Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function

Boggs, Joan M.

doi:10.1016/0304-4157(87)90017-7

Cited by 709 publications

(489 citation statements)

References 321 publications

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“…A proton that is participating in a hydrogen bond will dissociate less easily, resulting in a higher pK a for the protonatable group (36)(37)(38).…”

Section: Discussionmentioning

confidence: 99%

What Makes the Bioactive Lipids Phosphatidic Acid and Lysophosphatidic Acid So Special?

et al. 2005

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Phosphatidic acid and lysophosphatidic acid are minor but important anionic bioactive lipids involved in a number of key cellular processes, yet these molecules have a simple phosphate headgroup.To find out what is so special about these lipids, we determined the ionization behavior of phosphatidic acid (PA) and lysophosphatidic acid (LPA) in extended (flat) mixed lipid bilayers using magic angle spinning 31 P NMR. Our data show two surprising results. First, despite identical phosphomonoester headgroups, LPA carries more negative charge than PA when present in a phosphatidylcholine bilayer. Dehydroxy-LPA [1-oleoyl-3-(phosphoryl)propanediol] behaves in a manner identical to that of PA, indicating that the difference in negative charge between LPA and PA is caused by the hydroxyl on the glycerol backbone of LPA and its interaction with the phosphomonoester headgroup. Second, deprotonation of phosphatidic acid and lysophosphatidic acid was found to be strongly stimulated by the inclusion of phosphatidylethanolamine in the bilayer, indicating that lipid headgroup charge depends on local lipid composition and will vary between the different subcellular locations of (L)PA. Our findings can be understood in terms of a hydrogen bond formed within the phosphomonoester headgroup of (L)PA and its destabilization by competing intra-or intermolecular hydrogen bonds. We propose that this hydrogen bonding property of (L)PA is involved in the various cellular functions of these lipids.Phosphatidic acid (PA) 1 and the related lipid lysophosphatidic acid (LPA) are important minor lipid species in the cell. They are involved in many intracellular processes, and are important intermediates in lipid biosynthesis (1). For example, binding of LPA to its receptors evokes various cellular responses, and the local formation of (L)PA is part of signaling cascades, in particular in the regulation of membrane dynamics such as fusion and fission events, either indirectly through the recruitment of downstream effectors or directly by mediating (local) changes in the biophysical properties of the membrane (2-12).PA and LPA have a relatively simple chemical structure consisting of only a glycerol, one (LPA) or two (PA) acyl chains, and a phosphate, and it is interesting to note that these simple phospholipids are involved in such diverse processes, and are able to bind specifically to so many different types of proteins (3, 13). The question then is what is so special about these lipids. An obvious suggestion relates to the phosphate headgroup, which is attached to the glycerol backbone as a phosphomonoester, a unique feature of these lipids. Phosphomonoesters have two pK a 's, one of which is expected to be in the physiological pH range. As a consequence, small changes in (physiological) pH will affect the charge and influence the molecular shape and lipid phase behavior of these lipids (14,15). Under physiological conditions at neutral pH, phosphatidic acid is a cone (type II)-shaped lipid with a negative spontaneous curvature clos...

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“…A proton that is participating in a hydrogen bond will dissociate less easily, resulting in a higher pK a for the protonatable group (36)(37)(38).…”

Section: Discussionmentioning

confidence: 99%

What Makes the Bioactive Lipids Phosphatidic Acid and Lysophosphatidic Acid So Special?

et al. 2005

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“…This specific region of the membrane is also known to participate in intermolecular charge interactions (Yeagle, 1987) and hydrogen bonding through the polar headgroup (Boggs, 1987;Gennis, 1989;Shin et al, 1991). These structural features which slow down the rate of solvent reorientation have previously been recognized as typical features of solvents giving rise to significant red edge effects (Itoh & Azumi, 1975).…”

Section: 'Vv Crlvhmentioning

confidence: 99%

Fluorophore environments in membrane-bound probes: A red edge excitation shift study

