Chemically reactive derivatives of gramicidin A for developing ion channel-based nanoprobes

Bioconjugate Chemistry

Volumn 19, Issue 8, 2008, Pages 1614-1624

  Blake, Steven ^a   Capone, Ricardo ^a   Mayer, Michael ^a   Yang, Jerry ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CYCLOADDITION; IONS; LIPID BILAYERS; MOLECULES;

AMIDATION; BUILDING BLOCKES; CHANNEL FORMING; CHEMICAL AND PHYSICAL PROPERTIES; CLICK REACTION; GRAMICIDIN A; ION CHANNEL; SIMPLE++; SYNTHETIC METHODS; SYNTHETIC ROUTES;

PEPTIDES;

2 AMINOETHYL GRAMICIDATE; DESETHANOLAMINE GRAMICIDIN A; GRAMICIDAMINE; GRAMICIDAZIDE; GRAMICIDIN A; GRAMICIDIN DERIVATIVE; ION CHANNEL; UNCLASSIFIED DRUG;

AMIDATION; ARTICLE; CHEMICAL STRUCTURE; CONDUCTANCE; CYCLOADDITION; LIGAND BINDING; LIPID BILAYER; NANOPROBE; SYNTHESIS;

EID: 50249120156     PISSN: 10431802     EISSN: None     Source Type: Journal    
DOI: 10.1021/bc800180z     Document Type: Article

References (101)

1. Antonenko, Y. N., Borisenko, V., Melik-Nubarov, N. S., Kotova, E. A., and Woolley, G. A. (2002) Polyanions decelerate the kinetics of positively charged gramicidin channels as shown by sensitized photoinactivation. Biophys. J. 82, 1308-1318.
2. Apell, H. J., Bamberg, E., and Alpes, H. (1979) Dicarboxylic-acid analogs of Gramicidin-A - dimerization kinetics and single channel properties. J. Membr. Biol. 50, 271-285.
3. Apell, H. J., Bamberg, E., Alpes, H., and Lauger, P. (1977) Formation of ion channels by a negatively charged analog of Gramicidin-A. J. Membr. Biol. 31, 171-188.
4. Apell, H. J., Bamberg, E., and Lauger, P. (1979) Effects of surface-charge on the conductance of the gramicidin channel. Biochim. Biophys. Acta 552, 369-378.
5. Bayley, H. (2007) Understanding and manipulating channels and pores. Mol. BioSyst. 3, 645-647.
6. Bayley, H., and Cremer, P. S. (2001) Stochastic sensors inspired by biology. Nature 413, 226-230.
7. Bayley, H., and Jayasinghe, L. (2004) Functional engineered channels and pores. Mol. Membr. Biol. 21, 209-220.
8. Bayley, H., Jayasinghe, L., and Wallace, M. (2005) Prepore for a breakthrough. Nat. Struct. Biol. 12, 385-386.
9. Blake, S., Mayer, T., Mayer, M., and Yang, J. (2006) Monitoring chemical reactions by using ion-channel-forming peptides. ChemBioChem 7, 433-435.
10. Capone, R., Blake, S., Rincon Restrepo, M., Yang, J., and Mayer, M. (2007) Designing nanosensors based on charged derivatives of Gramicidin A. J. Am. Chem. Soc. 129, 9737-9745.
11. Cornell, B. A., Braach-Maksvytis, V. L. B., King, L. G., Osman, P. D. J., Raguse, B., Wieczorek, L., and Pace, R. J. (1997) A biosensor that uses ion-channel switches. Nature 387, 580-583.
12. Futaki, S., Zhang, Y. J., Kiwada, T., Nakase, I., Yagami, T., Oiki, S., and Sugiura, Y. (2004) Gramicidin-based channel systems for the detection of protein-ligand interactions. Bioorg. Med. Chem. 12, 1343-1350.
13. Matile, S., Sakai, N., Mareda, J., Kumaki, J., and Yashima, E. (2006) Minireview - Sensing, threading, orienting, and cutting polymers with rigid-rod pores. J. Recept. Signal Transduct. Res. 26, 461-472.
