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Dependence of Lipid Chain and Head Group Packing of the Inverted Dependence of lipid chain and headgroup packing of the inverted hexagonal phase on hydration James R. Scherer Western Regional Research Center, Agricultural Research Service, United States Department of Agriculture, Albany, Californa 94710; and Laboratory of Connective Tissue Biochemistry, School of Dentistry, University of California, San Francisco, California 94143-0515 ABSTRACT A model which positions the the same boundary. Placement of the distances between hydrophobic hydrophobic/hydrophilic boundary in boundary within the lipid structure per- boundaries shows that the fluid chains phosphatidylethanolamine lipids at the mits a determination of the maximum are interdigitated between adjacent first CH2 group in the acyl or alkyl chain headgroup packing at hydration levels tubes, and not interdigitated in the cen- is used to calculate the surface area down to complete dehydration. The tral space between three tubes. At low per lipid, the mean chain and head- headgroup dimensions are consistent hydration the chains interdigitate in group dimensions and diameters of the with a 5 A diam void at the center of a both spaces. The number of lipids hydrophilic tubes of the inverted hex- hydrophilic tube at zero hydration. The packed around a tube at low hydration agonal phase of didodecylphosphati- calculated mean fluid chain length is .2 is only a function of the headgroup dylethanolamine. The calculated sur- A smaller than the mean chain length of geometry, whereas at high hydration, it face areas compare favorably with the lamellar phase at comparable lev- is a function of the number of carbon areas obtained for the lamellar liquid els of hydration. Comparison of the atoms in the chains. crystal phase of the same lipid using calculated mean fluid chain length and INTRODUCTION Recent work by White and King (1985), McIntosh and Simon (1986), and Scherer (1987, 1989) has clearly The interaction of water with lipids has been studied shown that the position of the hydrophobic/hydrophilic using a variety of techniques (Hauser, 1975). Generally, boundary of phospholipids in the lamellar phases should water affects the structural integrity and biological func- be placed near the average position of the first CH2 tion of lipid membranes in complex ways. Phosphatidyl- groups of the hydrocarbon chain instead of the outer edge choline (PC) and phosphatidylethanolamine (PE) lipids, of the lipid headgroup, as assumed in the Luzzati primary constituents of many biological membranes, formalism (1968). The position of the boundary has been exhibit differences in water affinity (Elworthy, 1961; shown to affect the dependence of the head and chain Jendrasiak and Hasty, 1974) that are remarkable in view length dimensions on hydration. of the seemingly minor replacement of three methyl In the following, the headgroup and chain length groups for three hydrogen atoms. dimensions of the HI, phase of didodecylphosphatidyl- Besides having an apparent lower affinity for water, PE ethanolamine (DDPE) and the surface area, S, are deter- membranes have a tendency to form nonlamellar struc- mined from the x-ray data of Seddon et al. (1984), using tures that seem antithetic to the bilayer structure which is the same boundary assumed for the lamellar phase of so common in biological membranes (Cullis and DDPE (Scherer, 1989). It will be shown that the calcu- DeKruijff, 1979). One such structure is the inverted lated dimensions of the fluid chains at maximum hydra- hexagonal phase HI, (Verkleij, 1984). Unlike the bilayer, tion require that they be interdigitated in the regions where hydrophilic headgroups cover both surfaces of a between adjacent tubes and not interdigitated in the hydrocarbon blanket, the headgroups of the HI, phase line central region between three tubes. At zero hydration the the surfaces of a hexagonal array of tubes that extend chains are interdigitated in both regions. The headgroup through a hydrocarbon filled volume (Luzzati, 1968). packing at maximum and minimum hydration may be Also in contrast, the lamellar to HI, phase transition obtained from calculated surface area and shape. temperature is lowered by a decrease in the hydration of the headgroups or lengthening of the acyl chains (Seddon et al., 1983), and phase stability is increased by disorder Volumetrics of the H,, phase in the acyl chains (Mantsch et al., 1981). As for the lamellar phase, the boundary between the hydrocarboir and hydrophilic regions is set at the average position of the C-2 carbon atom of the acyl chain of an Address correspondence to 1309 Arch