Prediction of charge-induced molecular alignment of biomolecules dissolved in dilute liquid-crystalline phases

Biophysical Journal

Volumn 86, Issue 6, 2004, Pages 3444-3460

  Zweckstetter, Markus ^a   Hummer, Gerhard ^b   Bax, Ad ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; OLIGOMER; PROTEIN;

AQUEOUS SOLUTION; ARTICLE; BACTERIOPHAGE; DIPOLE; ELECTRIC FIELD; ELECTRICITY; LIQUID CRYSTAL; MACROMOLECULE; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

EID: 2942653357     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.035790     Document Type: Article

References (72)

1. Al-Hashimi, H. M., H. Valafar, M. Terrell, E. R. Zartler, M. K. Eidsness, and J. H. Prestegard. 2000. Variation of molecular alignment as a means of resolving orientational ambiguities in protein structures from dipolar couplings. J. Magn. Reson. 143:402-406.
2. Almond, A., and J. B. Axelsen. 2002. Physical interpretation of residual dipolar couplings in neutral aligned media. J. Am. Chem. Soc. 124:9986-9987.
3. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1994. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:415-436.
4. Azurmendi, H. F., and C. A. Bush. 2002. Conformational studies of blood group A and blood group B oligosaccharides using NMR residual dipolar couplings. Carbohydr. Res. 337:905-915.
5. Barrientos, L. G., C. Dolan, and A. M. Gronenborn. 2000. Characterization of surfactant liquid crystal phases suitable for molecular alignment and measurement of dipolar couplings. J. Biomol. NMR. 16:329-337.
6. Barrientos, L. G., J. M. Louis, and A. M. Gronenborn. 2001. Characterization of the cholesteric phase of filamentous bacteriophage fd for molecular alignment. J. Magn. Reson. 149:154-158.
7. BenTal, N., B. Honig, C. Miller, and S. McLaughlin. 1997. Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles. Biophys. J. 73:1717-1727.
8. BenTal, N., B. Honig, R. M. Peitzsch, G. Denisov, and S. McLaughlin. 1996. Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys. J. 71:561-575.
9. Bewley, C. A. 2001. Rapid validation of the overall structure of an internal domain-swapped mutant of the anti-HIV protein cyanovirin-N using residual dipolar couplings. J. Am. Chem. Soc. 123:1014-1015.
10. Bewley, C. A., and G. M. Clore. 2000. Determination of the relative orientation of the two halves of the domain-swapped dimer of cyanovirin-N in solution using dipolar couplings and rigid body minimization. J. Am. Chem. Soc. 122:6009-6016.
11. Chapman, D. L. 1913. A contribution to the theory of electrocapillarity. Philosoph. Magaz. 25:475-481.
12. Clore, G. M., and C. D. Schwieters. 2003. Docking of protein-protein 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.
13. Clore, G. M., M. R. Starich, and A. M. Gronenbom. 1998. Measurement of residual dipolar couplings of macromolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J. Am. Chem. Soc. 120:10571-10572.
14. Comilescu, G., J. L. Marquardt, M. Ottiger, and A. Bax. 1998. Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120:6836-6837.
15. Davis, M. E., and J. A. McCammon. 1990. Electrostatics in biomolecular structure and dynamics. Chem. Rev. 90:509-521.
16. Debye, P., and E. Hueckel. 1923. Zur Theorie der Elektrolyte. I. Gefrierpunktsemiedrigung und verwandte Erscheinungen. Phys. Zeitschr. 24:185-206.
17. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, and A. Bax. 1995. NMRPIPE-a multidimensional spectral processing system based on unix pipes. J. Biomol. NMR. 6:277-293.
18. Delaglio, F., G. Kontaxis, and A. Bax. 2000. Protein structure determination using molecular fragment replacement and NMR dipolar couplings. J. Am. Chem. Soc. 122:2142-2143.
19. Derrick, J. P., and D. B. Wigley. 1994. The 3rd Igg-binding domain from streptococcal protein-G-an analysis by x-ray crystallography of the structure alone and in a complex with FAB. J. Mol. Biol. 243:906-918.
20. Dickerson, R. E., and H. R. Drew. 1981. Structure of a B-DNA dodecamer. II. Influence of base sequence on helix structure. J. Mol. Biol. 149:761-786.
21. Dingemans, T., D. J. Photinos, E. T. Samulski, A. F. Terzis, and C. Wutz. 2003. Ordering of apolar and polar solutes in nematic solvents. J. Chem. Phys. 118:7046-7061.
22. Eisenberg, D., and A. D. McLachlan. 1986. Solvation energy in protein folding and binding. Nature. 319:199-203.
