Abstract
Many proteins have modular design with multiple globular domains connected via flexible linkers. As a simple model of such system, we study a tandem construct consisting of two identical SH3 domains and a variable-length Gly/Ser linker. When the linker is short, this construct represents a dumbbell-shaped molecule with limited amount of domain–domain mobility. Due to its elongated shape, this molecule efficiently aligns in steric alignment media. As the length of the linker increases, the two domains become effectively uncoupled and begin to behave as independent entities. Consequently, their degree of alignment drops, approaching that found in the (near-spherical) isolated SH3 domains. To model the dependence of alignment parameters on the length of the interdomain linker, we have generated in silico a series of conformational ensembles representing SH3 tandems with different linker length. These ensembles were subsequently used as input for alignment prediction software PALES. The predicted alignment tensors were compared with the results of experimental measurements using a series of tandem-SH3 samples in PEG/hexanol alignment media. This comparison broadly confirmed the expected trends. At the same time, it has been found that the isolated SH3 domain aligns much stronger than expected. This finding can be attributed to complex morphology of the PEG/hexanol media and/or to weak site-specific interactions between the protein and the media. In the latter case, there are strong indications that electrostatic interactions may play a role. The fact that PEG/hexanol does not behave as a simple steric media should serve as a caution for studies that use PALES as a quantitative prediction tool (especially for disordered proteins). Further progress in this area depends on our ability to accurately model the anisotropic media and its site-specific interactions with protein molecules. Once this ability is improved, it should be possible to use the alignment parameters as a measure of domain–domain cooperativity, thus identifying the situations where two domains transiently interact with each other or become coupled through a partially structured linker.
Similar content being viewed by others
Notes
In contrast, we found that alignment of ubiquitin in PEG/hexanol is insensitive to salt.
References
Akakura S, Kar B, Singh S, Cho L, Tibrewal N, Sanokawa-Akakura R, Reichman C, Ravichandran KS, Birge RB (2005) C-terminal SH3 domain of Crkll regulates the assembly and function of the DOCK180/ELMO Rac-GEF. J Cell Physiol 204:344–351
Alexandrescu AT, Kammerer RA (2003) Structure and disorder in the ribonuclease S-peptide probed by NMR residual dipolar couplings. Protein Sci 12:2132–2140
Andre I, Linse S, Mulder FAA (2007) Residue-specific pKa determination of lysine and arginine side chains by indirect 15N and 13C NMR spectroscopy: Application to apo calmodulin. J Am Chem Soc 129:15805–15813
Aroulanda C, Celebre G, De Luca G, Longeri M (2006) Molecular ordering and structure of quasi-spherical solutes by liquid crystal NMR and Monte Carlo simulations: the case of norbornadiene. J Phys Chem B 110:10485–10496
Bae SH, Dyson HJ, Wright PE (2009) Prediction of the rotational tumbling time for proteins with disordered segments. J Am Chem Soc 131:6814–6821
Balzer D (1993) Cloud point phenomena in the phase behavior of alkyl polyglucosides in water. Langmuir 9:3375–3384
Bas DC, Rogers DM, Jensen JH (2008) Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins 73:765–783
Bax A (2003) Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci 12:1–16
