Redox-regulated ion channel activity of a cysteine-containing gramicidin A analogue

Biochimica et Biophysica Acta - Biomembranes

Volumn 1758, Issue 4, 2006, Pages 493-498

  Antonenko, Yuri N ^a   Stoilova, Tatyana B ^b   Kovalchuk, Sergey I ^b   Egorova, Natalya S ^b   Pashkovskaya, Alina A ^a   Sobko, Alexander A ^a   Kotova, Elena A ^a   Surovoy, Andrey Y ^b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

Ion channel; Phospholipid membrane; Transmembrane peptide

Indexed keywords

CATION; CYSTEINE; GRAMICIDIN A; HYDROGEN PEROXIDE; ION CHANNEL; PEPTIDE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; LIPID MEMBRANE; MEMBRANE CURRENT; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; SOLUTION AND SOLUBILITY;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; CYSTEINE; GRAMICIDIN; HYDROGEN PEROXIDE; ION CHANNELS; KINETICS; OLIGOPEPTIDES; OXIDATION-REDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 33646814017     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2006.02.028     Document Type: Article

References (57)

1. Ruppersberg J.P., Stocker M., Pongs O., Heinemann S.H., Frank R., and Koenen M. Regulation of fast inactivation of cloned mammalian IK(A) channels by cysteine oxidation. Nature 352 (1991) 711-714
2. 2+ release channel from skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 270 (1995) 25557-25563
3. + channels in T lymphocytes and Xenopus oocytes. Pflugers Arch. 433 (1997) 626-632
4. Sun J., Xu L., Eu J.P., Stamler J.S., and Meissner G. Classes of thiols that influence the activity of the skeletal muscle calcium release channel. J. Biol. Chem. 276 (2001) 15625-15630
5. + channels. J. Biol. Chem. 276 (2001) 35564-35570
6. Zeng X.H., Xia X.M., and Lingle C.J. Redox-sensitive extracellular gates formed by auxiliary beta subunits of calcium-activated potassium channels. Nat. Struct. Biol. 10 (2003) 448-454
7. Tang X.D., Garcia M.L., Heinemann S.H., and Hoshi T. Reactive oxygen species impair Slo1 BK channel function by altering cysteine-mediated calcium sensing. Nat. Struct. Mol. Biol. 11 (2004) 171-178
8. Li Y., Yu W.P., Lin C.W., and Chen T.Y. Oxidation and reduction control of the inactivation gating of Torpedo ClC-0 chloride channels. Biophys. J. 88 (2005) 3936-3945
9. Wang W., Oliva C., Li G., Holmgren A., Lillig C.H., and Kirk K.L. Reversible silencing of CFTR chloride channels by glutathionylation. J. Gen. Physiol. 125 (2005) 127-141
10. Andrey F., Tsintsadze T., Volkova T., Lozovaya N., and Krishtal O. Acid sensing ionic channels: modulation by redox reagents. Biochim. Biophys. Acta 1745 (2005) 1-6
11. Novgorodov S.A., Kultayeva E.V., Yaguzhinsky L.S., and Lemeshko V.V. Ion permeability induction by the SH cross-linking reagents in rat liver mitochondria is inhibited by the free radical scavenger, butylhydroxytoluene. J. Bioenerg. Biomembr. 19 (1987) 191-202
12. Petronilli V., Costantini P., Scorrano L., Colonna R., Passamonti S., and Bernardi P. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J. Biol. Chem. 269 (1994) 16638-16642
13. Chernyak B.V., and Bernardi P. The mitochondrial permeability transition pore is modulated by oxidative agents through both pyridine nucleotides and glutathione at two separate sites. Eur. J. Biochem. 238 (1996) 623-630
14. Feng W., Liu G., Allen P.D., and Pessah I.N. Transmembrane redox sensor of ryanodine receptor complex. J. Biol. Chem. 275 (2000) 35902-35907
15. Xia R., Stangler T., and Abramson J.J. Skeletal muscle ryanodine receptor is a redox sensor with a well defined redox potential that is sensitive to channel modulators. J. Biol. Chem. 275 (2000) 36556-36561
