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. 1998 Apr;74(4):1937–1948. doi: 10.1016/S0006-3495(98)77902-0

Electrochemical measurement of lateral diffusion coefficients of ubiquinones and plastoquinones of various isoprenoid chain lengths incorporated in model bilayers.

D Marchal 1, W Boireau 1, J M Laval 1, J Moiroux 1, C Bourdillon 1
PMCID: PMC1299536  PMID: 9545054

Abstract

The long-range diffusion coefficients of isoprenoid quinones in a model of lipid bilayer were determined by a method avoiding fluorescent probe labeling of the molecules. The quinone electron carriers were incorporated in supported dimyristoylphosphatidylcholine layers at physiological molar fractions (<3 mol%). The elaborate bilayer template contained a built-in gold electrode at which the redox molecules solubilized in the bilayer were reduced or oxidized. The lateral diffusion coefficient of a natural quinone like UQ10 or PQ9 was 2.0 +/- 0.4 x 10(-8) cm2 s(-1) at 30 degrees C, two to three times smaller than the diffusion coefficient of a lipid analog in the same artificial bilayer. The lateral mobilities of the oxidized or reduced forms could be determined separately and were found to be identical in the 4-13 pH range. For a series of isoprenoid quinones, UQ2 or PQ2 to UQ10, the diffusion coefficient exhibited a marked dependence on the length of the isoprenoid chain. The data fit very well the quantitative behavior predicted by a continuum fluid model in which the isoprenoid chains are taken as rigid particles moving in the less viscous part of the bilayer and rubbing against the more viscous layers of lipid heads. The present study supports the concept of a homogeneous pool of quinone located in the less viscous region of the bilayer.

