Behavior of fluorescent cholesterol analogues dehydroergosterol and cholestatrienol in lipid bilayers: A molecular dynamics study

Journal of Physical Chemistry B

Volumn 117, Issue 19, 2013, Pages 5806-5819

  Robalo, João R ^a,b   Do Canto, António M T Martins ^a,b   Carvalho, A J Palace ^a,b   Ramalho, J P Prates ^a,b   Loura, Luís M S ^c,d  

^a Escola de Cieîncias e Tecnologia   (Portugal)

^b UNIVERSITY OF ÉVORA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLS; CHOLESTEROL; LIPID BILAYERS; LIPIDS; MOLECULAR DYNAMICS;

BI-LAYER STRUCTURE; CONTROL PROPERTIES; DEHYDROERGOSTEROL; DYNAMICAL PROPERTIES; FLUORESCENT PROBES; MOLECULAR DYNAMICS SIMULATIONS; STRUCTURAL DIFFERENCES; STRUCTURAL SIMILARITY;

FLUORESCENCE;

EID: 84878080095     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp312026u     Document Type: Article

References (70)

1. Ipsen, J. H.; Karlström, G.; Mouritsen, O. G.; Wennerström, H.; Zuckermann, M. J. Phase Equilibria in the Phosphatidylcholine-Cholesterol System Biochim. Biophys. Acta 1987, 905, 162-172
2. Vist, M. R.; Davis, J. H. Phase Equilibria of Cholesterol/ Dipalmitoylphosphatidylcholine Mixtures: 2H Nuclear Magnetic Resonance and Differential Scanning Calorimetry Biochemistry 1990, 29, 451-464
3. Almeida, P. F.; Vaz, W. L.; Thompson, T. E. Lateral Diffusion in the Liquid Phases of Dimyristoylphosphatidylcholine/Cholesterol Lipid Bilayers: a Free Volume Analysis Biochemistry 1992, 31, 6739-6747
4. Thewalt, J. L.; Bloom, M. Phosphatidylcholine: Cholesterol Phase Diagrams Biophys. J. 1992, 63, 1176-1181
5. Gennis, R. B. Biomembranes: Molecular Structure and Function; Springer: New York, 1989.
6. Ipsen, J. H.; Mouritsen, O. G.; Bloom, M. Relationships Between Lipid Membrane Area, Hydrophobic Thickness and Acyl Chain Orientational Order. The Effects of Cholesterol Biophys. J. 1990, 57, 405-412
7. Needham, D.; Nunn, R. S. Elastic Deformation and Failure of Lipid Bilayer Membranes Containing Cholesterol Biophys. J. 1990, 58, 997-1009
8. Yeagle, P. L. Modulation of Membrane Function by Cholesterol Biochimie 1991, 73, 1303-1310
9. Simons, K.; Vaz, W. L. C. Model Systems, Lipid Rafts, and Cell Membranes Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 269-295
10. Lingwood, D.; Simons, K. Lipid Rafts as a Membrane Organizing Principle Science 2010, 327, 46-50
11. de Almeida, R. F. M.; Loura, L. M. S.; Prieto, M. Membrane Lipid Domains and Rafts: Current Applications of Fluorescence Lifetime Spectroscopy and Imaging Chem. Phys. Lipids 2009, 157, 61-77
12. Wüstner, D. Fluorescent Sterols as Tools in Membrane Biophysics and Cell Biology Chem. Phys. Lipids 2007, 146, 1-25
13. Loura, L. M. S.; Fedorov, A.; Prieto, M. Exclusion of a Cholesterol Analog from the Cholesterol Rich Phase in Model Membranes Biochim. Biophys. Acta 2001, 1511, 236-243
14. Scheidt, H. A.; Müller, P.; Herrmann, A.; Huster, D. The Potential of Fluorescent and Spin Labelled Steroid Analogs to Mimic Natural Cholesterol J. Biol. Chem. 2003, 278, 45563-45569
