An Entropic Mechanism of Generating Selective Ion Binding in Macromolecules

PLoS Computational Biology

Volumn 9, Issue 2, 2013, Pages

  Thomas, Michael ^a   Jayatilaka, Dylan ^b   Corry, Ben ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; ION EXCHANGE; IONS;

CELL FUNCTIONS; COORDINATING LIGANDS; FLUCTUATION MECHANISMS; ION BINDING; ION CHANNEL; ION SELECTIVITY; ION TRANSPORTERS; LIGAND BINDING; MODELLING SYSTEMS; THERMAL FLUCTUATIONS;

LIGANDS;

AMINO ACID TRANSPORTER; ION CHANNEL; LITHIUM; POTASSIUM; POTASSIUM CHANNEL; SCAFFOLD PROTEIN; SODIUM;

ARTICLE; BINDING SITE; CELL FUNCTION; CHEMICAL PHENOMENA; CHEMICAL REACTION; CONCEPTUAL FRAMEWORK; CRYSTAL STRUCTURE; ENTROPY; ION SELECTIVITY; LIGAND BINDING; MACROMOLECULE; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PROTEIN BINDING; SIGNAL TRANSDUCTION; THERMAL ANALYSIS;

EID: 84874788248     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002914     Document Type: Article

References (51)