Bax A, Tjandra N (1997) High-resolution heteronuclear NMR of human ubiquitin in an aqueous liquid crystalline medium. J Biomol NMR 10:289–292
Bax A, Kontaxis G, Tjandra N (2001) Dipolar couplings in macromolecular structure determination. Method Enzymol 339:127–174
Berlin K, O’Leary DP, Fushman D (2009) Improvement and analysis of computational methods for prediction of residual dipolar couplings. J Magn Reson 201:25–33
Bernado P, Blanchard L, Timmins P, Marion D, Ruigrok RWH, 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
Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzani A, Zoroddu MA (2004) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 101:6841–6846
Bertini I, Gupta YK, Luchinat C, Parigi G, Peana M, Sgheri L, Yuan J (2007) Paramagnetism-based NMR restraints provide maximum allowed probabilities for the different conformations of partially independent protein domains. J Am Chem Soc 129:12786–12794
Bewley CA (2001) Solution structure of a cyanovirin-N: Manα1-2Manα complex: structural basis for high-affinity carbohydrate-mediated binding to gp120. Structure 9:931–940
Blanco FJ, Ortiz AR, Serrano L (1997) 1H and 15N NMR assignment and solution structure of the SH3 domain of spectrin: comparison of unrefined and refined structure sets with the crystal structure. J Biomol NMR 9:347–357
Braddock DT, Cai ML, Baber JL, Huang Y, Clore GM (2001) Rapid identification of medium- to large-scale interdomain motion in modular proteins using dipolar couplings. J Am Chem Soc 123:8634–8635
Braddock DT, Baber JL, Levens D, Clore GM (2002) Molecular basis of sequence-specific single-stranded DNA recognition by KH domains: solution structure of a complex between hnRNP KKH3 and single-stranded DNA. EMBO J 21:3476–3485
Briggman KB, Tolman JR (2003) De Novo determination of bond orientations and order parameters from residual dipolar couplings with high accuracy. J Am Chem Soc 125:10164–10165
Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30:1545–1614
Brosey CA, Chagot ME, Ehrhardt M, Pretto DI, Weiner BE, Chazin WJ (2009) NMR analysis of the architecture and functional remodeling of a modular multidomain protein, RPA. J Am Chem Soc 131:6346–6347
Bryngelson JD, Wolynes PG (1987) Spin glasses and the statistical mechanics of protein folding. Proc Natl Acad Sci USA 84:7524–7528
Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins Struct Funct Genet 21:167–195
Cesareni G, Gimona M, Sudol M, Yaffe M (eds) (2005) Modular protein domains. Wiley-VCH, Weinheim
Chen K, Tjandra N (2008) Extended model free approach to analyze correlation functions of multidomain proteins in the presence of motional coupling. J Am Chem Soc 130:12745–12751
Chevelkov V, Faelber K, Diehl A, Heinemann U, Oschkinat H, Reif B (2005) Detection of dynamic water molecules in a microcrystalline sample of the SH3 domain of α-spectrin by MAS solid-state NMR. J Biomol NMR 31:295–310
Chevelkov V, Zhuravleva AV, Xue Y, Reif B, Skrynnikov NR (2007) Combined analysis of 15N relaxation data from solid- and solution-state NMR spectroscopy. J Am Chem Soc 129:12594–12595
Chevelkov V, Xue Y, Linser R, Skrynnikov NR, Reif B (2010) Comparison of solid-state dipolar couplings and solution relaxation data provides insight into protein backbone dynamics. J Am Chem Soc 132:5015–5017
Cipres A, Abassi YA, Vuori K (2007) Abl functions as a negative regulator of Met-induced cell motility via phosphorylation of the adapter protein CrkII. Cell Signal 19:1662–1670
Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836–6837
de la Torre JG, Huertas ML, Carrasco B (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 78:719–730
Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe—a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6:277–293
Denisov AY, Kloser E, Gray DG, Mittermaier AK (2010) Protein alignment using cellulose nanocrystals: practical considerations and range of application. J Biomol NMR 47:195–204
Dingemans T, Photinos DJ, Samulski ET, Terzis AF, Wutz C (2003) Ordering of apolar and polar solutes in nematic solvents. J Chem Phys 118:7046–7061
Dominy BN, Brooks CL (1999) Development of a generalized Born model parametrization for proteins and nucleic acids. J Phys Chem B 103:3765–3773
Donaldson LW, Gish G, Pawson T, Kay LE, Forman-Kay JD (2002) Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Proc Natl Acad Sci USA 99:14053–14058
Elworthy PH, Rogers JA, Florence AT (1971) Stabilization of oil-in-water emulsions by nonionic detergents. 5. Effect of salts on rates of coalescence in a chlorobenzene emulsion. J Colloid Interf Sci 35:23–33
Emsley JW, Palke WE, Shilstone GN (1991) The inclusion of electrostatic and dispersion interactions into potentials of mean torque for solutes dissolved in uniaxial liquid-crystal solvents. Liq Cryst 9:643–648
Feldman HJ, Hogue CWV (2000) A fast method to sample real protein conformational space. Proteins Struct Funct Genet 39:112–131
Feller SM (2001) Crk family adaptors—signalling complex formation and biological roles. Oncogene 20:6348–6371
Fischer D, Geyer A (2005) NMR spectroscopic characterization of the membrane affinity of polyols. Magn Reson Chem 43:893–901
Fitzkee NC, Rose GD (2004) Reassessing random-coil statistics in unfolded proteins. Proc Natl Acad Sci USA 101:12497–12502
Freyssingeas É, Nallet F, Roux D (1996) Measurement of the membrane flexibility in lamellar and ‘‘sponge’’ phases of the C12E5/hexanol/water system. Langmuir 12:6028–6035
Futterer K, Wong J, Grucza RA, Chan AC, Waksman G (1998) Structural basis for syk tyrosine kinase ubiquity in signal transduction pathways revealed by the crystal structure of its regulatory SH2 domains bound to a dually phosphorylated ITAM peptide. J Mol Biol 281:523–537
Gaemers S, Bax A (2001) Morphology of three lyotropic liquid crystalline biological NMR media studied by translational diffusion anisotropy. J Am Chem Soc 123:12343–12352
Gelis I, Bonvin AMJJ, Keramisanou D, Koukaki M, Gouridis G, Karamanou S, Economou A, Kalodimos CG (2007) Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131:756–769
Gordon JC, Myers JB, Folta T, Shoja V, Heath LS, Onufriev A (2005) H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucl Acids Res 33:W368–W371
Hakansson KO (2009) The structure of Mg-ATPase nucleotide-binding domain at 1.6 angstrom resolution reveals a unique ATP-binding motif. Acta Crystallogr D 65:1181–1186
Heikkinen O, Permi P, Koskela H, Ylanne J, Kilpelainen I (2009) 1H, 13C and 15N resonance assignments of the human filamin A tandem immunoglobulin-like domains 16–17 and 18–19. Biomol NMR Assign 3:53–56
Holland NB, Nishimiya Y, Tsuda S, Sonnichsen FD (2008) Two domains of RD3 antifreeze protein diffuse independently. Biochemistry 47:5935–5941
Huston JS, Levinson D, Mudgetthunter M, Tai MS, Novotny J, Margolies MN, Ridge RJ, Bruccoleri RE, Haber E, Crea R, Oppermann H (1988) Protein engineering of antibody-binding sites: recovery of specific activity in an anti-digoxin single-chain Fv analog produced in Escherichia Coli. Proc Natl Acad Sci USA 85:5879–5883
Ikegami T, Verdier L, Sakhaii P, Grimme S, Pescatore B, Saxena K, Fiebig KM, Griesinger C (2004) Novel techniques for weak alignment of proteins in solution using chemical tags coordinating lanthanide ions. J Biomol NMR 29:339–349
