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Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals

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Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals LBNL-42162 |BERKELEY LAB] Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals Mei Hong Materials Sciences Division RECEIVE MAR 1 8 1999 May 1996 Ph.D. Thesis OSTS DISCLAIMER This document was prepared as an account of work sponsored by the United States Government. While this document is believed to contain correct information, neither the United States Government nor any agency thereof, nor The Regents of the University of California, nor any of their employees, makes any warranty, express or implied, or assumes any legal responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed, or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process, or service by its trade name, trademark, manufacturer, or otherwise, does not necessarily constitute or imply its endorsement, recommendation, or favoring by the United States Government or any agency thereof, or The Regents of the University of California. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or any agency thereof, or The Regents of the University of California. Ernest Orlando Lawrence Berkeley National Laboratory is an equal opportunity employer. DISCLAIMER Portions of this document may be illegible in electronic image products. Images are produced from the best available original document. LBNL-42162 Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals Mei Hong Ph.D. Thesis Department of Chemistry University of California, Berkeley and Materials Sciences Division Ernest Orlando Lawrence Berkeley National Laboratory University of California Berkeley, CA 94720 May 1996 This work was supported by the Director, Office of Energy Research, Office of Basic Energy Sciences, Materials Sciences Division, of the U.S. Department of Energy under Contract No. DE-AC03-76SF00098. Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals by Mei Hong B.A. (Mount Holyoke College) 1992 A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Chemistry in the GRADUATE DIVISION of the UNIVERSITY OF CALIFORNIA, BERKELEY Committee in charge: Professor Alexander Pines, Chair Professor Paul Alivisatos Professor Jeffrey A. Reimer 1996 Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals Copyright© 1996 by Mei Hong The U.S. Department of Energy has the right to use this document for any purpose whatsoever including the right to reproduce all or any part thereof Abstract Two-Dimensional NMR Investigations of the Dynamic Conformations of Phospholipids and Liquid Crystals by Mei Hong Doctor of Philosophy in Chemistry University of California, Berkeley Professor Alexander Pines, Chair Two-dimensional 13C, JH and 31P nuclear magnetic resonance (NMR) techniques are developed and used to study molecular structure and dynamics in liquid-crystalline systems, primarily phospholipids and nematic liquid crystals. NMR spectroscopy characterizes molecular conformation in terms of orientations and distances of molecular segments. In anisotropically mobile systems, this is achieved by measuring motionally-averaged nuclear dipolar couplings and chemical shift anisotropies. The short-range couplings yield useful bond order parameters, while the long-range interactions constrain the overall conformation. In this work, techniques for probing proton dipolar local fields are further developed to obtain highly- resolved dipolar couplings between protons and rare spins. By exploiting variable-angle sample spinning techniques, orientation-sensitive NMR spectra are resolved according to site- specific isotropic chemical shifts. Moreover, the signs and magnitudes of various short-range dipolar couplings are obtained. They are used in novel theoretical analyses that provide information about segmental orientations and their distributions. Such information is obtained in a model-independent fashion or with physically reasonable assumptions. The structural investigation of phospholipids is focused on the dynamic conformations of the headgroup and glycerol backbone of liquid-crystalline phosphocholine. Several structural features are identified, including the headgroup bend from the glycerol backbone, the 1 relative stiffness of the glycerol and its adjacent segments, the proximity of the headgroup a segment to the sn-2 chain carboxyl group, and the estimated relative populations of various headgroup conformations. Constrained by the dipolar couplings and chemical shift anisotropies measured here and NMR data from the literature, a new single-conformation model is proposed for the core of the phosphocholine