Engineering light-gated ion channels

Biochemistry

Volumn 45, Issue 51, 2006, Pages 15129-15141

  Banghart, Matthew R ^a   Volgraf, Matthew ^a   Trauner, Dirk ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGHT GATED ION CHANNELS; MEMBRANE TENSION; NICOTINIC ACETYLCHOLINE RECEPTORS; VOLTAGE GATED POTASSIUM CHANNEL;

LIGHT PROPAGATION; LIGHT TRANSMISSION; MEDICINE; OPTICAL PROPERTIES; POSITIVE IONS; POTASSIUM;

MOLECULAR BIOLOGY;

ALPHA HEMOLYSIN; CATION CHANNEL; GRAMICIDIN A; HEMOLYSIN; ION CHANNEL; IONOTROPIC RECEPTOR; LIGAND; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO TERMINAL SEQUENCE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DIMERIZATION; HYDROPHOBICITY; ISOMERIZATION; LIGAND BINDING; LIGHT; MEMBRANE; MEMBRANE CONDUCTANCE; MEMBRANE DEPOLARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; REVIEW; STIMULUS; TEMPERATURE; TENSION;

ANIMALS; HUMANS; ION CHANNEL GATING; ION CHANNELS; LIGHT; PROTEIN ENGINEERING;

EID: 33845921612     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0618058     Document Type: Review

References (85)

