Monitoring biophysical properties of lipid membranes by environment-sensitive fluorescent probes

Biophysical Journal

Volumn 96, Issue 9, 2009, Pages 3461-3470

  Demchenko, Alexander P ^a   Mély, Yves ^b   Duportail, Guy ^b   Klymchenko, Andrey S ^b  

^a PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; FLUORESCENT DYE; GLYCEROL; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN; WATER;

APOPTOSIS; BILAYER MEMBRANE; BIOCHEMISTRY; BIOPHYSICS; CELL STRUCTURE; DIPOLE; ELECTRICITY; ENVIRONMENT; HYDRATION; HYDROGEN BOND; HYDROSTATIC PRESSURE; INFORMATION; LAMELLAR BODY; LIPID BILAYER; LIPID MEMBRANE; LIQUID; MEMBRANE; MEMBRANE POTENTIAL; MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PROBE; MONITORING; PHYSIOLOGY; POLARIZATION; REVIEW; SENSITIVITY ANALYSIS; SPECTROSCOPY; SURFACE PROPERTY; VISCOSITY; ANIMAL; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CHEMISTRY; FLUORESCENCE; FLUORESCENCE MICROSCOPY; HUMAN; MEMBRANE FLUIDITY; SPECTROFLUOROMETRY; STATIC ELECTRICITY;

ANIMALS; CELL MEMBRANE; FLUORESCENCE; FLUORESCENT DYES; HUMANS; LIPID BILAYERS; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; SPECTROMETRY, FLUORESCENCE; STATIC ELECTRICITY; WATER;

EID: 67650391443     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.012     Document Type: Review

References (73)

