Electrogenic proton transport across lipid bilayer membranes mediated by cationic derivatives of rhodamine 19: Comparison with anionic protonophores

European Biophysics Journal

Volumn 42, Issue 6, 2013, Pages 477-485

  Rokitskaya, Tatyana I ^a   Ilyasova, Tatyana M ^a   Severina, Inna I ^a   Antonenko, Yuri N ^a   Skulachev, Vladimir P ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Bilayer lipid membrane; Dipole potential; Protonophore; SkQR1; Uncoupling activity

Indexed keywords

ANION; CATION; LIPID; PLASTOQUINONE; PROTON; RHODAMINE;

ARTICLE; CELL MEMBRANE; CHEMICAL MODEL; CHEMISTRY; ELECTRODE; ESCHERICHIA COLI; LIPID BILAYER; MEMBRANE POTENTIAL; METABOLISM; PH;

ANIONS; CATIONS; CELL MEMBRANE; ELECTRODES; ESCHERICHIA COLI; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; LIPIDS; MEMBRANE POTENTIALS; MODELS, CHEMICAL; PLASTOQUINONE; PROTONS; RHODAMINES;

EID: 84878599026     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-013-0898-9     Document Type: Article

References (36)

1. Andersen OS, Finkelstein A, Katz I (1976) Effect of phloretin on the permeability of thin lipid membranes. J Gen Physiol 67:749-771
2. Antonenko YN, Avetisyan AV, Bakeeva LE, Chernyak BV, Chertkov VA, Domnina LV, Ivanova OYu, Izyumov DS, Khailova LS, Klishin SS, Korshunov SS, Korshunova GA, Kovaleva NA, Lyamzaev KG, Muntyan MS, Nepryakhina OK, Pashkovskaya AA, Pletjushkina OY, Pustovidko AV, Rokitskaya TI, Ruuge EK, Saprunova VB, Severina II, Simonyan RA, Skulachev IV, Skulachev MV, Sumbatyan NV, Sviryaeva IV, Tashlitsky VN, Tikhomirova NK, Vassiliev YM, Vyssokikh MY, Yaguzhinsky LS, Skulachev VP (2008) Mitochondria-targeted derivative of plastoquinone as tool to interrupt execution of an aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc) 73:1273-1287
3. Antonenko YN, Avetisyan AV, Cherepanov DA, Knorre DA, Korshunova GA, Markova OV, Ojovan SM, Perevoshchikova IV, Pustovidko AV, Rokitskaya TI, Severina II, Simonyan RA, Smirnova EA, Sobko AA, Sumbatyan NV, Severin FF, Skulachev VP (2011) Derivatives of rhodamine 19 as mild mitochondria-targeted cationic uncouplers. J Biol Chem 286:17831-17840
4. Antonenko YN, Perevoshchikova IV, Rokitskaya TI, Simonyan RA, Tashlitsky VV, Skulachev VP (2012) Effect of liposomes on energy-dependent uptake of the antioxidant SkQR1 by isolated mitochondria. J Bioenerg Biomembr 44:453-460
5. Balaz S, Sturdik E, Durcova E, Antalik M, Sulo P (1986) Quantitative structure-activity relationship of carbonylcyanide phenylhydrazones as uncouplers of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 851:93-98
6. Benz R, McLaughlin S (1983) The molecular mechanism of action of the proton ionophore FCCP (carbonylcyanide p-trifluoromethoxyphenylhydrazone). Biophys J 41:381-398
7. Berkovich AK, Lukashev EP, Melik-Nubarov NS (2012) Dipole potential as a driving force for the membrane insertion of polyacrylic acid in slightly acidic milieu. Biochim Biophys Acta 1818:375-383
8. Blaikie FH, Brown SE, Samuelsson LM, Brand MD, Smith RA, Murphy MP (2006) Targeting dinitrophenol to mitochondria: limitations to the development of a self-limiting mitochondrial protonophore. Biosci Rep 26:231-243
9. Borisova MP, Ermishkin LN, Liberman EA, Silberstein AY, Trofimov EM (1974) Mechanism of conductivity of bimolecular lipid membranes in the presence of tetrachlorotrifluoromethylbenzimidazole. J Membr Biol 18:243-261
10. Brockman H (1994) Dipole potential of lipid membranes. Chem Phys Lipids 73:57-79
11. Cunha FM, Caldeira da Silva CC, Cerqueira FM, Kowaltowski AJ (2011) Mild mitochondrial uncoupling as a therapeutic strategy. Curr Drug Targets 12:783-789
12. Duvvuri M, Gong Y, Chatterji D, Krise JP (2004) Weak base permeability characteristics influence the intracellular sequestration site in the multidrug-resistant human leukemic cell line HL-60. J Biol Chem 279:32367-32372
13. Franklin JC, Cafiso DS (1993) Internal electrostatic potentials in bilayers: measuring and controlling dipole potentials in lipid vesicles. Biophys J 65:289-299
