Structural determinants of the packing and electrostatic behavior of unsaturated phosphoglycerides

Abstract

Docosahexaenoic acid-containing phosphoglycerides accumulate preferentially in membranes of the retina, brain, and spermatozoa, but the functional significance of this largely remains to be determined. Previously we compared the physical properties of homogeneous monolayers of these and other phosphoglyceride species to obtain insights into their physiological roles. Particularly noteworthy were the unusually low dipole moments of species having sn-2-docosahexaenoyl chains. In this study, we have investigated the electrostatic and lateral packing properties of related phosphoglycerides and found that: 1), The dipole moment-lowering effect of the docosahexaenoyl group arises from its having a Z double bond at chain position n-3. 2), The large dipole moment-lowering effects at sn-1 of an ether bond to an alkyl or a 1Z alkenyl chain and that of a sn-2-esterified n-3 fatty acid are additive. 3), The 1Z double bond in an alkenyl chain lowers the molecular area of a phosphoglyceride and, concomitantly, makes it less compressible. 4), Ethanolamine-containing phosphoglycerides are generally less compressible than their corresponding choline analogs. Our data showing that relatively small lipid structural changes markedly alter lipid physical properties in fluid phases underscores the need to study the function of peripheral and integral membrane proteins in the presence of appropriate lipid species.

FIGURE 1

Typical liquid-expanded surface pressure-area and dipole potential-concentration isotherms showing the origin of measured and calculated descriptors. Shown are representative experimental points obtained with DhDhPE. Solid lines are obtained by fitting π-A and ΔV₋₁/A data as described in Materials and Methods over the range of data indicated by the range of the line. Descriptors depicted are the dehydrated lipid molecular area, (A_∞); the modulus of compression, (); the lipid area-independent component of the dipole potential, (ΔV₀); and the perpendicular component of the lipid dipole moment (μ_⊥ = [dΔV/d(1/A)]/37.7).

FIGURE 2

Effect of Z double bond position on the dipole moment of otherwise identical sn-2-docosapentaenoyl phosphoglyceride molecular species. The Z-double bond closest to the chain terminal carbon (n) was either n-3 (Dp3) or n-6 (Dp6). The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Table 4.

FIGURE 3

Effect of the linkage of the 18-carbon sn-1 substituent on the dipole moment of otherwise identical phosphoglyceride molecular species. Values of μ_⊥ for alkyl ether (sn-1-Od) PCs and PEs (•) and alkenyl ether (sn-1-Oe) species of PEs (▪) and PCs (□) are plotted against those of the corresponding ester (sn-1-S) species. The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Tables 3 and 4.

FIGURE 4

Effect of the linkage of the 18-carbon sn-1 substituent on the area-independent potential of otherwise identical phosphoglyceride molecular species. Values of ΔV₀ for alkenyl ether (sn-1-Oe) species of PCs (▪) and alkenyl ether (sn-1-Oe) species of PEs plus alkyl ether species of PEs and PCs (○) are plotted against those of the corresponding ester (sn-1-S) species. The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Tables 3 and 4.

FIGURE 5

Effect of the sn-3 phosphoglyceride headgroup on the limiting molecular area of otherwise identical phosphoglyceride species. Values of A_∞ for PE species having an n-3 acyl chain at sn-2 (▪), n-6 sn-2-acyl chain and sn-1-S or sn-1-Od (•), n-6 sn-2-acyl chain and sn-1-Od (○), and n-9 sn-2-acyl chain and sn-1-S or -Oe (Δ) are plotted against those of the corresponding PC species. The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Tables 2–4.

FIGURE 6

Effect of the linkage of the 18-carbon sn-1 substituent on the hydrated area at 35 mN/m of otherwise identical phosphoglyceride molecular species. Values of A₃₅-A_∞ for species having either an ether (sn-1-Od) (○) or vinyl ether (sn-1-Oe) (▪) linkage are plotted against those of the corresponding acyl (sn-1-S) species. The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Tables 3 and 4.

FIGURE 7

Effect of the sn-3 phosphoglyceride headgroup on the modulus of compression at 35 mN/m of otherwise identical phosphoglyceride species. Values of for PE species are plotted against those of corresponding PC species for phosphoglycerides having an 18-carbon substituent (S, Od, or Od; ▪) or Dh (▴) at sn-1. The dotted line is a line of identity (intercept = 0, slope = 1). Data are from Tables 2–4.

FIGURE 8

Effect of the dipole moment of a phosphoglyceride species on its lipid area-independent dipole potential. Values of ΔV₀ for PCs having an sn-1ester or ether (S, Dh, Od; •), PCs having an sn-1 alkenyl ether (Oe, ▪), PEs having an sn-1 ester or ether (S, Dh, Od; □), PEs having an sn-1 alkenyl ether (Oe, ○) or PSs having an sn-1 ester (S, Dh; ▴) are plotted against the μ_⊥ of the same species. The solid lines are least-squares fit lines through each data set. Data are from Tables 2–4 and (16).

FIGURE 9

Relationship between the water activity parameter of a phosphoglyceride species and its compressibility at 35 mN/m. Values of dπ/dA₃₅, the slope of the π-A isotherm of a phosphoglyceride at 35mN/m, are plotted against the value of f₁ for that species. The line shows a least-squares fit of the data taken from Tables 2–4.