An Implicit Membrane Generalized Born Theory for the Study of Structure, Stability, and Interactions of Membrane Proteins

Biophysical Journal

Volumn 85, Issue 5, 2003, Pages 2900-2918

  Im, Wonpil ^a   Feig, Michael ^a   Brooks III, Charles L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEE VENOM; GLYCOPHORIN A; MELITTIN; MEMBRANE PROTEIN;

ANALYTIC METHOD; ARTICLE; CRYSTALLIZATION; HYDROPHOBICITY; MOLECULAR INTERACTION; MOLECULAR MIMICRY; NONHUMAN; PHENOMENOLOGY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SOLVATION; SURFACE TENSION; THEORY;

APOIDEA;

EID: 0242322528     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74712-2     Document Type: Article

References (79)

1. Adams, P. D., and A. T. Brunnger. 2001. Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching. Proteins. 26:257-261.
2. Almeida, F. C. L., and S. J. Opella. 1997. Fd coat protein structure in membrane environments: structural dynamics of the loop between the hydrophobic transmembrane helix and the amphipathic in-plane helix. J. Mol. Biol. 270:481-495.
3. Arkin, I. T. 2002. Structural aspects of oligomerization taking place between the transmembrane α-helices of bitopic membrane proteins. Biochim. Biophys. Acta. 1565:347-363.
4. Bachar, M., and O. M. Becker. 2000. Protein-induced membrane disorder: a molecular dynamics study of melittin in a dipalmitoylphosphatidylcholine bilayer. Biophys. J. 78:1359-1375.
5. 1H-NMR study in methanol. Eur. J. Biochem. 173:139-146.
6. Bernèche, S., M. Nina, and B. Roux. 1998. Molecular dynamics simulation of melittin in a dimyristoylphosphatidylcholine bilayer membrane. Biophys. J. 75:1603-1618.
7. Born, M. 1920. Volumen und hydratationswarme der ionen. Z. Phys. 1: 45-48.
8. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:187-217.
9. Brooks III, C. L., M. Karplus, and B. M. Pettitt. 1988. Proteins, a theoretical perspective of dynamics, structure and thermodynamics. In Advances in Chemical Physics, Vol. LXXI. I. Prigogine, and S. A. Rice, editors. John Wiley & Sons, New York.
10. Cowan, S. W., T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, R. A. Pauptit, J. N. Jansonius, and J. P. Rosenbusch. 1992. Crystal structures explain functional properties of two E. coli porins. Nature. 358:727-733.
11. David, L., R. Luo, and M. K. Gilson. 2000. Comparison of generalized Born and Poisson models: energetics and dynamics of HIV protease. J. Comput. Chem. 21:295-309.
12. 2H NMR and EPR study using designed transmembrane α-helical peptides and gramicidin A. Biochemistry. 37:9333-9345.
13. Dominy, B. N., and C. L. Brooks III. 1999. Development of a generalized Born model parametrization for proteins and nucleic acids. J. Phys. Chem. B. 103:3765-3773.
14. + conduction and selectivity. Science. 280:69-77.
15. Feig, M., A. D. MacKerell, Jr., and C. L. Brooks III. 2003. Force field influence on the observation of π-helical protein structures in molecular dynamics simulations. J. Phys. Chem. B. 107:2831-2836.
16. Fischer, W. B., and M. S. P. Sansom. 2002. Viral ion channels: structure and function. Biochim. Biophys. Acta. 1561:27-45.
17. Fleishman, S. J., and N. Ben-Tai. 2002. A novel scoring function for predicting the conformations of tightly packed pairs of transmembrane α-helices. J. Mol. Biol. 321:363-378.
18. Fleming, K. G., and D. M. Engelman. 2001. Computation and mutagenesis suggest a right-handed structure for the synaptobrevin transmembrane dimer. Proteins. 45:313-317.
19. Gabdoulline, R. R., and R. C. Wade. 1996. Effective charges for macromolecules in solvent. J. Phys. Chem. 100:3868-3878.
20. Ghosh, A., C. S. Rapp, and R. A. Friesner. 1998. Generalized Born model based on a surface integral formulation. J. Phys. Chem. B. 102:10983-10990.
21. Gilson, M. K., M. E. Davis, B. A. Luty, and J. A. McCammon. 1993. Computation of electrostatic forces on solvated molecules using the Poisson-Boltzmann equation. J. Phys. Chem. 97:3591-3600.
22. Habermann, E. 1972. Bee and wasp venoms. Science. 177:314-322.
23. Hansmann, U. H. E. 1997. Parallel tempering algorithm for conformational studies of biological molecules. Chem. Phys. Lett. 281:140-150.
24. Hassan, S. A., F. Guarnieri, and E. L. Mehler. 2000. A general treatment of solvent effects based on screened Coulomb potentials. J. Phys. Chem. B. 104:6478-6489.