14. Gawrisch K, Ruston D, Zimmerberg J, Parsegian VA, Rand RP, Fuller N (1992) Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. Biophys J 61:1213-1223
15. Hall JE, Mead CA, Szabo G (1973) A barrier model for current flow in lipid bilayer membranes. J Membr Biol 11:75-97
16. Hladky SB (1974) The energy barriers to ion transport by nonactin across thin lipid membranes. Biochim Biophys Acta 352:71-85
17. Il'yasova TM, Rokitskaya TI, Severina II, Antonenko YN, Skulachev VP (2012) Substitution of ether linkage for ester bond in phospholipid increases permeability of bilayer lipid membrane for SkQ1-type penetrating cations. Biochemistry (Mosc) 77:1038-1043
18. Kasianowicz J, Benz R, McLaughlin S (1984) The kinetic mechanism by which CCCP (carbonyl cyanide m-chlorophenylhydrazone) transports protons across membranes. J Membr Biol 82:179-190
19. Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15-18
20. Langner M, Isac T, Hui SW (1995) Interaction of free fatty acids with phospholipid bilayers. Biochim Biophys Acta 1236:73-80
21. LeBlanc OH (1971) Effect of uncouplers of oxidative phosphorylation on bilayer membranes: carbonylcyanide-m-chlorophenylhydrazone. J Membr Biol 4:227-251
22. Liberman EA, Topaly VP (1969) Permeability of biomolecular phospholipid membranes for fat-soluble ions. Biofizika 14:452-461
23. Lou PH, Hansen BS, Olsen PH, Tullin S, Murphy MP, Brand MD (2007) Mitochondrial uncouplers with an extraordinary dynamic range. Biochem J 407:129-140
24. McLaughlin S (1972) The mechanism of action of DNP on phospholipid bilayer membranes. J Membr Biol 9:361-372
25. Mueller P, Rudin DO, Tien HT, Wescott WC (1963) Methods for the formation of single bimolecular lipid membranes in aqueous solution. J Phys Chem 67:534-535
26. Nagamune H, Fukushima Y, Takada J, Yoshida K, Unami A, Shimooka T, Terada H (1993) The lipophilic weak base (Z)-5-methyl-2-[2-(1-naphthyl)ethenyl]-4- piperidinopyridine (AU-1421) is a potent protonophore type cationic uncoupler of oxidative phosphorylation in mitochondria. Biochim Biophys Acta 1141:231-237
27. O'Shaughnessy K, Hladky SB (1983) Transient currents carried by the uncoupler, carbonyl cyanide m-chlorophenylhydrazone. Biochim Biophys Acta 724:381-387
28. Pickar AD, Benz R (1978) Transport of oppositely charged lipophilic probe ions in lipid bilayer membranes having various structures. J Membr Biol 44:353-376
29. Ptak M, Egret-Charlier M, Sanson A, Bouloussa O (1980) A NMR study of the ionization of fatty acids, fatty amines and N-acylamino acids incorporated in phosphatidylcholine vesicles. Biochim Biophys Acta 600:387-397
30. Rokitskaya TI, Klishin SS, Severina II, Skulachev VP, Antonenko YN (2008) Kinetic analysis of permeation of mitochondria-targeted antioxidants across bilayer lipid membranes. J Membr Biol 224:9-19
31. Schwaller MA, Allard B, Lescot E, Moreau F (1995) Protonophoric activity of ellipticine and isomers across the energy-transducing membrane of mitochondria. J Biol Chem 270:22709-22713
32. Severin FF, Severina II, Antonenko YN, Rokitskaya TI, Cherepanov DA, Mokhova EN, Vyssokikh MY, Pustovidko AV, Markova OV, Yaguzhinsky LS, Korshunova GA, Sumbatyan NV, Skulachev MV, Skulachev VP (2010) Penetrating cation/fatty acid anion pair as a mitochondria-targeted protonophore. Proc Natl Acad Sci USA 107:663-668
33. Severina II (1982) Nystatin-induced increase in photocurrent in the system 'bacteriorhodopsin proteoliposome/bilayer planar membrane'. Biochim Biophys Acta 681:311-317
34. Skulachev VP (2007) A biochemical approach to the problem of aging: "megaproject" on membrane-penetrating ions. The first results and prospects. Biochemistry (Mosc) 72:1385-1396
35. Sun X, Garlid KD (1992) On the mechanism by which bupivacaine conducts protons across the membranes of mitochondria and liposomes. J Biol Chem 267:19147-19154
36. Von Tscharner V, Radda GK (1981) The effect of fatty acids on the surface potential of phospholipid vesicles measured by condensed phase radioluminescence. Biochim Biophys Acta 643:435-448