1. Goeldner, M., and Givens, R. (2005) Dynamic Studies in Biology, Wiley-VCH, Weinheim, Germany.
2. Anzai, J., and Osa, T. (1994) Photosensitive artificial membranes based on azobenzene and spiropyran derivatives, Tetrahedron 50, 4039-4070.
3. Folgering, J. H., Kuiper, J. M., de Vries, A. H., Engberts, J. B., and Poolman, B. (2004) Lipid-mediated light activation of a mechanosensitive channel of large conductance, Langmuir 20, 6985-6987.
4. Rau, H. (1990) Azo Compounds, in Photochromism: Molecules and Systems (Duerr, H., and Bouas-Laurent, H., Eds.) pp 165-192, Elsevier, Amsterdam, The Netherlands.
5. Guglielmetti, R. (1990) 4n+2 Systems: Spiropyrans, in Photochromism: Molecules and Systems (Duerr, H., and Bouas-Laurent, H., Eds.) pp 314-466, Elsevier, Amsterdam, The Netherlands.
6. Siebert, F. (1990) Retinal Proteins, in Photochromism: Molecules and Systems (Duerr, H., and Bouas-Laurent, H., Eds.) pp 756-792, Elsevier, Amsterdam, The Netherlands.
7. Zimmerman, G., Chow, L. Y., and Paik, U. J. (1958) The photochemical isomerization of azobenzene, J. Am. Chem. Soc. 80, 3528-3531.
8. Lester, H. A., Krouse, M. E., Nass, M. M., Wassermann, N. H., and Erlanger, B. F. (1980) A covalently bound photoisomerizable agonist. Comparison with reversibly bound agonists at Electrophorus electroplaques, J. Gen. Physiol. 75, 207-232.
9. Brejc, K., van Dijk, W. J., Klaassen, R. V., Schuurmans, M., van der Oost, J., Smit, A. B., and Sixma, L. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors, Nature 411, 269-276.
10. Celie, P. H. N., Van Rossum-Fikkert, S. E., Van, Dijk, W. J., Brejc, K., Smit, A. B., and Sixma, T. K. (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures, Neuron 41, 907-914.
11. Hansen, S. B., Sulzenbacher, G., Huxford, T., Marchot, P., Taylor, P., and Bourne, Y. (2005) Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations, EMBO J. 24, 3635-3646.
12. Cashin, A. L., Petersson, E. J., Lester, H. A., and Dougherty, D. A. (2004) Using physical chemistry to differentiate nicotinic from cholinergic agonists at the nicotinic acetylcholine receptor, J. Am. Chem. Soc. 127, 350-356.
13. Bartels, E., Wasserman, N. H., and Erlanger, B. F. (1971) Photochromic activators of the acetylcholine receptor, Proc. Natl. Acad. Sci. U.S.A. 68, 1820-1823.
14. Lester, H. A., and Chang, H. W. (1977) Response of acetylcholine receptors to rapid photochemically produced increases in agonist concentration, Nature 266, 373-374.
15. Karlin, A., and Winnik, M. (1968) Reduction and specific alkylation of the receptor for acetylcholine, Proc. Natl. Acad. Sci. U.S.A. 60, 668-674.
16. Silman, I., and Karlin, A. (1969) Acetylcholine receptor: covalent attachment of depolarizing groups at the active site, Science 164, 1420-1421.
17. Chabala, L. D., and Lester, H. A. (1986) Activation of acetylcholine receptor channels by covalently bound agonists in cultured rat myoballs, J. Physiol. 379, 83-108.
18. Woolley, G. A., and Wallace, B. A. (1992) Model ion channels: gramicidin and alamethicin, J. Membr. Biol. 129, 109-136.
19. Stankovic, C. J., Heinemann, S. H., and Schreiber, S. L. (1991) Photo-modulated ion channels based on covalently linked gramicidins, Biochim. Biophys. Acta 1061, 163-170.
20. Stankovic, C. J., Heinemann, S. H., Delphino, J. M., Sigworth, F. J., and Schreiber, S. L. (1989) Transmembrane channels based on tartaric acid-gramicidin A hybrids, Science 244, 813-817.
21. Stankovic, C. J., Heinemann, S. H., and Schreiber, S. L. (1990) Immobilizing the gate of a tartaric acid-gramicidin A hybrid channel molecule by rational design, J. Am. Chem. Soc. 112, 3702-3704.
22. Sukhanov, S. V., Ivanov, B. B., Orekhov, S. Y., Barsukov, L. I., and Arseniev, A. S. (1994) Molecular design of photo-modulated ion channels based on gramicidin A and their electrochemical properties, Biol. Membr. 7, 519-526.
23. Woolley, G. A., Jaikaran, A. S. I., Zhang, Z., and Peng, S. (1995) Design of regulated ion channels using measurements of cis-trans isomerization in single molecules, J. Am. Chem. Soc. 117, 4448-4454.
24. Lien, L., Jaikaran, D. C. J., Zhang, Z., and Woolley, G. A. (1996) Photomodulated blocking of gramicidin ion channels, J. Am. Chem. Soc. 118, 12222-12223.
25. Chung, S. H., Allen, T. W., Hoyles, M., and Kuyucak, S. (1999) Permeation of ions across the potassium channel: brownian dynamics studies, Biophys. J. 77, 2517-2533.
26. Roux, B., and MacKinnon, R. (1999) The cavity and pore helices in the KcsA K+ channel: electrostatic stabilization of monovalent cations, Science 285, 100-102.
27. Russell, E. W., Weiss, L. B., Navetta, F. I., Koeppe, R. E., II, and Andersen, O. S. (1986) Single-channel studies on linear gramicidins with altered amino acid side chains. Effects of altering the polarity of the side chain at position 1 in gramicidin A, Biophys. J. 49, 673-686.