14. Ashkenasy, N., Sanchez-Quesada, J., Bayley, H., and Ghadiri, M. R. (2005) Recognizing a single base in an individual DNA strand: A step toward DNA sequencing in nanopores. Angew. Chem., Int. Ed. 44, 1401-1404.
15. Banghart, M. R., Volgraf, M., and Trauner, D. (2006) Engineering light-gated ion channels. Biochemistry 45, 15129-15141.
16. Gokel, G. W., Schlesinger, P. H., Djedovic, N. K., Ferdani, R., Harder, E. C., Hu, J. X., Leevy, W. M., Pajewska, J., Pajewski, R., and Weber, M. E. (2004) Functional, synthetic organic chemical models of cellular ion channels. Bioorg. Med. Chem. 12, 1291-1304.
17. Hirano, A., Wakabayashi, M., Matsuno, Y., and Sugawara, M. (2003) A single-channel sensor based on gramicidin controlled by molecular recognition at bilayer lipid membranes containing receptor. Biosens. Bioelectron. 18, 973-983.
18. Schoen, P., Degefa, T. H., Asaftei, S., Meyer, W., and Walder, L. (2005) Charge propagation in ion channel sensors based on protein-modified electrodes and redox marker ions. J. Am. Chem. Soc. 127, 11486-11496.
19. Terrettaz, S., Mayer, M., and Vogel, H. (2003) Highly electrically insulating tethered lipid bilayers for probing the function of ion channel proteins. Langmuir 19, 5567-5569.
20. Borisenko, V., Burns, D. C., Zhang, Z. H., and Woolley, G. A. (2000) Optical switching of ion-dipole interactions in a gramicidin channel analogue. J. Am. Chem. Soc. 122, 6364-6370.
21. 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.
22. 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.
23. Trauner, D. (2003) Potassium channels: symmetric, selective, and sensitive. Angew. Chem., Int. Ed. 42, 5671-5675.
24. Aidley, D. J., Stanfield, P. R. (1996) Ion Channels: Molecules in Action, Cambridge University Press, Cambridge.
25. Bamberg, E., Alpes, H., Apell, H. J., Bradley, R., Harter, B., Quelle, M. J., and Urry, D. W. (1979) Formation of ionic channels in black lipid-membranes by succinic derivatives of Gramicidin-A. J. Membr. Biol. 50, 257-270.
26. Bamberg, E., Apell, H. J., Alpes, H., Gross, E., Morell, J. L., Harbaugh, J. F., Janko, K., and Lauger, P. (1978) Ion channels formed by chemical analogs of Gramicidin-A. Fed. Proc. 37, 2633-2638.
27. Bamberg, E., and Lauger, P. (1973) Channel formation kinetics of Gramicidin-A in lipid bilayer membranes. J. Membr. Biol. 11, 177-194.
28. Bamberg, E., and Lauger, P. (1974) Temperature-dependent properties of Gramicidin-A channels. Biochim. Biophys. Acta 367, 127-133.
29. Bamberg, E., and Lauger, P. (1977) Blocking of gramicidin channel by divalent-cations. J. Membr. Biol. 35, 351-375.
30. Bamberg, E., Noda, K., Gross, E., and Lauger, P. (1976) Single-channel parameters of Gramicidin-A, Gramicidin-B and Gramicidin-C. Biochim. Biophys. Acta 419, 223-228.
31. Rostovtseva, T. K., Aguilella, V. M., Vodyanoy, I., Bezrukov, S. M., and Parsegian, V. A. (1998) Membrane surface-charge titration probed by gramicidin A channel conductance. Biophys. J. 75, 1783-1792.
32. Rostovtseva, T. K., Petrache, H. I., Kazemi, N., Hassanzadeh, E., and Bezrukov, S. M. (2008) Interfacial polar interactions affect gramicidin channel kinetics. Biophys. J. 94, L23-L25.
33. Bamberg, E., and Benz, R. (1976) Voltage-induced thickness changes of lipid bilayer membranes and the effect of an electric field on gramicidin A channel formation. Biochim. Biophys. Acta 426, 570-580.