1. Lentz, B. R. 1989. Membrane 'fluidity' as detected by diphenylhexatriene probes. Chem. Phys. Lipids. 50:171-190.
2. Haidekker, M. A., and E. A. Theodorakis. 2007. Molecular rotors - fluorescent biosensors for viscosity and flow. Org. Biomol. Chem. 5:1669-1678.
3. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
4. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
5. Reichardt, C. 1994. Solvatochromic dyes as solvent polarity indicators. Chem. Rev. 94:2319-2358.
6. Lippert, E. L. 1975. Laser-spectroscopic studies of reorientation and other relaxation processes in solution. In Organic Molecular Photophysics J. B. Birks, editor. Wiley, New York. 1-31.
7. Cevc, G. 1990. Membrane electrostatics. Biochim. Biophys. Acta. 1031:311-382.
8. Kraayenhof, R., G. J. Sterk, and H. W. Wong Fong Sang. 1993. Probing biomembrane interfacial potential and pH profiles with a new type of float-like fluorophores positioned at varying distance from the membrane surface. Biochemistry. 32:10057-10066.
9. Gross, E., R. S. Bedlack, Jr., and L. M. Loew. 1994. Dual-wavelength ratiometric fluorescence measurement of the membrane dipole potential. Biophys. J. 67:208-216.
10. Fluhler, E., V. G. Burnham, and L. M. Loew. 1985. Spectra, membrane binding, and potentiometric reponses of new charge shift probes. Biochemistry. 24:5749-5755.
11. Disalvo, E. A., F. Lairion, F. Martini, E. Tymczyszyn, M. Frias, et al. 2008. Structural and functional properties of hydration and confined water in membrane interfaces. Biochim. Biophys. Acta. 1778:2655-2670.
12. Gawrisch, K., D. Ruston, J. Zimmerberg, V. A. Parsegian, R. P. Rand, et al. 1992. Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. Biophys. J. 61:1213-1223.
13. Parasassi, T., M. Di Stefano, M. Loiero, G. Ravagnan, and E. Gratton. 1994. Cholesterol modifies water concentration and dynamics in phospholipid bilayers: a fluorescence study using Laurdan probe. Biophys. J. 66:763-768.
14. Ho, C., S. J. Slater, and C. D. Stubbs. 1995. Hydration and order in lipid bilayers. Biochemistry. 34:6188-6195.
15. Jurkiewicz, P., J. Sýkora, A. Olżyńska, J. Humpoličkovà, and M. Hof. 2005. Solvent relaxation in phospholipid bilayers: principles and recent applications. J. Fluoresc. 15:883-894.
16. Klymchenko, A. S., G. Duportail, A. P. Demchenko, and Y. Mély. 2004. Bimodal distribution and fluorescence response of environment-sensitive probes in lipid bilayers. Biophys. J. 86:2929-2941.
17. Loew, L. M., and L. L. Simpson. 1981. Charge-shift probes of membrane potential. A probable electrochromic mechanism for p-aminostyrylpyridinium probes on a hemispherical lipid bilayer. Biophys. J. 34:353-365.
18. Klymchenko, A. S., G. Duportail, Y. Mély, and A. P. Demchenko. 2003. Ultrasensitive two-color fluorescence probes for dipole potential in phospholipid membranes. Proc. Natl. Acad. Sci. USA. 100:11219-11224.
19. Vivian, J. T., and P. R. Callis. 2001. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80:2093-2109.
20. Sýkora, J., P. Kapusta, V. Fidler, and M. Hof. 2002. On what time scale does solvent relaxation in phospholipid bilayers happen? Langmuir. 18:571-574.
21. Catalan, J., P. Perez, J. Laynez, and F. G. Blanco. 1991. Analysis of the solvent effect on the photophysics properties of 6-propionyl-2-(dimethylamino) naphthalene (PRODAN). J. Fluoresc. 1:215-223.
22. Bublitz, G. U., and S. G. Boxer. 1997. Stark spectroscopy: applications in chemistry, biology, and materials science. Annu. Rev. Phys. Chem. 48:213-242.
23. Clarke, R. J., and D. J. Kane. 1997. Optical detection of membrane dipole potential: avoidance of fluidity and dye-induced effects. Biochim. Biophys. Acta. 1323:223-239.
24. Jin, L., A. C. Millard, J. P. Wuskell, X. Dong, D. Wu, et al. 2006. Characterization and application of a new optical probe for membrane lipid domains. Biophys. J. 90:2563-2575.
25. Vitha, M. F., and R. J. Clarke. 2007. Comparison of excitation and emission ratiometric fluorescence methods for quantifying the membrane dipole potential. Biochim. Biophys. Acta. 1768:107-114.
26. De Silva, A. P., H. Q. N. Gunaratne, T. Gunnlaugsson, A. J. M. Huxley, C. P. McCoy, et al. 1997. Signaling recognition events with fluorescent sensors and switches. Chem. Rev. 97:1515-1566.
27. Demchenko, A. P., A. S. Klymchenko, V. G. Pivovarenko, S. Ercelen, G. Duportail, et al. 2003. Multiparametric color-changing fluorescence probes. J. Fluoresc. 13:291-295.
