Sensitized photoinactivation of minigramicidin channels in bilayer lipid membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 5, 2007, Pages 1230-1237

  Dutseva, Elena A ^a   Antonenko, Yuri N ^a   Kotova, Elena A ^a   Pfeifer, Jochen R ^b   Koert, Ulrich ^b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Channel forming peptide; Hydrophobic mismatch; Ionic current; Membrane thickness; Planar lipid bilayer; Sensitized photoinactivation

Indexed keywords

DIMER; GRAMICIDIN; GRAMICIDIN A; ION CHANNEL; MINIGRAMICIDIN; PHTHALOCYANINE ALUMINUM; ROSE BENGAL; UNCLASSIFIED DRUG;

ARTICLE; BILAYER MEMBRANE; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE CURRENT; MEMBRANE DEPOLARIZATION; MOLECULAR DYNAMICS; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEOMICS;

DIMERIZATION; ELECTRIC CONDUCTIVITY; GRAMICIDIN; ION CHANNELS; LIGHT; LIPID BILAYERS; PHOTOSENSITIZING AGENTS; TEMPERATURE; TIME FACTORS;

EID: 34047274769     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.01.006     Document Type: Article

References (63)

1. Mouritsen O.G., and Bloom M. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46 (1984) 141-153
2. Killian J.A. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta 1376 (1998) 401-415
3. Dumas F., Lebrun M.C., and Tocanne J.F. Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions?. FEBS Lett. 458 (1999) 271-277
4. Kleinschmidt J.H., and Tamm L.K. Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J. Mol. Biol. 324 (2002) 319-330
5. Ramakrishnan M., Qu J., Pocanschi C.L., Kleinschmidt J.H., and Marsh D. Orientation of beta-barrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism. Biochemistry 44 (2005) 3515-3523
6. Lee K.J. Energetics of rotational gating mechanisms of an ion channel induced by membrane deformation. Phys. Rev., E Stat. Nonlinear Soft Matter Phys. 73 (2006) 021909
7. Hladky S.B., and Haydon D.A. Ion transfer across lipid membranes in the presence of gramicidin A: I. Studies of the unit conductance channel. Biochim. Biophys. Acta 274 (1972) 294-312
8. Kolb H.A., and Bamberg E. Influence of membrane thickness and ion concentration on the properties of the gramicidin A channel. Autocorrelation, spectral power density, relaxation and single-channel studies. Biochim. Biophys. Acta 464 (1977) 127-141
9. Rudnev V.S., Ermishkin L.N., Fonina L.A., and Rovin Yu.G. The dependence of the conductance and lifetime of gramicidin channels on the thickness and tension of lipid bilayers. Biochim. Biophys. Acta 642 (1981) 196-202
10. Elliott J.R., Needham D., Dilger J.P., and Haydon D.A. The effects of bilayer thickness and tension on gramicidin single-channel lifetime. Biochim. Biophys. Acta 735 (1983) 95-103
11. Mobashery N., Nielsen C., and Andersen O.S. The conformational preference of gramicidin channels is a function of lipid bilayer thickness. FEBS Lett. 412 (1997) 15-20
12. Dzikovski B.G., Borbat P.P., and Freed J.H. Spin-labeled gramicidin A: channel formation and dissociation. Biophys. J. 87 (2004) 3504-3517
13. 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
14. Arndt H.D., Knoll A., and Koert U. Synthesis of minigramicidin ion channels and test of their hydrophobic match with the membrane. ChembioChem 2 (2001) 221-223
15. Hwang T.C., Koeppe R.E., and Andersen O.S. Genistein can modulate channel function by a phosphorylation-independent mechanism: importance of hydrophobic mismatch and bilayer mechanics. Biochemistry 42 (2003) 13646-13658
16. 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices. FEBS Lett. 186 (1985) 168-174
17. Smith R., Thomas D.E., Separovic F., Atkins A.R., and Cornell B.A. Determination of the structure of a membrane-incorporated ion channel. Solid-state nuclear magnetic resonance studies of gramicidin A. Biophys. J. 56 (1989) 307-314