28. Borisenko, V., Burns, D. C., Zhang, Z., and Woolley, G. A. (2000) Optical switching of ion-dipole interactions in a gramicidin channel analogue, J. Am. Chem. Soc. 122, 6364-6370.
29. Lougheed, T., Borisenko, V., Hennig, T., Rueck-Braun, K., and Woolley, G. A. (2004) Photomodulation of ionic current through hemithioindigo-modified gramicidin channels, Org. Biomol. Chem. 2, 2798-2801.
30. Anrather, D., Smetazko, M., Saba, M., Alguel, Y., and Schalkhammer, T. (2004) Supported membrane nanodevices, J. Nanosci. Nanotechnol. 4, 1-22.
31. Banghart, M., Borges, K., Isacoff, E., Trauner, D., and Kramer, R. H. (2004) Light-activated ion channels for remote control of neuronal firing, Nat. Neurosci. 7, 1381-1386.
32. Yu, F. H., Yarov-Yarovoy, V., Gutman, G. A., and Catterall, W. A. (2005) Overview of molecular relationships in the voltage-gated ion channel superfamily, Pharmacol. Rev. 57, 387-395.
33. Doyle, D. A., Cabral, J. M., Pfuetzner, R. A., Kuo, A., Gulbis, J. M., Cohen, S. L., Chait, B. T., and MacKinnon, R. (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity, Science 280, 69-77.
34. Long, S. B., Campbell, E. B., and MacKinnon, R. (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel, Science 309, 897-903.
35. Webster, S. M., Del Camino, D., Dekker, J. P., and Yellen, G. (2004) Intracellular gate opening in Shaker K+ channels defined by high-affinity metal bridges, Nature 428, 864-868.
36. Blaustein, R. O., Cole, P. A., Williams, C., and Miller, C. (2000) Tethered blockers as molecular "tape measures" for a voltage-gated K+ channel, Nat. Struct. Biol. 7, 309-311.
37. Hoshi, T., Zagotta, W. N., and Aldrich, R. W. (1990) Biophysical and molecular mechanisms of Shaker potassium channel inactivation, Science 250, 533-538.
38. Lopez-Barneo, J., Hoshi, T., Heinemann, S. H., and Aldrich, R. W. (1993) Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels, Recept. Channels 1, 61-71.
39. Lopez, G. A., Jan, Y. N., and Jan, L. Y. (1991) Hydrophobic substitution mutations in the S4 sequence alter voltage-dependent gating in Shaker potassium channels, Neuron 7, 327-336.
40. Johns, D. C., Marx, R., Mains, R. E., O'Rourke, B., and Marban, E. (1999) Inducible genetic suppression of neuronal excitability, J. Neurosci. 19, 1691-1697.
41. Nitabach, M. N., Blau, J., and Holmes, T. C. (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock, Cell 109, 485-495.
42. Fortin, D. L., Banghart, M. R., Karakossian, M., Dunn, T. W., Otis, T. S., Trauner, D., and Kramer, R. H., unpublished data.
43. Heginbotham, L., Lu, Z., Abramson, T., and MacKinnon, R. (1994) Mutations in the K+ channel signature sequence, Biophys. J. 66, 1061-1067.
44. Chambers, J. J., Banghart, M. R., Trauner, D., and Kramer, R. H. (2006) Light-induced depolarization of neurons using a modified Shaker K+ channel and a molecular photoswitch, J. Neurophysiol. 96, 2792-2796.
45. Volgraf, M., Gorostiza, P., Numano, R., Kramer, R. H., Isacoff, E. Y., and Trauner, D. (2006) Allosteric control of an ionotropic glutamate receptor with an optical switch, Nat. Chem. Biol. 2, 47-52.
46. Mayer, M. L. (2006) Glutamate receptors at atomic resolution, Nature 440, 456-462.
47. Armstrong, N., and Gouaux, E. (2000) Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core, Neuron 28, 165-181.
48. Mayer, M. L. (2005) Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity, Neuron 45, 539-552.
49. Jin, R. S., Banke, T. G., Mayer, M. L., Traynelis, S. F., and Gouaux, E. (2003) Structural basis for partial agonist action at ionotropic glutamate receptors, Nat. Neurosci. 6, 803-810.
50. Szobota, S., Gorostiza, P., Volgraf, M., Fortin, D., Tulyathan, O., Kolstad, K., Numano, R., Aaron, H., Ruzin, S., Flannery, J., Kramer, R., Trauner, D., and Isacoff, E., unpublished data.
51. Loudwig, S., and Bayley, H. (2006) Photoisomerization of an individual azobenzene molecule in water: an on-off switch triggered by light at a fixed wavelength, J. Am. Chem. Soc. 128, 2404-2405.
52. Song, L. Z., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore, Science 274, 1859-1866.
53. Kasianowicz, J. J., Brandin, E., Branton, D., and Deamer, D. W. (1996) Characterization of individual polynucleotide molecules using a membrane channel, Proc. Natl. Acad. Sci. U.S.A. 93, 13770-13773.
54. Chang, C. Y., Niblack, B., Walker, B., and Bayley, H. (1995) A photogenerated pore-forming protein, Chem. Biol. 2, 391-400.
55. Bayley, H., and Cremer, P. S. (2001) Stochastic sensors inspired by biology, Nature 413, 226-230.
56. Braha, O., Gu, L. Q., Zhou, L., Lu, X. F., Cheley, S., and Bayley, H. (2000) Simultaneous stochastic sensing of divalent metal ions, Nat. Biotechnol. 18, 1005-1007.