34. Wu, M., Maier, E., Benz, R., and Hancock, R. E. (1999) Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38, 7235-7242.
35. Boheim, G., Hanke, W., and Eibl, H. (1980) Lipid phase transition in planar bilayer membrane and its effect on carrier-and pore-mediated ion transport. Proc. Natl. Acad. Sci. U.S.A. 77, 3403-3407.
36. Das, G., Talukdar, P., and Matile, S. (2002) Fluorometric detection of enzyme activity with synthetic supramolecular pores. Science 298, 1600-1602.
37. Litvinchuk, S., Sorde, N., and Matile, S. (2005) Sugar sensing with synthetic multifunctional pores. J. Am. Chem. Soc. 127, 9316-9317.
38. Sakai, N., Mareda, J., and Matile, S. (2007) Ion channels and pores, made from scratch. Mol. BioSyst. 3, 658-666.
39. Gorteau, V., Bollot, G., Mareda, J., Pasini, D., Tran, D. H., Lazar, A. N., Coleman, A. W., Sakai, N., and Matile, S. (2005) Synthetic multifunctional pores that open and close in response to chemical stimulation. Bioorg. Med. Chem. 13, 5171-5180.
40. Talukdar, P., Bollot, G., Mareda, J., Sakai, N., and Matile, S. (2005) Ligand-gated synthetic ion channels. Chem.-Eur. J. 11, 6525-6532.
41. Talukdar, P., Bollot, G., Mareda, J., Sakai, N., and Matile, S. (2005) Synthetic ion channels with rigid-rod jr-stack architecture that open in response to charge-transfer complex formation. J. Am. Chem. Soc. 127, 6528-6529.
42. Sakai, N., Ni, C., Bezrukov, S. M., and Matile, S. (1998) Voltage-dependent ion channel formation by rigid rod-shaped polyols in planar lipid bilayers. Bioorg. Med. Chem. Lett. 8, 2743-2746.
43. Mayer, M., Semetey, V., Gitlin, I., Yang, J., and Whitesides, G. M. (2008) Using ion channel-forming peptides to quantify protein-ligand interactions. J. Am. Chem. Soc. 130, 1453-1465.
44. Bali, D., King, L., and Kim, S. (2003) Syntheses of new gramicidin A derivatives. Aust. J. Chem. 56, 293-300.
45. Jin, X. Z., Durrant, J. D., Duffin, R., and Busath, D. D. (2004) The impact of the negative charge on cation permeation in the taurine(16)-gramicidin A channel. Biophys. J. 86, 206A-206A.
46. Borisenko, V., Zhang, Z. H., and Woolley, G. A. (2002) Gramicidin derivatives as membrane-based pH sensors. Biochim. Biophys. Acta 1558, 26-33.
47. Kovalchuk, S. I., Kotova, E. A., Stoilova, T. B., Sychev, S. V., Egorova, N. S., Surovoy, A. Y., Antonenko, Y. N., and Ivanov, V. T. (2007) Positively charged gramicidin A based peptides form two types of membrane channels. Biopolymers 88, 624-624.
48. Antonenko, Y. N., Rokitskaya, T. I., Kotova, E. A., Reznik, G. O., Sano, T., and Cantor, C. R. (2004) Effect of streptavidins with varying biotin binding affinities on the properties of biotinylated gramicidin channels. Biochemistry 43, 4575-4582.
49. Diociaiuti, M., Molinari, A., Ruspantini, I., Gaudiano, M. C., Ippoliti, R., Lendaro, E., Bordi, F., Chistolini, P., and Arancia, G. (2002) P-glycoprotein inserted in planar lipid bilayers formed by liposomes opened on amorphous carbon and Langmuir-Blodgett monolayer. Biochim. Biophys. Acta 1559, 21-31.
