Artificial cation-conducting channels: Design, synthesis, and characterization

Cell Biochemistry and Biophysics

Volumn 35, Issue 3, 2001, Pages 211-231

  Gokel, George W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cation channel; Fluorescence; Ionophore; Membrane; Synthetic channel; Transport

Indexed keywords

CATION; ION CHANNEL; IONOPHORE; SODIUM;

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE MICROSCOPY; ION TRANSPORT; LIPID BILAYER; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATCH CLAMP; PROTEIN ENGINEERING; SYNTHESIS;

CATIONS; ION CHANNELS; ION TRANSPORT; IONOPHORES; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, FLUORESCENCE; MODELS, CHEMICAL; MODELS, MOLECULAR; PATCH-CLAMP TECHNIQUES; PROTEIN ENGINEERING; SODIUM;

EID: 0035757494     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:35:3:211     Document Type: Article

References (80)

1. Hille, B. (1992) Ionic Channels of Excitable Membranes, 2nd ed. Sunderland, MA, Sinauer.
2. Aidley, D. J. and Stanfield, P. R. (1996) Ion Channels: Molecules in Action. Cambridge, Cambridge University Press.
3. Miller, C. (2000) Ion channels: doing hard chemistry with hard ions. Curr. Opin. Chem. Biol. 4, 148-151.
4. + conduction and selectivity. Science 280, 69-77.
5. Chang, G., Spencer, R. H., Lee, A. T., Barclay, M. T., and Rees, D. C. (1998) Structure of the MscL homolog from mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282, 2220-2226.
6. Spencer, R. H., Chang, G., and Rees, D. C. (1999) Feeling the pressure: structural insights into a gated mechanosensitive channel. Curr. Opin. Struct. Biol. 9, 448-454.
7. Rees, D. C., Chang, G., and Spencer, R. H. (2000) Crystallographic analyses of ion channels: lessons and challenges. J. Biol. Chem. 275, 713-716.
8. Sato, C., Ueno, Y., Asai, K., Takahashi, K., Sato, M., Engel, A. et al. (2001) The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature 409, 1047-1051.
9. Reusch, R. N. and Sadoff, H. L. (1988) Putative structure and functions of a poly-I-hydroxybutyrate/calcium polyphosphate channel in bacterial plasma membranes. Proc. Natl. Acad. Sci. USA 85, 4176-4180.
10. 2+ channels in the plasma membranes of Escherichia coli. Biophys. J. 69, 754-766.
11. Das, S., Kurcok, P., Jedlinski, Z., and Reusch, R. N. (1999) Ion channels formed by biomimetic oligo-(R)-3-hydroxybutyrates and inorganic polyphosphates in planar lipid bilayers. Macromolecules 32, 8781-8785.
12. Reusch, R. N. (2000) Ion recognition and transport by poly-(R)-3-hydroxybutanoates and inorganic polyphosphates. Adv. Supramol. Chem. 7, 49.
13. Seebach, D., Brunner, A., Buerger, H. M., Reusch, R. N., and Bramble, L. L. (1996) Channel-forming activity of 3-hydroxybutanoic acid oligomers in planar lipid bilayers. Helv. Chim. Acta 79, 507-517.
14. Das, S., Lengweiler, U. D., Seebach, D., and Reusch, R. N. (1997) Proof for a non-proteinaceous calcium-selective channel in Escherichia coli by total synthesis for (R)-3-hydroxybutanoic acid and inorganic polyphosphate. Proc. Nat. Acad. Sci. (USA) 94, 9075-9079.
15. DeGrado, W. F., Wasserman, Z. R., and Lear, J. D. (1989) Protein design, a minimalist approach. Science 243, 622-628.
16. Lear, J. D., Wasserman, Z. R., and DeGrado, W. F. (1988) Synthetic amphiphilic peptide models for protein ion channels. Science 240, 1177-1181.
17. Åkerfeldt, K. S., Lear, J. D., Wasserman, Z. R., Chung, L. A., and DeGrado, W. F. (1993) Synthetic peptides as models for ion channel proteins. Acc. Chem. Res. 26, 191-197.
18. Dieckmann, G. R. and DeGrado, W. F. (1997) Modeling transmembrane helical oligomers. Curr. Opin. Struct. Biol. 7, 486-494.
19. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) The structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Angstrom resolution. Nature 318, 618-624.
20. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E., and Downing, K. H. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213, 899-929.
21. Ionov, R., El-Abed, A., Angelova, A., Goldmann, M., and Peretti, P. (2000) Asymmetrical ion-channel model inferred from two-dimensional crystallization of a peptide antibiotic. Biophys. J. 78, 3026-3035.
22. Harrison, R. and Lunt, G. G. (1980) Biological Membranes: Their Structure and Function, 2nd ed. Blackie & Son, London.
23. Yeagle, P. (1987) The Membranes of Cells. Academic, London.
24. Yeagle, P. (ed.) (1992) The Structure of Biological Membranes. CRC, Boca Raton, FL.
25. Merz, Jr., K. M. and Roux, B. (eds.) (1996) Biological Membranes: A Molecular Prespective from Computation to Experiment. Boston, Birkhäuser.
26. Abel, E., Fedders, M. F., and Gokel, G. W. (1995) Vesicle formation from N-alkylindoles: implications for tryptophan-water interactions. J. Am. Chem. Soc. 117, 1265-1270.
27. Abel, E., De Wall, S. L., Edwards, W. B., Lalitha, S., Covey, D. F., and Gokel, G. W. (2000) Aggregate formation from 3-alkylindoles: amphiphilic models for interfacial helix anchoring groups. Chem. Comm. 433-434.
28. Abel, E., De Wall, S. L., Edwards, W. B., Lalitha, S., Covey, D. F., and Gokel, G. W. (2000) The formation of stable vesicles from N- or 3-alkylindoles: possible evidence for tryptophan as a membrane anchor in proteins, J. Org. Chem. 65, 5901-5909.
29. Fleming, P. J., Koppel, D. E., Lau, A. L. Y., and Strittmatter, P. (1979) Intramembrane position of the fluorescent tryptophanyl residue in membrane-bound cytochrome b5. Biochemistry 18, 5458-5464.
30. Jain, M. K., Rogers, J., Simpson, L., and Gierasch, L. M. (1985) Effect of tryptophan derivatives on the phase properties of bilayers. Biochim. Biophys. Acta 816, 153-162.
31. Masotti, L., Cavatorta, P., Sartor, G., Casali, E., and Szabo, A. G. (1986) Tryptophan interactions of gramicidin A' channels in lipids: a time-resolved fluorescence study. Biochim. Biophys. Acta 862, 265-272.
32. Wimley, W. C. and White, S. H. (1992) Partitioning of tryptophan side-chain analogs between water and cyclohexane. Biochemistry 31, 12,813-12,818.
33. Schiffer, M., Chang, C.-H., and Stevens, F. J. (1992) The functions of tryptophan residues in membrane proteins. Protein Eng. 5, 213-214.
34. Hu, W., Lee, K.-C., and Cross, T. A. (1993) Tryptophans in membrane proteins: indole ring orientations and functional implications in the gramicidin channel. Biochemistry 32, 7035-7047.
35. Kachel, K., Ascuncion-Punzalan, E., and London, E. (1995) Anchoring of tryptophan and tyrosine analogs at the hydrocarbon-polar boundary in model membrane vesicles: parallax analysis of fluorescence quenching induced by nitroxide-labeled phospholipids. Biochemistry 34, 15,475-15,479.
36. Yau, W.-M., Wimley, W. C., Gawrisch, K., and While, S. H. (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37, 14,713-14,718.
37. Salom, D., Pérez-Payá, E., Pascal, J., and Abad, C. (1998) Environment- and sequence-dependent modulation of double-stranded to single-stranded conformational transition of gramicidin a in membranes. Biochemistry 37, 14,279-14,291.
38. DePlanque, M. R. R., Kruijtzer, J. A. W., Liskamp, R. M. J., Marsh, D., Greathouse, D. V., Koeppe II, R. E., et al. (1999) Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides. J. Biol. Chem. 274, 20,839-20,846.
39. Mons, M., Dimicoli, I., Tardivel, B., Piuzzi, F., Brenner, V., and Millié, P. (1999) Site dependence of the binding energy of water to indole: microscopic approach to the sidechain hydration of tryptophan. J. Phys. Chem. A 103, 9958.