57. Astier, Y., Braha, O., and Bayley, H. (2006) Toward single molecule DNA sequencing: Direct identification of ribonucleoside and deoxyribonucleoside 5′-monophosphates by using an engineered protein nanopore equipped with a molecular adapter, J. Am. Chem. Soc. 128, 1705-1720.
58. Guan, X. Y., Gu, L. Q., Cheley, S., Braha, O., and Bayley, H. (2005) Stochastic sensing of TNT with a genetically engineered pore, ChemBioChem 6, 1875-1881.
59. Luchian, T., Shin, S. H., and Bayley, H. (2003) Kinetics of a three-step reaction observed at the single-molecule level, Angew. Chem., Int. Ed. 42, 1925-1929.
60. Kocer, A., Walko, M., Meijberg, W., and Feringa, B. L. (2005) A light-actuated nanovalve derived from a channel protein, Science 309, 755-758.
61. Perozo, E., and Rees, D. C. (2003) Structure and mechanism in prokaryotic mechanosensitive channels, Curr. Opin. Struct. Biol. 13, 432-442.
62. Cruickshank, C. C., Minchin, R. F., LeDain, A. C., and Martinac, B. (1997) Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli, Biophys. J. 73, 1925-1931.
63. Ajouz, B., Berrier, C., Garrigues, A., Besnard, M., and Ghazi, E. (1998) Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells, J. Biol. Chem. 273, 26670-26674.
64. Yoshimura, K., Batiza, A., Schroeder, M., Blount, P., and Kung, C. (1999) Hydrophilicity of a single residue within MscL correlates with increased channel mechanosensitivity, Biophys. J. 77, 1960-1972.
65. Yoshimura, K., Batiza, A., and Kung, C. (2001) Chemically charging the pore constriction opens the mechanosensitive channel MscL, Biophys. J. 80, 2198-2206.
66. Anishkin, A., Chiang, C. S., and Sukharev, S. (2005) Gain-of-function mutations reveal expanded intermediate states and a sequential action of two gates in MscL, J. Gen. Physiol. 125, 155-170.
67. Kocer, A., Walko, M., Bulten, E., Halza, E., Feringa, B. L., and Meijberg, W. (2006) Rationally designed chemical modulators convert a bacterial channel protein into a pH-sensory valve, Angew. Chem., Int. Ed. 45, 3126-3130.
68. Astier, Y., Bayley, H., and Howorka, S. (2005) Protein components for nanodevices, Curr. Opin. Chem. Biol. 9, 576-584.
69. Harz, H., Nonnengasser, C., and Hegemann, P. (1992) The photoreceptor current of the green-alga Chlamydomonas, Philos. Trans. R. Soc. London, Ser. B 338, 39-52.
70. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Mustl, A. M., Bamberg, E., and Hegemann, P. (2002) Channelrhodopsin-1: a light-gated proton channel in green algae, Science 296, 2395-2398.
71. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel, Proc. Natl. Acad. Sci. U.S.A. 100, 13940-13945.
72. Nagel, G., Szellas, T., Kateriya, S., Adeishvili, N., Hegemann, P., and Bamberg, E. (2005) Channelrhodopsins: directly light-gated cation channels, Biochem. Soc. Trans. 33, 863-866.
73. Suzuki, T., Yamasaki, K., Fujita, S., Oda, K., Iseki, M., Yoshida, K., Watanabe, M., Daiyasu, H., Toh, H., Asamizu, E., Tabata, S., Miura, K., Fukuzawa, H., Nakamura, S., and Takahashi, T. (2003) Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization, Biochem. Biophys. Res. Commun. 301, 711-717.
74. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005) Millisecond-timescale, genetically targeted optical control of neural activity, Nat. Neurosci. 8, 1263-1268.
75. Ishizuka, T., Kakuda, M., Araki, R., and Yawo, H. (2006) Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels, Neurosci. Res. 54, 85-94.
76. Nagel, G., Brauner, M., Liewald, J. F., Adeishvili, N., Bamberg, E., and Gottschalk, A. (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses, Curr. Biol. 15, 2279-2284.
77. Li, X., Gutierrez, D. V., Hanson, M. G., Han, J., Mark, M. D., Chiel, H., Hegemann, P., Landmesser, L. T., and Herlitze, S. (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin, Proc. Natl. Acad. Sci. U.S.A. 102, 17816-17821.
78. Bi, A. D., Cui, J. J., Ma, Y. P., Olshevskaya, E., Pu, M. L., Dizhoor, A. M., and Pan, Z. H. (2006) Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration, Neuron 50, 23-33.
79. Briggs, W., and Spudich, J. (2005) Handbook of Photosensory Receptors, Wiley-VCH, Weinheim, Germany.
80. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 angstrom resolution, J. Mol. Biol. 291, 899-911.
81. Luecke, H., Schobert, B., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction, Science 293, 1499-1503.
82. Kolbe, M., Besir, H., Essen, L. O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 angstrom resolution, Science 288, 1390-1396.
83. Singh, A. K., and Hota, P. K. (2006) Development of bacteriorhodopsin analogues and studies of charge separated excited states in the photoprocesses of linear polyenes, Photochem. Photobiol., in press.
84. Zhang, F., Wang, L. P., Boyden, E. S., and Deisselroth, K. (2006) Channelrhodopsin-2 and optical control of excitable cells, Nat. Methods 3, 785-792.
85. Prescher, J. A., and Bertozzi, C. R. (2005) Chemistry in living systems, Nat. Chem. Biol. 1, 13-21.