The pH-dependent induction of lipid membrane ionic permeability by N-terminally lysine-substituted analogs of gramicidin A

European Biophysics Journal

Volumn 41, Issue 2, 2012, Pages 129-138

  Rokitskaya, Tatyana I ^a   Sorochkina, Alexandra I ^a   Kovalchuk, Sergey I ^b   Egorova, Natalya S ^b   Kotova, Elena A ^a   Sychev, Sergey V ^b   Antonenko, Yuri N ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

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

Author keywords

Circular dichroism; Double helix; Gramicidin channel; Ionic current; pH dependence; Planar bilayer lipid membrane

Indexed keywords

DRUG DERIVATIVE; GRAMICIDIN; LYSINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHEMICAL PHENOMENA; CHEMISTRY; DRUG EFFECT; ELECTRIC CONDUCTIVITY; LIPID BILAYER; METABOLISM; MOLECULAR GENETICS; PH;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; ELECTRIC CONDUCTIVITY; GRAMICIDIN; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; LYSINE; MOLECULAR SEQUENCE DATA;

EID: 84857357887     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-011-0764-6     Document Type: Article

References (70)

1. OS Andersen RE Koeppe 1992 Molecular determinants of channel function Physiol Rev 72 S89 S158 1279736 1:CAS:528:DyaK3sXjsVGjsA%3D%3D
2. OS Andersen RE Koeppe 2007 Bilayer thickness and membrane protein function: an energetic perspective Annu Rev Biophys Biomol Struct 36 107 130 17263662 10.1146/annurev.biophys.36.040306.132643 1:CAS:528:DC%2BD2sXnsVahuro%3D (Pubitemid 46998112)
3. OS Andersen HJ Apell E Bamberg DD Busath RE Koeppe FJ Sigworth G Szabo DW Urry GA Woolley 1999 Gramicidin channel controversy-the structure in a lipid environment Nat Struct Biol 6 609 612 10404209 10.1038/10648 1:STN:280:DyaK1Mzjt1SnsQ%3D%3D (Pubitemid 29318944)
4. YN Antonenko V Borisenko NS Melik-Nubarov EA Kotova GA Woolley 2002 Polyanions decelerate the kinetics of positively charged gramicidin channels as shown by sensitized photoinactivation Biophys J 82 1308 1318 11867447 10.1016/S0006-3495(02)75486-6 1:CAS:528:DC%2BD38Xit1KjtrY%3D (Pubitemid 34204753)
5. YN Antonenko TB Stoilova SI Kovalchuk NS Egorova AA Pashkovskaya AA Sobko EA Kotova SV Sychev AY Surovoy 2005 Large unselective pore in lipid bilayer membrane formed by positively charged peptides containing a sequence of gramicidin A FEBS Lett 579 5247 5252 16165129 10.1016/j.febslet.2005.08.049 1:CAS:528:DC%2BD2MXhtVehsr3K (Pubitemid 41318099)
6. YN Antonenko TB Stoilova SI Kovalchuk NS Egorova AA Pashkovskaya AA Sobko EA Kotova AY Surovoy 2006 Redox-regulated ion channel activity of a cysteine-containing gramicidin A analogue Biochim Biophys Acta 1758 493 498 16624254 10.1016/j.bbamem.2006.02.028 1:CAS:528:DC%2BD28XltFCrsbc%3D (Pubitemid 43767725)
7. HJ Apell E Bamberg H Alpes P Lauger 1977 Formation of ion channels by a negatively charged analog of gramicidin A J Membr Biol 31 171 188 65475 10.1007/BF01869403 1:CAS:528:DyaE2sXhvVCrtLo%3D (Pubitemid 8042666)
8. 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices FEBS Lett 186 168 174 2408920 10.1016/0014-5793(85)80702-X 1:STN:280:DyaL2M3jtFaitQ%3D%3D (Pubitemid 15070299)
9. K Asami T Okazaki Y Nagai Y Nagaoka 2002 Modifications of alamethicin ion channels by substitution of Glu-7 for Gln-7 Biophys J 83 219 228 12080114 10.1016/S0006-3495(02)75163-1 1:CAS:528:DC%2BD38XlsVWisrg%3D (Pubitemid 34694733)
