Cyclic and Linear Monoterpenes in Phospholipid Membranes: Phase Behavior, Bilayer Structure, and Molecular Dynamics

Langmuir

Volumn 31, Issue 40, 2015, Pages 11067-11077

  Pham, Quoc Dat ^a   Topgaard, Daniel ^a   Sparr, Emma ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL SYSTEMS; DIFFERENTIAL SCANNING CALORIMETRY; ESSENTIAL OILS; LIPID BILAYERS; MOLECULAR DYNAMICS; PHOSPHOLIPIDS; X RAY SCATTERING;

ANTI-MICROBIAL ACTIVITY; COMPLEMENTARY TECHNIQUES; DIFFERENT WATER CONTENTS; HYDROPHOBIC MOLECULES; MELTING POINT DEPRESSIONS; SMALL AND WIDE ANGLE X RAY SCATTERINGS; SOLID-STATE NUCLEAR MAGNETIC RESONANCE; STRUCTURE AND DYNAMICS;

MONOTERPENES;

DIMYRISTOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; TERPENE;

CHEMISTRY; DIFFERENTIAL SCANNING CALORIMETRY; LIPID BILAYER; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RADIATION SCATTERING;

CALORIMETRY, DIFFERENTIAL SCANNING; DIMYRISTOYLPHOSPHATIDYLCHOLINE; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; MONOTERPENES; SCATTERING, RADIATION;

EID: 84944128628     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/acs.langmuir.5b00856     Document Type: Article

References (41)

1. Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M. Biological Effects of Essential Oils-A Review Food Chem. Toxicol. 2008, 46, 446-475 10.1016/j.fct.2007.09.106
2. Hyldgaard, M.; Mygind, T.; Meyer, R. L. Essential Oils in Food Preservation: Mode of Action, Aynergies, and Interactions with Food Matrix Components Front. Microbiol. 2012, 3, 12 10.3389/fmicb.2012.00012
3. Lucera, A.; Mastromatteo, M.; Sinigaglia, M.; Corbo, M. R. Combined Effects of Thymol, Carvacrol and Grapefruit Seed Extract on Lipid Oxidation and Colour Stability of Poultry Meat Preparations Int. J. Food Sci. Technol. 2009, 44, 2256-2267 10.1111/j.1365-2621.2009.02067.x
4. Bard, M.; Albrecht, M. R.; Gupta, N.; Guynn, C. J.; Stillwell, W. Geraniol Interferes with Membrane Functions in Strains of Candida and Saccharomyces Lipids 1988, 23, 534-538 10.1007/BF02535593
5. Gonzalez-Burgos, E.; Gomez-Serranillos, M. P. Terpene Compounds in Nature: A Review of Their Potential Antioxidant Activity Curr. Med. Chem. 2012, 19, 5319-5341 10.2174/092986712803833335
6. Carnesecchi, S.; Bradaia, A.; Fischer, B.; Coelho, D.; Scholler-Guinard, M.; Gosse, F.; Raul, F. Perturbation by Geraniol of Cell Membrane Permeability and Signal Transduction Pathways in Human Colon Cancer Cells J. Pharmacol. Exp. Ther. 2002, 303, 711-715 10.1124/jpet.102.039263
7. Aqil, M.; Ahad, A.; Sultana, V.; Ali, A. Status of Terpenes as Skin Penetration Enhancers Drug Discovery Today 2007, 12, 1061-1067 10.1016/j.drudis.2007.09.001
8. Cristani, M.; D'Arrigo, M.; Mandalari, G.; Castelli, F.; Sarpietro, M. G.; Micieli, D.; Venuti, V.; Bisignano, G.; Saija, A.; Trombetta, D. Interaction of Four Monoterpenes Contained in Essential Oils with Model Membranes: Implications for Their Antibacterial Activity J. Agric. Food Chem. 2007, 55, 6300-6308 10.1021/jf070094x
9. Janiak, M. J.; Small, D. M.; Shipley, G. G. Temperature and Compositional Dependence of the Structure of Hydrated Dimyristoyl Lecithin J. Biol. Chem. 1979, 254, 6068-6078
10. Xiang, T. X.; Anderson, B. D. Phase Structures of Binary Lipid Bilayers as Revealed by Permeability of Small Molecules Biochim. Biophys. Acta, Biomembr. 1998, 1370, 64-76 10.1016/S0005-2736(97)00244-7
11. Van Geet, A. L. Calibration of Methanol Nuclear Magnetic Resonance Thermometer at Low Temperature Anal. Chem. 1970, 42, 679-680 10.1021/ac60288a022
12. Pines, A.; Gibby, M. G.; Waugh, J. S. Proton-Enhanced Nuclear Induction Spectroscopy. A Method for High Resolution NMR of Dilute Spins in Solids J. Chem. Phys. 1972, 56, 1776-1777 10.1063/1.1677439
13. Morris, G. A.; Freeman, R. Enhancement of Nuclear Magnetic-Resonance Signals by Polarization Transfer J. Am. Chem. Soc. 1979, 101, 760-762 10.1021/ja00497a058
14. Nowacka, A.; Mohr, P. C.; Norrman, J.; Martin, R. W.; Topgaard, D. Polarization Transfer Solid-State NMR for Studying Surfactant Phase Behavior Langmuir 2010, 26, 16848-16856 10.1021/la102935t
15. Nowacka, A.; Bongartz, N. A.; Ollila, O. H.; Nylander, T.; Topgaard, D. Signal Intensities in 1H-13C CP and INEPT MAS NMR of Liquid Crystals J. Magn. Reson. 2013, 230, 165-75 10.1016/j.jmr.2013.02.016
16. Bennett, A. E.; Rienstra, C. M.; Auger, M.; Lakshmi, K. V.; Griffin, R. G. Heteronuclear Decoupling in Rotating Solids J. Chem. Phys. 1995, 103, 6951-6958 10.1063/1.470372
17. Dvinskikh, S. V.; Zimmermann, H.; Maliniak, A.; Sandström, D. Measurements of Motionally Averaged Heteronuclear Dipolar Couplings in MAS NMR Using R-type Recoupling J. Magn. Reson. 2004, 168, 194-201 10.1016/j.jmr.2004.03.001
18. van Beek, J. D. matNMR: A Flexible Toolbox for Processing, Analyzing and Visualizing Magnetic Resonance Data in Matlab J. Magn. Reson. 2007, 187, 19-26 10.1016/j.jmr.2007.03.017
19. Ferreira, T. M.; Coreta-Gomes, F.; Ollila, O. H. S.; Moreno, M. J.; Vaz, W. L. C.; Topgaard, D. Cholesterol and POPC Segmental Order Parameters in Lipid Membranes: Solid State 1H-13C NMR and MD Simulation Studies Phys. Chem. Chem. Phys. 2013, 15, 1976-1989 10.1039/C2CP42738A
20. Dvinskikh, S. V.; Castro, V.; Sandström, D. Efficient Solid-State NMR Methods for Measuring Heteronuclear Dipolar Couplings in Unoriented Lipid Membrane Systems Phys. Chem. Chem. Phys. 2005, 7, 607-613 10.1039/b418131j