Ikura M, Kay LE, Krinks M, Bax A (1991) Triple-resonance multidimensional NMR study of calmodulin complexed with the binding domain of skeletal muscle Myosin Light-Chain Kinase: indication of a conformational change in the central helix. Biochemistry 30:5498–5504
Jensen MR, Houben K, Lescop E, Blanchard L, Ruigrok RWH, Blackledge M (2008) Quantitative conformational analysis of partially folded proteins from residual dipolar couplings: Application to the molecular recognition element of Sendai virus nucleoprotein. J Am Chem Soc 130:8055–8061
Jeon SI, Lee JH, Andrade JD, De Gennes PG (1991) Protein surface interactions in the presence of polyethylene oxide. I. Simplified theory. J Colloid Interf Sci 142:149–158
Jonstromer M, Strey R (1992) Nonionic bilayers in dilute solutions: effect of additives. J Phys Chem 96:5993–6000
Jung YS, Cai ML, Clore GM (2010) Solution structure of the IIAChitobiose-IIBChitobiose complex of the N,N‘-diacetylchitobiose branch of the Escherichia Coli phosphotransferase system. J Biol Chem 285:4173–4184
Karraker KA, Radke CJ (2002) Disjoining pressures zeta potentials and surface tensions of aqueous non-ionic surfactant/electrolyte solutions: theory and comparison to experiment. Adv Colloid Interfac 96:231–264
Keizers PHJ, Desreux JF, Overhand M, Ubbink M (2007) Increased paramagnetic effect of a lanthanide protein probe by two-point attachment. J Am Chem Soc 129:9292–9293
Khandogin J, Brooks CL (2006) Toward the accurate first-principles prediction of ionization equilibria in proteins. Biochemistry 45:9363–9373
Kobashigawa Y, Sakai M, Naito M, Yokochi M, Kumeta H, Makino Y, Ogura K, Tanaka S, Inagaki F (2007) Structural basis for the transforming activity of human cancer-related signaling adaptor protein CRK. Nat Struct Mol Biol 14:503–510
Koenig BW, Hu JS, Ottiger M, Bose S, Hendler RW, Bax A (1999) NMR measurement of dipolar couplings in proteins aligned by transient binding to purple membrane fragments. J Am Chem Soc 121:1385–1386
Korzhnev DM, Religa TL, Banachewicz W, Fersht AR, Kay LE (2010) A transient and low-populated protein-folding intermediate at atomic resolution. Science 329:1312–1316
Lakomek NA, Carlomagno T, Becker S, Griesinger C, Meiler J (2006) A thorough dynamic interpretation of residual dipolar couplings in ubiquitin. J Biomol NMR 34:101–115
Lazar GA, Desjarlais JR, Handel TM (1997) De novo design of the hydrophobic core of ubiquitin. Protein Sci 6:1167–1178
Li H, Robertson AD, Jensen JH (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61:704–721
Lim K, Herron JN (1992) Molecular simulation of protein-PEG interactions. In Harris JM (ed) Poly(ethylene glycol) chemistry: biotechnical and biomedical applications. Plenum Press, New York, pp 29–56
Linghu H, Tsuda M, Makino Y, Sakai M, Watanabe T, Ichihara S, Sawa H, Nagashima K, Mochizuki N, Tanaka S (2006) Involvement of adaptor protein Crk in malignant feature of human ovarian cancer cell line MCAS. Oncogene 25:3547–3556
Maltsev AS, Ahmed AH, Fenwick MK, Jane DE, Oswald RE (2008) Mechanism of partial agonism at the GluR2 AMPA receptor: Measurements of lobe orientation in solution. Biochemistry 47:10600–10610
Martinez JC, Pisabarro MT, Serrano L (1998) Obligatory steps in protein folding and the conformational diversity of the transition state. Nat Struct Biol 5:721–729
McPherson T, Kidane A, Szleifer I, Park K (1998) Prevention of protein adsorption by tethered poly(ethylene oxide) layers: experiments and single-chain mean-field analysis. Langmuir 14:176–186
Miller CT, Chen G, Gharib TG, Wang H, Thomas DG, Misek DE, Giordano TJ, Yee J, Orringer MB, Hanash SM, Beer DG (2003) Increased c-Crk proto-oncogene expression is associated with an aggressive phenotype in lung adenocarcinomas. Oncogene 22:7950–7957
