Viscosity heterogeneity inside lipid bilayers of single-component phosphatidylcholine liposomes observed with picosecond time-resolved fluorescence spectroscopy

Journal of Physical Chemistry B

Volumn 118, Issue 29, 2014, Pages 8631-8641

  Nojima, Yuki ^a   Iwata, Koichi ^a  

^a GAKUSHUIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL PROPERTIES; EXCITED STATES; FLUORESCENCE SPECTROSCOPY; LIPOSOMES; RATE CONSTANTS; VISCOSITY;

BIOCHEMICAL REACTIONS; EXCITED SINGLET STATE; HETEROGENEOUS STRUCTURES; HYDROCARBON CHAIN LENGTH; LIPID BILAYER MEMBRANES; PHOSPHATIDYL CHOLINE; ROTATIONAL RELAXATIONS; TIME-RESOLVED FLUORESCENCE SPECTROSCOPY;

LIPID BILAYERS;

LIPID BILAYER; LIPOSOME; PHOSPHATIDYLCHOLINE; STILBENE DERIVATIVE;

CELL MEMBRANE; CHEMISTRY; LIPID BILAYER; ROTATION; SOLUBILITY; SPECTROFLUOROMETRY; STEREOISOMERISM; TEMPERATURE; TIME; VISCOSITY;

CELL MEMBRANE; LIPID BILAYERS; LIPOSOMES; PHOSPHATIDYLCHOLINES; ROTATION; SOLUBILITY; SPECTROMETRY, FLUORESCENCE; STEREOISOMERISM; STILBENES; TEMPERATURE; TIME FACTORS; VISCOSITY;

EID: 84904972323     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp503921e     Document Type: Article

References (71)