Chattopadhyay

Mukherjee²

1993

Biochemistry

141

158

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A shift in the wavelength of maximum fluorescence emission toward higher wavelengths, caused by a shift in the excitation wavelength toward the red edge of the absorption band, is termed the Red Edge Excitation Shift (REES). This effect is mostly observed with polar fluorophores in motionally restricted media such as very viscous solutions or condensed phases. In this paper, we report the red edge excitation shift of a membrane-bound phospholipid molecule whose headgroup is covalently labeled with a 7-nitrobenz-2-oxa-1,3-diazol-4-y1 (NBD) moiety. When incorporated into model membranes of dioleoyl-sn-glycero-3-phosphocholine (DOPC), the NBD-labeled phospholipid (NBD-PE), exhibits a red edge excitation shift of 10 nm. In addition, fluorescence polarization of NBD-PE in membranes shows both excitation and emission wavelength dependence. The nonpolar membrane probe 1,6-diphenyl-1,3,5-hexatriene (DPH) does not show red edge excitation shift in model membranes. The lifetime of NBD-PE in DOPC vesicles was found to be dependent on both excitation and emission wavelengths. These wavelength-dependent lifetimes are correlated to the reorientation of solvent dipoles around the excited-state dipole of the NBD moiety in the membrane. The magnitude of the red shift in the emission maximum for NBD-PE was found to be independent of temperature, between 12 and 54 O C , and of the physical state (gel or fluid) of the membrane. Taken together, these observations are indicative of the motional restriction experienced by this fluorophore in the membrane. Red edge excitation shift promises to be a powerful tool in probing membrane organization and dynamics.Organized molecular assemblies such as membranes can be considered as large cooperative units with characteristics very different from the individual structural units which constitute them. Fluorescence spectroscopy has been one of the principal techniques to study organization and dynamics of biological and model membranes because of its suitable time scale, noninvasive nature, and intrinsic sensitivity (Radda, 1975;Lakowicz, 1980Lakowicz, , 1981. For a fluorophore in a bulk nonviscous solvent, the dipolar relaxation of the solvent molecules around the fluorophore in the excited state is much faster than the fluorescence lifetime. The fluorescence decay rates and the wavelength of maximum emission, in such a case, are therefore usually independent of the excitation wavelength. However, these parameters do show excitation wavelength dependence if the dipolar relaxation of the solvent molecules is slow in the excited state, such that the relaxation time is comparable to or longer than the fluorescence lifetime (Chen, 1967;Fletcher, 1968;Galley & Purkey, 1970;Rubinov & Tomin, 1970;Castelli & Forster, 1973;Itoh & Azumi, 1975;Demchenko, 1982; Lakowicz & Keating-Nakamoto, 1984). Such a shift in the wavelength of maximum emission toward higher wavelengths, caused by a shift in the excitation wavelength toward the red edge of the absorption band, is termed the red edge excitatio...

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“…The sugar-containing lipids increase the hydrogen bonding capacity of the bilayer surface. The hydrogen bonding between the hydroxyls of the sugar rings and the surrounding water or the phospholipid neighbors [44,45] takes place and certainly contributes to structure stabilization of the membrane, minimizing the thermal disordering induced by high temperatures. Also, the anticancer drug tamoxifen and the insecticide DDT, which incorporate into the membranes of B. stearothermophilus [46,47] a¡ecting the physical state of bacterial lipids [20,46], signi¢cantly increase the PGL level [21,28].…”

Section: Lipid Composition Studiesmentioning

confidence: 99%

“…PE is prone to formation of nonlamellar structures like the reversed hexagonal phase [48]. The hexagonal phase propensity of a few membrane lipids is a localized property that relates to the fusion capacity of the membrane and regulates the activity of a variety of enzymes [44]. Under a variety of environmental circumstances, cells carefully balance the contents of lamellar phase-forming and hexagonal phase-forming lipids in membranes.…”

Section: Lipid Composition Studiesmentioning

confidence: 99%

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Lipid composition and dynamics of cell membranes of Bacillus stearothermophilus adapted to amiodarone

Rosa¹,

Antunes-Madeira²,

Matos³

et al. 2000

Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biolog

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Bacillus stearothermophilus, a useful model to evaluate membrane interactions of lipophilic drugs, adapts to the presence of amiodarone in the growth medium. Drug concentrations in the range of 1^2 WM depress growth and 3 WM completely suppresses growth. Adaptation to the presence of amiodarone is reflected in lipid composition changes either in the phospholipid classes or in the acyl chain moieties. Significant changes are observed at 2 WM and expressed by a decrease of phosphatidylethanolamine (relative decrease of 23.3%) and phosphatidylglycerol (17.9%) and by the increase of phosphoglycolipid (162%). The changes in phospholipid acyl chains are expressed by a decrease of straight-chain saturated fatty acids (relative decrease of 12.2%) and anteiso-acids (22%) with a parallel increase of the iso-acids (9.8%). Consequently, the ratio straight-chain/branched iso-chain fatty acids decreases from 0.38 (control cultures) to 0.30 (cultures adapted to 2 WM amiodarone). The physical consequences of the lipid composition changes induced by the drug were studied by fluorescence polarization of diphenylhexatriene and diphenylhexatriene-propionic acid, and by differential scanning calorimetry. The thermotropic profiles of polar lipid dispersions of amiodarone-adapted cells are more similar to control cultures (without amiodarone) than those resulting from a direct interaction of the drug with lipids, i.e., when amiodarone was added directly to liposome suspensions. It is suggested that lipid composition changes promoted by amiodarone occur as adaptations to drug tolerance, providing the membrane with physico-chemical properties compatible with membrane function, counteracting the effects of the drug. ß

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Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function

Cited by 709 publications

References 321 publications

What Makes the Bioactive Lipids Phosphatidic Acid and Lysophosphatidic Acid So Special?

What Makes the Bioactive Lipids Phosphatidic Acid and Lysophosphatidic Acid So Special?

Fluorophore environments in membrane-bound probes: A red edge excitation shift study

Lipid composition and dynamics of cell membranes of Bacillus stearothermophilus adapted to amiodarone

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