15. Shaw, J. E.; Epand, R. F.; Epand, R. M.; Li, Z.; Bittman, R.; Yip, C. M. Correlated Fluorescence Atomic Force Microscopy of Membrane Domains: Structure of Fluorescence Probes Determines Lipid Localization Biophys. J. 2006, 90, 2170-2178
16. Hölttä-Vuori, M.; Uronen, R. L.; Repakova, J.; Salonen, E.; Vattulainen, I.; Panula, P.; Li, Z.; Bittman, R.; Ikonen, E. BODIPY Cholesterol. A New Tool to Visualize Sterol Trafficking in Living Cells and Organisms Traffic (Copenhagen, Den.) 2008, 9, 1839-1849
17. Garvik, O.; Benediktson, P.; Simonsen, A. C.; Ipsen, J. H.; Wüstner, D. The Fluorescent Cholesterol Analog Dehydroergosterol Induces Liquid Ordered Domains in Model Membranes Chem. Phys. Lipids 2009, 159, 114-118
18. Staneva, G.; Chachaty, C.; Wolf, C.; Quinn, P. J. Comparison of the Liquid Ordered Biayer Phases Containing Cholesterol or 7-Dehydroergosterol in Modelling Smith Lemli Opitz Syndrome J. Lipid Res. 2010, 51, 1810-1822
19. Mouritsen, O. G.; Zuckermann, M. J. What's so Special about Cholesterol? Lipids 2004, 39, 1101-1113
20. Lyubartsev, A. P.; Rabinovich, A. L. Recent Development in Computer Simulations of Lipid Bilayers Soft Matter 2011, 7, 25-39
21. Loura, L. M. S.; Ramalho, J. P. P. Fluorescent Membrane Probes' Behaviour in Lipid Bilayers: Insights from Molecular Dynamics Simulations Biophys. Rev. 2009, 1, 141-148
22. Loura, L. M. S.; Ramalho, J. P. P. Recent Developments in Molecular Dynamics Simulations of Fluorescent Membrane Probes Molecules 2011, 16, 5437-5452
23. Smondyrev, A. M.; Berkowitz, M. L. Molecular Dynamics Simulation of the Structure of Dimyristoylphosphatidylcholine Bilayers with Cholesterol, Ergosterol and Lanosterol Biophys. J. 2001, 80, 1649-1658
24. Róg, T.; Pasenkiewicz-Gierula, M.; Vattulainen, I.; Karttunen, M. What Happens if Cholesterol Is Made Smoother: Importance of Methyl Substituents in Cholesterol Ring Structure on Phosphatidylcholine-Sterol Interaction Biophys. J. 2007, 92, 3346-3357
25. Ollila, O. H. S.; Róg, T.; Karttunen, M.; Vattulainen, I. Role of Sterol Type on Lateral Pressure Profiles of Lipid Membranes Affecting Membrane Protein Functionality: Comparison Between Cholesterol, Desmosterol, 7-Dehydrocholesterol and Ketosterol J. Struct. Biol. 2007, 159, 311-323
26. Vainio, S.; Jansen, M.; Koivusalo, M.; Róg, T.; Karttunen, M.; Vattulainen, I.; Ikonen, E. Significance of Sterol Structural Specificity. Desmosterol cannot replace Cholesterol in Lipid Rafts J. Biol. Chem. 2006, 281, 348-355
27. Aittoniemi, J.; Róg, T.; Niemela, P.; Pasenkiewicz-Gierula, M.; Karttunen, M.; Vattulainen, I. Tilt: Major Factor in Sterols' Ordering Capability in Membranes J. Phys. Chem. B 2006, 110, 25562-25564
28. Róg, T.; Vattulainen, I.; Jansen, M.; Ikonen, E.; Karttunen, M. Comparison of Cholesterol and Its Direct Precursors Along The Biosynthetic Pathway: Effects of Cholesterol, Desmosterol and 7-Dehydrocholesterol on Saturated and Unsaturated Lipid Bilayers J. Chem. Phys. 2008, 129, 154508
29. Berger, O.; Edholm, O.; Jähnig, F. Molecular Dynamics Simulations of a Fluid Bilayer of Dipalmitoylphosphatidylcholine at Full Hydration, Constant Pressure and Constant Temperature Biophys. J. 1997, 72, 2002-2013