1. Gaber, B. P.; Peticolas, W. L. On the quantitative interpretation of biomembrane structure by Raman spectroscopy Biochim. Biophys. Acta, Biomembr. 1977, 465, 260-274
2. Pink, D. A.; Green, T. J.; Chapman, D. Raman Scattering in Bilayers of Saturated Phosphatidylcholines. Experiment and Theory Biochemistry 1980, 19, 349-356
3. Jackson, M.; Mantsch, H. H. Biomembrane structure from FT-IR spectroscopy Spectrochim. Acta Rev. 1993, 15, 53-69
4. Saiz, L.; Bandypadhyay, S.; Klein, M. L. Towards an Understanding of Complex Biological Membranes from Atomistic Molecular Dynamics Simulations Bioscience Rep. 2002, 22, 151-173
5. Leonenko, Z. V.; Finot, E.; Ma, H.; Dahms, T. E. S; Cramb, D. T. Investigation of Temperature-Induced Phase Transitions in DOPC and DPPC Phospholipid Bilayers Using Temperature-Controlled Scanning Force Microscopy Biophys. J. 2004, 86, 3783-3793
6. Collawn, J. F.; Bebok, Z. Chapter 1 Structure and Functions of Biomembranes Curr. Top. Membr. 2008, 61, 1-21
7. Cved, G. How Membrane Chain Melting Properties Are Regulated by the Polar Surface of the Lipid Bilayer Biochemistry 1987, 26, 6305-6310
8. Bloom, M.; Evans, E.; Mouriten, O. G. Physical properties of the fluid-bilayer component of cell membranes: a perspective Q. Rev. Biophys. 1991, 24, 293-397
9. Subczynski, W. K.; Widomska, J.; Feix, J. B. Physical properties of lipid bilayers from EPR spin labeling and their influence on chemical reactions in a membrane environment Free Radic. Biol. Med. 2009, 46, 707-718
10. Smith, A. M.; Vinchurkar, M.; Gronbech-Jensen, N.; Parikh, A. N. Order at the Edge of the Bilayer: Membrane Remodeling at the Edge of a Planar Supported Bilayer Is Accompanied by a Localized Phase Change J. Am. Chem. Soc. 2010, 132, 9320-9327
11. Krysinski, P. Redox reactions on TCNQ-modified self-assembled monomolecular films Adv. Mater. Opt. Electron. 1993, 2, 107-113
12. Sumino, A.; Dewa, T.; Takeuchi, T.; Sugiura, R.; Sasaki, N.; Misawa, N.; Tero, R.; Urisu, T.; Gardiner, A. T.; Cogdell, R. J.; Hashimoto, H.; Nango, M. Construction and Structural Analysis of Tethered Lipid Bilayer Containing Photosynthetic Antenna Proteins for Functional Analysis Biomacromolecules 2011, 12, 2850-2858
13. Tero, R. Substrate Effects on the Formation Process, Structure and Physicochemical Properties of Supported Lipid Bilayers Materials 2012, 5, 2658-2680
14. Simons, K.; Ikonen, E. Functional rafts in cell membranes Nature 1997, 387, 569-572
15. Lingwood, D.; Simons, K. Lipid Rafts As a Membrane-Organizing Principle Science 2010, 327, 46-50
16. Munro, S. Lipid Rafts: Elusive or Illusive? Cell 2003, 115, 377-388
17. Saslowsky, S. E.; Lawrence, J.; Ren, X.; Brown, D. A.; Henderson, R. M.; Edwardson, J. M. Placental Alkaline Phosphatase Is Efficiently Targeted to Rafts in Supported Lipid Bilayers J. Biol. Chem. 2002, 277, 26966-26970
18. Pralle, A.; Keller, P.; Florin, E. L.; Simons, K.; Hoerber, J. K. H. Sphingolipid-Cholesterol Rafts Diffuse as Small Entities in the Plasma Membrane of Mammalian Cells J. Cell Biol. 2000, 148, 997-1007
19. Eggeling, C.; Ringemann, S.; Belov, V. N.; Middendorf, C.; Schoenle, A.; Hell, S. W. Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 2009, 457, 1159-1162
20. Lajoie, P.; Goetz, J. G.; Dennis, J. W.; Nabi, I. R. Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane J. Cell Biol. 2009, 185, 381-385
21. Bogonez, E.; Koshland, D. E., Jr. Solubilization of a vectorial transmembrane receptor in functional form: Aspartate receptor of chemotaxis Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4891-4895
22. Shoda, K.; Sugawara, T. DNA polymerization on the inner surface of a giant liposome for synthesizing an artificial cell model Soft Matter 2006, 2, 402-408
23. Shoda, K.; Toyota, T.; Yomo, T.; Sugawara, T. Direct Visualization of DNA Duplex Formation on the Surface of a Giant Liposome ChemBioChem 2003, 4, 778-781
24. Bialek-Pietras, M.; Olejniczak, A. B.; Tachikawa, S.; Nakamura, H.; Lesnikowski, Z. J. Towards new boron carriers for boron neutron capture therapy: metallacarboranes bearing cobalt, iron and chromium and their cholesterol conjugates Bioorg. Med. Chem. 2013, 21, 1136-1142
25. Koganei, H.; Ueno, M.; Tachikawa, S.; Tasaki, L.; Bang, H. S.; Suzuki, M.; Shiraishi, K.; Kawano, K.; Yokoyama, M.; Maitani, Y.; Ono, K.; Nakamura, H. Development of High Boron Content Liposomes and Their Promising Antitumor Effect for Neutron Capture Therapy of Cancers Bioconjugate Chem. 2013, 24, 124-132