50. Miller, C. (1986) Ion Channel Reconstitution, Plenum Press, New York.
51. Ohlsson, P. A., Tjarnhage, T., Herbai, E., Lofas, S., and Puu, G. (1995) Liposome and proteoliposome fusion onto solid substrates, studies using atomic-force microscopy, quartz-crystal microbalance and surface-plasmon resonance - biological-activities of incorporated components. Bioelectrochem. Bioenerg. 38, 137-148.
52. Pizzolato, F., Morelis, R. M., and Coulet, P. R. (2000) Enzymatic nanolayers from proteolipidic Langmuir-Blodgett films for biosensors. Quim. Anal. 19, 32-37.
53. Gennis, R. B. (1989) Biomembranes: Molecular Structure and Function, Springer-Verlag, New York.
54. Hladky, S. B., and Haydon, D. A. (1970) Discreteness of conductance change in bimolecular lipid membranes in presence of certain antibiotics. Nature 225, 451.
55. Stankovic, C. J., Heinemann, S. H., Delfino, J. M., Sigworth, F. J., and Schreiber, S. L. (1989) Transmembrane channels based on tartaric acid Gramicidin-A hybrids. Science 244, 813-817.
56. Roeske, R. W., Hrinyopavlina, T. P., Pottorf, R. S., Bridal, T., Jin, X. Z., and Busath, D. (1989) Synthesis and channel properties of [tau-16]Gramicidin-A. Biochim. Biophys. Acta 982, 223-227.
57. Fields, C. G., Fields, G. B., Noble, R. L., and Cross, T. A. (1989) Solid phase peptide synthesis of 15N-gramicidins A, B, and C and high performance liquid chromatographic purification. Int. J. Pept. Protein Res. 33, 298-303.
58. Fields, G. B., Fields, C. G., Petefish, J., Van Wart, H. E., and Cross, T. A. (1988) Solid-phase peptide synthesis and solid-state NMR spectroscopy of [Ala3-15N][Val1]gramicidin A. Proc. Natl. Acad. Sci. U.S.A. 85, 1384-1388.
59. Rizzolo, F., Sabatino, G., Chelli, M., Rovero, P., and Papini, A. M. (2007) Optimized solid-phase synthesis of difficult peptide sequences: Case study of gramicidin A. Biopolymers 88, 620-620.
60. Suarez, E., De, E., Molle, G., Lazaro, R., and Viallefont, P. (1998) Synthesis and characterization of a new biotinylated gramicidin. J. Pept. Sci. 4, 371-377.
61. Kolb, H. C., Finn, M. G., and Sharpless, K. B. (2001) Click chemistry: Diverse chemical function from a few good reactions. Angew. Chem., Int. Ed. 40, 2004-2021.
62. Stankovic, C. J., Delfino, J. M., and Schreiber, S. L. (1990) Purification of Gramicidin-A. Anal. Biochem. 184, 100-103.
63. Ryu, E. H., and Zhao, Y. (2005) Efficient synthesis of water-soluble calixarenes using click chemistry. Org. Lett. 7, 1035-1037.
64. Forster, M. O., and Newman, S. H. (1911) The triazo-group. Part XVII. Nitrosoazides of pinene and terpineol. J. Chem. Soc. 99, 244-250.
65. Wilkinson, B. L., Bornaghi, L. F., Houston, T. A., Innocenti, A., Supuran, C. T., and Poulsen, S. A. (2006) A novel class of carbonic anhydrase inhibitors: glycoconjugate benzene sulfonamides prepared by "click"- tailing. J. Med. Chem. 49, 6539-6548.
66. Mayer, M., Kriebel, J. K., Tosteson, M. T., and Whitesides, G. M. (2003) Microfabricated Teflon membranes for low-noise recordings of ion channels in planar lipid bilayers. Biophys. J. 85, 2684-2695.
67. Nefkens, G. H., and Tesser, G. I. (1961) A novel activated ester in peptide synthesis. J. Am. Chem. Soc. 83, 1263-1263.
68. Gee, K. R., Archer, E. A., and Kang, H. C. (1999) 4- Sulfotetrafluorophenyl (STP) esters: New water-soluble amine-reactive reagents for labeling biomolecules. Tetrahedron Lett. 40, 1471-1474.
