Molecular dynamics simulation of the antiamoebin ion channel: Linking structure and conductance

Biophysical Journal

Volumn 100, Issue 10, 2011, Pages 2394-2402

  Wilson, Michael A ^a,b   Wei, Chenyu ^a,c   Bjelkmar, Pär ^b,e   Wallace, B A ^d   Pohorille, Andrew ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MS 239 4   (United States)

^c NASA AMES RESEARCH CENTER   (United States)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959643733     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.054     Document Type: Article

References (62)

1. Walz, T., T. Hirai,..., A. Engel. 1997. The three-dimensional structure of aquaporin-1. Nature. 387:624-627. (Pubitemid 27248769)
2. + conduction and selectivity. Science. 280:69-77. (Pubitemid 28169082)
3. Fischer, W. B., and M. S. P. Sansom. 2002. Viral ion channels: structure and function. Biochim. Biophys. Acta. 1561:27-45. (Pubitemid 34449687)
4. Chugh, J. K., and B. A. Wallace. 2001. Peptaibols: models for ion channels. Biochem. Soc. Trans. 29:565-570. (Pubitemid 32783658)
5. Duclohier, H. 2007. Peptaibiotics and peptaibols: an alternative to classical antibiotics? Chem. Biodivers. 4:1023-1026. (Pubitemid 47072861)
6. Brogden, K. A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250. (Pubitemid 40298223)
7. Pandey, R. C., H. Meng,..., K. L. Rinehart, Jr. 1977. Structure of antiamoebin I from high resolution field desorption and gas chromatographic mass spectrometry studies. J. Am. Chem. Soc. 99:5203-5205. (Pubitemid 8156796)
8. Karle, I. L., M. A. Perozzo,..., P. Balaram. 1998. Crystal structure of the channel-forming polypeptide antiamoebin in a membrane-mimetic environment. Proc. Natl. Acad. Sci. USA. 95:5501-5504. (Pubitemid 28224123)
9. Snook, C. F., G. A. Woolley,..., B. A. Wallace. 1998. The structure and function of antiamoebin I, a proline-rich membrane-active polypeptide. Structure. 6:783-792. (Pubitemid 28301211)
10. Galbraith, T. P., R. Harris,..., B. A. Wallace. 2003. Solution NMR studies of antiamoebin, a membrane channel-forming polypeptide. Biophys. J. 84:185-194. (Pubitemid 36026389)
11. Duclohier, H., C. F. Snook, and B. A. Wallace. 1998. Antiamoebin can function as a carrier or as a pore-forming peptaibol. Biochim. Biophys. Acta. 1415:255-260. (Pubitemid 29050778)
12. Leitgeb, B., A. Szekeres,..., L. Kredics. 2007. The history of alamethicin: a review of the most extensively studied peptaibol. Chem. Biodivers. 4:1027-1051. (Pubitemid 47072862)
13. Breed, J., P. C. Biggin,..., M. S. Sansom. 1997. Alamethicin channels-modeling via restrained molecular dynamics simulations. Biochim. Biophys. Acta. 1325:235-249. (Pubitemid 27193279)
14. Tieleman, D. P., B. Hess, and M. S. Sansom. 2002. Analysis and evaluation of channel models: simulations of alamethicin. Biophys. J. 83:2393-2407. (Pubitemid 35265736)
15. Gordon, L. G., and D. A. Haydon. 1972. The unit conductance channel of alamethicin. Biochim. Biophys. Acta. 255:1014-1018.
16. Sansom, M. S. 1991. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 55:139-235. (Pubitemid 121004226)
17. O'Reilly, A. O., and B. A. Wallace. 2003. The peptaibol antiamoebin as a model ion channel: similarities to bacterial potassium channels. J. Pept. Sci. 9:769-775. (Pubitemid 37493361)
18. Kurnikova, M. G., R. D. Coalson,..., A. Nitzan. 1999. A lattice relaxation algorithm for three-dimensional Poisson-Nernst-Planck theory with application to ion transport through the gramicidin A channel. Biophys. J. 76:642-656. (Pubitemid 29264548)