30. 2H-NMR Study and Molecular Dynamics Simulation of the Location, Alignment and Mobility of Pyrene in POPC Bilayers Biophys. J. 2005, 88, 1818-1827
31. Berendsen, H.; Postma, J.; van Gunsteren, W.; Hermans, J. Intermolecular Forces; Reidel: Dordrecht, The Netherlands, 1981.
32. Höltje, M.; Förster, T.; Brandt, B.; Engels, T.; von Rybinski, W.; Höltje, H. Molecular Dynamics Simulations of Stratum Corneum Lipid Models: Fatty Acids and Cholesterol Biochim. Biophys. Acta 2001, 1511, 156-167
33. Becke, A. Density-Functional Thermochemistry III. The Role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
34. Lee, C.; Yang, W.; Parr, R. Development of the Colle-Salvetti Correlation-Energy Formula into a Functional of the Electron Density Phys. Rev. [Sect.] B 1988, 37, 785-789
35. Vosko, S.; Wilk, L.; Nussair, M. Accurate Spin-Dependant Electron Liquid Correlation Energies for Local Spin Density Calculations: a Critical Analysis Can. J. Phys. 1980, 58, 1200-1211
36. Stephens, P.; Devlin, F.; Chabalowski, C.; Frisch, M. Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields J. Phys. Chem. 1994, 98, 11623-11627
37. Granovsky, A. Firefly v 7.1.G, http://classic.chem.msu.su/gran/firefly/ index.html.
38. Schüttelkopf, A.; Aalten, D. PRODRG: a Tool for High-Throughput Crystallography of Protein-Ligand Complexes Acta Crystallogr. 2004, 60, 1355-1363
39. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Molec. Graphics 1996, 14, 33-38
40. Murzyn, K.; Róg, T.; Jezierski, G.; Takaoka, Y.; Pasenkiewicz-Gierula, M. Effects of Phospholipid Unsaturation on the Membrane/Water Interface: a Molecular Simulation Study Biophys. J. 2001, 81, 170-183
41. Berendsen, H.; Postma, J.; DiNola, A.; Haak, J. Molecular Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684-3690
42. Myamoto, S.; Kollman, P. SETTLE an Analytical Version of the SHAKE and RATTLE Algorithms for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
43. Hess, B.; Bekker, H.; Berendsen, H.; Fraaije, J. LINCS: a Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
44. Feenstra, K.; Hess, B.; Berendsen, H. Improving efficiency of Large Timescale Molecular Dynamics Simulations of Hydrogen-Rich Systems J. Comput. Chem. 1999, 20, 786-798
45. Anézo, C.; de Vries, A. H.; Höltje, H. D.; Tieleman, D. P.; Marrink, S. J. Methodological Issues in Lipid Bilayer Simulations J. Phys. Chem. B 2003, 107, 9424-9433
46. Essman, U.; Perela, L.; Berkowitz, M.; Darden, T.; Lee, H.; Pedersen, L. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8592
47. Berendsen, H.; van der Spoel, D.; van Drunen, R. GROMACS: a Message-Passing Parallel Molecular Dynamics Implementation Comput. Phys. Commun. 1995, 91, 43-56
48. Lindhal, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: a Package for Molecular Simulation and Trajectory Analysis J. Mol. Modeling 2001, 7, 306-317
49. van der Spoel, D.; Lindhal, E.; Hess, B.; Groenhof, G.; Mark, A.; Berendsen, H. GROMACS: Fast, Flexible and Free J. Comput. Chem. 2005, 26, 1701-1718
50. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindhal, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