10. E Bamberg P Lauger 1977 Blocking of the gramicidin channel by divalent cations J Membr Biol 35 351 375 10.1007/BF01869959 1:CAS:528:DyaE2sXls1ehs7g%3D (Pubitemid 8149178)
11. E Bamberg HJ Apell H Alpes 1977 Structure of the gramicidin A channel: discrimination between the piL, D and the beta helix by electrical measurements with lipid bilayer membranes Proc Natl Acad Sci USA 74 2402 2406 70038 10.1073/pnas.74.6.2402 1:CAS:528:DyaE2sXksl2qtLc%3D (Pubitemid 8112977)
12. E Bamberg H Alpes HJ Apell R Bradley B Harter MJ Quelle DW Urry 1979 Formation of ionic channels in black lipid membranes by succinic derivatives of gramicidin A J Membr Biol 50 257 270 92569 10.1007/BF01868892 1:CAS:528:DyaL3cXhtVKitLw%3D (Pubitemid 10217075)
13. SM Bezrukov AI Irkhin EI Melnik 1984 Desformylgramicidin: a proton selective channel Biol Membr 1 659 665 1:CAS:528:DyaL2cXkvVGku7g%3D
14. V Borisenko Z Zhang GA Woolley 2002 Gramicidin derivatives as membrane-based pH sensors Biochim Biophys Acta 1558 26 33 11750261 10.1016/S0005-2736(01)00415-1 1:CAS:528:DC%2BD3MXptFymsrc%3D (Pubitemid 34031951)
15. Borisenko V, Saparov SM, Woolley GA, Pohl P (2003) Modelling of the aquaporin water selective filter by a gramicidin derivative. Biophys J 84(Suppl 2 Pt 2):349a
16. BM Burkhart N Li DA Langs WA Pangborn WL Duax 1998 The conducting form of gramicidin A is a right-handed double-stranded double helix Proc Natl Acad Sci USA 95 12950 12955 9789021 10.1073/pnas.95.22.12950 1:CAS:528:DyaK1cXntFWktLo%3D (Pubitemid 28509504)
17. DD Busath 1993 The use of physical methods in determining gramicidin channel structure and function Annu Rev Physiol 55 473 501 7682046 10.1146/annurev.ph.55.030193.002353 1:CAS:528:DyaK3sXkvVGisr4%3D (Pubitemid 23102142)
18. Y Chen BA Wallace 1997 The effects of calcium ions on double-helical forms of gramicidin Eur Biophys J 26 299 306 9378098 10.1007/s002490050084 1:CAS:528:DyaK2sXmvVSisrg%3D (Pubitemid 27402533)
19. A Chernyshev KM Armstrong S Cukierman 2003 Proton transfer in gramicidin channels is modulated by the thickness of monoglyceride bilayers Biophys J 84 238 250 12524278 10.1016/S0006-3495(03)74845-0 1:CAS:528:DC%2BD3sXisVSgsA%3D%3D (Pubitemid 36026393)
20. TA Cross AS Arseniev BA Cornell JH Davis JA Killian RE Koeppe LK Nicholson F Separovic BA Wallace 1999 Gramicidin channel controversy-revisited Nat Struct Biol 6 610 611 10404210 10.1038/10650 1:CAS:528:DyaK1MXksVentbc%3D
21. AE Daily JH Kim DV Greathouse OS Andersen RE Koeppe 2010 Polar groups in membrane channels: consequences of replacing alanines with serines in membrane-spanning gramicidin channels Biochemistry 49 6856 6865 20695525 10.1021/bi100857g 1:CAS:528:DC%2BC3cXpt12hsr8%3D
22. BL de Groot DP Tieleman P Pohl H Grubmuller 2002 Water permeation through gramicidin A: desformylation and the double helix: a molecular dynamics study Biophys J 82 2934 2942 12023216 10.1016/S0006-3495(02)75634-8 (Pubitemid 34547636)
23. JT Durkin LL Providence RE Koeppe OS Andersen 1992 Formation of non-beta 6.3-helical gramicidin channels between sequence-substituted gramicidin analogues Biophys J 62 145 157 1376164 10.1016/S0006-3495(92)81801-5 1:CAS:528:DyaK38Xlt1KmtLs%3D
24. EA Dutseva YN Antonenko EA Kotova JR Pfeifer U Koert 2007 Sensitized photoinactivation of minigramicidin channels in bilayer lipid membranes Biochim Biophys Acta 1768 1230 1237 17306219 10.1016/j.bbamem.2007.01.006 1:CAS:528:DC%2BD2sXkt1ejs7c%3D (Pubitemid 46550352)