16. 2+ release channels: cellular redox sensors?. IUBMB Life 57 (2005) 315-322
17. + channel may function as an oxygen sensor complex in airway chemoreceptors and small cell lung carcinoma cell lines. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 13182-13187
18. 2 sensors of lungs and blood vessels and their role in the antioxidant defense of the body. Biochemistry (Moscow) 66 (2001) 1153-1156
19. Cornell B.A., Braach-Maksvytis V.L., King L.G., Osman P.D., Raguse B., Wieczorek L., and Pace R.J. A biosensor that uses ion-channel switches. Nature 387 (1997) 580-583
20. Futaki S., Fukuda M., Omote M., Yamauchi K., Yagami T., Niwa M., and Sugiura Y. Alamethicin-leucine zipper hybrid peptide: a prototype for the design of artificial receptors and ion channels. J. Am. Chem. Soc. 123 (2001) 12127-12134
21. Bayley H., and Cremer P.S. Stochastic sensors inspired by biology. Nature 413 (2001) 226-230
22. Howorka S., Cheley S., and Bayley H. Sequence-specific detection of individual DNA strands using engineered nanopores. Nat. Biotechnol. 19 (2001) 636-639
23. Das G., Talukdar P., and Matile S. Fluorometric detection of enzyme activity with synthetic supramolecular pores. Science 298 (2002) 1600-1602
24. Woolley G.A., and Lougheed T. Modeling ion channel regulation. Curr. Opin. Chem. Biol. 7 (2003) 710-714
25. Litvinchuk S., Sorde N., and Matile S. Sugar sensing with synthetic multifunctional pores. J. Am. Chem. Soc. 127 (2005) 9316-9317
26. Borisenko V., Zhang Z., and Woolley G.A. Gramicidin derivatives as membrane-based pH sensors. Biochim. Biophys. Acta 1558 (2002) 26-33
27. Wright L.S., and Harding M.M. Detection of DNA via an ion channel switch biosensor. Anal. Biochem. 282 (2000) 70-79
28. Hirano A., Wakabayashi M., Matsuno Y., and Sugawara M. A single-channel sensor based on gramicidin controlled by molecular recognition at bilayer lipid membranes containing receptor. Biosens. Bioelectron. 18 (2003) 973-983
29. Futaki S., Zhang Y., Kiwada T., Nakase I., Yagami T., Oiki S., and Sugiura Y. Gramicidin-based channel systems for the detection of protein-ligand interaction. Bioorg. Med. Chem. 12 (2004) 1343-1350
30. Urry D.W., Goodall M.C., Glickson J.D., and Mayers D.F. The gramicidin A transmembrane channel: characteristics of head-to-head dimerized (L,D) helices. Proc. Natl. Acad. Sci. U. S. A. 68 (1971) 1907-1911
31. Arseniev A.S., Barsukov I.L., Bystrov V.F., Lomize A.L., and Ovchinnikov Yu.A. 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices. FEBS Lett. 186 (1985) 168-174
32. Ketchem R.R., Hu W., and Cross T.A. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 261 (1993) 1457-1460
33. Woolley G.A., Zunic V., Karanicolas J., Jaikaran A.S., and Starostin A.V. Voltage-dependent behavior of a "ball-and-chain" gramicidin channel. Biophys. J. 73 (1997) 2465-2475
34. Foong L.Y., You S., Jaikaran D.C., Zhang Z., Zunic V., and Woolley G.A. Development of a novel thiol reagent for probing ion channel structure: studies in a model system. Biochemistry 36 (1997) 1343-1348
35. Antonenko Y.N., Borisenko V., Melik-Nubarov N.S., Kotova E.A., and Woolley G.A. Polyanions decelerate the kinetics of positively charged gramicidin channels as shown by sensitized photoinactivation. Biophys. J. 82 (2002) 1308-1318
36. Goforth R.L., Chi A.K., Greathouse D.V., Providence L.L., Koeppe R.E., and Andersen O.S. Hydrophobic coupling of lipid bilayer energetics to channel function. J. Gen. Physiol. 121 (2003) 477-493
37. Antonenko Y.N., Stoilova T.B., Kovalchuk S.I., Egorova N.S., Pashkovskaya A.A., Sobko A.A., Kotova E.A., Sychev S.V., and Surovoy A.Y. Large unselective pore in lipid bilayer membrane formed by positively charged peptides containing a sequence of gramicidin A. FEBS Lett. 579 (2005) 5247-5252