28. Shynkar, V. V., Y. Mély, G. Duportail, E. Piémont, A. S. Klymchenko, et al. 2003. Picosecond time-resolved fluorescence studies are consistent with reversible excited-state intramolecular proton transfer in 4′-(dialkylamino)-3-hydroxyflavones. J. Phys. Chem. A. 107:9522-9529.
29. Klymchenko, A. S., and A. P. Demchenko. 2003. Multiparametric probing of intermolecular interactions with fluorescent dye exhibiting excited state intramolecular proton transfer. Phys. Chem. Chem. Phys. 5:461-468.
30. Chou, P. T., S. C. Pu, Y. M. Cheng, W. S. Yu, Y. C. Yu, et al. 2005. Femtosecond dynamics on excited-state proton/ Charge-transfer reaction in 4′-N,N-diethylamino-3-hydroxyflavone. The role of dipolar vectors in constructing a rational mechanism. J. Phys. Chem. A. 109:3777-3787.
31. Yesylevskyy, S. O., A. S. Klymchenko, and A. P. Demchenko. 2005. Semi-empirical study of two-color fluorescent dyes based on 3-hydroxychromone. J. Mol. Struct. Theochem. 755:229-239.
32. Klymchenko, A. S., and A. P. Demchenko. 2002. Electrochromic modulation of excited-state intramolecular proton transfer: the new principle in design of fluorescence sensors. J. Am. Chem. Soc. 124:12372-12379.
33. Klymchenko, A. S., Y. Mély, A. P. Demchenko, and G. Duportail. 2004. Simultaneous probing of hydration and polarity of lipid bilayers with 3-hydroxyflavone fluorescent dyes. Biochim. Biophys. Acta. 1665:6-19.
34. Das, R., A. S. Klymchenko, G. Duportail, and Y. Mély. 2008. Excited state proton transfer and solvent relaxation of a 3-hydroxyflavone probe in lipid bilayers. J. Phys. Chem. B. 112:11929-11935.
35. Krishna, M. M. G. 1999. Excited-state kinetics of the hydrophobic probe Nile red in membranes and micelles. J. Phys. Chem. A. 103:3589-3595.
36. Sýkora, J., P. Jurkiewicz, R. M. Epand, R. Kraayenhof, M. Langner, et al. 2005. Influence of the curvature on the water structure in the head-group region of phospholipid bilayer studied by the solvent relaxation technique. Chem. Phys. Lipids. 135:213-221.
37. Jurkiewicz, P., A. Olżyńska, M. Langner, and M. Hof. 2006. Headgroup hydration and mobility of DOTAP/DOPC bilayers: a fluorescence solvent relaxation study. Langmuir. 22:8741-8749.
38. Chong, P. L. G. 1988. Effects of hydrostatic pressure on the location of PRODAN in lipid bilayers and cellular membranes. Biochemistry. 27:399-404.
39. Bagatolli, L. A. 2006. To see or not to see: lateral organization of biological membranes and fluorescence microscopy. Biochim. Biophys. Acta. 1758:1541-1556.
40. Bondar, O. P., and E. S. Rowe. 1999. Preferential interactions of fluorescent probe Prodan with cholesterol. Biophys. J. 76:956-962.
41. Alakoskela, J. M. I., and P. K. J. Kinnunen. 2001. Probing phospholipid main phase transition by fluorescence spectroscopy and a surface redox reaction. J. Phys. Chem. B. 105:11294-11301.
42. Demchenko, A. P., and N. V. Shcherbatska. 1985. Nanosecond dynamics of charged fluorescent probes at the polar interface of a membrane phospholipid bilayer. Biophys. Chem. 22:131-143.
43. Loura, L. M., and J. P. Ramalho. 2007. Location and dynamics of acyl chain NBD-labeled phosphatidylcholine (NBD-PC) in DPPC bilayers. A molecular dynamics and time-resolved fluorescence anisotropy study. Biochim. Biophys. Acta. 1768:467-478.
44. Huster, D., P. Muller, K. Arnold, and A. Herrmann. 2001. Dynamics of membrane penetration of the fluorescent 7-nitrobenz-2-oxa-1,3-diazol-4-yl (NBD) group attached to an acyl chain of phosphatidylcholine. Biophys. J. 80:822-831.
45. Kim, H. M., H. J. Choo, S. Y. Jung, Y. G. Ko, W. H. Park, et al. 2007. A two-photon fluorescent probe for lipid raft imaging: C-Laurdan. ChemBioChem. 8:553-559.
46. Klymchenko, A. S., G. Duportail, T. Oztürk, V. G. Pivovarenko, Y. Mély, et al. 2002. Novel two-band ratiometric fluorescence probes with different location and orientation in phospholipid membranes. Chem. Biol. 9:1199-1208.
47. Shynkar, V. V., A. S. Klymchenko, C. Kunzelmann, G. Duportail, C. D. Muller, et al. 2007. Fluorescent biomembrane probe for ratiometric detection of apoptosis. J. Am. Chem. Soc. 129:2187-2193.
48. Klymchenko, A. S., H. Stoeckel, K. Takeda, and Y. Mély. 2006. Fluorescent probe based on intramolecular proton transfer for fast ratiometric measurement of cellular transmembrane potential. J. Phys. Chem. B. 110:13624-13632.
