado P, Grankowski N, Akke M, Tchorzewski M (2007) Structural characterization of the ribosomal P1A-P2B protein dimer by smallangle X-Ray scattering and NMR spectroscopy. Biochemistry 46:1988-1998.
123. Wells M, Tidow H, Rutherford TJ, Markwick P, Jensen MR, Mylonas E, Svergun DI, Blackledge M, Fersht AR (2008) Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc Natl Acad Sci USA 105:5762-5767.
124. Bernado P, Blackledge M (2009) A self-Consistent description of the conformational behavior of chemically denatured proteins from NMR and small angle scattering. Biophys J 97:2839-2845.
125. Xu R, Ayers B, Cowburn D, Muir TW (1999) Chemical ligation of folded recombinant proteins: Segmental isotopic labeling of domains for NMR studies. Proc Natl Acad Sci USA 96:388-393.
126. Muona M, Aranko AS, Raulinaitis V, Iwai H (2010) Segmental isotopic labeling of multi-Domain and fusion proteins by protein trans-Splicing in vivo and in vitro. Nat Protoc 5:574-587.
127. Mao H, Hart SA, Schink A, Pollok BA (2004) Sortasemediated protein ligation: A new method for protein engineering. J Am Chem Soc 126:2670-2671.
128. Chen I, Dorr BM, Liu DR (2011) A general strategy for the evolution of bond-Forming enzymes using yeast display. Proc Natl Acad Sci USA 108:11399-11404.
129. Refaei MA, Combs A, Kojetin DJ, Cavanagh J, Caperelli C, Rance M, Sapitro J, Tsang P (2011) Observing selected domains in multi-Domain proteins via sortase-Mediated ligation and NMR spectroscopy. J Biomol NMR 49:3-7.
130. Barraud P, Allain FH (2013) Solution structure of the two RNA recognition motifs of hnRNP A1 using segmental isotope labeling: How the relative orientation between RRMs influences the nucleic acid binding topology. J Biomol NMR 55:119-138.
131. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76:2879-2886.
132. Uversky VN (2031) A decade and a half of protein intrinsic disorder: Biology still waits for physics. Protein Sci 22:693-724.
133. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 3 Ligands, posttranslational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6:1917-1932.
134. Vucetic S, Xie H, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 6:1899-1916.
135. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6:1882-1898.
136. Mukrasch MD, Markwick P, Biernat J, Bergen M, Bernado P, Griesinger C, Mandelkow E, Zweckstetter M, Blackledge M (2007) Highly populated turn conformations in natively unfolded tau protein identified from residual dipolar couplings and molecular simulation. J Am Chem Soc 129:5235-5243.
137. 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 17:1169-1185.
138. Salmon L, Nodet G, Ozenne V, Yin G, Jensen MR, Zweckstetter M, Blackledge M (2010) NMR characterization of long-Range order in intrinsically disordered proteins. J Am Chem Soc 132:8407-8418.
139. Guttman M, Weinkam P, Sali A, Lee KK (2013) Allatom ensemble modeling to analyze small-Angle x-Ray scattering of glycosylated proteins. Structure 21:321-331
140. Johansen D, Trewhella J, Goldenberg DP (2011) Fractal dimension of an intrinsically disordered protein: Small-Angle X-Ray scattering and computational study of the bacteriophage lambda N protein. Protein Sci 20:1955-1970.
141. Gabel F (2012) Small angle neutron scattering for the structural study of intrinsically disordered proteins in solution: A practical guide.Methods Mol Biol 896:123-135.
142. Bernado P, Blanchard L, Timmins P, Marion D, Ruigrok RW, Blackledge M (2005) A structural model for unfolded proteins from residual dipolar couplings and small-Angle x-Ray scattering. Proc Natl Acad Sci USA 102:17002-17007.
143. Johansen D, Jeffries CM, Hammouda B, Trewhella J, Goldenberg DP (2011) Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-Angle neutron scattering with contrast matching. Biophys J 100:1120-1128.
144. Ito Y, Selenko P (2010) Cellular structural biology. Curr Opin Struct Biol 20:640-648.
145. Selenko P, Wagner G (2006) NMR mapping of protein interactions in living cells. Nat Methods 3:80-81.
146. Selenko P, Serber Z, Gadea B, Ruderman J, Wagner G (2006) Quantitative NMR analysis of the protein G B1 domain in Xenopus laevis egg extracts and intact oocytes. Proc Natl Acad Sci USA 103:11904-11909.
147. Serber Z, Selenko P, Hansel R, Reckel S, Lohr F, Ferrell JE, Jr, Wagner G, Dotsch V (2006) Investigating macromolecules inside cultured and injected cells by in-Cell NMR spectroscopy. Nat Protoc 1:2701-2709.
148. Selenko P, Frueh DP, Elsaesser SJ, Haas W, Gygi SP, Wagner G (2008) In situ observation of protein phosphorylation by high-Resolution NMR spectroscopy. Nat Struct Mol Biol 15:321-329.
149. Inomata K, Ohno A, Tochio H, Isogai S, Tenno T, Nakase I, Takeuchi T, Futaki S, Ito Y, Hiroaki H, Shirakawa M (2009) High-Resolution multidimensional NMR spectroscopy of proteins in human cells. Nature 458:106-109.
150. Huang JR, Gabel F, Jensen MR, Grzesiek S, Blackledge M (2012) Sequence-Specific mapping of the interaction between urea and unfolded ubiquitin from ensemble analysis of NMR and small angle scattering data. J Am Chem Soc 134:4429-4436.
151. Silvers R, Sziegat F, Tachibana H, Segawa S, Whittaker S, Gunther UL, Gabel F, Huang JR, Blackledge M, Wirmer-Bartoschek J, Schwalbe H (2012) Modulation of structure and dynamics by disulfide bond formation in unfolded states. J Am Chem Soc 134:6846-6854.
152. Leyrat C, Yabukarski F, Tarbouriech N, Ribeiro EA, Jr, Jensen MR, Blackledge M, Ruigrok RW, Jamin M (2011) Structure of the vesicular stomatitis virus N(0)-P complex. PLoS Pathog 7:e1002248.
153. Leyrat C, Jensen MR, Ribeiro EA, Jr, Gerard FC, Ruigrok RW, Blackledge M, Jamin M (2011) The N(0)- binding region of the vesicular stomatitis virus phosphoprotein is globally disordered but contains transient alpha-helices. Protein Sci 20:542-556.
154. Leyrat C, Schneider R, Ribeiro EA, Jr, Yabukarski F, Yao M, Gerard FC, Jensen MR, Ruigrok RW, Blackledge M, Jamin M (2012) Ensemble structure of the modular and flexible full-Length vesicular stomatitis virus phosphoprotein. J Mol Biol 423:182-197.
155. Jensen MR, Communie G, Ribeiro EA, Jr, Martinez N, Desfosses A, Salmon L, Mollica L, Gabel F, Jamin M, Longhi S, Ruigrok RW, Blackledge M (2011) Intrinsic disorder in measles virus nucleocapsids. Proc Natl Acad Sci USA 108:9839-9844.