Proton magnetic resonance spectroscopic studies of the interaction of ubiquinone‐10 with phospholipid model membranes

Abstract

Proton magnetic resonance spectra of ubiquinone-10 and ubiquinone-10 dispersed with dipalmitoylglycerophosphocholine or egg phosphatidylcholine in aqueous medium have been obtained. The dispersions are in the form of multilamellar liposomes as judged by 31P-NMR spectra and the thermal history of the samples have ensured that ubiquinone not incorporated into the phospholipid structure only gives rise to a broad-line NMR proton spectrum. A high-resolution proton spectrum of ubiquinone is observed with upfield shifts of the 0-methyl protons of the benzoquinone rings, indicating close proximity of the molecules but with an arrangement different from the pure liquid ubiquinone. Spectra obtained in the presence of the lanthanide shift reagents, dysprosium fluorooctanedionate and Dy(NO&, which have a preferred location in the hydrophobic and hydrophilic domains, respectively, of ubiquinone/phospholipid codispersions, are consistent with the partitioning of ubiquinone into a hydrophobic phospholipid environment remote from the aqueous phase. The type of arrangements of ubiquinone that could be accomodated within bilayers of phospholipid are discussed.Ubiquinone is an integral component of mitochondria1 electron transport chains, where it is believed to function as a mobile carrier of electrons and protons through the hydrophobic domain of the energy-transducing membrane [l -41. The coenzyme can be classified as a lipid because the fully substituted benzoquinone ring and polyisoprene chain, numbering usually about ten units, renders the molecule soluble in solvents of low polarity [5]. These properties imply that the ubiquinone will be located predominantly within the hydrophobic domain of the membrane although some workers have suggested that there is binding of the molecule to specific membrane proteins [6-81, which may influence their disposition in the structure.Attempts to define the location of ubiquinones in model membrane systems have not been altogether conclusive. A variety of physicochemical approaches have been adopted including ultraviolet spectroscopy [9], fluorescence probes [lo, 111, nuclear magnetic resonance [12, 131 and electronspin resonance spectroscopy [14, 151, differential scanning calorimetry [16, 171, X-ray diffraction [18], and monomolecular film techniques [I9 -211. There seems to be general agreement that short-chain homologues of ubiquinone, i.e. with polyisoprenoid chains shorter than five units, are intercalated between the molecules of a phospholipid bilayer. The location of the longer-chain, physiologically relevant homologues in membranes is, however, conjectural. It has been argued that because long-chain ubiquinones are able to translocate electrons across phospholipid bilayers the benzoquinone-ring substituent must be accessible to the lipid/water interface at either side of the bilayer. Models to account for this process

Electrochemical modeling of electron and proton transfer to ubiquinone-10 in a self-assembled phospholipid monolayer

“…-0.8 -0.4 0 DISCUSSION A variety of techniques have been applied to understand the physical organization and orientation of UQ in a membrane, but a general consensus among researchers has yet to emerge. The most widely accepted model suggests that the isoprene tail and the quinone ring lie in the midplane of the bilayer (Quinn and Esfahani, 1980;Katsikas and Quinn, 1982a;Ondarroa and Quinn, 1986;Ulrich et al, 1984;Cornell et al, 1987), whereas another model places the isoprene tail in the midplane but the headgroup in the polar head region, where it can have access to the membrane surface (Mitchell, 1976;Stidham et al, 1984). The view is widely accepted that a large fraction of UQ segregates within the membrane into a phase that is not constrained by the ordered chains of the membrane lipid, but there is disagreement regarding the UQ mole fraction beyond which such a segregation occurs.…”

Tuning ubiquinone position in biomimetic monolayer membranes

“…The swimming position of UQ is more stable and confers higher lateral diffusion [31,32] than the diving position, which is explained by the fact that the hydrophobic interactions between lipid chains are not disturbed by the presence of UQ besides the lower viscosity of the hydrocarbon tails in the midplain compared to the polar head region [33,34]. The "swimming" position has been confirmed using several techniques like fluorescence quenching [35], voltammetric techniques [30,36], performing surface-pressure isotherms [22,26,27], nuclear magnetic resonance [22,[37][38][39][40][41][42], differential infrared spectroscopy [21], DSC [18,20,43,44], neutron diffraction [45], surface-enhanced infrared adsorption spectroscopy [28] and linear dicroism [25].…”

Electron Transport Lipids Fold Within Membrane-Like Interfaces

“…Briefly, there is no consensus regarding the location of UQ-10 with its locations spanning the entire width of the membrane bilayer leaflet. Out of these studies, three schools of thought have emerged; the quinone headgroup is located: 1) at or near the lipid headgroups ( Kingsley and Feigenson, 1981 ; Stidham et al, 1984 ; Lenaz et al, 1992 ; Salgado et al, 1993 ; Galassi and Arantes, 2015 ; Gómez-Murcia et al, 2016 ; Kaurola et al, 2016 ; Quirk et al, 2016 ; Teixeira and Arantes, 2019 ), 2) within the acyl chains ( Michaelis and Moore, 1985 ; Cornell et al, 1987 ; Chazotte et al, 1991 ; Salgado et al, 1993 ; Metz et al, 1995 ; Afri et al, 2004 ; Hauss et al, 2005 ), or 3) within the bilayer midplane ( Ulrich et al, 1985 ; Ondarroa and Quinn, 1986 ; Soderhall and Laaksonen, 2001 ) ( Figure 2 ). Even though the location of the headgroup is controversial, the field does seem to agree that at least part of the isoprenyl side chain is embedded within the bilayer midplane, and the headgroup is thought to extend into one of the membrane leaflets.…”