69. Rostovtsev, V. V., Green, L. G., Fokin, V. V., and Sharpless, K. B. (2002) A stepwise Huisgen cycloaddition process: Copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew. Chem., Int. Ed. 41, 2596-2599.
70. Wu, P., Hilgraf, R., and Fokin, V. V. (2006) Osmium-catalyzed olefin dihydroxylation and aminohydroxylation in the second catalytic cycle. Adv. Synth. Catal. 348, 1079-1085.
71. Culf, A. S., Gerig, J. T., and Williams, P. G. (1997) Tritium NMR studies of the human carbonic anhydrase I-benzene-sulfonamide complex. J. Biomol. NMR 10, 293-299.
72. Mahmood Ul, H., Chohan, Z. H., Scozzafava, A., and Supuran, C. T. (2004) Carbonic anhydrase inhibitors: Schiff's bases of aromatic and heterocyclic sulfonamides and their metal complexes. J. Enzyme. Inhib. Med. Chem. 19, 263-267.
73. Menziani, M. C., Debenedetti, P. G., Gago, F., and Richards, W. G. (1989) The binding of benzenesulfonamides to carbonic - anhydrase enzyme - a molecular mechanics study and quantitative structure activity relationships. J. Med. Chem. 32, 951-956.
74. Merz, K. M., Murcko, M. A., and Kollman, P. A. (1991) Inhibition of carbonic-anhydrase. J. Am. Chem. Soc. 113, 4484-4490.
75. Saczewski, F., Innocenti, A., Brzozowski, Z., Slawinski, J., Pomarnacka, E., Kornicka, A., Scozzafava, A., and Supuran, C. T. (2006) Carbonic anhydrase inhibitors. Selective inhibition of human tumor-associated isozymes IX and XII and cytosolic isozymes I and II with some substituted-2-mercapto-benzene- sulfonamides. J. Enzyme. Inhib. Med. Chem. 21, 563-568.
76. Santos, M. A., Marques, S., Vullo, D., Innocenti, A., Scozzafava, A., and Supuran, C. T. (2007) Carbonic anhydrase inhibitors: Inhibition of cytosolic/tumor-associated isoforms I, II, and IX with iminodiacetic carboxylates/hydroxamates also incorporating benzenesulfonamide moieties. Bioorg. Med. Chem. Lett. 17, 1538-1543.
77. Supuran, C. T., and Scozzafava, A. (2000) Carbonic anhydrase inhibitors: Aromatic sulfonamides and disulfonamides act as efficient tumor growth inhibitors - Part 95. J. Enzyme. Inhib. 15, 597-610.
78. Gitlin, I., Mayer, M., and Whitesides, G. M. (2003) Significance of charge regulation in the analysis of protein charge ladders. J. Phys. Chem. B 107, 1466-1472.
79. Rokitskaya, T. I., Kotova, E. A., and Antonenko, Y. N. (2003) Tandem gramicidin channels cross-linked by streptavidin. J. Gen. Physiol. 121, 463-476.
80. Lahiri, J., Isaacs, L., Grzybowski, B., Carbeck, J. D., and Whitesides, G. M. (1999) Biospecific binding of carbonic anhydrase to mixed SAMs presenting benzenesulfonamide ligands: A model system for studying lateral steric effects. Langmuir 15, 7186-7198.
81. Bastug, T., Gray-Weale, A., Patra, S. M., and Kuyucak, S. (2006) Role of protein flexibility in ion permeation: A case study in gramicidin A. Biophys. J. 90, 2285-2296.
82. Biswas, S. C., Rananavare, S. B., and Hall, S. B. (2005) Effects of gramicidin-A on the adsorption of phospholipids to the airwater interface. Biochim. Biophys. Acta 1717, 41-49.
83. Broniatowski, M., Obidowicz, K., Vila Romeu, N., Broniatowska, E., and Dynarowicz-Latka, P. (2007) Mixed Langmuir monolayers of gramicidin A and fluorinated alcohols. J. Colloid Interface Sci. 313, 600-607.