23. Eisenhaber, F., and P. Argos. 1993. Improved strategy in analytic surface calculation for molecular systems: handling of singularities and computational efficiency. J. Comput. Chem. 14:1272-1280.
24. Eisenhaber, F., P. Lijnzaad, P. Argos, C. Sander, and M. Scharf. 1995. The double cubic lattice method: efficient approaches to numerical integration of surface area and volume and to dot surface contouring of molecular assemblies. J. Comput. Chem. 16:273-284.
25. Emsley, J. W., W. E. Palke, and G. N. Shilstone. 1991. The inclusion of electrostatic and dispersion interactions into potentials of mean torque for solutes dissolved in uniaxial liquid-crystal solvents. Liq. Crystals. 9:643-648.
26. Fernandes, M. X., P. Bemado, M. Pons, and J. G. de la Torre. 2001. An analytical solution to the problem of the orientation of rigid particles by planar obstacles. Application to membrane systems and to the calculation of dipolar couplings in protein NMR spectroscopy. J. Am. Chem. Soc. 123:12037-12047.
27. Ferrarini, A. 2003. Modeling of macromolecular alignment in nematic virus suspensions. Application to the prediction of NMR residual dipolar couplings. J. Phys. Chem. B. 107:7923-7931.
28. Fleming, K., D. Gray, S. Prasannan, and S. Matthews. 2000. Cellulose crystallites: a new and robust liquid crystalline medium for the measurement of residual dipolar couplings. J. Am. Chem. Soc. 122:5224-5225.
29. Gallagher, K., and K. Sharp. 1998. Electrostatic contributions to heat capacity changes of DNA-ligand binding. Biophys. J. 75:769-776.
30. Gallagher, T., P. Alexander, P. Bryan, and G. L. Gilliland. 1994. Two crystal structures of the B I immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry. 33:4721-4729.
31. Gouy, D. L. 1910. Sur la constitution de la charge électrique a la surface d'un électrolyte. Ann. Phys. 9:457-468.
32. Gronenbom, A. M., D. R. Filpula, M. Z. Essiz, A. Achari, M. Whitlow, P. T. Wingfield, and G. M. Clore. 1991. A novel, highly stable form of the immunoglobulin binding domain of streptococcal protein G. Science. 253:657-661.
33. Hansen, M. R., L. Mueller, and A. Pardi. 1998. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat. Struct. Biol. 5:1065-1074.
34. Honig, B., K. Sharp, and A. S. Yang. 1993. Macroscopic models of aqueous solutions: biological and chemical applications. J. Phys. Chem. 97:1101-1109.
35. Hummer, G., L. R. Pratt, and A. E. Garcia. 1998. Molecular theories and simulation of ions and polar molecules in water. J. Phys. Chem. A. 102:7885-7895.
36. Hus, J. C., D. Marion, and M. Blackledge. 2001. Determination of protein backbone structure using only residual dipolar couplings. J. Am. Chem. Soc. 123:1541-1542.
37. Koradi, R., M. Billeter, and K. Wuthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55.
38. Losonczi, J. A., and J. H. Prestegard. 1998. Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules. J. Biomol. NMR. 12:447-451.
39. Meiler, J., J. J. Prompers, W. Peti, C. Griesinger, and R. Bruschweiler. 2001. Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J. Am. Chem. Soc. 123:6098-6107.
40. Mills, P., C. F. Anderson, and M. T. Record. 1985. Monte Carlo studies of counterion-DNA interactions. Comparison of the radial distribution of counterions with predictions of other polyelectrolyte theories. J. Phys. Chem. 89:3984-3994.
41. Murray, D., and B. Honig. 2002. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell. 9:145-154.
42. Murthy, C. S., R. J. Bacquet, and P. J. Rossky. 1985. Ionic distributions near polyelectrolytes: a comparison of theoretical approaches. J. Phys. Chem. 89:701-710.
43. Ottiger, M., and A. Bax. 1999. Bicelle-based liquid crystals for NMR measurement of dipolar couplings at acidic and basic pH values. J. Biomol. NMR. 13:187-191.
44. Ottiger, M., F. Delaglio, and A. Bax. 1998. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131:373-378.
45. Peitzsch, R. M., M. Eisenberg, K. A. Sharp, and S. McLaughlin. 1995. Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys. J. 68:729-738.
46. Peti, W., J. Meiler, R. Bruschweiler, and C. Griesinger. 2002. Model-free analysis of protein backbone motion from residual dipolar couplings. J. Am. Chem. Soc. 124:5822-5833.