St., Berkeley, CA 94708. ester PE or the first CH2 group in the alkyl chain for an Biophys. J. e Biophysical Society 0006-3495/89/05/965/07 $2.00 965 Volume 55 1989 965-971 ether PE. The total volume (per lipid) is divided into a hydrophobic and hydrophilic part. V-= Vh,C + VH. (1) By defining the area per lipid, S, at the hc/H boundary, S may be compared with S for the bilayer at all hydrations. The approach introduced by Luzzati (1968), places the boundary at the end of the lipid headgroup, and leads to values of S that are progressively smaller than the value of S for the bilayer at maximum hydration, and 0 A2 at complete dehydration (Seddon, 1984). S is related to the 0 10 20 30 volumes by n V 2d2S/ xf-rdH (2) FIGURE 1 The calculated variation of S with hydration for the H, phase of DDPE (1350C); the La phases of DMPC (370C), EPC (room VH = dHS/4 temperature), and DDPE (400C); and the L, phases of DMPC (10°C) and DDPE (290C). The dashed curve is obtained by extrapolation of the and curve above n = 4 and is preferred from a consideration of headgroup packing below n = 4 (see text). Vhc = d.S, (4) where d is the x-ray long spacing, dH the diameter of the hydrophilic tube, and nonhydrated PE group. Wilkinson and Nagle (1981) have found the value of VPE for acyl chain lipids to be 246 A3. d. = 2d2/ l3rdH - dH/4. (5) In the case of DDPE, the value of VPE is smaller by the d* represents the average (fluid) chain length if all chains volume of two carbonyl groups which, according to Bondi were fit into extended volumes with uniform cross sec- (1964), is 39 A3. Subtracting this from the volume of VPE tional areas S/2. The value of d. for chains that are not for an acyl chain lipid gives an estimate of 207 A3 for VPE extensively interdigitated should be between b 2d/ of a diether PE. VH is obtained by adding the volume of 3 - dH/2 and c d/ x3- dH/2. Rewriting Eq. 5, we the PE portion of the headgroup to the volume of water in obtain the headgroup, 2 dH/2 -d. + (d + 2d2/ X3T.)I/2 (6) VH = V(1 - 0) + VPE = n VW + VPE (1 1) Assuming that the volume of the hydrocarbon phase is and S is obtained from independent of hydration, 6VhC/3n = 0, where n is the S = (2 V3r VVH) /2/d. number of water molecules per lipid, (12) The change in d spacing of DDPE with hydration was ad.bn = -(d.I/S)bS/n (7) determined by Seddon et al., 1984. The dependence of the and calculated values of S, d., b, c, and dH/2 on hydration is shown in Figs. 1-3. For comparison, the corresponding dimensions of S, dhc/2, and dH/2 for the lamellar phases = 2(1/V + l/VH)-1 (bln d/ln + bln S/ln), (8) of dismyristoyl phosphatidylcholine (DMPC), egg phos- where Vw is the partial molar volume of water. Vw and the phatidylcholine (EPC) and DDPE are also shown.' An illustration of the PE bilayer and the PE phase partial specific volume of lipid ivl are assumed to be Hi, independent of hydration. Consequently, the total volume (enveloped by a bilayer) at minimum and maximum V is given by hydration is shown in Fig. 4. The average hydrocarbon chain lengths (dhC/2 and d.), hydrophilic tube diameters V = , Mr 102 4/4N (9) (dH), and lipid packing around the tubes are drawn scaled to the calculated dimensions. Head and chain packing or shown in this figure will be discussed in the following V= VPE + Vh. + nVW, section. where 0 is the volume fraction of lipid, (1 + [1 -c]3Vw/ cv,)- , c is the weight fraction of lipid, and V. is the 'Labeling of the polymorphic phases of lipids follows the accepted volume of a water molecule. VPE is the volume of a conventions defined by Tardieu et al., 1973. Volume 55 May 1989~~~~~~~~~~ 966 966 Biophysical Journal Volume 55 May 1989 18 r Ip DDPE 14 DDMPC, La DMPC -U = _ ~~~~b 10 d. Hi, DDPE 6 0I 10 20 30 n FIGURE 2 The calculated variation of dh,/2, d., b, and c with hydration for the HI, phase of DDPE, and lamellar phases of DMPC, EPC, and DDPE. Conditions are consistent with those listed in Fig. 1. The dashed line for the HI, phase of DDPE shows the result of assuming that 6S/bn has a constant value equal to that indicated by the dashed line in Fig. 1. RESULTS AND DISCUSSION CH2 chain dimensions We begin by considering the calculated dimensions of the CH2 chains given by the solid lines in Fig. 2. We note that the values of c (half the hydrocarbon distance between adjacent tubes) increase by little more than 1 A going from maximum to zero hydration. The values for b are FIGURE 4 Illustration of the calculated structure for the HI, phase of DDPE at zero and maximum and the essentially invariant over the same range. This behavior (above) (below) hydration bilayer structures Lg (n = 3) and L,, (n = 12) for DDPE.
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