40. De Wall, S. L., Meadows, E. S., Barbour, L. J., and Gokel, G. W. (1999) Solution and solid state evidence for alkali metal, cation-π interactions with indole, the sidechain of tryptophan. J. Am. Chem. Soc. 121, 5613-5614.
41. De Wall, S. L., Barbour, L. J., and Gokel, G. W. (1999) Cation-π complexation of potassium cation with the phenolic sidechain of tyrosine. J. Am. Chem. Soc. 121, 8405-8406.
42. De Wall, S. L., Meadows, E. S., Barbour, L. J., and Gokel, G. W. (2000) Synthetic receptors as models for alkali metal cation-π binding sites in proteins. Proc. Natl. Acad. Sci. USA 97, 6271-6276.
43. Meadows, E. S., De Wall, S. L., Barbour, L. J., and Gokel, G. W. (2001) Alkali metal cation-π interactions observed by using a lariat ether model system. J. Am. Chem. Soc. 123, 3092-3107.
44. Gokel, G. W. (1991) Complexation by crowns and cryptands, In Crown Ethers and Cryptands, J. F. Stoddart (ed.). Monographs in Supramolecular Chemistry, Vol. 3. London, The Royal Society of Chemistry.
45. Kuwamura, T. and Kawachi, T. (1979) Surface active crown ethers. I. Macrocyclic polyethers of acetal type with long alkyl chain. Yukagaku, 195-198 (Chem. Abstr. 90, 206, 248)
46. Kuwamura, T. and Kawachi, T. (1979) Surface active crown ethers. I. Macrocyclic polyethers of acetal type with long alkyl chain. Yukagaku, 195-198 (Chem. Abstr. 90, 206, 248)
47. Kuwamura, T., Akimaru, M., Takahashi, H. L., and Arai, M. (1979) Studies on the properties and application of nonionic surface active substances with multi-chain alkyl and alicyclic groups as a hydrophobic part. Kenkyu Hokoku-Asahi Garasu Kogyo Gijutsu Shorekai 35, 45 (Chem. Abstr. 95, 61,394q).
48. Kuwamura, T., Akimaru, M., Takahashi, H. L., and Arai, M. (1979) Studies on the properties and application of nonionic surface active substances with multi-chain alkyl and alicyclic groups as a hydrophobic part. Kenkyu Hokoku-Asahi Garasu Kogyo Gijutsu Shorekai 35, 45 (Chem. Abstr. 95, 61,394q).
49. Kuwamura, T. and Yoshida, S. (1980) Surface-active crown ethers. 2. Synthesis, surfactant properties, and catalytic action of macrocyclic polyethers possessing a 4-alkyl-1,3,5-triazine subunit. Nippon Kagaku Kaishi 427-434 (Chem. Abstr. 93, 28,168e).
50. Kuwamura, T. and Yoshida, S. (1980) Surface-active crown ethers. 2. Synthesis, surfactant properties, and catalytic action of macrocyclic polyethers possessing a 4-alkyl-1,3,5-triazine subunit. Nippon Kagaku Kaishi 427-434 (Chem. Abstr. 93, 28,168e).
51. Okahara, M., Kuo, P. L., Yamamura, S., and Ikeda, I. (1980) Effect of metal salts on the cloud point of alkyl crown compounds, J. Chem. Soc., Chem. Commun. 586-588.
52. Ikeda, I., Iwaisako, K., Nakatsuji, Y., and Okahara, M. (1986) Surface active properties of long chain alkoxymethyl hydroxy crown ethers. Yukagaku 35, 1001 (Chem. Abstr. 106, 86,714).
53. Ikeda, I., Iwaisako, K., Nakatsuji, Y., and Okahara, M. (1986) Surface active properties of long chain alkoxymethyl hydroxy crown ethers. Yukagaku 35, 1001 (Chem. Abstr. 106, 86,714).
54. Echegoyen, L. E., Hernandez, J. C., Kaifer, A., Gokel, G. W., and Echegoyen, L. (1988) Aggregation of steroidal lariat ethers: the first example of nonionic liposomes (niosomes) formed from neutral crown ether compounds. J. Chem. Soc. Chem. Commun. 836-837.
55. De Wall, S. L., Wang, K., Berger, D. L., Watanabe, S., Hernandez, J. C., and Gokel, G. W. (1997) Azacrown ethers as amphiphile head-groups: formation of stable aggregates from two- and three-armed lariat ethers, J. Org. Chem. 62, 6784-6791.
56. De Wall, S. L., Barbour, L. J., and Gokel, G. W. (2001) Solid state bilayer formation from a dialkyl-substituted lariat ether that forms stable vesicles in aqueous suspension. J. Phys. Org. Chem. 14, 383-391.
57. Kano, K. and Fendler, J. H. (1978) Pyranine as a sensitive pH probe for liposome interactions and surfaces. pH gradients across phospholipid vesicles. Biochim. Biophys. Acta 509, 289-299.