Mohana-Borges R, Goto NK, Kroon GJA, Dyson HJ, Wright PE (2004) Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J Mol Biol 340:1131–1142
Moltke S, Grzesiek S (1999) Structural constraints from residual tensorial couplings in high resolution NMR without an explicit term for the alignment tensor. J Biomol NMR 15:77–82
Moreno-Murciano MP, Monleon D, Marcinkiewcz C, Calvete JJ, Celda B (2003) NMR solution structure of the non-RGD disintegrin obtustatin. J Mol Biol 329:135–145
Muralidharan V, Dutta K, Cho J, Vila-Perello M, Raleigh DP, Cowburn D, Muir TW (2006) Solution structure and folding characteristics of the C-terminal SH3 domain of c-Crk-II. Biochemistry 45:8874–8884
Musacchio A, Noble M, Pauptit R, Wierenga R, Saraste M (1992) Crystal structure of a Src-homology 3 (SH3) domain. Nature 359:851–855
Nishihara H, Tanaka S, Tsuda M, Oikawa S, Maeda M, Shimizu M, Shinomiya H, Tanigami A, Sawa H, Nagashima K (2002) Molecular and immunohistochemical analysis of signaling adaptor protein Crk in human cancers. Cancer Lett 180:55–61
Ogawa S, Toyoshima H, Kozutsumi H, Hagiwara K, Sakai R, Tanaka T, Hirano N, Mano H, Yazaki Y, Hirai H (1994) The C-Terminal SH3 domain of the mouse c-Crk protein negatively regulates tyrosine phosphorylation of Crk associated p130 in rat 3Y1 cells. Oncogene 9:1669–1678
Ohnishi S, Shortle D (2003) Observation of residual dipolar couplings in short peptides. Proteins Struct Funct Genet 50:546–551
Opella SJ, De Angelis AA (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat Protoc 2:2332–2338
Ottiger M, Bax A (1998) Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J Biomol NMR 12:361–372
Ottiger M, Delaglio F, Bax A (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Reson 131:373–378
Peterson ME, Long EO (2008) Inhibitory receptor signaling via tyrosine phosphorylation of the adaptor Crk. Immunity 29:578–588
Pinheiro AS, Marsh JA, Forman-Kay JD, Peti W (2011) Structural Signature of the MYPT1-PP1 Interaction. J Am Chem Soc 133:73–80
Polyansky AA, Volynsky PE, Nolde DE, Arseniev AS, Efremov RG (2005) Role of lipid charge in organization of water/lipid bilayer interface: Insights via computer simulations. J Phys Chem B 109:15052–15059
Poon DKY, Withers SG, McIntosh LP (2007) Direct demonstration of the flexibility of the glycosylated proline-threonine linker in the Cellulomonas fimi xylanase Cex through NMR spectroscopic analysis. J Biol Chem 282:2091–2100
Prestegard JH, Al-Hashimi HM, Tolman JR (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q Rev Biophys 33:371–424
Rodriguez-Castaneda F, Haberz P, Leonov A, Griesinger C (2006) Paramagnetic tagging of diamagnetic proteins for solution NMR. Magn Reson Chem 44:S10–S16
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
Sarkar P, Reichman C, Saleh T, Birge RB, Kalodimos CG (2007) Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol Cell 25:413–426
Sass J, Cordier F, Hoffmann A, Rogowski M, Cousin A, Omichinski JG, Lowen H, Grzesiek S (1999) Purple membrane induced alignment of biological macromolecules in the magnetic field. J Am Chem Soc 121:2047–2055
Sass HJ, Musco G, Stahl SJ, Wingfield PT, Grzesiek S (2000) Solution NMR of proteins within polyacrylamide gels: Diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes. J Biomol NMR 18:303–309
Schomacker R, Strey R (1994) Effect of ionic surfactants on nonionic bilayers: bending elasticity of weakly charged membranes. J Phys Chem 98:3908–3912