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Selected References

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  1. Balcom B. J., Petersen N. O. Lateral diffusion in model membranes is independent of the size of the hydrophobic region of molecules. Biophys J. 1993 Aug;65(2):630–637. doi: 10.1016/S0006-3495(93)81106-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bassolino-Klimas D., Alper H. E., Stouch T. R. Solute diffusion in lipid bilayer membranes: an atomic level study by molecular dynamics simulation. Biochemistry. 1993 Nov 30;32(47):12624–12637. doi: 10.1021/bi00210a010. [DOI] [PubMed] [Google Scholar]
  3. Blackwell M. F., Gounaris K., Zara S. J., Barber J. A method for estimating lateral diffusion coefficients in membranes from steady-state fluorescence quenching studies. Biophys J. 1987 May;51(5):735–744. doi: 10.1016/S0006-3495(87)83400-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blackwell M. F., Whitmarsh J. Effect of integral membrane proteins on the lateral mobility of plastoquinone in phosphatidylcholine proteoliposomes. Biophys J. 1990 Nov;58(5):1259–1271. doi: 10.1016/S0006-3495(90)82466-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brian A. A., McConnell H. M. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6159–6163. doi: 10.1073/pnas.81.19.6159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Castresana J., Alonso A., Arrondo J. L., Goñi F. M., Casal H. The physical state of ubiquinone-10, in pure form and incorporated into phospholipid bilayers. A Fourier-transform infrared spectroscopic study. Eur J Biochem. 1992 Mar 15;204(3):1125–1130. doi: 10.1111/j.1432-1033.1992.tb16737.x. [DOI] [PubMed] [Google Scholar]
  7. Chazotte B., Hackenbrock C. R. Lateral diffusion as a rate-limiting step in ubiquinone-mediated mitochondrial electron transport. J Biol Chem. 1989 Mar 25;264(9):4978–4985. [PubMed] [Google Scholar]
  8. Chazotte B., Hackenbrock C. R. The multicollisional, obstructed, long-range diffusional nature of mitochondrial electron transport. J Biol Chem. 1988 Oct 5;263(28):14359–14367. [PubMed] [Google Scholar]
  9. Chazotte B., Wu E. S., Hackenbrock C. R. The mobility of a fluorescent ubiquinone in model lipid membranes. Relevance to mitochondrial electron transport. Biochim Biophys Acta. 1991 Jul 5;1058(3):400–409. doi: 10.1016/s0005-2728(05)80136-7. [DOI] [PubMed] [Google Scholar]
  10. Cornell B. A., Keniry M. A., Post A., Robertson R. N., Weir L. E., Westerman P. W. Location and activity of ubiquinone 10 and ubiquinone analogues in model and biological membranes. Biochemistry. 1987 Dec 1;26(24):7702–7707. doi: 10.1021/bi00398a025. [DOI] [PubMed] [Google Scholar]
  11. Fato R., Battino M., Degli Esposti M., Parenti Castelli G., Lenaz G. Determination of partition and lateral diffusion coefficients of ubiquinones by fluorescence quenching of n-(9-anthroyloxy)stearic acids in phospholipid vesicles and mitochondrial membranes. Biochemistry. 1986 Jun 3;25(11):3378–3390. doi: 10.1021/bi00359a043. [DOI] [PubMed] [Google Scholar]
  12. Fato R., Battino M., Parenti Castelli G., Lenaz G. Measurement of the lateral diffusion coefficients of ubiquinones in lipid vesicles by fluorescence quenching of 12-(9-anthroyl)stearate. FEBS Lett. 1985 Jan 7;179(2):238–242. doi: 10.1016/0014-5793(85)80526-3. [DOI] [PubMed] [Google Scholar]
  13. Galla H. J., Hartmann W., Theilen U., Sackmann E. On two-dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes. J Membr Biol. 1979 Jul 31;48(3):215–236. doi: 10.1007/BF01872892. [DOI] [PubMed] [Google Scholar]
  14. Gupte S., Wu E. S., Hoechli L., Hoechli M., Jacobson K., Sowers A. E., Hackenbrock C. R. Relationship between lateral diffusion, collision frequency, and electron transfer of mitochondrial inner membrane oxidation-reduction components. Proc Natl Acad Sci U S A. 1984 May;81(9):2606–2610. doi: 10.1073/pnas.81.9.2606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson M. E., Berk D. A., Blankschtein D., Golan D. E., Jain R. K., Langer R. S. Lateral diffusion of small compounds in human stratum corneum and model lipid bilayer systems. Biophys J. 1996 Nov;71(5):2656–2668. doi: 10.1016/S0006-3495(96)79457-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kalb E., Frey S., Tamm L. K. Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers. Biochim Biophys Acta. 1992 Jan 31;1103(2):307–316. doi: 10.1016/0005-2736(92)90101-q. [DOI] [PubMed] [Google Scholar]
  17. Lenaz G., Samorì B., Fato R., Battino M., Parenti Castelli G., Domini I. Localization and preferred orientations of ubiquinone homologs in model bilayers. Biochem Cell Biol. 1992 Jun;70(6):504–514. doi: 10.1139/o92-078. [DOI] [PubMed] [Google Scholar]
  18. Marchal D., Boireau W., Laval J. M., Moiroux J., Bourdillon C. An electrochemical approach of the redox behavior of water insoluble ubiquinones or plastoquinones incorporated in supported phospholipid layers. Biophys J. 1997 Jun;72(6):2679–2687. doi: 10.1016/S0006-3495(97)78911-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Parpaleix T., Laval J. M., Majda M., Bourdillon C. Potentiometric and voltammetric investigations of H2/H+ catalysis by periplasmic hydrogenase from Desulfovibrio gigas immobilized at the electrode surface in an amphiphilic bilayer assembly. Anal Chem. 1992 Mar 15;64(6):641–646. doi: 10.1021/ac00030a013. [DOI] [PubMed] [Google Scholar]
  20. Rajarathnam K., Hochman J., Schindler M., Ferguson-Miller S. Synthesis, location, and lateral mobility of fluorescently labeled ubiquinone 10 in mitochondrial and artificial membranes. Biochemistry. 1989 Apr 18;28(8):3168–3176. doi: 10.1021/bi00434a009. [DOI] [PubMed] [Google Scholar]
  21. Rich P. R. Electron and proton transfers through quinones and cytochrome bc complexes. Biochim Biophys Acta. 1984 Apr 9;768(1):53–79. doi: 10.1016/0304-4173(84)90007-7. [DOI] [PubMed] [Google Scholar]
  22. Saffman P. G., Delbrück M. Brownian motion in biological membranes. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3111–3113. doi: 10.1073/pnas.72.8.3111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Seelig J., Seelig A. Lipid conformation in model membranes and biological membranes. Q Rev Biophys. 1980 Feb;13(1):19–61. doi: 10.1017/s0033583500000305. [DOI] [PubMed] [Google Scholar]
  24. Stidham M. A., McIntosh T. J., Siedow J. N. On the localization of ubiquinone in phosphatidylcholine bilayers. Biochim Biophys Acta. 1984 Dec 18;767(3):423–431. doi: 10.1016/0005-2728(84)90040-9. [DOI] [PubMed] [Google Scholar]
  25. Tocanne J. F., Dupou-Cézanne L., Lopez A. Lateral diffusion of lipids in model and natural membranes. Prog Lipid Res. 1994;33(3):203–237. doi: 10.1016/0163-7827(94)90027-2. [DOI] [PubMed] [Google Scholar]
  26. Torchut E., Laval J. M., Bourdillon C., Majda M. Electrochemical measurements of the lateral diffusion of electroactive amphiphiles in supported phospholipid monolayers. Biophys J. 1994 Mar;66(3 Pt 1):753–762. doi: 10.1016/s0006-3495(94)80851-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ulrich E. L., Girvin M. E., Cramer W. A., Markley J. L. Location and mobility of ubiquinones of different chain lengths in artificial membrane vesicles. Biochemistry. 1985 May 7;24(10):2501–2508. doi: 10.1021/bi00331a016. [DOI] [PubMed] [Google Scholar]
  28. Vaz W. L., Clegg R. M., Hallmann D. Translational diffusion of lipids in liquid crystalline phase phosphatidylcholine multibilayers. A comparison of experiment with theory. Biochemistry. 1985 Jan 29;24(3):781–786. doi: 10.1021/bi00324a037. [DOI] [PubMed] [Google Scholar]
  29. Venable R. M., Zhang Y., Hardy B. J., Pastor R. W. Molecular dynamics simulations of a lipid bilayer and of hexadecane: an investigation of membrane fluidity. Science. 1993 Oct 8;262(5131):223–226. doi: 10.1126/science.8211140. [DOI] [PubMed] [Google Scholar]
  30. Wilson M. A., Pohorille A. Molecular dynamics of a water-lipid bilayer interface. J Am Chem Soc. 1994;116(4):1490–1501. doi: 10.1021/ja00083a038. [DOI] [PubMed] [Google Scholar]
  31. von Tscharner V., McConnell H. M. Physical properties of lipid monolayers on alkylated planar glass surfaces. Biophys J. 1981 Nov;36(2):421–427. doi: 10.1016/S0006-3495(81)84741-8. [DOI] [PMC free article] [PubMed] [Google Scholar]

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