25. Hawkins, G. D., C. J. Cramer, and D. G. Truhlar. 1996. Parametrized models of aqueous free energies of solvation based on pairwise descreening of solute atomic charges from a dielectric medium. J. Phys. Chem. 100:19824-19839.
26. Hermann, R. B. 1972. Theory of hydrophobic bonding. II. The correlation of hydrocarbon solubility in water with solvent cavity surface area. J. Phys. Chem. 76:2754-2759.
27. Im, W., D. Beglov, and B. Roux. 1998. Continuum solvation model: electrostatic forces from numerical solutions to the Poisson-Boltzmann equation. Comput. Phys. Comm. 111:59-75.
28. Im, W., S. Bernèche, and B. Roux. 2001. Generalized solvent boundary potential for computer simulations. J. Chem. Phys. 114:2924-2937.
29. Im, W., M. S. Lee, and C. L. Brooks III. 2003. Generalized Born model with a simple smoothing function. J. Comput. Chem. 24:1691-1702.
30. Im, W., and B. Roux. 2002a. Ion permeation and selectivity of OMPF porin: a theoretical study based on molecular dynamics, Brownian dynamics, and continuum electrodiffusion theory. J. Mol. Biol. 322:851-869.
31. Im, W., and B. Roux. 2002b. Ions and counterions in a biological channel: a molecular dynamics simulation of OMPF porin from Escherichia coli in an explicit membrane with 1 m kcl aqueous salt solution. J. Mol. Biol. 319:1177-1197.
32. Jiang, Y., A. Lee, J. Chen, M. Cadene, B. T. Chait, and R. MacKinnon. 2002. The open pore conformation of potassium channels. Nature. 417:523-526.
33. Klapper, I., R. Hagstrom, R. Fine, K. Sharp, and B. Honig. 1986. Focusing of electric fields in the active site of Cu-Zn superoxide dismutase: effects of ionic strength and amino-acid modification. Proteins. 1:47-59.
34. Kovacs, F. A., J. K. Denny, Z. Song, J. R. Quine, and T. A. Cross. 2000. Helix tilt of the M2 transmembrane peptide from Influenza A virus: an intrinsic property. J. Mol. Biol. 295:117-125.
35. Lamb, R. A., L. J. Holsinger, and L. H. Pinto. (1994). The Influenza A virus M2 ion channel protein and its role in the Influenza virus life cycle. In Receptor-Mediated Virus Entry into Cell. E. Wimmer, editor. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 303-321.
36. Lamberth, S., H. Schmid, M. Muenchbach, T. Vorherr, J. Krebs, E. Carafoli, and C. Griesinger. 2000. NMR solution structure of phospholamban. Helv. Chim. Acta. 83:2141-2152.
37. Lazaridis, T., and M. Karplus. 1999. Effective energy functions for proteins in solution. Proteins. 35:133-152.
38. Lazaridis, T., and M. Karplus. 2000. Effective energy functions for protein structure prediction. Curr. Opin. Struct. Biol. 10:139-145.
39. Lebedev, V. I., and D. N. Laikov. 1999. A quadrature formula for the sphere of the 131st algebraic order of accuracy. Doklady Math. 59:477-481.
40. Lee, M. S., M. Feig, F. R. Salsbury, Jr., and C. L. Brooks III. 2003. A new analytical approximation to the standard molecular volume definition and its application to generalized Born calculations. J. Comput. Chem. 24:1348-1356.
41. Lee, M. S., F. R. Salsbury, Jr., and C. L. Brooks III. 2002. Novel generalized Born methods. J. Chem. Phys. 116:10606-10614.
42. Lin, J.-H., and A. Baumgaertner. 2000. Stability of a melittin pore in a lipid bilayer: a molecular dynamics study. Biophys. J. 78:1714-1724.
43. Luo, R., L. David, and M. K. Gilson. 2002. Accelerated Poisson-Boltzmann calculations for static and dynamic systems. J. Comput. Chem. 23:1244-1253.
44. MacKenzie, K. R., J. H. Prestegard, and D. M. Engelman. 1997. A transmembrane helix dimer: structure and implications. Science. 276:131-133.
45. MacKerell Jr., A. D., D. Bashford, M. Bellot, R. L. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, D. Joseph-McCarthy, S. Ha, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher III, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
46. 2 domains. Mol. Cell. 9:145-154.
47. 13C NMR spectroscopy. Biophys. J. 78:2405-2417.
48. Nicholls, A., and B. Honig. 1991. A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation. J. Comput. Chem. 12:435-445.
49. Nina, M., D. Beglov, and B. Roux. 1997. Atomic radii for continuum electrostatics calculations based on molecular dynamics free energy simulations. J. Phys. Chem. B. 101:5239-5248.
50. Nina, M., W. Im, and B. Roux. 1999. Optimized atomic radii for protein continuum electrostatics solvation forces. Biophys. Chem. 78:89-96.
