Skip to main content
SpringerLink
Log in

On coenzyme Q orientation in membranes: A linear dichroism study of ubiquinones in a model bilayer

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

A general approach is developed to interpret linear dichroism (LD) spectra of ubiquinones (Q n) in host bilayers. Information is reported in terms of guest-host mutual orientation and localization. The overall orientational anisotropy of guest ubiquinone molecules is described by a basic set of limiting orientation/localization modes. Assignments of the UV transitions of the ubiquinone chromophore were obtained by the liquid crystal-linear dichroism technique and molecular orbital (CNDO/S) calculations. The LD spectra of Q n in the bilayers provided by the lyotropic nematic mesophase exhibited by water solutions of potassium laurate and decanol were interpreted on the basis of the above assignments. The resulting experimental evidence showed a multisite distribution in the host bilayer for the aromatic heads of all the investigated Q n derivatives except Q0. The orientational distribution suggested by the LD spectra fits the solubilization model recently proposed by G. Lenaz [J. Membrane Biol. (1988) 104:193–209] for ubiquinone in lipid membranes. Within this model Q n molecules are located in the midplane and their headgroups oscillate transversally across the membrane. Q 0 instead has a single site location, close to the polar bilayer interface. Experimental evidence that the headgroup carbonyls tend to grasp the polar interface of the host bilayer was also obtained. Orientation and location distributions of Q n guest molecules are therefore likely to result from the tendency of their aromatic heads to grasp the polar heads of the host bilayer and from the concurrent tendency of their chains to settle into the hydrocarbon host interior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AA:

average absorption

OD∥, OD⊥ :

optical densities for plane polarized radiations parallel (∥) and perpendicular (⊥) to the sample optical axis

Δ OD:

OD∥ — OD⊥

EPR:

electron paramagnetic resonance

LC-LD:

liquid crystal-linear dichroism

LD:

linear dichroism

LD r :

reduced linear dichroism.

MO:

molecular orbital

N:

nematic

NMR:

nuclear magnetic resonance

S jj :

order parameters of the directions j of the transition moments of the guest chromophore

S ii :

order parameters of the orientational axes i of the guest molecule with respect to the magnetic field

S′ ii :

order parameters of the axes i of the guest molecules with respect to the bilayer axis a

S a :

order parameters of the host bilayer axis a with respect to the orienting magnetic field

θ j,i :

deflection angles between the directions j and the axes i

O i :

optical factors of the i axis see Eq. (A4)]

Qn :

ubiquinone whose isoprenoid chain contains n isoprenoid units

References

  • Albertini, G., Bossi, G., Dubini, B., Ponzi Bossi, M.G., Rustichelli, F. 1988. Structural analysis of the Γ phase in cholesterol-distearoylphosphatidyl choline multilamellar vesicles. Il Nuovo Cimento D 10:1385–1398

    Google Scholar 

  • Alonso, A., Gomez-Fernandez, J.C., Aranda, F.J., Belda, F.J.F., Goni, F. 1981. On the interaction of the ubiquinones with phospholipid bilayers. FEBS Lett. 132:19–22

    Google Scholar 

  • Battino, M., Domini, I., Fato, R., Lenaz, G., Marconi, G., Samorì, B. 1990. A linear dichroism approach to studies of ubiquinones in lyotropic bilayers. In: Highlights in Ubiquinone Research. G. Lenaz, O. Barnabei, A. Rabbi, M. Battino, editors. pp. 70–74. Taylor & Francis, London

    Google Scholar 

  • Battino, M., Fahmy, T., Lenaz, G. 1986. Determination of the critical micelle concentration of short-chain ubiquinones in model systems. Biochim. Biophys. Acta 851:377–384

    Google Scholar 

  • Charvolin, J. 1983. Polymorphism of interfaces. J. Chimie Phys. 80:15–23

    Google Scholar 

  • Charvolin, J., Hendrikx, Y. 1985. Amphiphilic molecules in lyotropic liquid crystal and micellar phases. In: Nuclear Magnetic Resonance of Liquid Crystals. J.W. Emsley, editor. pp. 449–471. Reidel, Dordrecht

    Google Scholar 

  • Chatelier, R.L., Sawyer, W.H. 1985. The transverse organization of ubiquinones in mitocondrial membranes as determined by fluorescence quenching. Evidence for a two-site model. Eur. Biophys. J. 11:179–185

