Visualization of membrane rafts using a perylene monoimide derivative and fluorescence lifetime imaging

Biophysical Journal

Volumn 93, Issue 8, 2007, Pages 2877-2891

  Margineanu, Anca ^a   Hotta, Jun Ichi ^a   Van Der Auweraer, Mark ^a   Ameloot, Marcel ^b   Stefan, Alina ^a   Beljonne, David ^c   Engelborghs, Yves ^a   Herrmann, Andreas ^d   Müllen, Klaus ^d   De Schryver, Frans C ^a   Hofkens, Johan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b HASSELT UNIVERSITY   (Belgium)

^c UNIVERSITY OF MONS   (Belgium)

^d MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYE; IMIDE; ORGANIC SOLVENT; PERYLENE;

ABSORPTION; ARTICLE; ARTIFICIAL MEMBRANE; CELL ACTIVATION; CELL MEMBRANE; CHROMATOPHORE; FLUORESCENCE ANALYSIS; IMAGING; LIFESPAN; LIQUID; MOLECULE; QUANTUM YIELD; SEPARATION TECHNIQUE; TIME;

EID: 35348953114     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.100743     Document Type: Article

References (77)

1. Simons, K., and E. Ikonen. 1997. The fluid mosaic model of the structure of cell membranes. Nature. 387:569-572.
2. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
3. Dietrich, C., Z. N. Volovyk, M. Levi, N. L. Thompson, and K. Jacobson. 2001. Partitioning of Thy-1, GM1, and cross-linked phospholipids analogs into lipid rafts reconstituted in supported model membranes monolayers. Proc. Natl. Acad. Sci. USA. 98:10642-10647.
4. Dietrich, C., L. A. Bagatolli, Z. N. Volovyk, N. L. Thompson, M. Levi, K. Jacobson, and E. Gratton. 2001. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417-1428.
5. Crane, J. M., and L. K. Tamm. 2004. Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes. Biophys. J. 86:2965-2979.
6. Samsonov, A. V., I. Mihalyov, and F. S. Cohen. 2001. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys. J. 81:1486-1500.
7. Korlach, J., P. Schwille, W. W. Webb, and G. W. Feigenson. 1999. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA. 96: 8461-8466.
8. Feigenson, G. W., and J. T. Buboltz. 2001. Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol. Biophys. J. 80:2775-2788.
9. Veatch, S. L., and S. L. Keller. 2003. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85:3074-3083.
10. Baumgart, T., S. T. Hess, and W. W. Webb. 2003. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature. 425:821-824.
11. Scherfeld, D., N. Kahya, and P. Schwille. 2003. Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol. Biophys. J. 85:3758-3768.
12. Kahya, N., D. Scherfeld, K. Bacia, B. Poolman, and P. Schwille. 2003. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 278:28109-28115.
13. Kahya, N., D. Scherfeld, K. Bacia, and P. Schwille. 2004. Lipid domain formation and dynamics in giant unilamellar vesicles explored by fluorescence correlation spectroscopy. J. Struct. Biol. 147:77-89.
14. Bacia, K., D. Scherfeld, N. Kahya, and P. Schwille. 2004. Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87:1034-1043.
15. Janes, P. W., S. C. Ley, and A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:447-461.
16. Janes, P. W., S. C. Ley, A. I. Magee, and P. S. Kabouridis. 2000. The role of lipid rafts in T cell antigen receptor (TCR) signaling. Sem. Immunol. 12:23-34.
17. Subczynski, W. K., and A. Kusumi. 2003. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochim. Biophys. Acta. 1610:231-243.
18. Kusumi, A., I. Koyama-Honda, and K. Suzuki. 2004. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic. 5:213-230.
19. Pike, L. J. 2006. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47:1597-1598.
20. Kenworthy, A. K., N. Petranova, and M. Edidin. 2000. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol. Biol. Cell. 11:1645-1655.