18. Woolley G.A., and Wallace B.A. Model ion channels: gramicidin and alamethicin. J. Membr. Biol. 129 (1992) 109-136
19. 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
20. Busath D.D. The use of physical methods in determining gramicidin channel structure and function. Annu. Rev. Physiol. 55 (1993) 473-501
21. Koeppe R.E., and Andersen O.S. Engineering the gramicidin channel. Annu. Rev. Biophys. Biomol. Struct. 25 (1996) 231-258
22. Andersen O.S., Apell H.J., Bamberg E., Busath D.D., Koeppe R.E., Sigworth F.J., Szabo G., Urry D.W., and Woolley A. Gramicidin channel controversy-The structure in a lipid environment. Nat. Struct. Biol. 6 (1999) 609-610
23. Cross T.A., Arseniev A.S., Cornell B.A., Davis J.H., Killian J.A., Koeppe R.E., Nicholson L.K., Separovic F., and Wallace B.A. Gramicidin channel controversy-Revisited. Nat. Struct. Biol. 6 (1999) 610-611
24. Bamberg E., and Janko K. The action of a carbonsuboxide dimerized gramicidin A on lipid bilayer membranes. Biochim. Biophys. Acta 465 (1977) 486-499
25. Irkhin A.I., Bezrukov S.M., and Melnik E.I. Properties of ionic channels formed by gramicidin A dimeric analogs in lipid bilayer membranes. Biol. Membr. 1 (1984) 739-749
26. Stark G., Straessle M., and Takacz Z. Temperature-jump and voltage-jump experiments at planar lipid membranes support an aggregational (micellar) model of the gramicidin A ion channel. J. Membr. Biol. 89 (1986) 23-37
27. Arndt H.D., Bockelmann D., Knoll A., Lamberth S., Griesinger C., and Koert U. Cation control in functional helical programming: structures of a d,l-peptide ion channel. Angew. Chem., Int. Ed. Engl. 41 (2002) 4062-4065
28. Sychev S.V., Sukhanov S.V., Barsukov L.I., and Ivanov V.T. Structural polymorphism of gramicidin A channels: ion conductivity and spectral studies. J. Pept. Sci. 2 (1996) 141-156
29. 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
30. 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
31. Rokitskaya T.I., Antonenko Y.N., Kotova E.A., Anastasiadis A., and Separovic F. Effect of avidin on channel kinetics of biotinylated gramicidin. Biochemistry 39 (2000) 13053-13058
32. Rokitskaya T.I., Kotova E.A., and Antonenko Y.N. Tandem gramicidin channels cross-linked by streptavidin. J. Gen. Physiol. 121 (2003) 463-476
33. Rokitskaya T.I., Kotova E.A., and Antonenko Y.N. Cytochrome c decelerates channel kinetics of negatively charged gramicidin due to electrostatic interaction. Biochem. Biophys. Res. Commun. 302 (2003) 865-868
34. Krylov A.V., Antonenko Y.N., Kotova E.A., Rokitskaya T.I., and Yaroslavov A.A. Polylysine decelerates kinetics of negatively charged gramicidin channels as shown by sensitized photoinactivation. FEBS Lett. 440 (1998) 235-238
35. Krylov A.V., Kotova E.A., Yaroslavov A.A., and Antonenko Y.N. Stabilization of O-pyromellitylgramicidin channels in bilayer lipid membranes through electrostatic interaction with polylysines of different chain lengths. Biochim. Biophys. Acta 1509 (2000) 373-384
36. Krylov A.V., Rokitskaya T.I., Kotova E.A., Yaroslavov A.A., and Antonenko Y.N. Kinetically different populations of O-pyromellityl-gramicidin channels induced by poly-l-lysines in lipid bilayers. J. Membr. Biol. 189 (2002) 119-130
37. 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
38. 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
39. Kotova E.A., and Antonenko Y.N. Sensitized photoinactivation of gramicidin channels: technique and applications. In: Tien H.T., and Ottova-Leitmannova A. (Eds). Advances in Planar Lipid Bilayers and Liposomes (2005), Academic Press, Amsterdam 159-180
40. Kotova E.A., Rokitskaya T.I., and Antonenko Y.N. Two phases of gramicidin photoinactivation in bilayer lipid membranes in the presence of a photosensitizer. Membr. Cell Biol. 13 (2000) 411-420