38. Mueller P., Rudin D.O., Tien H.T., and Wescott W.C. Methods for the formation of single bimolecular lipid membranes in aqueous solution. J. Phys. Chem. 67 (1963) 534-535
39. Sobko A.A., Kotova E.A., Antonenko Y.N., Zakharov S.D., and Cramer W.A. Effect of lipids with different spontaneous curvature on the channel activity of colicin E1: evidence in favor of a toroidal pore. FEBS Lett. 576 (2004) 205-210
40. Hladky S.B., and Haydon D.A. Ion movements in gramicidin channels. Curr. Topics in Membr. Transport 21 (1984) 327-372
41. Woolley G.A., Jaikaran A.S., Zhang Z., and Peng S. Design of regulated ion channels using measurements of cis-trans isomerization in single molecules. J. Am. Chem. Soc. 117 (1995) 4448-4454
42. Rokitskaya T.I., Antonenko Y.N., and Kotova E.A. Photodynamic inactivation of gramicidin channels: a flash-photolysis study. Biochim. Biophys. Acta 1275 (1996) 221-226
43. Rokitskaya T.I., Antonenko Y.N., and Kotova E.A. Effect of the dipole potential of a bilayer lipid membrane on gramicidin channel dissociation kinetics. Biophys. J. 73 (1997) 850-854
44. Straessle M., and Stark G. Photodynamic inactivation of an ion channel: gramicidin A. Photochem. Photobiol. 55 (1992) 461-463
45. Sobko A.A., Vigasina M.A., Rokitskaya T.I., Kotova E.A., Zakharov S.D., Cramer W.A., and Antonenko Y.N. Chemical and photochemical modification of colicin E1 and gramicidin A in bilayer lipid membranes. J. Membr. Biol. 199 (2004) 51-62
46. Rokitskaya T.I., Kotova E.A., and Antonenko Y.N. Tandem gramicidin channels cross-linked by streptavidin. J. Gen. Physiol. 121 (2003) 463-476
47. Antonenko Y.N., Rokitskaya T.I., Kotova E.A., Reznik G.O., Sano T., and Cantor C.R. Effect of streptavidins with varying biotin binding affinities on the properties of biotinylated gramicidin channels. Biochemistry 43 (2004) 4575-4582
48. Al Momani L., Reiss P., and Koert U. A lipid dependence in the formation of twin ion channels. Biochem. Biophys. Res. Commun. 328 (2005) 342-347
49. Sansom M.S. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 55 (1991) 139-235
50. Sakoh M., Okazaki T., Nagaoka Y., and Asami K. N-terminal insertion of alamethicin in channel formation studied using its covalent dimer N-terminally linked by disulfide bond. Biochim. Biophys. Acta 1612 (2003) 117-121
51. Kotova E.A., and Antonenko Y.N. In: Tien H.T., and Ottova-Leitmannova A. (Eds). Advances in Planar Lipid Bilayers and Liposomes (2005), Academic Press, Amsterdam 159-180
52. Szabo G., and Urry D.W. N-acetyl gramicidin: single-channel properties and implications for channel structure. Science 203 (1979) 55-57
53. Seoh S.A., and Busath D.D. Formamidinium-induced dimer stabilization and flicker block behavior in homo- and heterodimer channels formed by gramicidin A and N-acetyl gramicidin A. Biophys. J. 65 (1993) 1817-1827
54. Koeppe R.E., and Andersen O.S. Engineering the gramicidin channel. Annu. Rev. Biophys. Biomol. Struct. 25 (1996) 231-258
55. Saparov S.M., Antonenko Y.N., Koeppe R.E., and Pohl P. Desformylgramicidin: a model channel with an extremely high water permeability. Biophys. J. 79 (2000) 2526-2534
56. Takei J., Remenyi A., and Dempsey C.E. Generalised bilayer perturbation from peptide helix dimerisation at membrane surfaces: vesicle lysis induced by disulphide-dimerised melittin analogues. FEBS Lett. 442 (1999) 11-14
57. Dempsey C.E., Ueno S., and Avison M.B. Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue. Biochemistry 42 (2003) 402-409