25. BG Dzikovski PP Borbat JH Freed 2011 Channel and nonchannel forms of spin-labeled gramicidin in membranes and their equilibria J Phys Chem B 115 176 185 21142163 10.1021/jp108105k 1:CAS:528:DC%2BC3cXhsFGlu7zL
26. F Gambale A Menini G Rauch 1987 Effects of calcium on the gramicidin A single channel in phosphatidylserine membranes. Screening and blocking Eur Biophys J 14 369 374 2439324 10.1007/BF00262322 1:CAS:528:DyaL2sXlvFeitrc%3D (Pubitemid 17079171)
27. MC Goodall 1971 Thickness dependence in the action of gramicidin A on lipid bilayers Arch Biochem Biophys 147 129 135 4329858 10.1016/0003-9861(71) 90318-3 1:CAS:528:DyaE38XjtVyisA%3D%3D
28. 2+-gramicidin A interactions and blocking effects on the ionic channel Biophys Chem 18 153 163 6194829 10.1016/0301-4622(83)85010-8 1:CAS:528:DyaL3sXlsFeqtb0%3D
29. SB Hladky DA Haydon 1984 Ion movements in gramicidin channels Curr Topics Membr Transp 21 327 372 1:CAS:528:DyaL2MXhs1aht74%3D
30. - ions in micellar-packaged gramicidin A Biochim Biophys Acta 1238 12 21 7544623 10.1016/0005-2736(95)00094-J
31. TL Jones R Fu F Nielson TA Cross DD Busath 2010 Gramicidin channels are internally gated Biophys J 98 1486 1493 20409467 10.1016/j.bpj.2009.11.055 1:CAS:528:DC%2BC3cXht1Wnsr3F
32. RR Ketchem W Hu TA Cross 1993 High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR Science 261 1457 1460 7690158 10.1126/science.7690158 1:CAS:528:DyaK3sXlvVWhsLo%3D (Pubitemid 23334269)
33. RR Ketchem B Roux TA Cross 1997 High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR-derived orientational constraints Structure 5 1655 1669 9438865 10.1016/S0969-2126(97)00312-2 1:CAS:528:DyaK1cXmtVaisw%3D%3D (Pubitemid 28051978)
34. JA Killian KU Prasad D Hains DW Urry 1988 The membrane as an environment of minimal interconversion. A circular dichroism study on the solvent dependence of the conformational behavior of gramicidin in diacylphosphatidylcholine model membranes Biochemistry 27 4848 4855 2458757 10.1021/bi00413a040 1:CAS:528:DyaL1cXktF2jsrY%3D
35. RE Koeppe OS Andersen 1996 Engineering the gramicidin channel Annu Rev Biophys Biomol Struct 25 231 258 8800470 10.1146/annurev.bb.25.060196.001311 1:CAS:528:DyaK28Xjslyis7o%3D (Pubitemid 26197499)
36. A Kusel Z Khattari PE Schneggenburger A Banerjee T Salditt U Diederichsen 2007 Conformation and Interaction of a D,L-alternating peptide with a bilayer membrane: x-ray reflectivity, CD, and FTIR spectroscopy ChemPhysChem 8 2336 2343 17935092 10.1002/cphc.200700477
37. DA Langs 1988 Three-dimensional structure at 0.86 Å of the uncomplexed form of the transmembrane ion channel peptide gramicidin A Science 241 188 191 2455345 10.1126/science.2455345 1:CAS:528:DyaL1cXkvVygu70%3D
38. AL Lomize VI Orekhov AS Arseniev 1992 Refinement of the spatial structure of the gramicidin A ion channel Bioorg Khim 18 182 200 1376600 1:CAS:528:DyaK38XhvV2ks7c%3D
39. GL Mattice RE Koeppe LL Providence OS Andersen 1995 Stabilizing effect of d-alanine2 in gramicidin channels Biochemistry 34 6827 6837 7538788 10.1021/bi00020a029 1:CAS:528:DyaK2MXls1yrs7c%3D
40. N Mobashery C Nielsen OS Andersen 1997 The conformational preference of gramicidin channels is a function of lipid bilayer thickness FEBS Lett 412 15 20 9257681 10.1016/S0014-5793(97)00709-6 1:CAS:528:DyaK2sXks12murY%3D (Pubitemid 27309991)