84. Durrant, J. D., Caywood, D., and Busath, D. D. (2006) Tryptophan contributions to the empirical free-energy profile in gramicidin A/M heterodimer channels. Biophys. J. 91, 3230-3241.
85. Portella, G., Pohl, P., and de Groot, B. L. (2007) Invariance of single-file water mobility in gramicidin-like peptidic pores as function of pore length. Biophys. J. 92, 3930-3937.
86. Wang, Z., and Fried, J. R. (2007) A hierarchical approach for predicting the transport properties of the gramicidin A channel. Soft Matter 3, 1041-1052.
87. Woolley, G. A., Zunic, V., Karanicolas, J., Jaikaran, A. S. I., and Starostin, A. V. (1997) Voltage-dependent behavior of a "ball-and- chain" gramicidin channel. Biophys. J. 73, 2465-2475.
88. Anastasiadis, A., Morton, C. J., Talbo, G. H., Koeppe, R. E., and Separovic, F. (2006) Effect of linker length on avidin binding to biotinylated gramicidin A. Int. J. Pept. Res. Therap. 12, 243-252.
89. Schmidt, C., Mayer, M., and Vogel, H. (2000) A chip-based biosensor for the functional analysis of single ion channels. Angew. Chem., Int. Ed. 39, 3137-3140.
90. Uram, J. D., Ke, K., Hunt, A. J., and Mayer, M. (2006) Label-free affinity assays by rapid detection of immune complexes in submicrometer pores. Angew. Chem., Int. Ed. 45, 2281-2285.
91. An, R., Uram, J. D., Yusko, E. C., Ke, K., Mayer, M., and Hunt, A. J. (2008) Ultrafast laser fabrication of submicrometer pores in borosilicate glass. Opt. Lett. 33, 1153-1155.
92. Fertig, N., Meyer, C., Blick, R. H., Trautmann, C., and Behrends, J. C. (2001) Microstructured glass chip for ion-channel electrophysiology. Phys. Rev. E: Stat. Nonlin. Soft Matter Phys. 64, 040901.
93. Borisenko, V., Lougheed, T., Hesse, J., Fureder-Kitzmuller, E., Fertig, N., Behrends, J. C., Woolley, G. A., and Schutz, G. J. (2003) Simultaneous optical and electrical recording of single gramicidin channels. Biophys. J. 84, 612-622.
94. Jeon, T. J., Malmstadt, N., and Schmidt, J. J. (2006) Hydrogel-encapsulated lipid membranes. J. Am. Chem. Soc. 128, 42-43.
95. Malmstadt, N., Jeon, L. J., and Schmidt, J. J. (2008) Long-lived planar lipid bilayer membranes anchored to an in situ polymerized hydrogel. Adv. Mater. 20, 84+.
96. Malmstadt, N., Nash, M. A., Purnell, R. F., and Schmidt, J. J. (2006) Automated formation of lipid-bilayer membranes in a microfluidic device. Nano Lett. 6, 1961-1965.
97. Shim, J. W., and Gu, L. Q. (2007) Stochastic sensing on a modular chip containing a single-ion channel. Anal. Chem. 79, 2207-2213.
98. White, R. J., Ervin, E. N., Yang, T., Chen, X., Daniel, S., Cremer, P. S., and White, H. S. (2007) Single ion-channel recordings using glass nanopore membranes. J. Am. Chem. Soc. 129, 11766-11775.
99. Peterman, M. C., Ziebarth, J. M., Braha, O., Bayley, H., Fishman, H. A., and Bloom, D. M. (2002) Ion channels and lipid bilayer membranes under high potentials using microfabricated apertures. Biomed. Microdevices 4, 231-236.
100. Gross, E., Morell, J. L., Bamberg, E., and Lauger, P. (1977) The synthesis and ion transport properties of gramicidin analogs. Fed. Proc. 36, 864.
101. Janko, K., Bamberg, R. R., E., Apell, H.-J., Alpes, H., Lauger P. (1983) Peptides: Structure and Function, Pierce Chemical Company, Rockford.