Sodium channel selectivity and conduction: Prokaryotes have devised their own molecular strategy

Journal of General Physiology

Volumn 143, Issue 2, 2014, Pages 157-171

  Finol Urdaneta, Rocio K ^a,b   Wang, Yibo ^a   Al Sabi, Ahmed ^a,b   Zhao, Chunfeng ^a   Noskov, Sergei Y ^a   French, Robert J ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; MOLECULAR GENETICS; PHYSIOLOGY; PROKARYOTIC CELL;

AMINO ACID SEQUENCE; ANIMALS; MOLECULAR SEQUENCE DATA; PROKARYOTIC CELLS; SODIUM CHANNELS;

EID: 84893077319     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311037     Document Type: Article

References (66)

1. Adams, D.J., T.M. Dwyer, and B. Hille. 1980. The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75:493-510. http://dx.doi.org/10.1085/jgp.75.5.493
2. Allen, T.W., O.S. Andersen, and B. Roux. 2004. Energetics of ion conduction through the gramicidin channel. Proc. Natl. Acad. Sci. USA. 101:117-122. http://dx.doi.org/10.1073/pnas.2635314100
3. Backx, P.H., D.T. Yue, J.H. Lawrence, E. Marban, and G.F. Tomaselli. 1992. Molecular localization of an ion-binding site within the pore of mammalian sodium channels. Science. 257:248-251. http://dx .doi.org/10.1126/science.1321496
4. Bezanilla, F., and C.M. Armstrong. 1972. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J. Gen. Physiol. 60:588-608. http://dx.doi .org/10.1085/jgp.60.5.588
5. Brooks, B.R., C.L. Brooks III, A.D. Mackerell Jr., L. Nilsson, R.J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, et al. 2009. CHARMM: the biomolecular simulation program. J. Comput. Chem. 30:1545-1614. http://dx.doi.org/10.1002/jcc.21287
6. Busath, D., and T. Begenisich. 1982. Unidirectional sodium and potassium fluxes through the sodium channel of squid giant axons. Biophys. J. 40:41-49. http://dx.doi.org/10.1016/S0006-3495(82)84456-1
7. Corry, B., and M. Thomas. 2012. Mechanism of ion permeation and selectivity in a voltage gated sodium channel. J. Am. Chem. Soc. 134:1840-1846. http://dx.doi.org/10.1021/ja210020h
8. Derebe, M.G., D.B. Sauer, W. Zeng, A. Alam, N. Shi, and Y. Jiang. 2011. Tuning the ion selectivity of tetrameric cation channels by changing the number of ion binding sites. Proc. Natl. Acad. Sci. USA. 108:598-602. http://dx.doi.org/10.1073/pnas.1013636108
9. Doyle, D.A., J. Morais Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 280:69-77. http://dx.doi.org/10.1126/science.280.5360.69
10. Eisenman, G. 1962. Cation selective glass electrodes and their mode of operation. Biophys. J. 2:259-323. http://dx.doi.org/10.1016/ S0006-3495(62)86959-8
11. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J. Membr. Biol. 76:197-225. http://dx.doi.org/10.1007/BF01870364
12. Eisenman, G., R. Latorre, and C. Miller. 1986. Multi-ion conduction and selectivity in the high-conductance Ca++-activated K+ channel from skeletal muscle. Biophys. J. 50:1025-1034. http://dx.doi.org/10.1016/S0006-3495(86)83546-9
13. Essmann, U., L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593. http://dx.doi.org/10.1063/1.470117
14. Feller, S.E., and A.D. MacKerell. 2000. An improved empirical potential energy function for molecular simulations of phospholipids. J. Phys. Chem. B. 104:7510-7515.
15. French, R.J., J.F. Worley III, W.F. Wonderlin, A.S. Kularatna, and B.K. Krueger. 1994. Ion permeation, divalent ion block, and chemical modification of single sodium channels. Description by single- and double-occupancy rate-theory models. J. Gen. Physiol. 103:447-470. http://dx.doi.org/10.1085/jgp.103.3.447
16. Furini, S., and C. Domene. 2012. On conduction in a bacterial sodium channel. PLOS Comput. Biol. 8:e1002476. http://dx.doi.org/10.1371/journal.pcbi.1002476
17. Garber, S.S. 1988. Symmetry and asymmetry of permeation through toxin-modified Na+ channels. Biophys. J. 54:767-776. http://dx.doi.org/10.1016/S0006-3495(88)83014-5
18. Gillespie, D., and D. Boda. 2008. The anomalous mole fraction effect in calcium channels: a measure of preferential selectivity. Biophys. J. 95:2658-2672. http://dx.doi.org/10.1529/biophysj.107.127977