21. Torchia, D. A. The Measurement of Proton-Enhanced Carbon-13 T1 Values by A Method Which Suppresses Artifacts J. Magn. Reson. 1978, 30, 613-616 10.1016/0022-2364(78)90288-3
22. Ferreira, T. M.; Ollila, O. H.; Pigliapochi, R.; Dabkowska, A. P.; Topgaard, D. Model-Free Estimation of The Effective Correlation Time for C-H Bond Reorientation in Amphiphilic Bilayers: H-C Solid-State NMR and MD Simulations J. Chem. Phys. 2015, 142, 044905 10.1063/1.4906274
23. Alper, J. S.; Gelb, R. I. Standard Errors and Confidence-Intervals in Nonlinear-Regression-Comparison of Monte-Carlo and Parametric Statistics J. Phys. Chem. 1990, 94, 4747-4751 10.1021/j100374a068
24. Smith, G. S.; Sirota, E. B.; Safinya, C. R.; Plano, R. J.; Clark, N. A. X-ray Structural Studies of Freely Suspended Ordered Hydrated DMPC Multimembrane Films J. Chem. Phys. 1990, 92, 4519-4529 10.1063/1.457764
25. Guldbrand, L.; Jönsson, B.; Wennerström, H. Hydration Forces and Phase-Equilibria in the Dipalmitoyl Phosphatidylcholine-Water System J. Colloid Interface Sci. 1982, 89, 532-541 10.1016/0021-9797(82)90204-1
26. Nowacka, A.; Douezan, S.; Wadsö, L.; Topgaard, D.; Sparr, E. Small Polar Molecules Like Glycerol and Urea Can Preserve The Fluidity of Lipid Bilayers Under Dry Conditions Soft Matter 2012, 8, 1482-1491 10.1039/C1SM06273E
27. Earl, W. L.; VanderHart, D. L. Observations in Solid Polyethylenes by Carbon-13 Nuclear Magnetic Resonance with Magic Angle Sample Spinning Macromolecules 1979, 12, 762-767 10.1021/ma60070a045
28. Seelig, J. Deuterium Magnetic-Resonance-Theory and Application to Lipid-Membranes Q. Rev. Biophys. 1977, 10, 353-418 10.1017/S0033583500002948
29. Dvinskikh, S. V.; Castro, V.; Sandström, D. Probing Segmental Order in Lipid Bilayers at Variable Hydration Levels by Amplitude- and Phase-Modulated Cross-Polarization NMR Phys. Chem. Chem. Phys. 2005, 7, 3255-3257 10.1039/b508190d
30. Vermeer, L. S.; de Groot, B. L.; Reat, V.; Milon, A.; Czaplicki, J. Acyl Chain Order Parameter Profiles in Phospholipid Bilayers: Computation from Molecular Dynamics Simulations and Comparison with 2H NMR Experiments Eur. Biophys. J. 2007, 36, 919-31 10.1007/s00249-007-0192-9
31. Gross, J. D.; Warschawski, D. E.; Griffin, R. G. Dipolar Recoupling in MAS NMR: A Probe for Segmental Order in Lipid Bilayers J. Am. Chem. Soc. 1997, 119, 796-802 10.1021/ja962951b
32. Petrache, H. I.; Dodd, S. W.; Brown, M. F. Area per Lipid and Acyl Length Distributions in Fluid Phosphatidylcholines Determined by 2H NMR Spectroscopy Biophys. J. 2000, 79, 3172-3192 10.1016/S0006-3495(00)76551-9
33. Evans, D. F.; Wennerström, H. The Colloidal Domain: Where Physics, Chemistry, Biology, and Technology Meet, 2 nd ed.; Wiley-VCH: New York, 1999; pp 311, 523.
34. Lohner, K. Effects of Small Organic Molecules on Phospholipid Phase Transitions Chem. Phys. Lipids 1991, 57, 341-62 10.1016/0009-3084(91)90085-P
35. Vist, M. R.; Davis, J. H. Phase Equilibria of Cholesterol/Dipalmitoylphosphatidylcholine Mixtures: 2H Nuclear Magnetic Resonance and Differential Scanning Calorimetry Biochemistry 1990, 29, 451-64 10.1021/bi00454a021
36. Pope, J. M.; Dubro, D.; Doane, J. W.; Westerman, P. W. The Ordering of Benzyl Alcohol and Its Influence on Phospholipid Order in Bilayer-Membranes J. Am. Chem. Soc. 1986, 108, 5426-5433 10.1021/ja00278a009
37. Hung, W. C.; Lee, M. T.; Chen, F. Y.; Huang, H. W. The Condensing Effect of Cholesterol in Lipid Bilayers Biophys. J. 2007, 92, 3960-3967 10.1529/biophysj.106.099234
38. Sparr, E.; Wennerström, H. Responding Phospholipid Membranes-Interplay between Hydration and Permeability Biophys. J. 2001, 81, 1014-1028 10.1016/S0006-3495(01)75759-1
39. Lawaczeck, R. On The Permeability of Water Molecules across Vesicular Lipid Bilayers J. Membr. Biol. 1979, 51, 229-261 10.1007/BF01869086
40. Carruthers, A.; Melchior, D. L. Study of The Relationship between Bilayer Water Permeability and Bilayer Physical State Biochemistry 1983, 22, 5797-5807 10.1021/bi00294a018
41. Leslie, S. B.; Israeli, E.; Lighthart, B.; Crowe, J. H.; Crowe, L. M. Trehalose and Sucrose Protect Both Membranes and Proteins in Intact Bacteria during Drying Appl. Environ. Microbiol. 1995, 61, 3592-3597