26. Nakamura, H.; Ueda, N.; Ban, H. S.; Ueno, M.; Tachikawa, S. Design and synthesis of fluorescence-labeled closo-dodecaborate lipid: its liposome formation and in vivo imaging targeting of tumors for boron neutron capture therapy Org. Biomol. Chem. 2012, 10, 1374-1380
27. Nagel, J. F. Theory of the Main Lipid Bilayer Phase Transition Annu. Rev. Phys. Chem. 1980, 31, 157-196
28. Izuyama, T.; Akutsu, Y. Statiscal Mechanics of Biomembrane Phase Transition. I. Excluded Volume Effects of Lipid Chains in Their Conformation Change J. Phys. Soc. Jpn. 1982, 51, 50-58
29. Rinia, H. A.; Snel, M. M. E.; van der Eerden, J. P. J. M.; de Kruijiff, B. Visualizing detergent resistant domains in model membranes with atomic force microscopy FEBS Lett. 2001, 501, 92-96
30. Giocondi, M. C.; Milhiet, P. E.; Dosset, P.; Grimellec, C. L. Use of Cyclodextrin for AFM Monitoring of Model Raft Formation Biophys. J. 2004, 86, 861-869
31. Shinitzky, M.; Barenholz, Y. Dynamics of the Hydrocarbon Layer in Liposomes of Lecithin and Sphingomyelin Containing Dicetylphosphate J. Biol. Chem. 1974, 249, 2652-2657
32. Vanderkooi, J. M.; Callis, J. B. Pyrene. A Probe of Lateral Diffusion in the Hydrophobic Region of Membranes Biochemistry 1974, 13, 4000-4006
33. Kung, C. E.; Reed, J. K. Microviscosity Measurements of Phospholipid Bilayers Using Fluorescent Dyes That Undergo Torsional Relaxation Biochemistry 1986, 25, 6114-6121
34. Lewis, R. N. A. H.; Mark, N.; Mcelhaney, R. N. A Differential Scanning Calorimetric Study of the Thermotropic Phase Behavior of Model Membranes Composed of Phosphatidylcholines Containing Linear Saturated Fatty Acyl Chains Biochemistry 1987, 26, 6118-6126
35. Kinoshita, K., Jr.; Kataoka, R.; Kimura, Y.; Gotoh, O.; Ikegami, A. Dynamic Structure of Biological Membranes As Probed by 1,6-Diphenyl- 1,3,5-hexatriene: A Nanosecond Fluorescence Depolarization Study Biochemistry 1981, 20, 4270-4277
36. Wu, Y.; Stefl, M.; Olzynska, A.; Hof, M.; Yahioglu, G.; Yip, P.; Casey, D. R.; Ces, O.; Humpolickova, J.; Kuimova, M. K. Molecular rheometry: direct determination of viscosity in Lo and Ld lipid phases via fluorescence lifetime imaging Phys. Chem. Chem. Phys. 2013, 15, 14986-14993
37. Holmes, A. S.; Birch, D. J. B.; Sanderson, A.; Aloisi, G. G. Time-resolved fluorescence photophysics of trans -stilbene in a DPPC lipid bilayer: evidence for a free rotation, location within two sites and a pre-liquid crystalline phase transition Chem. Phys. Lett. 1997, 266, 309-318
38. Courtney, S. H.; Kim, S. K.; Canonica, S.; Fleming, G. R. Rotational Diffusion of Stilbene in Alkane and Alcohol Solutions J. Chem. Soc., Faraday Trans. 2 1986, 82, 2065-2072
39. Korlach, J.; Schwille, P.; Webb, W. W.; Feigenson, G. W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 8461-8466
40. Easteal, A. J.; Price, W. E.; Woolf, L. A. Diaphragm Cell for High-temperature Diffusion Measurements Tracer Diffusion Coefficients for Water to 363 K J. Chem. Soc., Faraday Trans. 1 1989, 85, 1091-1097
41. Nojima, Y.; Iwata, K. Lipid Bilayer Membrane of Egg-PC Liposome Evaluated as Chemical Reaction Field with Picosecond Time-Resolved Fluorescence Spectroscopy Chem.-Asian J. 2011, 6, 1817-1824
42. Bangham, A. D.; Horne, R. W. Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope J. Mol. Biol. 1964, 8, 660-668
43. Arifin, D. R.; Palmer, A. F. Determination of Size Distribution and Encapsulation Efficiency of Liposome-Encapsulated Hemoglobin Blood Substitutes Using Asymmetric Flow Field-Flow Fractionation Coupled with Multi-Angle Static Light Scattering Biotechnol. Prog. 2003, 19, 1798-1811
44. Koynova, R.; Caffrey, M. Phases and phase transitions of the phosphatidylcholines Biochim. Biophys. Acta 1998, 1376, 91-145
45. Iwata, K.; Kakita, M.; Hamaguchi, H. Picosecond Time-Resolved Fluorescence Study on Solute-Solvent Interaction of 2-Aminoquinoline in Room-Temperature Ionic Liquids: Aromaticity of Imidazolium-Based Ionic Liquids J. Phys. Chem. B 2007, 111, 4914-4919
46. Duveneck, G. L.; Sitzmann, E. V.; Eisenthal, K. B.; Turro, N. J. Picosecond Laser Studies on Photochemical Reactions in Restricted Environments: The Photoisomerization of trans-Stfibene Complexed to Cyciodextrins J. Phys. Chem. 1989, 93, 7166-7170
47. Lee, M.; Hochstrasser, G. R.; Weisman, R. B. Observation of the Kramers Turnover Region in the Isomerism of Trans-stilbene in Fluid Ethane Chem. Phys. Lett. 1985, 118, 359-363