Schwieters CD, Clore GM (2001) Internal coordinates for molecular dynamics and minimization in structure determination and refinement. J Magn Reson 152:288–302
Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:65–73
Shakhnovich EI, Gutin AM (1989) Formation of unique structure in polypeptide chains. Theoretical investigation with the aid of a replica approach. Biophys Chem 34:187–199
Simon K, Xu J, Kim C, Skrynnikov NR (2005) Estimating the accuracy of protein structures using residual dipolar couplings. J Biomol NMR 33:83–93
Skrynnikov NR, Goto NK, Yang DW, Choy WY, Tolman JR, Mueller GA, Kay LE (2000) Orienting domains in proteins using dipolar couplings measured by liquid-state NMR: differences in solution and crystal forms of maltodextrin binding protein loaded with beta-cyclodextrin. J Mol Biol 295:1265–1273
Slupsky CM, Kay CM, Reinach FC, Smillie LB, Sykes BD (1995) Calcium-induced dimerization of troponin C: mode of interaction and use of trifluoroethanol as a denaturant of quaternary structure. Biochemistry 34:7365–7375
Sprangers R, Kay LE (2007) Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445:618–622
Strey R, Schomacker R, Roux D, Nallet F, Olsson U (1990) Dilute lamellar and L3 phases in the binary water-C12E5 system. J Chem Soc Faraday T 86:2253–2261
Stubenrauch C, von Klitzing R (2003) Disjoining pressure in thin liquid foam and emulsion films—new concepts and perspectives. J Phys Condens Matt 15:R1197–R1232
Suh JY, Cai ML, Clore GM (2008) Impact of phosphorylation on structure and thermodynamics of the interaction between the N-terminal domain of enzyme I and the histidine phosphocarrier protein of the bacterial phosphotransferase system. J Biol Chem 283:18980–18989
Syvitski RT, Burnell EE (2000) Dipole-induced ordering in nematic liquid crystals. II. The elusive holy grail. J Chem Phys 113:3452–3465
Takino T, Nakada M, Miyamori H, Yamashita J, Yamada KM, Sato H (2003) CrkI adapter protein modulates cell migration and invasion in glioblastoma. Cancer Res 63:2335–2337
Terzis AF, Photinos DJ (1994) Electrostatic interactions in liquid crystals: ordering of rigid solutes in nematic solvents. Mol Phys 83:847–865
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
Tollinger M, Forman-Kay JD, Kay LE (2002) Measurement of side-chain carboxyl pKa values of glutamate and aspartate residues in an unfolded protein by multinuclear NMR spectroscopy. J Am Chem Soc 124:5714–5717
Tolman JR, Al-Hashimi HM, Kay LE, Prestegard JH (2001) Structural and dynamic analysis of residual dipolar coupling data for proteins. J Am Chem Soc 123:1416–1424
Tzakos AG, Grace CRR, Lukavsky PJ, Riek R (2006) NMR techniques for very large proteins and RNAs in solution. Annu Rev Biophys Biomol Struct 35:319–342
Ulmer TS, Werner JM, Campbell ID (2002) SH3-SH2 domain orientation in Src kinases: NMR studies of Fyn. Structure 10:901–911
Ulmer TS, Ramirez BE, Delaglio F, Bax A (2003) Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy. J Am Chem Soc 125:9179–9191
Valafar H, Prestegard JH (2004) REDCAT: a residual dipolar coupling analysis tool. J Magn Reson 167:228–241
van Dam L, Karlsson G, Edwards K (2006) Morphology of magnetically aligning DMPC/DHPC aggregates-perforated sheets, not disks. Langmuir 22:3280–3285
van Rossum BJ, Castellani F, Pauli J, Rehbein K, Hollander J, de Groot HJM, Oschkinat H (2003) Assignment of amide proton signals by combined evaluation of HN, NN and HNCA MAS-NMR correlation spectra. J Biomol NMR 25:217–223
Vega MC, Martínez JC, Serrano L (2000) Thermodynamic and structural characterization of Asn and Ala residues in the disallowed II’ region of the Ramachandran plot. Protein Sci 9:2322–2328