51. Róg, T.; Pasenkiewicz-Gierula, M. Cholesterol Effects on a Mixed-Chain Phosphatidylcholine Bilayer: a Molecular Dynamics Simulation Study Biochimie 2006, 88, 449-460
52. Kinosita, K.; Kawato, S.; Ikegami, A. A Theory of Fluorescence Polarization Decay in Membranes Biophys. J. 1977, 20, 289-305
53. Hofsäβ, C.; Lindhal, E.; Edholm, O. Molecular Dynamics Simulatons of Phospholipid Bilayers with Cholesterol Biophys. J. 2003, 84, 2192-2206
54. Voss, N.; Gerstein, M. 3V: Cavity, Channel and Cleft Volume Calculator and Extractor Nucleic Acid Res. 2010, 38, 555-562
55. Greenwood, A. I.; Tristram-Nagle, S.; Nagle, J. F. Partial Molecular Volumes of Lipids and Cholesterol Chem. Phys. Lipids. 2006, 143, 1-10
56. n Membranes Biophys. Chem. 1996, 58, 289-302
57. Konig, B.; Dietrich, U.; Klose, G. Hydration and Structural Properties of Mixed Lipid/Surfactant Model Membranes Langmuir 1997, 13, 525-532
58. Smaby, J.; Momsen, M.; Brockman, H.; Brown, R. Phosphatidylcholine Acyl Unsaturation Modulates the Decrease in Interfacial Elasticity Induced by Cholesterol Biophys. J. 1997, 73, 1492-1505
59. Bockmann, R.; Hac, A.; Heimburg, T.; Grubmuller, H. Effects of Sodium Chloride on a Lipid Bilayer Biophys. J. 2003, 85, 1647-1655
60. Mukhopadhyay, P.; Vogel, H.; Tieleman, D. Distribution of Pentachlorophenol in Phospholipid Bilayers: a Molecular Dynamics Study Biophys. J. 2004, 86, 337-345
61. Gurtovenko, A.; Anwar, J. Interaction of Ethanol with Biological Membranes: the Formation of Non-Bilayer Structures within the Membrane Interior and their Significance J. Phys. Chem. B 2009, 113, 1983-1992
62. Pandit, S.; Chiu, S.; Jakobsson, E.; Grama, A.; Scott, H. Cholesterol Packing around Lipids with Saturated and Unsaturated Chains: a Simulation Study Langmuir 2008, 24, 6858-6865
63. Hung, W.; Lee, M.; Chen, F.; Huang, H. The Condensing Effect of Cholesterol in Lipid Bilayers Biophys. J. 2007, 92, 3960-3967
64. Róg, T.; Pasenkiewicz-Gierula, M.; Vattulainen, I.; Karttunen, M. Ordering Effects of Cholesterol and its Analogues Biochim. Biophys. Acta 2009, 1788, 97-121
65. Douliez, J.; Leonard, A.; Dufourc, E. Restatement of Order Parameters in Biomembranes: Calculation of C-C Bond Order Parameters from C-D Quadrupolar Splittings Biophys. J. 1995, 68, 1727-1739
66. Seelig, J.; Waespesarcevic, N. Molecular Order in cis and trans Unsaturated Phospholipid Bilayers Biochemistry 1978, 17, 3310-3315
67. 2H NMR J. Phys. Chem. B 1999, 103, 3022-3029
68. Patra, M.; Salonen, E.; Terama, E.; Vattulainen, I.; Faller, R.; Lee, B.; Holopainen, J.; Karttunen, M. Under the Influence of Alcohol: the Effect of Ethanol and Methanol on Lipid Bilayers Biophys. J. 2006, 90, 1121-1135
69. Falck, E.; Patra, M.; Karttunen, M.; Hyvönen, M.; Vattulainen, I. Lessons of Slicing Membranes: Interplay of Packing, Free Area, and Lateral Diffusion in Phospholipid/Cholesterol Bilayers Biophys. J. 2004, 87, 1076-1091
70. Wüstner, D.; Brewer, J. R.; Bagatolli, L.; Sage, D. Potential of Ultraviolet Wide-Field Imaging and Multiphoton Microscopy for Analysis of Dehydroergosterol in Cellular Membranes Microsc. Res. Tech. 2011, 74, 92-108