1. Hille B (2001) Ionic Channels of Excitable Membranes. 3rd edition. Massachusetts: Sinauer Associates Inc. 814 p.
2. Yellen G, (1984) Ionic permeation and blockade in Ca2+ activated K+ channels of bovine chromaffin cells. J Gen Physiol 84: 157-186.
3. Heginbotham L, MacKinnon R, (1993) Conduction properties of the cloned Shaker channel. Biophys J 65: 2089-2096.
4. LeMasurier M, Heginbotham L, Miller C, (2001) KscA: it's an ion channel. J Gen Physiol 118: 303-314.
5. Nimigean CM, Miller C, (2002) Na+ block and permeation in K+ channel of known structure. J Gen Physiol 120: 323-325.
6. Eisenman G, (1962) Cation selective glass electrodes and their mode of operation. Biophys J 2: 259-323.
7. Åqvist J, Alvarez O, Eisenman G, (1992) Ion-selective properties of a small ionophore in methanol studied by free energy perturbation simulations. J Phys Chem 96: 10019-10025.
8. Noskov S, Bernèche S, Roux B, (2004) Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands. Nature 431: 830-834.
9. Noskov S, Roux B, (2006) Ion selectivity in potassium channels. Biophys Chem 124: 279-291.
10. Yu H, Noskov S, Roux B, (2010) Two mechanisms of ion selectivity in protein binding sites. Proc Natl Acad Sci USA 107: 20329-20334.
11. Roux B, Bernèche S, Egwolf B, Lev B, Noskov S, et al. (2011) Ion selectivity in channels and transporters. J Gen Physiol 317: 415-426.
12. Thomas M, Jayatilaka D, Corry B, (2011) Mapping the importance of four factors in creating monovalent ion selectivity in biological molecules. Biophys J 100: 60-69.
13. Thomas M, Jayatilaka D, Corry B, (2007) The predominant role of coordination number in potassium channel selectivity. Biophys J 93: 2635-2643.
14. Varma S, Rempe S, (2007) Tuning ion coordination architectures to enable selective partitioning. Biophys J 93: 1093-1099.
15. Bostick DL, Brooks III CL, (2007) Selectivity in K+ channels is due to topological control of the permeant ion's coordinated state. Proc Natl Acad Sci USA 104: 9260-9265.
16. Fowler P, Tai K, Sansom M, (2008) The selectivity of K+ ion channels: Testing the hypotheses. Biophys J 95: 5062-5072.
17. Dixit PD, Merchant S, Asthagiri D, (2009) Ion selectivity in the KcsA potassium channel from the perspective of the ion binding site. Biophys J 96: 2138-2145.
18. Bostick DL, Arora K, Brooks III CL, (2009) K+/Na+ selectivity in toy cation binding site models is determined by the 'host'. Biophys J 96: 3887-3896.
19. Bostick DL, Arora K, Brooks III CL, (2009) Statistical determinants of selective ionic complexation: ions in solvent, transport proteins, and other "hosts". Biophys J 96: 4470-4492.
20. Dudev T, Lim C, (2009) Determinants of K+ vs Na+ selectivity in potassium channels. JACS 131: 8092-8101.
21. Yu H, Noskov S, Roux B, (2009) Hydration number, topological control, and ion selectivity. J Phys Chem 113: 8725-8730.
22. Bostick DL, Brooks CL III, (2010) Selective complexation of K+ and Na+ in simple polarizable ion-ligating systems. JACS 132: 13185-13187.
23. Varma S, Rogers D, Pratt L, Rempe S, (2011) Design principles for K+ selectivity in membrane transport. J Gen Physiol 137: 479-488.
24. Mullins LJ, (1959) The penetration of some cations into muscle. J Gen Physiol 42: 817-829.
25. Bezanilla F, Armstrong C, (1972) Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J Gen Physiol 60: 588-608.
26. Doyle D, Cabral JM, Pfuetzner R, Kuo A, Gulbis J, et al. (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280: 69-77.
27. Noskov S, Roux B, (2007) Importance of hydration and dynamics on the selectivity on the KcsA and NaK channels. J Gen Physiol 129: 135-143.
28. Lockless S, Zhou M, MacKinnon R, (2007) Structural and thermodynamic properties of selective ion binding in a K+ channel. Plos Biology 2: 1079-1088.
29. Mullins L, (1959) An analysis of conductance changes in squid axon. J Gen Physiol 42: 1013-1035.
30. Mullins L, (1960) An analysis of pore size in excitable membranes. J Gen Physiol 43: 105-117.
31. Rose M, Henkens R, (1974) Stability of sodium and potassium complexes of valinomycin. BBA 372: 426-435.
32. Mayers D, Urry D, (1971) Valinomycin-cation complex. Comformational energy aspects. J Am Chem Soc 94: 77-81.
33. Varma S, Sabo D, Rempe S, (2008) K+ and Na+ selectivity in K channels and valinomycin: over-coordination versus cavity-size constraints. J Mol Biol 376: 13-22.
34. Celik L, Schiøtt B, Tajkhorshid E, (2008) Substrate binding and formation of an occluded state in the leucine transporter. Biophys J 94: 1600-1612.
35. Corry B, Thomas M, (2012) Mechanism of ion permeation and selectivity in a voltage gated sodium channel. J Am Chem Soc 93: 1840-1846.
36. Vijayan R, Plested AJR, Mayer ML, Biggin PC, (2009) Selectivity and cooperativity of modulatory ions in a neurotransmitter recepter. Biophys J 96: 1751-1760.
37. Buddenhagen J, Kottwitz D (2001) Multiplicity and symmetry breaking in (conjectured) densest packings of congruent circles on a sphere. E-pub ahead of print. Available at http://home.earthlink.net/wjbuddenh/pack/sphere/intro.htm.
38. Joung IS, Cheatham TE III, (2008) Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J Phys Chem B 112: 9020-9041.
39. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comp Chem 26: 1781-1802.
40. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modelling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
41. Humphrey W, Dalke A, Schulten K, (1996) VMD - Visual Molecular Dynamics. Journal of Molecular Graphics 14: 33-38.
42. Boudker O, Ryan R, Yernool D, Shimamoto K, Gouaux E, (2007) Coupling substrate and ion binding to extracellular gate of a sodiumdependent aspartate transporter. Nature 445: 387-393.
43. Yamashita A, Singh S, Kawate T, Jin Y, Gouaux E, (2005) Crystal structure of a bacterial homologue of Na+/Cl--dependent neurotransmitter transporters. Nature 437: 215-223.
44. Noskov S, Roux B, (2008) Control of ion selectivity in LeuT: two Na+ binding sites with two different mechanisms. J Mol Biol 377: 804-818.
45. Hooey DC, Kavanaugh MP, (2009) Interactions of alkali cations with glutamate transporters. Phil Trans R Soc 364: 155-161.
46. Huang Z, Tajkhorshid E, (2010) Indentification of the third Na+ site and the sequence of extracellular binding events in the glutamate transporter. Biophys J 99: 1416-1425.
47. Larsson HP, Wang X, Lev B, Baconguis I, Caplan DA, et al. (2010) Evidence for a third sodium-binding site in glutamate transporters suggests an ion/substrate coupling model. Proc Natl Acad Sci USA 107: 13912-13917.
48. Thompson AN, Kim I, Panosian TD, Iverson TM, Allen TW, et al. (2009) Mechanism of potassium-channel selectivity revealed by Na+ and Li+ binding sites within the KcsA pore. Nat Struct Mol Biol 16: 1317-1324.
49. Nimigean C, Allen T, (2011) Origins of ion selectivity in potassium channels from the perspective of channel block. J Gen Physiol 137: 405-413.
50. Kim I, Allen TW, (2011) On the selective ion binding hypothesis for potassium channels. Proc Nat Acad Soc USA 108: 17963-17968.
51. Caplan D, Subbotina J, Noskov S, (2008) Molecular mechanism of ionion and ion-substrate coupling in the Na+ dependent leucine transporter leut. Biophys J 95: 4613-4621.