21. de Almeida, R. F. M., L. M. S. Loura, A. Fedorov, and M. Prieto. 2005. Lipid rafts have different sizes depending on membrane composition: a time-resolved fluorescence resonance energy transfer study. J. Mol. Biol. 346:1109-1120.
22. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:798-801.
23. Schütz, G. J., G. Kada, V. P. Pastushenko, and H. Schindler. 2000. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J. 19:892-901.
24. Kuerschner, L., C. S. Ejsing, K. Ekroos, A. Shevchenko, K. I. Anderson, and C. Thiele. 2005. Polyene-lipids: a new tool to image lipids. Nat. Methods. 2:39-45.
25. Bagatolli, L. A., and E. Gratton. 2000. A correlation between lipid domain shape and binary phospholipids mixture composition in free standing bilayers: a two-photon fluorescence microscopy study. Biophys. J. 79:434-447.
26. Mukherjee, S., X. Zha, I. Tabas, and F. R. Maxfield. 1998. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75:1915-1925.
27. Wassif, C. A., D. Vied, M. Tsokos, W. E. Connor, R. D. Steiner, and F. D. Porter. 2002. Cholesterol storage defect in RSH/Smith-Lemli-Opitz syndrome fibroblasts. Mol. Genet. Metab. 75:325-334.
28. Parton, R. G., and A. A. Richards. 2003. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic. 4:724-738.
29. Weiss, S. 1999. Fluorescence spectroscopy of single biomolecules. Science. 283:1676-1683.
30. Margineanu, A., J. Hofkens, M. Cotlet, S. Habuchi, A. Stefan, J. Qu, C. Kohl, K. Muellen, J. Vercammen, Y. Engelborghs, T. Gensch, and F. C. De Schryver. 2004. Photophysics of a water-soluble rylene dye: comparison with other fluorescent molecules for biological applications. J. Phys. Chem. B. 108:12242-12251.
31. Verveer, P. J., F. S. Wouters, A. R. Reynolds, and P. I. H. Bastiaens. 2000. Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. Science. 290:1567-1570.
32. Herreros, J., T. Ng, and G. Schiavo. 2001. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell. 12:2947-2960.
33. Bastiaens, P. I. H., and A. Squire. 1999. Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in cells. Trends Cell Biol. 9:48-51.
34. Tadrous, P. J. 2000. Methods for imaging the structure and function of living tissues and cells: 2. Fluorescence lifetime imaging. J. Pathol. 191:229-234.
35. Barrow, D. A., and B. R. Lenz. 1985. Membrane ultrastructural domains. Resolution limits using diphenylhexatriene fluorescence decay. Biophys. J. 48:221-234.
36. Fiorini, R., E. Gratton, and G. Curatola. 1989. Effects of cholesterol on membrane microheterogeneity: a study using 1,6-diphenyl-1,3,5-hexatriene fluorescence lifetime distributions. Biochim. Biophys. Acta. 1006: 198-202.
37. Bernsdorff, C., R. Winter, T. L. Hazlett, and E. Gratton. 1995. Influence of cholesterol and β-sitosterol on the dynamic behavior of DPPC as detected by TMA-DPH and PyrPC fluorescence. A fluorescence lifetime distribution and time-resolved anisotropy study. Ber. Bunsenges. Phys. Chem. 99:1479-1488.
38. Mateo, C. R., A. U. Acuña, and J.-C. Brochon. 1995. Liquid-crystalline phases of cholesterol/lipid bilayers as revealed by the fluorescence of trans-parinaric acid. Biophys. J. 68:978-987.
39. Nyholm, T., M. Nylund, A. Söderholm, and J. P. Slotte. 2003. Properties of palmitoyl phosphatidylcholine, sphingomyelin, and dihydrosphingomyelin bilayer membranes as reported by different fluorescent reporter molecules. Biophys. J. 84:987-997.
40. Sinha, M., S. Mishra, and P. G. Joshi. 2003. Liquid-ordered microdomains in lipid rafts and plasma membrane of U-87 MG cells: a timeresolved fluorescence study. Eur. Biophys. J. 32:381-391.
41. Jin, L., A. C. Millard, J. P. Wuskell, X. Dong, D. Wu, H. A. Clark, and L. M. Loew. 2006. Characterization and application of a new optical probe for membrane lipid domains. Biophys. J. 90:2563-2575.