19. Goldman, D.E. 1943. Potential, impedance, and rectification in membranes. J. Gen. Physiol. 27:37-60. http://dx.doi.org/10.1085/jgp.27.1.37
20. Grossfield, A. 2012. WHAM: the weighted histogram analysis method. Version 2.0.6. http://membrane.urmc.rochester.edu/content/wham(accessed December 27, 2013).
21. Heginbotham, L., Z. Lu, T. Abramson, and R. MacKinnon. 1994. Mutations in the K+ channel signature sequence. Biophys. J. 66:1061- 1067. http://dx.doi.org/10.1016/S0006-3495(94)80887-2
22. Heinemann, S.H., H. Terlau, W. Stühmer, K. Imoto, and S. Numa. 1992. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature. 356:441-443. http://dx.doi.org/10.1038/356441a0
23. Hess, P., and R.W. Tsien. 1984. Mechanism of ion permeation through calcium channels. Nature. 309:453-456. http://dx.doi.org/10.1038/309453a0
24. Hille, B. 1971. The permeability of the sodium channel to organic cations in myelinated nerve. J. Gen. Physiol. 58:599-619. http://dx.doi.org/10.1085/jgp.58.6.599
25. Hille, B. 1972. The permeability of the sodium channel to metal cations in myelinated nerve. J. Gen. Physiol. 59:637-658. http://dx.doi.org/10.1085/jgp.59.6.637
26. Hille, B. 1973. Potassium channels in myelinated nerve. Selective permeability to small cations. J. Gen. Physiol. 61:669-686. http://dx.doi.org/10.1085/jgp.61.6.669
27. Hille, B. 1975a. Ionic selectivity of Na and K channels of nerve membranes. Membranes. 3:255-323.
28. Hille, B. 1975b. Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J. Gen. Physiol. 66:535-560. http://dx.doi.org/10.1085/jgp.66.5.535
29. Hille, B. 2001. Ion channels of Excitable Membranes. Third edition. Sinauer Associates, Sunderland, MA. 814 pp.
30. Hille, B., and W. Schwarz. 1978. Potassium channels as multi-ion singlefile pores. J. Gen. Physiol. 72:409-442. http://dx.doi.org/10.1085/jgp.72.4.409
31. Hodgkin, A.L., and R.D. Keynes. 1955. The potassium permeability of a giant nerve fibre. J. Physiol. 128:61-88.
32. Hodgkin, A.L., A.F. Huxley, and B. Katz. 1952. Measurement of current- voltage relations in the membrane of the giant axon of Loligo. J. Physiol. 116:424-448.
33. Jo, S., T. Kim, V.G. Iyer, and W. Im. 2008. CHARMM-GUI: a web-based graphical user interface for CHARMM. J. Comput. Chem. 29:1859- 1865. http://dx.doi.org/10.1002/jcc.20945
34. Khan, A., L. Romantseva, A. Lam, G. Lipkind, and H.A. Fozzard. 2002. Role of outer ring carboxylates of the rat skeletal muscle sodium channel pore in proton block. J. Physiol. 543:71-84. http://dx.doi.org/10.1113/jphysiol.2002.021014
35. Kim, I., and T.W. Allen. 2011. On the selective ion binding hypothesis for potassium channels. Proc. Natl. Acad. Sci. USA. 108:17963-17968. http://dx.doi.org/10.1073/pnas.1110735108
36. Kim, M.S., T. Morii, L.X. Sun, K. Imoto, and Y. Mori. 1993. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett. 318:145-148. http://dx.doi.org/10.1016/0014-5793(93)80009-J
37. Krauss, D., B. Eisenberg, and D. Gillespie. 2011. Selectivity sequences in a model calcium channel: role of electrostatic field strength. Eur. Biophys. J. 40:775-782. http://dx.doi.org/10.1007/s00249-011-0691-6
38. Kumar, S., D. Bouzida, R.H. Swendsen, P.A. Kollman, and J.M. Rosenberg. 1992. THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13:1011-1021. http://dx.doi.org/10.1002/jcc.540130812
39. Lev, B., B. Roux, and S.Y. Noskov. 2013. Relative free energies for hydration of monovalent ions from QM and QM/MM simulations. J. Chem. Theory Comput. 9:4165-4175. http://dx.doi.org/10.1021/ct400296w
40. Li, Y., O.S. Andersen, and B. Roux. 2010. Energetics of double-ion occupancy in the gramicidin A channel. J. Phys. Chem. B. 114:13881- 13888. http://dx.doi.org/10.1021/jp105820u
41. Light, P.E., C. Bladen, R.J. Winkfein, M.P. Walsh, and R.J. French. 2000. Molecular basis of protein kinase C-induced activation of ATP-sensitive potassium channels. Proc. Natl. Acad. Sci. USA. 97: 9058-9063. http://dx.doi.org/10.1073/pnas.160068997
42. MacKerell, A.D., D. Bashford, M. Bellott, R.L. Dunbrack, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
43. Margolskee, R.F., B. McHendry-Rinde, and R. Horn. 1993. Panning transfected cells for electrophysiological studies. Biotechniques. 15:906-911.