    Google Scholar 

  • Cornell, B.A., Keniry, M.A., Post, A., Robertson, R.N., Weir, L.E., Westerman, P.W. 1987. Location and activity of ubiquinone 10 and ubiquinone analogues in model and biological membranes. Biochemistry 26:7702–7707

    Google Scholar 

  • Crane, F.L., Barr, R. 1985. Chemical structure and properties of Coenzyme Q and related compounds. In: Coenzyme Q. G. Lenaz, editor. pp. 1–37. John Wiley & Sons, Chichester

    Google Scholar 

  • Davidsson, A., Norden, B. 1976. Aspects on the conversion of Legrand-Grosjean circular dichroism spectrometers to linear dichroism detection. Chem. Scripta 9:49–53

    Google Scholar 

  • Degli Esposti, M., Bertoli, E., Parenti-Castelli, G., Fato, R., Mascarello, S., Lenaz, G., 1981. Incorporation of ubiquinone homologs into lipid vesicles and mitochondrial membranes. Arch. Biochem. Biophys. 210:21–32

    Google Scholar 

  • den Engelsen, D. 1972. Transmission ellipsometry and polarization spectrometry of thin layers. J. Phys. Chem. 76:3390–3397

    Google Scholar 

  • Dunlap, D., Samori, B., Bustamante, C. 1988. Why does synussoidally modulated polarization introduce a systematic error in linear dichroism measurements? In: Polarized Spectroscopy of Ordered Systems. B. Samorì and E.W. Thulstrup, editors. pp. 275–297. Kluwer Academic, Dordrecht.

    Google Scholar 

  • Erecinska, M., Blasie, K., Wilson, D.F. 1977. Orientation of the hemes of cytochrome c oxidase and cytochrome c in mitochondria. FEBS. Lett. 76:235–239

    Google Scholar 

  • Erecinska, M., Wilson, D.F., Blasie, J.K. 1978. Studies on the orientations of the mitochondrial redox carriers. I. Orientation of the hemes of the cytochrome oxidase with respect to the plane of a cytochrome oxidase lipid model membrane. Biochim. Biophys. Acta 501:53–62

    Google Scholar 

  • Fato, R., Battino, M., Degli Esposti, M., Parenti-Castelli, G., Lenaz, G. 1986. 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 25:3378–3390

    Google Scholar 

  • Figueiredo Neto, A.M., Liebert, L., Galerne, Y. 1985. Temperature and concentration range of the biaxial nematic lyomesophase in the mixture potassium laurate/1-decanol/D2O. J. Phys. Chem. 89:3737–3739

    Google Scholar 

  • Forni, A., Marconi, G., Moretti, I., Samori, B., Torre, G. 1989. Nucleic acids-drug interactions. The monomeric chromophores of netropsin and distamycins. Biopolymers 28:2161–2176

    Google Scholar 

  • Hendrikx, Y., Charvolin, Y., Rawiso, M., Liebert, M., Holmes, M.C. 1983. Anisotropie aggregates of amphiphilic molecules in lyotropic nematic phases. J. Phys. Chem. 87:3391–4005

    Google Scholar 

  • Hentschel, M., Hosemann, R. 1983. Small and wide angle X-ray scattering of oriented lecithin multilayers. Mol. Cryst. Liq. Cryst. 94:291–316

    Google Scholar 

  • Jacques, P., Faure, J., Chalvet, O., Jaffe, H.H. 1981. A reexamination of the oxigen parameters in the CNDO/method-application to UV and photoelectron spectra of p-benzoquinone. J. Phys. Chem. 85:473–479

    Google Scholar 

  • Jensen, H.P., Shellman, J.A., Troxell, T. 1978. Modulation techniques in polarization spectroscopy. Appl. Spectrosc. 32:192–200

    Google Scholar 

  • Johansson, L.B.A., Davidsson, A., Lindblom, G., Norden, B. 1978. Linear dichroism as a tool for studying molecular orientation in membrane systems. J. Phys. Chem. 82:2604–2609

    Google Scholar 

  • Johansson, L.B.A., Wikander, G., Lindblom, G., Davidsson, A. 1987. Linear dichroism of molecules with cubic symmetry. Chem. Phys. 112:373–378

    Google Scholar 

  • Katsikas, H., Quinn, P.J. 1982a. The polyisoprenoid chain length influences the interaction of ubiquinones with phospholipid bilayers. Biochim. Biophys. Acta 689:363–369

