LIPID BILAYER DYNAMICS FROM SIMULTANEOUS ANALYSIS OF ORIENTATION AND FREQUENCY-DEPENDENCE OF DEUTERIUM SPIN-LATTICE AND QUADRUPOLAR ORDER RELAXATION

Simultaneous analysis of the deuterium (H-2) NMR spin relaxation rates of lipid bilayers as a function of both frequency and sample orientat ion may be decisive in evaluating different models for the dynamics of membranes. Angular dependent H-2 spin-lattice (R-1Z) and quadrupolar order (R-1Q) H-2 relaxation rates have been measured at 46.1 and 76.8 MHz for macroscopic ally oriented bilayers of 1, diperdeuteriomyristoy l-sn-glycero-3-phosphocholine (DMPC-d(54)), with perdeuterated acyl ch ains, in the liquid-crystalline (L-alpha) state. The data have been si multaneously fitted to various dynamical models, together with frequen cy dependent H-2 R-1Z data for vesicles of specifically H-2-labeled DM PC. The same mechanism for the nuclear spin relaxation in lipids has b een assumed for both oriented bilayers and vesicles, except for the pr esence of orientational averaging and a possible contribution from ves icle tumbling in the latter case. A noncollective model describing ind ividual molecular reorientations in the presence of a potential of mea n torque is able to adequately account for the orientation dependence; however, the quality of the fits to the frequency dispersion is less satisfactory. By contrast, a three-dimensional director fluctuation mo del accounts for the frequency dispersion for DMPC vesicles, but does not fit the orientation dependence of the R-1Z and R-1Q relaxation dat a. Higher-order director fluctuations have also been included, which d o not significantly improve the quality of the fits to the collective model. Therefore, a composite membrane model is proposed including bot h noncollective molecular motions and director fluctuations. The model adequately describes both the frequency and orientation dependent dat a along the entire acyl chain simultaneously, which suggests that both dynamical processes can be detected by analyzing the H-2 NMR relaxati on rates in the MHz range. Quantitative information about the bilayer dynamics including lipid reorientation rates, degree of molecular orde ring, relative contributions from collective and noncollective motions , and director-frame spectral densities of motion has been obtained. T he results suggest the bilayer dynamics in the MHz regime reflect mole cular reorientations that are superimposed onto nematiclike deformatio ns of the membrane interior in the liquid crystalline state.