41. Rokitskaya T.I., Antonenko Y.N., and Kotova E.A. The interaction of phthalocyanine with planar lipid bilayers-Photodynamic inactivation of gramicidin channels. FEBS Lett. 329 (1993) 332-335
42. Rokitskaya T.I., Block M., Antonenko Y.N., Kotova E.A., and Pohl P. Photosensitizer binding to lipid bilayers as a precondition for the photoinactivation of membrane channels. Biophys. J. 78 (2000) 2572-2580
43. Chernyshev A., Armstrong K.M., and Cukierman S. Proton transfer in gramicidin channels is modulated by the thickness of monoglyceride bilayers. Biophys. J. 84 (2003) 238-250
44. Hladky S.B., and Haydon D. Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel. Biochim. Biophys. Acta 274 (1972) 294-312
45. Bamberg E., and Lauger P. Temperature-dependent properties of gramicidin A channels. Biochim. Biophys. Acta 367 (1974) 127-133
46. 5.6 helix of gramicidin A predominates in unsaturated lipid membranes. Eur. Biophys. J. 22 (1993) 279-288
47. Greathouse D.V., Hinton J.F., Kim K.S., and Koeppe R.E. Gramicidin A/short-chain phospholipid dispersions: chain length dependence of gramicidin conformation and lipid organization. Biochemistry 33 (1994) 4291-4299
48. Saparov S.M., Pfeifer J.R., Al Momani L., Portella G., de Groot B.L., Koert U., and Pohl P. Mobility of a one-dimensional confined file of water molecules as a function of file length. Phys. Rev. Lett. 96 (2006) 148101
49. Straessle M., and Stark G. Photodynamic inactivation of an ion channel: gramicidin A. Photochem. Photobiol. 55 (1992) 461-463
50. Stark G. Functional consequences of oxidative membrane damage. J. Membr. Biol. 205 (2005) 1-16
51. Kunz L., Zeidler U., Haegele K., Przybylski M., and Stark G. Photodynamic and radiolytic inactivation of ion channels formed by gramicidin A: oxidation and fragmentation. Biochemistry 34 (1995) 11895-11903
52. 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
53. Cifu A.S., Koeppe R.E., and Andersen O.S. On the supramolecular organization of gramicidin channels-The elementary conducting unit is a dimer. Biophys. J. 61 (1992) 189-203
54. Borisenko V., Lougheed T., Hesse J., Fureder-Kitzmuller E., Fertig N., Behrends J.C., Woolley G.A., and Schutz G.J. Simultaneous optical and electrical recording of single gramicidin channels. Biophys. J. 84 (2003) 612-622
55. Harms G.S., Orr G., Montal M., Thrall B.D., Colson S.D., and Lu H.P. Probing conformational changes of gramicidin ion channels by single-molecule patch-clamp fluorescence microscopy. Biophys. J. 85 (2003) 1826-1838
56. Pope C.G., Urban B.W., and Haydon D.A. The influence of n-alkanols and cholesterol on the duration and conductance of gramicidin single channels in monoolein bilayers. Biochim. Biophys. Acta 688 (1982) 279-283
57. Elliott J.R., Needham D., Dilger J.P., Brandt O., and Haydon D.A. A quantitative explanation of the effects of some alcohols on gramicidin single-channel lifetime. Biochim. Biophys. Acta 814 (1985) 401-404
58. Lundbaek J.A., Birn P., Girshman J., Hansen A.J., and Andersen O.S. Membrane stiffness and channel function. Biochemistry 35 (1996) 3825-3830
59. Partenskii M.B., Miloshevsky G.V., and Jordan P.C. Stabilization of ion channels due to membrane-mediated elastic interaction. J. Phys. Chem. 118 (2003) 10306-10311
60. Harroun T.A., Heller W.T., Weiss T.M., Yang L., and Huang H.W. Theoretical analysis of hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys. J. 76 (1999) 3176-3185
61. Nielsen C., and Andersen O.S. Inclusion-induced bilayer deformations: effects of monolayer equilibrium curvature. Biophys. J. 79 (2000) 2583-2604
62. 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
63. Killian J.A. Gramicidin and gramicidin-lipid interactions. Biochim. Biophys. Acta 1113 (1991) 391-425