von Berlepsch H, de Vries R (2000) Weakly charged lamellar bilayer system: interplay between thermal undulations and electrostatic repulsion. Eur Phys J E1:141–152
Walsh JD, Meier K, Ishima R, Gronenborn AM (2010) NMR studies on domain diffusion and alignment in modular GB1 repeats. Biophys J 99:2636–2646
Wang W, Weng J, Zhang X, Liu M, Zhang M (2009) Creating conformational entropy by increasing interdomain mobility in ligand binding regulation: a revisit to N-terminal tandem PDZ domains of PSD-95. J Am Chem Soc 131:787–796
Wardle KE, Carlson E, Henderson D, Rowley RL (2004) Molecular-dynamics simulation of the effect of ions on a liquid–liquid interface for a partially miscible mixture. J Chem Phys 120:7681–7688
Watanabe T, Tsuda M, Makino Y, Ichihara S, Sawa H, Minami A, Mochizuki N, Nagashima K, Tanaka S (2006) Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder 1 and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res 4:499–510
Wong V, Case DA, Szabo A (2009) Influence of the coupling of interdomain and overall motions on NMR relaxation. Proc Natl Acad Sci USA 106:11016–11021
Wu B, Petersen M, Girard F, Tessari M, Wijmenga SS (2006) Prediction of molecular alignment of nucleic acids in aligned media. J Biomol NMR 35:103–115
Yang DW, Nagayama K (1996) A sensitivity-enhanced method for measuring heteronuclear long-range coupling constants from the displacement of signals in two 1D subspectra. J Magn Reson Ser A 118:117–121
Zangi R, Engberts JBFN (2005) Physisorption of hydroxide ions from aqueous solution to a hydrophobic surface. J Am Chem Soc 127:2272–2276
Zhang YB, Zuiderweg ERP (2004) The 70-kDa heat shock protein chaperone nucleotide-binding domain in solution unveiled as a molecular machine that can reorient its functional subdomains. Proc Natl Acad Sci USA 101:10272–10277
Zhang YJ, Oh H, Burton RA, Burgner JW, Geahlen RL, Post CB (2008) Tyr130 phosphorylation triggers Syk release from antigen receptor by long-distance conformational uncoupling. Proc Natl Acad Sci USA 105:11760–11765
Zheng J, Li LY, Chen SF, Jiang SY (2004) Molecular simulation study of water interactions with oligo (ethylene glycol)-terminated alkanethiol self-assembled monolayers. Langmuir 20:8931–8938
Zheng J, Li LY, Tsao HK, Sheng YJ, Chen SF, Jiang SY (2005) Strong repulsive forces between protein and oligo (ethylene glycol) self-assembled monolayers: A molecular simulation study. Biophys J 89:158–166
Zweckstetter M (2006) Prediction of charge-induced molecular alignment: residual dipolar couplings at pH 3 and alignment in surfactant liquid crystalline phases. Eur Biophys J Biophys Lett 35:170–180
Zweckstetter M (2008) NMR: prediction of molecular alignment from structure using the PALES software. Nat Protoc 3:679–690
Zweckstetter M, Bax A (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J Am Chem Soc 122:3791–3792
Zweckstetter M, Hummer G, Bax A (2004) Prediction of charge-induced molecular alignment of biomolecules dissolved in dilute liquid-crystalline phases. Biophys J 86:3444–3460
Acknowledgments
This work has been funded through NSF grant MCB-044563. We thank Ryan Muir for his help with early versions of the structure-generating scripts. We are also grateful to Etti Harms, Nina Gorenstein, Josh Ward, and Yi Xue for their advice on different aspects of experimental work.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yuwen, T., Post, C.B. & Skrynnikov, N.R. Domain cooperativity in multidomain proteins: what can we learn from molecular alignment in anisotropic media?. J Biomol NMR 51, 131 (2011). https://doi.org/10.1007/s10858-011-9548-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10858-011-9548-7