    Google Scholar 

  • Katsikas, H., Quinn, P.J. 1982b. The distribution of ubiquinone 10 in phospholipid bilayers. A study using differential scanning calorimetry. Eur. J. Biochem. 124:165–169

    Google Scholar 

  • Katsikas, H., Quinn, P.J. 1983. Fluorescence probe studies of the distribution of ubiquinone homologues in bilayers of dipalmitoylglycerophosphocholine. Eur. J. Biochem. 131:607–612

    Google Scholar 

  • Kingsley, P.B., Feigenson, G.W. 1981. H-NMR study of the localization and motion of ubiquinones in perdeuterated phosphatidylcholine bilayers. Biochim. Biophys. Acta 635:602–618

    Google Scholar 

  • Kutty, T.R.N., Fisher, A.G. 1983. Planar orientation of nematic liquid crystals by chemiadsorbed poly (vinylalcohol) surface layers. Mol. Cryst. Liq. Cryst. 99:301–318

    Google Scholar 

  • Laurent, M., Samorì, B. 1987. Linear dichroism of solute molecule within micelles. Preferred orientation and local ordering. J. Am. Chem. Soc. 109:5109–5113

    Google Scholar 

  • Lenaz, G. (Editor) 1985. Coenzyme Q. John Wiley & Sons, Chichester

    Google Scholar 

  • Lenaz, G. 1988. Role of mobility of redox components in the inner mitochondrial membrane. J. Membrane Biol. 104:193–209

    Google Scholar 

  • Lenaz, G., Degli Esposti, M. 1985. Physical properties of ubiquinones in model systems and membranes. In: Coenzyme Q. G. Lenaz, editor. pp. 83–105. John Wiley & Sons, Chichester

    Google Scholar 

  • Lenaz, G., Barnabei, O., Rabbi, A., Battino, M. editors. 1990. Highlights in Ubiquinone Research. Taylor & Francis, London

    Google Scholar 

  • Lenaz, G., Fato, R., Mandrioli, E. 1987. Localization and lateral diffusion of ubiquinone in the inner mitochondrial membrane. Chem. Scripts 27:139–144

    Google Scholar 

  • Michl, J., Thulstrup, E.W. 1987. Ultraviolet and infrared linear dichroism: Polarized light as a probe of molecular and electronic structure. Acc. Chem. Res. 20:192–199

    Google Scholar 

  • Michl, J., Thulstrup, E.W. 1988. Applications of IR and UV-visible linear dichroism. In: Polarized Spectroscopy of Ordered Systems. B. Samori and E.W. Thulstrup, editors. pp. 25–57. Kluwer Academic, Dordrecht

    Google Scholar 

  • Mitchell, P. 1976. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 62:327–367

    Google Scholar 

  • Norden, B. 1980. Simple formulas for dichroism analysis. Orientation of solutes in stretched polymer matrices. J. Chem. Phys. 72:5032–5038

    Google Scholar 

  • Norden, B., Lindblom, G., Ionàs, I. 1977, Linear dichroism spectroscopy as a tool for studying molecular orientation in model membrane systems. J. Phys. Chem. 81:2086–2093

    Google Scholar 

  • Ohno, K. 1964. Some remarks on the Pariser-Parr-Pople method. Theoret. Chim. Acta 2:219–227

    Google Scholar 

  • Quinn, P.J. 1990. Physico-chemical properties of ubiquinone-10. In: Highlights in Ubiquinone Research. G. Lenaz, O. Bernabei, A. Rabbi and M. Battino, editors. pp. 21–26. Taylor & Francis, London

    Google Scholar 

  • Ragan, I.C., Cottingham, I.R. 1985. The kinetics of quinone pools in electron transport. Biochim. Biophys. Acta 811:13–31

    Google Scholar 

  • Rajarathnam, K., Hochman, J., Schindler, M., Ferguson-Miller, S. 1989. Synthesis, location and lateral mobility of fluorescently labeled ubiquinone-10 in mitochondrial and artificial membranes. Biochemistry 28:3168–3176

    Google Scholar 

  • Sackmann, E., Mohwald, J. 1973. On optical polarization measurements in liquid crystals. J. Chem. Phys. 58:5407–5416