41. JS Morrow WR Veatch L Stryer 1979 Transmembrane channel activity of gramicidin A analogs: effects of modification and deletion of the amino-terminal residue J Mol Biol 132 733 738 93642 10.1016/0022-2836(79)90386-3 1:CAS:528:DyaE1MXmtVGqsr4%3D
42. P Mueller DO Rudin HT Tien WC Wescott 1963 Methods for the formation of single bimolecular lipid membranes in aqueous solution J Phys Chem 67 534 535 1:CAS:528:DyaF3sXmsl2muw%3D%3D
43. R Neutze E Pebay-Peyroula K Edman A Royant J Navarro EM Landau 2002 Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport Biochim Biophys Acta 1565 144 167 12409192 10.1016/S0005-2736(02) 00566-7 1:CAS:528:DC%2BD38Xot1ajtLo%3D (Pubitemid 35284472)
44. RW Roeske TP Hrinyo-Pavlina RS Pottorf T Bridal XZ Jin DD Busath 1989 Synthesis and channel properties of [Tau 16]gramicidin A Biochim Biophys Acta 982 223 227 2473780 10.1016/0005-2736(89)90058-8 1:CAS:528:DyaL1MXlt12ju7g%3D (Pubitemid 19177656)
45. TI Rokitskaya YN Antonenko EA Kotova 1993 The interaction of phthalocyanine with planar lipid bilayers-photodynamic inactivation of gramicidin channels FEBS Lett 329 332 335 7689977 10.1016/0014-5793(93)80248-S 1:CAS:528:DyaK3sXlslKlu7w%3D (Pubitemid 23252750)
46. TI Rokitskaya YN Antonenko EA Kotova 1996 Photodynamic inactivation of gramicidin channels: a flash-photolysis study Biochim Biophys Acta 1275 221 226 8695636 10.1016/0005-2728(96)00025-4 (Pubitemid 26248992)
47. TK Rostovtseva VM Aguilella I Vodyanoy SM Bezrukov VA Parsegian 1998 Membrane surface-charge titration probed by gramicidin A channel conductance Biophys J 75 1783 1792 9746520 10.1016/S0006-3495(98)77620-9 1:CAS:528:DyaK1cXmsVCktLg%3D (Pubitemid 28455174)
48. SM Saparov YN Antonenko RE Koeppe P Pohl 2000 Desformylgramicidin: a model channel with an extremely high water permeability Biophys J 79 2526 2534 11053127 10.1016/S0006-3495(00)76493-9 1:CAS:528:DC%2BD3cXotFegt7w%3D
49. PE Schneggenburger S Mullar B Worbs C Steinem U Diederichsen 2010 Molecular recognition at the membrane-water interface: controlling integral peptide helices by off-membrane nucleobase pairing J Am Chem Soc 132 8020 8028 20481532 10.1021/ja1006349 1:CAS:528:DC%2BC3cXmt12ms7o%3D
50. P Schramm HJ Hofmann 2010 Double helix formation in alpha-peptides: a theoretical study J Pept Sci 16 276 283 20474039 1:CAS:528:DC%2BC3cXmtVyrsLo%3D
51. SA Seoh DD Busath 1993 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 1817 1827 7507714 10.1016/S0006-3495(93) 81239-6 1:CAS:528:DyaK2cXhvVGnurg%3D (Pubitemid 23334849)
52. F Separovic J Gehrmann T Milne BA Cornell SY Lin R Smith 1994 Sodium ion binding in the gramicidin a channel. Solid-state NMR studies of the tryptophan residues Biophys J 67 1495 1500 7529584 10.1016/S0006-3495(94)80623-X 1:CAS:528:DyaK2MXhtVGnsr4%3D (Pubitemid 24304322)
53. F Separovic S Barker M Delahunty R Smith 1999 NMR structure of C-terminally tagged gramicidin channels Biochim Biophys Acta 1416 48 56 9889316 10.1016/S0005-2736(98)00207-7 1:CAS:528:DyaK1MXivVWntg%3D%3D (Pubitemid 29065424)
54. F Separovic JA Killian M Cotten DD Busath TA Cross 2011 Modeling the membrane environment for membrane proteins Biophys J 100 2073 2074 21504744 10.1016/j.bpj.2011.02.058 1:CAS:528:DC%2BC3MXkvVKhsL0%3D
55. SW Siu RA Bockmann 2009 Low free energy barrier for ion permeation through double-helical gramicidin J Phys Chem B 113 3195 3202 19708166 10.1021/jp810302k 1:CAS:528:DC%2BD1MXhvFSmurs%3D