42. Owen, D. M., P. M. P. Lanigan, C. Dunsby, I. Munro, D. Grant, M. A. A. Neil, P. M. W. French, and A. I. Magee. 2006. Fluorescence lifetime imaging provides enhanced contrast when imaging the phase sensitive dye di-4-ANEPPDHQ in model membranes and live cells. Biophys. J. 90:L80-L82.
43. Vallée, R. A. L., M. Van der Auweraer, F. C. De Schryver, D. Beljonne, and M. Orrit. 2005. A microscopic model for the fluctuations of local field and spontaneous emission of single molecules in disordered media. ChemPhysChem. 6:81-91.
44. Weil, T., M. A. Abdalla, C. Jatzke, J. Hengstler, and K. Müllen. 2005. Water-soluble rylene dyes as high-performance colorants for the staining of cells. Biomacromolecules. 6:68-79.
45. Angelova, M. I., N. Hristova, and I. Tsoneva. 1999. DNA-induced endocytosis upon local microinjection to giant unilamellar cationic vesicles. Eur. Biophys. J. 28:142-150.
46. Angelova, M. I., and I. Tsoneva. 1999. Interactions of DNA with giant liposomes. Chem. Phys. Lipids. 101:123-137.
47. Lakowicz, J. R. 1986. Principles of Fluorescence Spectroscopy. Plenum Press, New York.
48. Lor, M., S. Jordens, G. De Belder, G. Schweitzer, E. Fron, L. Viaene, M. Cotlet, T. Weil, K. Müllen, J. W. Verhoeven, M. Van der Auweraer, and F. C. De Schryver. 2003. Direct proof of electron transfer in a rigid first generation triphenyl amine core dendrimer substituted with a peryleneimide acceptor. Photochem. Photobiol. Sci. 2:501-510.
49. Maus, M., M. Cotlet, J. Hofkens, T. Gensch, and F. De Schryver. 2001. An experimental comparison of the maximum likelihood estimator and nonlinear least-squares fluorescence lifetime analysis of single molecules. Anal. Chem. 73:2078-2086.
50. Cotlet, M., J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, and F. C. De Schryver. 2001. Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy. Proc. Natl. Acad. Sci. USA. 98:14398-14403.
51. Zerner, M. C., G. H. Loew, R. F. Kirchner, and U. T. Mueller-Westerhoff. 1980. Intermediate neglect of differential-overlap technique for spectroscopy of transition-metal complexes - ferrocene. J. Am. Chem. Soc. 102:589-599.
52. Vosch, T., M. Coltlet, J. Hofkens, K. Van Der Biest, M. Lor, K. Weston, P. Tinnefeld, M. Sauer, L. Latterini, K. Müllen, and F. C. De Schryver. 2003. Probing Förster type energy pathways in a first generation rigid dendrimer bearing two perylene imide chromophores. J. Phys. Chem. A. 107:6920-6931.
53. Lakowicz, J. R., H. Cherek, and B. P. Maliwal. 1985. Time-resolved fluorescence anisotropies of diphenylhexatriene and perylene in solvents and lipid bilayers obtained from multifrequency phasemodulation fluorometry. Biochemistry. 24:376-383.
54. Chong, P. L., B. W. van der Meer, and T. E. Thompson. 1985. The effects of pressure and cholesterol on rotational motions of perylene in lipid bilayers. Biochim. Biophys. Acta. 813:253-265.
55. Khan, T. K., and P. L. Chong. 2000. Studies of archaebacterial bipolar tetraether liposomes by perylene fluorescence. Biophys. J. 78:1390-1399.
56. Hofkens, J., M. Maus, T. Gensch, T. Vosch, M. Cotlet, F. Köhn, A. Herrmann, K. Müllen, and F. C. De Schryver. 2000. Probing photophysical processes in individual multichromophoric dendrimers by single-molecule spectroscopy. J. Am. Chem. Soc. 122:9278-9288.
57. Davenport, L., B. Shen, T. W. Joseph, and M. P. Straher. 2001. A novel fluorescent coronenyl-phospholipid analogue for investigations of submicrosecond lipid fluctuations. Chem. Phys. Lipids. 109:145-156.
58. Ballet, P., M. Van der Auweraer, F. C. De Schryver, H. Lemmetyinen, and E. Vuorimaa. 1996. Global analysis of the fluorescence decays of n,n′-dioctadecyl rhodamine B in Langmuir-Blodgett films of diacyl phosphatidic acids. J. Phys. Chem. 100:13701-13715.