58. 23Na-NMR spectroscopy. Biochem. Biophys. Acta 817, 313-317.
59. Riddell, F. G., Arumugam, S., and Cox, B. G. (1987) Ion transport through phospholipid bilayers studied by magnetization transfer; membrane transport of lithium mediated by monensin. J. Chem. Soc. Chem. Commun. 1890-1891.
60. 39K NMR spectroscopy. J. Am. Chem. Soc. 110, 734-738.
61. 7Li-NMR spectroscopy. Biochim. Biophys. Acta 945, 65-72.
62. 39K-NMR. Biochim. Biophys. Acta 984, 6-10.
63. 39K-NMR spectroscopy. Biochim. Biophys. Acta 990, 193-197.
64. Mronga, S., Mueller, G., Fischer, J., and Riddell, F. (1993) A model for ion transport across membranes: solution structure of the ionophore metal complex salinomycin-Na determined by NMR and molecular dynamics calculations. J. Am. Chem. Soc. 115, 8414-8420.
65. - transport through model biological membranes. J. Inorg. Biochem. 55, 279-293.
66. Riddell, F. G. and Zhou, Z. (1994) NMR study of ion transport through phospholipid bilayers mediated by the ionophoric antibiotic septamycin. Proc. Indian Acad. Sci. Chem. Sci. 106, 1505-1514.
67. - in human erythrocytes. Magn. Reson. Chem. 33, 66-69.
68. Riddell, F. G. (1998) Studying biological lithium using nuclear magnetic resonance techniques. J. Trace Microprobe Tech. 16, 99-110.
69. Murillo, O., Suzuki, I., Abel, E., and Gokel, G. W. (1996) Synthetic, cation-conducting channels obey the Hammett relationship in a phospholipid bilayer membrane. J. Am. Chem. Soc. 118, 7628-7629.
70. Gustowski, D. A., Gatto, V. J., Mallen, J., Echegoyen, L., and Gokel, G. W. (1987) Direct correlation of cation binding strengths to Hammett parameters in substituted N-benzylaza-15-crown-5 lariat ether and N,N′-dibenzyl-4,13-diaza-18-crown-6 BiBLE derivatives. J. Org. Chem. 52, 5172-5176.
71. Reichardt, C. (1994) Solvatochromic dyes as solvent polarity indicators. Chem. Rev. 94, 2319-2358.
72. Abel, E., Maguire, G. E. M., Murillo, O., Suzuki, I., and Gokel, G. W. (1999) Hydraphile channels: structural and fluorescent probes of position and function in a phospholipid bilayer. J. Am. Chem. Soc. 121, 9043-9052.
73. Reichardt, C. (1979) Solvent Effects in Organic Chemistry. Weinheim, Verlag Chemie, p. 272.
74. Murillo, O., Abel, E., Maguire, G. E. M., and Gokel, G. W. (1996) A tris(macrocycle) that exhibits H-bond-induced blockage of cation channel function in a phospholipid bilayer. J. Chem. Soc. Chem. Commun. 2147-2148.
75. Kachel, K., Ascuncion-Punzalan, E., and London, E. (1995) Anchoring of tryptophan and tyrosine analogs at the hydrocarbon-polar boundary in model membrane vesicles: parallax analysis of fluorescence quenching induced by nitroxide-labeled phospholipids. Biochemistry 34, 15,475-15,479.
76. Abel, E., Maguire, G. E. M., Meadows, E. S., Murillo, O., Jin, T., and Gokel, G. W., (1997) Planar bilayer conductance and fluorescent studies confirm the function and location of a synthetic sodium-ion-conducting channel in a phospholipid bilayer membrane. J. Am. Chem. Soc. 119, 9061-9062.
77. Abel, E., Meadows, E. S., Suzuki, I., Jin, T., and Gokel, G. W. (1997) Unusually long open times, determined by planar bilayer conductance studies, for a synthetic tris (macrocycle) that functions as a transmembrane channel in a phospholipid bilayer. J. Chem. Soc., Chem. Commun. 1145-1146.
78. Parsegian, A. (1969) Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature 221, 844-846.
79. + channel: electrostatic stabilization of monovalent cations. Science 285, 100-102.
80. Murray, C. L., Shabany, H., and Gokel, G. W. (2000) The central "relay" unit in hydraphile channels as a model for the water-and-ion capsule of channel proteins. J. Chem. Soc. Chem. Comm. 2371-2372.