molecule. In the nematic liquid crystal ^pentyM'-biphenylcarbonitrile, both short- and long- range dipolar couplings between carbons and protons are obtained. The directly-bonded dipolar couplings allow bond order parameters to be calculated for the aromatic core of the molecule, thus providing information on the conformational order of the molecule. For the first time, long-range dipolar couplings are resolved and assigned, yielding a large number of new constraints for structural modeling of this system. To Klaus TABLE OF CONTENTS CHAPTER 1 INTRODUCTION 1 CHAPTER 2 THEORY OF SOLID-STATE NMR 3 2.1 Nuclear Spin Interactions 3 2.2 Semiclassical Description of NMR - Magnetization 6 2.3 Quantum Mechanical Description of NMR - Density Operator 9 2.4 Two-Dimensional Fourier NMR 14 2.5 Powder Lineshapes - Orientation Dependence in Solid-State NMR 21 2.6 Sample Spinning - Averaging in Physical Space 26 2.7 Average Hamiltonian Theory - Averaging in Spin Space 29 2.8 Proton-Detected Local Field Spectroscopy 36 CHAPTER 3 PROPERTIES OF LIQUID-CRYSTALLINE PHOSPHOLIPIDS 43 3.1 Biological Importance 43 3.2 Chemical Structure 45 3.3 Organized Assemblies 48 3.4 Physical Techniques for Studying Phospholipids 51 3.5 Computer Simulations of Phospholipid Conformation and Dynamics 52 3.6 NMR Techniques for Studying Phospholipids 53 2H Quadrupolar Couplings 53 31P Chemical Shifts 54 13C Chemical Shifts 55 !HNMR 56 CHAPTER 4 THEORY OF ORDER TENSOR FOR PHOSPHOLIPIDS AND LIQUID CRYSTALS 60 4.1 Effects of Liquid Crystallinity on Phospholipid NMR Spectra 60 4.2 Derivation of Order Tensor 63 IV 4.3 Phenomenological Description of Order Tensor 68 4.4 Relation Between Order Tensor and Order Parameter 69 4.5 Strategies for Determining Order Tensors 72 4.6 Orientation Distributions from Order Tensors 74 4.7 Probability Limits from Bond Order Parameters 80 Model-Independent Probabilities from Negative Order Parameters 80 Probability Limits under the Assumption of Broadening 84 Probability Limits from Positive Order Parameters 86 Model-Independent Probabilities from Chemical Shift Anisotropies 89 CHAPTER 5 NMR MEASUREMENTS OF PHOSPHOCHOLINE LIPIDS 91 5.1 General Experimental Conditions 91 Materials 91 Sample Preparation 92 NMR Measurements 93 5.2 Short-Range 13C-]H Dipolar Couplings 95 5.3 Long-Range 13C-!H Dipolar Couplings 104 5.4 31p_lH Dipolar Couplings Ill 5.5 iH-lH Dipolar Couplings 116 5.6 31P-13C Dipolar Couplings ..' 123 5.7 13C-13C Dipolar Couplings 125 5.8 Determination of Dipolar Coupling Signs by DISTINCT NMR 129 DISTINCT with Proton-Detected-Local-Field Evolution 130 Effects of Powder Average 133 DISTINCT with Carbon-Detected-Local-Field Evolution 140 5.9 13C Chemical Shift Anisotropies 143 5.10 31P and *H Chemical Shifts 147 5.11 Summary of NMR Order Parameters in Lecithin 152 CHAPTER 6 PHOSPHOCHOLINE STRUCTURE IN THE HEADGROUP AND GLYCEROL BACKBONE 160 6.1 Acyl Chain Order and Mobility 160 6.2 Glycerol Rigidity 162 6.3 Rotational Axes Orientations 163 v 6.4 Headgroup and Acyl Chain Bends 167 6.5 Enantiomeric Headgroup Conformations 169 Evidence of Headgroup Exchange 169 Populations of Headgroup Conformers 172 General Requirements for C-H Degeneracies in Liquid-Crystalline Systems 174 6.6 Single-Conformation Model for Phosphocholine Core 176 6.7 Order Tensor of P Segment 179 CHAPTER 7 DETERMINATION OF C-H DIPOLAR COUPLINGS IN LIQUID CRYSTALS 181 7.1 Introduction 181 7.2 Experimental Conditions 183 7.3 Measurement of C-H Dipolar Couplings 188 7.4 Qualitative Assignment of Long-Range C-H Couplings 195 7.5 Quantitative Assignment of Long-Range C-H Couplings 198 7.6 Order Parameters from Short-Range C-H Couplings 204 7.7 Experimental Precision and Accuracy 207 7.8 Summary 208 APPENDICES 211 A 4-spin density matrix evolution 211 B Equivalence of Motional Averaging in Fast Motional Limit 213 C Epsilon Motor Controller System 215 D Computer Programs 217 Model-Independent Orientation Probabilities from a Negative Order Parameter 218 Orientation Distributions from Segmental Order Tensors 222 VI LIST OF FIGURES Figure 2.1 Larmor precession of a magnetic moment in a magnetic field 8 Figure 2.2 NMR powder spectra of polycrystalline solids 26 Figure 2.3 (a) PDLF and (b) SLF pulse sequences 38 Figure 2.4 Schematic (a) PDLF and (b) SLF stick spectra 39 Figure 3.1 Three main types of membrane structural lipids 46 Figure 3.2 Organized phospholipid assemblies 50 Figure 4.1 La-lecithin 31P single-pulse chemical shift spectrum 60 Figure 4.2 Schematic of phospholipid bilayers 61 Figure 4.3 La-lecithin 31P cross-polarized chemical shift spectrum 62 Figure 4.4 Dipolar spectra of a rigid solid and an anisotropically-mobile
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