59. Laguitton-Pasquier, H., M. Van der Auweraer, and F. C. De Schryver. 1998. Bidimensional distribution of a cyanine dye in LB monolayer studied by time-resolved and spatially resolved fluorescence. Langmuir. 14:5172-5183.
60. Janssens, L. D., N. Boens, M. Ameloot, and F. C. De Schryver. 1990. A systematic study of the global analysis of multi-exponential fluorescence decay surfaces using reference convolution. J. Phys. Chem. 94:3564-3576.
61. Beechem, J. M., E. Gratton, M. Ameloot, J. R. Knutson, and L. Brand. 1991. The global analysis of fluorescence intensity and anisotropy decay data:second-generation theory and programs. In Topics in Fluorescence Spectroscopy, Vol. 2, Principles. J. R. Lakowicz, editor. Plenum Press, New York.
62. Konopásek, I., P. Kvasnička, E. Amler, A. Kotyk, and G. Curatola. 1995. The transmembrane gradient of the dielectric constant influences the DPH lifetime distribution. FEBS Lett. 374:338-340.
63. Mitchell, D. C., and B. J. Litman. 1998. Effect of cholesterol on molecular order and dynamics in highly polyunsaturated phospholipid bilayers. Biophys. J. 75:896-908.
64. Arora, A., H. Raghuraman, and A. Chattopadhyay. 2004. Influence of cholesterol and ergosterol on membrane dynamics: a fluorescence approach. Biochem. Biophys. Res. Commun. 318:920-926.
65. Finkelstein, A. 1976. Water and nonelectrolyte permeability of lipid bilayer membranes. J. Gen. Physiol. 68:127-135.
66. Carruthers, A., and D. L. Melchior. 1983. Studies of the relationship between bilayer water permeability and physical state. Biochemistry. 22:5797-5807.
67. Tu, K., M. L. Klein, and D. J. Tobias. 1998. Constant-pressure molecular dynamics investigation of cholesterol effects in a dipalmitoylphosphatidylcholine bilayer. Biophys. J. 75:2147-2156.
68. Prendergast, F. G., R. P. Haugland, and P. J. Callahan. 1981. 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers. Biochemistry. 20:7333-7338.
69. El-Daly, S. A., M. H. Abdel-Kader, R. M. Issa, and E.-S. A. El-Sherbini. 2003. Influence of solvent polarity and medium acidity on the UV-Vis spectral behavior of 1-methyl-4-[4-amino-styryl] pyridinium iodide. Spectrochim. Acta [A]. 59:405-411.
70. Huang, J. 2002. Exploration of molecular interactions in cholesterol superlattices: effect of multibody interactions. Biophys. J. 83:1014-1025.
71. Vaz, W. L. C., and E. Melo. 2002. Fluorescence spectroscopic studies on phase heterogeneity in lipid bilayer membranes. J. Fluor. 11:255-271.
72. Bagatolli, L., and E. Gratton. 2000. A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: a two-photon fluorescence microscopy study. Biophys. J. 79: 434-447.
73. Cooper, G. M. 2000. The Cell: A Molecular Approach, 2nd Ed. American Society for Microbiology, Washington, DC. Sinauer Associates, Sunderland, MA.
74. Yu, W., P. T. C. So, T. French, and E. Gratton. 1996. Fluorescence generalized polarization of cell membranes: a two-photon scanning microscopy approach. Biophys. J. 70:626-636.
75. Gaus, K., E. Gratton, E. P. W. Kable, A. S. Jones, I. Gelissen, L. Kritharides, and W. Jessup. 2003. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. USA. 100:15554-15559.
76. Kim, H. M., H.-J. Choo, S.-Y. Jung, Y.-G. Ko, W.-H. Park, S.-J. Jeon, C. H. Kim, T. Joo, and B. R. Cho. 2007. A two-photon fluorescent probe for lipid raft imaging: C-laurdan. ChemBioChem. 8:553-559.
77. Cole, M. J., J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons-Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juškaitis, and T. Wilson. 2001. Timedomain whole-field fluorescence lifetime imaging with optical sectioning. J. Microsc. 203:246-257.