51. Onufriev, A., D. Bashford, and D. A. Case. 2000. Modification of the generalized Born model suitable for macromolecules. J. Phys. Chem. B. 104:3712-3720.
52. Onufriev, A., D. Bashford, and D. A. Case. 2002. Effective Born radii in the generalized Born approximation: the importance of being perfect. J. Comput. Chem. 23:1297-1304.
53. Petrache, H. I., A. Grossfield, K. R. MacKenzie, D. M. Engelman, and T. B. Woolf. 2000. Modulation of glycophorin a transmembrane helix interactions by lipid bilayers: molecular dynamics calculations. J. Mol. Biol. 302:727-746.
54. Philippsen, A. 2001. DINO: Visualizing structural biology. http://www.dino3d.org.
55. Popot, J. L., and D. M. Engelman. 2000. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:881-922.
56. Press, W. H., B. P. Flannery, S. A. Teukolsky, and W. T. Vetterling. 1989. Numerical Recipes: The Art of Scientific Computing. Cambridge University Press, Cambridge, MA.
57. Qiu, D., P. S. Shenkin, F. P. Hollinger, and W. C. Still. 1997. The GB/ SA continuum model for solvation. A fast analytical method for the calculation of approximate Born radii. J. Phys. Chem. A. 101:3005-3014.
58. Rastogi, V. K., and M. E. Girvin. 1999. Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature. 402:263-268.
59. Roux, B. 1997. The influence of the membrane potential on the free energy of an intrinsic protein. Biophys. J. 73:2980-2989.
60. Roux, B. 2002. Theoretical and computational models of ion channels. Curr. Opin. Struct. Biol. 12:182-189.
61. Roux, B., S. Bernèche, and W. Im. 2000. Ion channels, permeation, and electrostatics: insight into the function of KcsA. Biochemistry. 39:13295-13306.
62. Roux, B., and T. Simonson. 1999. Implicit solvent models. Biophys. Chem. 78:1-20.
63. Sanbonmatsu, K. Y., and A. E. Garcia. 2002. Structure of Met-Enkephalin in explicit aqueous solution using replica exchange molecular dynamics. Proteins. 46:225-234.
64. Scarsi, M., J. Apostolakis, and A. Caflisch. 1997. Continuum electrostatic energies of macromolecules in aqueous solutions. J. Phys. Chem. A. 101:8098-8106.
65. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301-332.
66. Simonson, T., and A. Brunger. 1994. Solvation free energies estimated from macroscopic continuum theory: an accuracy assessment. J. Phys. Chem. 98:4683-4694.
67. Smith, S. O., D. Song, S. Shekar, M. Groesbeek, M. Ziliox, and S. Aimoto. 2001. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry. 40:6553-6558.
68. Spassov, V. Z., L. Yan, and S. Szalma. 2002. Introducing an implicit membrane in generalized Born/solvent accessibility continuum solvent models. J. Phys. Chem. B. 106:8726-8738.
69. Still, W. C., A. Tempczyk, R. C. Hawley, and T. Hendrickson. 1990. Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112:6127-6129.
70. Sugita, Y., and Y. Okamoto. 1999. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314:141-151.
71. Terwilliger, T. C., and D. Eisenberg. 1982a. The structure of melittin. II. Interpretation of the structure. J. Biol. Chem. 257:6016-6022.
72. Terwilliger, T. C., and D. Eisenberg. 1982b. The structure of melittin: structure determination and partial refinement. J. Biol. Chem. 257:6010-6015.
73. Torres, J., J. A. G. Briggs, and I. T. Arkin. 2002. Contribution of energy values to the analysis of global searching molecular dynamics simulations of transmembrane helical bundles. Biophys. J. 82:3063-3071.
74. Toyoshima, C., M. Nakasako, H. Nomura, and H. Ogawa. 2000. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature. 405:647-655.
75. Vaidehi, N., W. B. Floriano, R. Trabanino, S. E. Hall, P. Freddolino, E. J. Choi, G. Zamanakos, and W. A. Goddard III. 2002. Prediction of structure and function of G protein-coupled receptors. Proc. Natl. Acad. Sci. USA. 99:12622-12627.
76. von Heijine, G. 1999. A day in the life of Dr. K. or how I learned to stop worrying and love lysozyme: a tragedy in six acts. J. Mol. Biol. 293:367-379.
77. + channel. Protein Sci. 10:2241-2250.
78. Warwicker, J., and H. C. Watson. 1982. Calculation of the electric potential in the active site cleft due to alpha-helix dipoles. J. Mol. Biol. 157:671-679.
79. Zhou, R., B. J. Berne, and R. Germain. 2002. The free energy landscape for β-hairpin folding in explicit water. Proc. Natl. Acad. Sci. USA. 98:14931-14936.