19. Noskov, S. Y., W. Im, and B. Roux. 2004. Ion permeation through the a-hemolysin channel: theoretical studies based on Brownian dynamics and Poisson-Nernst-Plank electrodiffusion theory. Biophys. J. 87:2299-2309. (Pubitemid 41071331)
20. Coalson, R. D., and M. G. Kurnikova. 2005. Poisson-Nernst-Planck theory approach to the calculation of current through biological ion channels. IEEE Trans. Nanobiosci. 4:81-93.
21. Chung, S. H., and S. Kuyucak. 2002. Ion channels: recent progress and prospects. Eur. Biophys. J. 31:283-293.
22. Cheng, M. H., M. Cascio, and R. D. Coalson. 2005. Theoretical studies of the M2 transmembrane segment of the glycine receptor: models of the open pore structure and current-voltage characteristics. Biophys. J. 89:1669-1680. (Pubitemid 41233524)
23. Aksimentiev, A., and K. Schulten. 2005. Imaging a-hemolysin with molecular dynamics: ionic conductance, osmotic permeability, and the electrostatic potential map. Biophys. J. 88:3745-3761. (Pubitemid 40991090)
24. Pezeshki, S., C. Chimerel,..., U. Kleinekathöfer. 2009. Understanding ion conductance on a molecular level: an all-atom modeling of the bacterial porin OmpF. Biophys. J. 97:1898-1906.
25. Biró, I., S. Pezeshki,..., U. Kleinekathöfer. 2010. Comparing the temperature-dependent conductance of the two structurally similar E. coli porins OmpC and OmpF. Biophys. J. 98:1830-1839.
26. Faraudo, J., C. Calero, and M. Aguilella-Arzo. 2010. Ionic partition and transport in multi-ionic channels: a molecular dynamics simulation study of the OmpF bacterial porin. Biophys. J. 99:2107-2115.
27. Pierce, B., W. Tong, and Z. Weng. 2005. M-ZDOCK: a grid-based approach for Cn symmetric multimer docking. Bioinformatics. 21:1472-1478. (Pubitemid 40542702)
28. Phillips, J. C., R. Braun,..., K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802. (Pubitemid 43078511)
29. Mackerell, Jr., A. D., M. Feig, and C. L. Brooks, 3rd. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25:1400-1415.
30. Feller, S. E., D. Yin,..., A. D. MacKerell, Jr. 1997. Molecular dynamics simulation of unsaturated lipid bilayers at low hydration: parameterization and comparison with diffraction studies. Biophys. J. 73:2269-2279. (Pubitemid 27471439)
31. MacKerell, Jr., A. D., B. Brooks,..., M. Karplus. 1998. CHARMM: the energy function and its parameterization with an overview of the program. In The Encyclopedia of Computational Chemistry, Vol. 1. P. v. R. Schleyer, N. L. Allinger, T. Clark, J. Gasteiger, P. Kollman, H. F. Schaefer, III, and P. R. Schreiner, editors. John Wiley and Sons, New York. 271-277.
32. Darve, E., and A. Pohorille. 2001. Calculating free energies using average force. J. Chem. Phys. 115:9169-9183. (Pubitemid 33128021)
33. Darve, E., M. A. Wilson, and A. Pohorille. 2002. Calculating free energies using a scaled-force molecular dynamics algorithm. Mol. Simul. 28:113-144. (Pubitemid 44121114)
34. Darve, E., D. Rodríguez-Gómez, and A. Pohorille. 2008. Adaptive biasing force method for scalar and vector free energy calculations. J. Chem. Phys. 128:144120.
35. Hénin, J., and C. Chipot. 2004. Overcoming free energy barriers using unconstrained molecular dynamics simulations. J. Chem. Phys. 121:2904-2914.
36. Rodriguez-Gomez, D., E. Darve, and A. Pohorille. 2004. Assessing the efficiency of free energy calculation methods. J. Chem. Phys. 120:3563-3578.
37. Hille, B. 2001. Ion Channels of Excitable Membranes, 3rd Ed. Sinauer Associates, Sunderland, MA.
38. Levitt, D. G. 1986. Interpretation of biological ion channel flux data-reaction-rate versus continuum theory. Annu. Rev. Biophys. Biophys. Chem. 15:29-57.