    Google Scholar 

  • Sale, L. 1966. The Molecular Orbital Theory of Conjugated Systems. Chap. 7, p. 453, W.A. Benjamin, Reading (MA)

    Google Scholar 

  • Samorì, B. 1979. Distortion of a cubic molecule in a liquid crystal by dichroic techniques. J. Phys. Chem. 83:375–378

    Google Scholar 

  • Samori, B. 1983. Applications of the modulated liquid crystal-linear dichroism (L.C.-L.D.) to spectro-and stereo-chemical problems. III. Mol. Cryst. Liq. Cryst. 98:395–397

    Google Scholar 

  • Samori, B. 1988. Liquid crystal-linear dichroism. Stereochemical applications of electronic state assignments. In: Polarized Spectroscopy of Ordered Systems. B. Samori and E.W. Thulstrup, editors. pp. 105–133. Kluwer Academic, Dordrecht

    Google Scholar 

  • Samorì, B., Mariani, P., Spada, G.P. 1982. The liquid crystal-linear dichroism of organic molecules by a modulation technique. J. Chem. Soc. Perkin Trans. 2:447–453

    Google Scholar 

  • Samorì, B., Mattivi, F. 1986. A new L.D. approach for determining solute orientation in anionic micelles. J. Am. Chem. Soc. 108:1679–1684

    Google Scholar 

  • Seelig, J., Borle, F., Cross, T.A. 1985. Magnetic ordering of phospholipid membranes. Biochim. Biophys. Acta 814:195–198

    Google Scholar 

  • Shellman, J.A. 1988. Polarization modulation spectroscopy. In: Polarized Spectroscopy of Ordered Systems. B. Samorì and E.W. Thulstrup, editors. pp. 231–275. Kluwer Academic, Dordrecht

    Google Scholar 

  • Stidham, M.A., McIntosh, T.J., Siedow, J.N. 1984. On the localization of ubiquinones in phosphatidylcholine bilayers. Biochim. Biophys. Acta 767:423–431

    Google Scholar 

  • Thulstrup, E.W., Michl, J., Eggers, J.H. 1970. Polarization spectroscopy in stretched polymer sheets. J. Phys. Chem. 74:3868–3878

    Google Scholar 

  • Trumpower, B.L. (Editor) 1983. Function of Quinones in Energy Conserving Systems. Academic, New York

    Google Scholar 

  • Ulrich, E.L., Girvin, M.C., Cramer, W.A., Markley, J.L. 1985. Location and mobility of ubiquinones of different chain lengths in artificial membrane vesicles. Biochemistry 24:2501–2508

    Google Scholar 

  • van Gurp, M., van Langen, H., van Ginkel, G., Levine, Y.K. 1988. Angle-resolved techniques in studies of organic molecules in ordered systems using polarized light. In: Polarized Spectroscopy of Ordered Systems. B. Samori and E.W. Thulstrup, editors. pp. 455–489. Kluwer Academic, Dordrecht

    Google Scholar 

  • Yu, C.A., Yu, L. 1981. Ubiquinone-binding proteins. Biochim. Biophys. Acta 639:99–128

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Chimica Organica, “A. Mangini,” Universitá, 40136, Bologna

    Bruno Samorì

  2. Dipartimento di Chimica, Università della Calabria, 87030, Arcavacata di Rende

    Bruno Samorì

  3. Dipartimento di Biochimica, 40126, Bologna

    Giorgio Lenaz

  4. Istituto di Biochimica, Università, Ancona

    Maurizio Battino

  5. CNR-FRAE, Bologna

    Giancarlo Marconi

  6. Dipartimento di Chimica Industriale e dei Materiali, Bologna, Italy

    Ida Domini

Authors
  1. Bruno Samorì
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giorgio Lenaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurizio Battino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giancarlo Marconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ida Domini
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dr. A. Rossi is gratefully acknowledged for the t.e.m. reduction of the spectra. Ubiquinone homologs were kind gifts from Eisai Co., Tokyo, Japan. This work was supported by M.U.R.S.T., and C.N.R. Target Project on Biotechnology and Bioinstrumentation, Rome, Italy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Samorì, B., Lenaz, G., Battino, M. et al. On coenzyme Q orientation in membranes: A linear dichroism study of ubiquinones in a model bilayer. J. Membarin Biol. 128, 193–203 (1992). https://doi.org/10.1007/BF00231812

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00231812

Key Words

Search

Navigation