56. R Smith DE Thomas F Separovic AR Atkins BA Cornell 1989 Determination of the structure of a membrane-incorporated ion channel. Solid-state nuclear magnetic resonance studies of gramicidin A Biophys J 56 307 314 2476189 10.1016/S0006-3495(89)82677-3 1:CAS:528:DyaL1MXls12murw%3D (Pubitemid 19200926)
57. TB Stoilova EA Dutseva AA Pashkovskaya SV Sychev SI Kovalchuk AA Sobko NS Egorova EA Kotova YN Antonenko AY Surovoy VT Ivanov 2007 Ion channels of various types induced in lipid membranes by gramicidin A derivatives carrying a cationic sequence at their C-termini Bioorg Khim 33 511 519 18050656 1:STN:280:DC%2BD2sjit1OgsA%3D%3D
58. M Strassle G Stark 1992 Photodynamic inactivation of an ion channel: gramicidin A Photochem Photobiol 55 461 463 1373241 10.1111/j.1751-1097.1992. tb04262.x 1:STN:280:DyaK383itVymug%3D%3D
59. FR Svensson P Lincoln B Norden EK Esbjorner 2011 Tryptophan orientations in membrane-bound gramicidin and melittin-a comparative linear dichroism study on transmembrane and surface-bound peptides Biochim Biophys Acta 1808 219 228 20951675 10.1016/j.bbamem.2010.10.004 1:CAS:528:DC%2BC3cXhsFart7vE
60. SV Sychev LI Barsukov VT Ivanov 1993 The double pi pi 5.6 helix of gramicidin A predominates in unsaturated lipid membranes Eur Biophys J 22 279 288 7504620 10.1007/BF00180262 1:CAS:528:DyaK2cXktVensbg%3D (Pubitemid 23337925)
61. SV Sychev SV Sukhanov LI Barsukov VT Ivanov 1996 Structural polymorphism of gramicidin A channels: ion conductivity and spectral studies J Pept Sci 2 141 156 9231323 10.1002/psc.59 1:CAS:528:DyaK28Xjtl2qu7s%3D (Pubitemid 126507441)
62. G Szabo DW Urry 1979 N-acetyl gramicidin: single-channel properties and implications for channel structure Science 203 55 57 83000 10.1126/science.83000 1:CAS:528:DyaE1MXhtFKksbc%3D (Pubitemid 9112448)
63. DW Urry 1971 The gramicidin A transmembrane channel: a proposed pi(L,D) helix Proc Natl Acad Sci USA 68 672 676 5276779 10.1073/pnas.68.3.672 1:CAS:528:DyaE3MXhtlGgsb0%3D
64. WR Veatch ET Fossel ER Blout 1974 The conformation of gramicidin A Biochemistry 13 5249 5256 4139971 10.1021/bi00723a001 1:CAS:528: DyaE2MXmvFCgtQ%3D%3D
65. BA Wallace 1998 Recent advances in the high resolution structures of bacterial channels: gramicidin A J Struct Biol 121 123 141 9618340 10.1006/jsbi.1997.3948 1:CAS:528:DyaK1cXjslGht7s%3D (Pubitemid 28361441)
66. BA Wallace K Ravikumar 1988 The gramicidin pore: crystal structure of a cesium complex Science 241 182 187 2455344 10.1126/science.2455344 1:CAS:528:DyaL1cXltVKksLY%3D
67. GA Woolley BA Wallace 1992 Model ion channels: gramicidin and alamethicin J Membr Biol 129 109 136 1279177 1:CAS:528:DyaK38XlvVKktrY%3D
68. GA Woolley AS Jaikaran Z Zhang S Peng 1995 Design of regulated ion channels using measurements of cis-trans isomerization in single molecules J Am Chem Soc 117 4448 4454 10.1021/ja00121a002 1:CAS:528:DyaK2MXltVygtLk%3D
69. GA Woolley V Zunic J Karanicolas AS Jaikaran AV Starostin 1997 Voltage-dependent behavior of a "ball-and-chain" gramicidin channel Biophys J 73 2465 2475 9370440 10.1016/S0006-3495(97)78275-4 1:CAS:528:DyaK2sXntFyltrc%3D (Pubitemid 27471455)
70. S Yoshikawa K Muramoto K Shinzawa-Itoh 2011 Proton-pumping mechanism of cytochrome C oxidase Annu Rev Biophys 40 205 223 21545285 10.1146/annurev- biophys-042910-155341 1:CAS:528:DC%2BC3MXnvFaitbc%3D