47. Photinos, D. J., C. D. Poon, E. T. Samulski, and H. Toriumi. 1992. NMR study of the effects of electric-dipole interactions on the ordering of chain solutes in the nematic phase. J. Phys. Chem. 96:8176-8180.
48. Photinos, D. J., and E. T. Samulski. 1993. Electric-dipole interactions of chain molecules in nematics-the analysis of segmental ordering in α,ω-dibromoalkanes. J. Chem. Phys. 98:10009-10016.
49. Prestegard, J. H., and A. I. Kishore. 2001. Partial alignment of biomolecules: an aid to NMR characterization. Curr. Opin. Chem. Biol. 5:584-590.
50. Prosser, R. S., J. A. Losonczi, and I. V. Shiyanovskaya. 1998. Use of a novel aqueous liquid crystalline medium for high-resolution NMR of macromolecules in solution. J. Am. Chem. Soc. 120:11010-11011.
51. Ramirez, B. E., and A. Bax. 1998. Modulation of the alignment tensor of macromolecules dissolved in a dilute liquid crystalline medium. J. Am. Chem. Soc. 120:9106-9107.
52. Ramirez, B. E., O. N. Voloshin, R. D. Camerini-Otero, and A. Bax. 2000. Solution structure of DinI provides insight into its mode of RecA inactivation. Protein Sci. 9:2161-2169.
53. Ruckert, M., and G. Otting. 2000. Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J. Am. Chem. Soc. 122:7793-7797.
54. Sass, J., F. Cordier, A. Hoffmann, M. Rogowski, A. Cousin, J. G. Omichinski, H. Lowen, and S. Grzesiek. 1999. Purple membrane induced alignment of biological macromolecules in the magnetic field. J. Am. Chem. Soc. 121:2047-2055.
55. Stigter, D. 1982a. Coil expansion in polyelectrolyte solutions. Macromolecules. 15:635-641.
56. Stigter, D. 1982b. Mobility of water near charged interfaces. Adv. Coll. Interf. Sci. 16:253-265.
57. Syvitski, R. T., and E. E. Burnell. 1997. Dipole-induced ordering in nematic liquid crystals-fact or fiction? Chem. Phys. Lett. 281:199-206.
58. Syvitski, R. T., and E. E. Burnell. 2000. Dipole-induced ordering in nematic liquid crystals. II. The elusive Holy Grail. J. Chem. Phys. 113:3452-3465.
59. Terzis, A. F., C. D. Poon, E. T. Samulski, Z. Luz, R. Poupko, H. Zimmermann, K. Muller, H. Toriumi, and D. J. Photinos. 1996. Shape-dominated ordering in nematic solvents. A deuterium NMR study of cycloalkane solutes. J. Am. Chem. Soc. 118:2226-2234.
60. Tjandra, N., and A. Bax. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science. 278:1111-1114.
61. Tjandra, N., J. G. Omichinski, A. M. Gronenbom, G. M. Clore, and A. Bax. 1997. Use of dipolar H1-N15 and H1-C13 couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 4:732-738.
62. Tjandra, N., S. Tate, A. Ono, M. Kainosho, and A. Bax. 2000. The NMR structure of a DNA dodecamer in an aqueous dilute liquid crystalline phase. J. Am. Chem. Soc. 122:6190-6200.
63. Tolman, J. R. 2002. A novel approach to the retrieval of structural and dynamic information from residual dipolar couplings using several oriented media in biomolecular NMR spectroscopy. J. Am. Chem. Soc. 124:12020-12030.
64. Tolman, J. R., J. M. Flanagan, M. A. Kennedy, and J. H. Prestegard. 1995. Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc. Natl. Acad. Sci. USA. 92:9279-9283.
65. Valafar, H., and J. H. Prestegard. 2003. Rapid classification of a protein fold family using a statistical analysis of dipolar couplings. Bioinformatics. 19:1549-1555.
66. Vroege, G. J., and H. N. W. Lekkerkerker. 1992. Phase transitions in lyotropic colloidal and polymer liquid crystals. Rep. Prog. Phys. 55:1241-1309.
67. Warren, J. J., and P. B. Moore. 2001. Application of dipolar coupling data to the refinement of the solution structure of the Sarcin-Ricin loop RNA. J. Biomol. NMR. 20:311-323.
68. Warshel, A., and J. Aqvist. 1991. Electrostatic energy and macromolecular. function. Annu. Rev. Biophys. Biophys. Chem. 20:267-298.
69. Zimmermann, K., H. Hagedom, C. C. Heuck, M. Hinrichsen, and H. Ludwig. 1986. The ionic properties of the filamentous bacteriophages Pf1 and fd. J. Biol. Chem. 261:1653-1655.
70. Zweckstetter, M., and A. Bax. 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.
71. Zweckstetter, M., and A. Bax. 2001. Characterization of molecular alignment in aqueous suspensions of Pf1 bacteriophage. J. Biomol. NMR. 20:365-377.
72. Zweckstetter, M., and A. Bax. 2002. Evaluation of uncertainty in alignment tensors obtained from dipolar couplings. J. Biomol. NMR. 23:127-137.