44. McCleskey, E.W., and W. Almers. 1985. The Ca channel in skeletal muscle is a large pore. Proc. Natl. Acad. Sci. USA. 82:7149-7153. http://dx.doi.org/10.1073/pnas.82.20.7149
45. McCusker, E.C., C. Bagnéris, C.E. Naylor, A.R. Cole, N. D'Avanzo, C.G. Nichols, and B.A. Wallace. 2012. Structure of a bacterial voltage- gated sodium channel pore reveals mechanisms of opening and closing. Nat Commun. 3:1102. http://dx.doi.org/10.1038/ncomms2077
46. Meech, R.W., and G.O. Mackie. 1993. Potassium channel family in giant motor axons of Aglantha digitale. J. Neurophysiol. 69:894-901.
47. Moczydlowski, E., S.S. Garber, and C. Miller. 1984. Batrachotoxinactivated Na+ channels in planar lipid bilayers. Competition of tetrodotoxin block by Na+. J. Gen. Physiol. 84:665-686. http://dx.doi.org/10.1085/jgp.84.5.665
48. + selectivity filter. Nature. 414:37-42. http://dx.doi.org/10.1038/35102000
49. Nonner, W., and B. Eisenberg. 1998. Ion permeation and glutamate residues linked by Poisson-Nernst-Planck theory in L-type calcium channels. Biophys. J. 75:1287-1305. http://dx.doi.org/10.1016/S0006-3495(98)74048-2
50. Nonner, W., D.P. Chen, and B. Eisenberg. 1998. Anomalous mole fraction effect, electrostatics, and binding in ionic channels. Biophys. J. 74:2327-2334. http://dx.doi.org/10.1016/S0006-3495(98)77942-1
51. Noskov, S.Y., and B. Roux. 2008. Control of ion selectivity in LeuT: two Na+ binding sites with two different mechanisms. J. Mol. Biol. 377:804-818. http://dx.doi.org/10.1016/j.jmb.2008.01.015
52. Noskov, S.Y., S. Bernèche, and B. Roux. 2004. Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands. Nature. 431:830-834. http://dx.doi.org/10.1038/nature02943
53. Patlak, C.S. 1960. Derivation of an equation for the diffusion potential. Nature. 188:944-945. http://dx.doi.org/10.1038/188944b0
54. Payandeh, J., T. Scheuer, N. Zheng, and W.A. Catterall. 2011. The crystal structure of a voltage-gated sodium channel. Nature. 475:353-358. http://dx.doi.org/10.1038/nature10238
55. Payandeh, J., T.M. Gamal El-Din, T. Scheuer, N. Zheng, and W.A. Catterall. 2012. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature. 486:135-139.
56. Rapaport, D.C. 2004. The art of Molecular Dynamics Simulation. Second edition. Cambridge University Press, Cambridge. 549 pp.
57. Ravindran, A., H. Kwiecinski, O. Alvarez, G. Eisenman, and E. Moczydlowski. 1992. Modeling ion permeation through batrachotoxin- modified Na+ channels from rat skeletal muscle with a multiion pore. Biophys. J. 61:494-508. http://dx.doi.org/10.1016/S0006-3495(92)81854-4
58. Ren, D., B. Navarro, H. Xu, L. Yue, Q. Shi, and D.E. Clapham. 2001. A prokaryotic voltage-gated sodium channel. Science. 294:2372- 2375. http://dx.doi.org/10.1126/science.1065635
59. Tang, S., G. Mikala, A. Bahinski, A. Yatani, G. Varadi, and A. Schwartz. 1993. Molecular localization of ion selectivity sites within the pore of a human L-type cardiac calcium channel. J. Biol. Chem. 268:13026-13029.
60. Thompson, A.N., I. Kim, T.D. Panosian, T.M. Iverson, T.W. Allen, and C.M. Nimigean. 2009. Mechanism of potassium-channel selectivity revealed by Na+ and Li+ binding sites within the KcsA pore. Nat. Struct. Mol. Biol. 16:1317-1324. http://dx.doi.org/10.1038/nsmb.1703
61. Treptow, W., and M.L. Klein. 2012. Computer simulations of voltage-gated cation channels. J. Phys. Chem. Lett. 3:1017-1023. http://dx.doi.org/10.1021/jz300089g
62. 2+ channels. Nature. 366:158-161. http://dx.doi.org/10.1038/366158a0
63. Yu, H.B., S.Y. Noskov, and B. Roux. 2010. Two mechanisms of ion selectivity in protein binding sites. Proc. Natl. Acad. Sci. USA. 107:20329-20334. http://dx.doi.org/10.1073/pnas.1007150107
64. 2+. J. Gen. Physiol. 95:911-939. http://dx.doi.org/10.1085/jgp.95.5.911
65. Yue, L., B. Navarro, D. Ren, A. Ramos, and D.E. Clapham. 2002. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 120:845-853. http://dx.doi.org/10.1085/jgp.20028699
66. Zhang, X., W. Ren, P. DeCaen, C. Yan, X. Tao, L. Tang, J. Wang, K. Hasegawa, T. Kumasaka, J. He, et al. 2012. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature. 486:130-134.