48. Kim, S. K.; Courtney, S. H.; Fleming, G. R. Isomerization of t -Stilbene in Alchols Chem. Phys. Lett. 1989, 159, 543-547
49. Ozawa, R.; Hamaguchi, H. Does Photoisomerization Proceed in an Ionic Liquid? Chem. Lett. 2001, 30, 736-737
50. Hamaguchi, H.; Iwata, K. Physical Chemistry of the Lowest Excited Singlet State of trans -Stilbene in Solution as Studied by Time-Resolved Raman Spectroscopy Bull. Chem. Soc. Jpn. 2002, 75, 883-897
51. 1 trans -Stilbene and the Mechanism of the trans to cis Isomerization: Dynamic Polarization Model of Vibrational Dephasing and the CdC Double-Bond Rotation J. Phys. Chem. A 2002, 106, 3614-3620
52. Waldeck, D. H. Photoisomerization Dynamics of Stilbenes Chem. Rev. 1991, 91, 415-436
53. Saltiel, J.; Sun, Y. P. In Photochromism: Molecules and Systems; Durr, H.; Bouras-Laurest, H.; Elsevier: Amsterdam, 1990; p 64.
54. Sumitani, M.; Nakashima, N.; Yoshihara, K.; Nagakura, S. Temperature Dependence of Fluorescence Lifetimes of trans -stilbene Chem. Phys. Lett. 1977, 51, 183-185
55. Soni, S. P.; LoCascio, D. S.; Liu, Y.; Williams, J. A.; Bittman, R.; Stillwell, W.; Wassall, S. R. Docosahexaenoic Acid Enhances Segregation of Lipids between Raft and Nonraft Domains: 2H-NMR Study Biophys. J. 2008, 95, 203-214
56. Risselada, H. J.; Marrink, S. J. The molecular face of lipid rafts in model membranes Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 17367-17372
57. Lewis, R. J. Hawleys Condensed Chemical Dictionary; Wiley: New York, 1997; p 1049.
58. Kim, Y. R.; Hochstrasser, R. M. Rotational DMuslon of Fluorene in Hydroxylic Solvents J. Phys. Chem. 1992, 96, 9595-9597
59. Soos, Z. G.; Ramasesha, S.; Galvao, D. S.; Etemad, S. Excitation and relaxation energies of trans-stilbene: Confined singlet, triplet, and charged bipolarons Phys. Rev. B 1993, 47, 1742-1753
60. Hagler, T. W.; Pakbaz, K.; Heeger, A. J. Polarized-electroabsorption spectroscopy of a soluble derivative of poly(p-phenylenvinylene) oriented by gel processing in polyethylene: Polarization anisotropy, the off-axis dipole moment, and excited-state delocalization Phys. Rev. B 1994, 49, 10968-10975
61. Hu, C. M.; Zwanzig, R. Rotational friction coefficients for spheroids with the slipping boundary condition J. Chem. Phys. 1974, 60, 4354-4357
62. Youngren, G. K.; Acrivos, A. Rotational friction coefficients for ellipsoids and chemical molecules with the slip boundary condition J. Chem. Phys. 1975, 63, 3846-3848
63. Sension, R. J.; Hochstrasser, R. M. Comment on: Rotational friction coefficients for ellipsoids and chemical molecules with slip boundary conditions J. Chem. Phys. 1993, 98, 2490
64. Subczynski, W. K.; Lewis, R. N. A. H.; McElhaney, R. N.; Hodges, R. S.; Hyde, J. S.; Kusumi, A. Molecular Organization and Dynamics of 1-Palmitoyl-2-oleoylphosphatidylcholine Bilayers Containing a Transmembrane R-Helical Peptide Biochemsitry 1998, 37, 3156-3164
65. Cruz, A.; Casals, C.; Plasencia, I.; Marsh, D.; Perez-Gil, J. Depth Profiles of Pulmonary Surfactant Protein B in Phosphatidylcholine Bilayers, Studied by Fluorescence and Electron Spin Resonance Spectroscopy Biochemistry 1998, 37, 9488-9496
66. Perissi, I.; Ristovi, S.; Rossi, S.; Dei, L.; Martini, G. Electron Spin Resonance and Differential Scanning Calorimetry as Combined Tools for the Study of Liposomes in the Presence of Long Chain Nitroxides J. Phys. Chem. B 2002, 106, 10468-10473
67. Chiang, Y.-W.; Shimoyama, Y.; Feigenson, G. W.; Freed, J. H. Dynamic Molecular Structure of DPPC-DLPC-Cholesterol Ternary Lipid System by Spin-Label Electron Spin Resonance Biophys. J. 2004, 87, 2483-2496
68. Swamy, M. J.; Ciani, L.; Ge, M.; Smith, A. K.; Holowka, D.; Baird, B.; Freed, J. H. Coexisting Domains in the Plasma Membranes of Live Cells Characterized by Spin-Label ESR Spectroscopy Biophys. J. 2006, 90, 4452-4465
69. Seelig, A.; Seelig, J. Effect of a Single Cis Double Bond on the Structure of a Phospholipid Bilayer Biochemistry 1977, 16, 45-50
70. Bahri, M. A.; Heyne, B. J.; Hans, P.; Seret, A. E.; Mouithys-Mickalad, A. A.; Hoebeke, M. D. Quantification of lipid bilayer effective microviscosity and fluidity effect induced by propofol Biophys. Chem. 2005, 114, 53-61
71. Suzuki, K. G. N.; Kasai, R. S.; Hirosawa, K. M.; Nemoto, Y.; Ishibashi, M.; Miwa, Y.; Fujiwara, T. K.; Kusumi, A. Transient GPI-anchored protein homodimers are units for raft organization and function Nat. Chem. Biol. 2012, 8, 774-783