39. Heller, H., M. Schaefer, and K. Schulten. 1993. Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid-crystal phases. J. Phys. Chem. 97:8343-8360.
40. Chiu, S. W., S. Subramaniam, and E. Jakobsson. 1999. Simulation study of a gramicidin/lipid bilayer system in excess water and lipid. I. Structure of the molecular complex. Biophys. J. 76:1929-1938. (Pubitemid 29266350)
41. Garcia-Celma, J. J., L. Hatahet,..., K. Fendler. 2007. Specific anion and cation binding to lipid membranes investigated on a solid supported membrane. Langmuir. 23:10074-10080. (Pubitemid 47548488)
42. Pandit, S. A., D. Bostick, and M. L. Berkowitz. 2003. Molecular dynamics simulation of a dipalmitoylphosphatidylcholine bilayer with NaCl. Biophys. J. 84:3743-3750. (Pubitemid 36644146)
43. Mouritsen, O. G., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
44. Smart, O. S., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460. (Pubitemid 24005977)
45. Zuckerman, D. M., and T. B. Woolf. 2001. Efficient dynamic importance sampling of rare events in one dimension. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 63:016702.
46. Roux, B., T. Allen,..., W. Im. 2004. Theoretical and computational models of biological ion channels. Q. Rev. Biophys. 37:15-103. (Pubitemid 38902193)
47. Wilson, M. A., and A. Pohorille. 1996. Mechanism of unassisted ion transport across membrane bilayers. J. Am. Chem. Soc. 118:6580-6587. (Pubitemid 26248152)
48. Levitt, D. G. 1973. Dynamics of a single-file pore: non-Fickian behavior. Phys. Rev. A. 8:3050-3054.
49. + channel. Proc. Natl. Acad. Sci. USA. 100:8644-8648. (Pubitemid 36899151)
50. Hummer, G., J. C. Rasaiah, and J. P. Noworyta. 2001. Water conduction through the hydrophobic channel of a carbon nanotube. Nature. 414:188-190. (Pubitemid 33051229)
51. Zwanzig, R. W. 1964. Elementary derivation of time-correlation formulas for transport coefficients. J. Chem. Phys. 40:2527-2533.
52. - ions in ion channel models. Biophys. Chem. 79:129-151. (Pubitemid 29246098)
53. Allen, T W., O. S. Andersen, and B. Roux. 2006. Molecular dynamics-potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels. Biophys. Chem. 124:251-267. (Pubitemid 44692362)
54. Hall, J. E., I. Vodyanoy,..., G. R. Marshall. 1984. Alamethicin. A rich model for channel behavior. Biophys. J. 45:233-247.
55. Woolley, G. A. 2007. Channel-forming activity of alamethicin: effects of covalent tethering. Chem. Biodivers. 4:1323-1337. (Pubitemid 47072878)
56. Duclohier, H. 2004. Helical kink and channel behavior: a comparative study with the peptaibols alamethicin, trichotoxin and antiamoebin. Eur. Biophys. J. 33:169-174. (Pubitemid 39118293)
57. Cooper, K., E. Jakobsson, and P. Wolynes. 1985. The theory of ion transport through membrane channels. Prog. Biophys. Mol. Biol. 46:51-96.
58. Eisenberg, R. S. 1996. Computing the field in proteins and channels. J. Membr. Biol. 150:1-25. (Pubitemid 26102439)
59. Illingworth, C. J., and C. Domene. 2009. Many-body effects and simulations of potassium channels. Proc. R. Soc. A. 465:1701-1716.
60. Bucher, D., and U. Rothlisberger. 2010. Molecular simulations of ion channels: a quantum chemist's perspective. J. Gen. Physiol. 135:549-554.
61. Patel, S., J. E. Davis, and B. A. Bauer. 2009. Exploring ion permeation energetics in gramicidin A using polarizable charge equilibration force fields. J. Am. Chem. Soc. 131:13890-13891.
62. Bucher, D., and S. Kuyucak. 2009. Importance of water polarization for ion permeation in narrow pores. Chem. Phys. Lett. 477:207-210.