49. Chattopadhyay, A., and S. Mukherjee. 1999. Depth-dependent solvent relaxation in membranes: wavelength-selective fluorescence as a membrane dipstick. Langmuir. 15:2142-2148.
50. Demchenko, A. P. 2002. The red-edge effects: 30 years of exploration. Luminescence. 17:19-42.
51. Sýkora, J., P. Slavicek, P. Jungwirth, J. Barucha, and M. Hof. 2007. Time-dependent stokes shifts of fluorescent dyes in the hydrophobic backbone region of a phospholipid bilayer: combination of fluorescence spectroscopy and ab initio calculations. J. Phys. Chem. B. 111:5869-5877.
52. Zhang, Y. L., J. A. Frangos, and M. Chachisvilis. 2006. Laurdan fluorescence senses mechanical strain in the lipid bilayer membrane. Biochem. Biophys. Res. Commun. 347:838-841.
53. Nicolini, C., A. Celli, E. Gratton, and R. Winter. 2006. Pressure tuning of the morphology of heterogeneous lipid vesicles: a two-photon-excitation fluorescence microscopy study. Biophys. J. 91:2936-2942.
54. Schuler, I., A. Milon, Y. Nakatani, G. Ourisson, A. M. Albrecht, et al. 1991. Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. USA. 88:6926-6930.
55. Hwan, M. K., H. J. Byeong, J. Y. Hyon, J. A. Myoung, S. S. Mun, et al. 2008. Two-photon fluorescent turn-on probe for lipid rafts in live cell and tissue. J. Am. Chem. Soc. 130:4246-4247.
56. Parasassi, T., G. De Stasio, G. Ravagnan, R. M. Rusch, and E. Gratton. 1991. Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophys. J. 60:179-189.
57. Bagatolli, L. A., and E. Gratton. 2000. Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys. J. 78:290-305.
58. Gidwani, A., D. Holowka, and B. Baird. 2001. Fluorescence anisotropy measurements of lipid order in plasma membranes and lipid rafts from RBL-2H3 mast cells. Biochemistry. 40:12422-12429.
59. M'Baye, G., Y. Mély, G. Duportail, and A. S. Klymchenko. 2008. Liquid ordered and gel phases of lipid bilayers: fluorescent probes reveal close fluidity but different hydration. Biophys. J. 95:1217-1225.
60. Dietrich, C., L. A. Bagatolli, Z. N. Volovyk, N. L. Thompson, M. Levi, et al. 2001. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417-1428.
61. Klymchenko, A. S., S. Oncul, P. Didier, E. Schaub, L. Bagatolli, et al. 2009. Visualization of lipid domains in giant unilamellar vesicles using an environment-sensitive membrane probe based on 3-hydroxyflavone. Biochim. Biophys. Acta. 1788:495-499.
62. Gibrat, R., C. Romieu, and C. Grignon. 1983. A procedure for estimating the surface potential of charged or neutral membranes with 8-anilino-1- naphthalenesulphonate probe. Adequacy of the Gouy-Chapman model. Biochim. Biophys. Acta. 736:196-202.
63. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods. 184:39-51.
64. Montana, V., D. L. Farkas, and L. M. Loew. 1989. Dual-wavelength ratiometric fluorescence measurements of membrane potential. Biochemistry. 28:4536-4539.
65. Kuhn, B., and P. Fromherz. 2003. Anellated hemicyanine dyes in a neuron membrane: molecular Stark effect and optical voltage recording. J. Phys. Chem. B. 107:7903-7913.
66. Malkov, D. Y., and V. S. Sokolov. 1996. Fluorescent styryl dyes of the RH series affect a potential drop on the membrane/solution boundary. Biochim. Biophys. Acta. 1278:197-204.
67. M'Baye, G., V. V. Shynkar, A. S. Klymchenko, Y. Mély, and G. Duportail. 2006. Membrane dipole potential as measured by ratiometric 3-hydroxyflavone fluorescence probes. Accounting for the hydration effects. J. Fluoresc. 7:1-8.
68. Shynkar, V. V., A. S. Klymchenko, G. Duportail, A. P. Demchenko, and Y. Mély. 2005. Two-color fluorescent probes for imaging the dipole potential of cell plasma membranes. Biochim. Biophys. Acta. 1712:128-136.
69. Antic, S., G. Major, and D. Zecevic. 1999. Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons. J. Neurophysiol. 82:1615-1621.
70. Bullen, A., and P. Saggau. 1999. High-speed, random-access fluorescence microscopy: II. Fast quantitative measurements with voltagesensitive dyes. Biophys. J. 76:2272-2287.
71. Wuskell, J. P., D. Boudreau, M. D. Wei, L. Jin, R. Engl, et al. 2006. Synthesis, spectra, delivery and potentiometric responses of new styryl dyes with extended spectral ranges. J. Neurosci. Methods. 151: 200-215.
72. Millard, A. C., L. Jin, M. D. Wei, J. P. Wuskell, A. Lewis, et al. 2004. Sensitivity of second harmonic generation from styryl dyes to transmembrane potential. Biophys. J. 86:1169-1176.
73. Fromherz, P., G. Hübener, B. Kuhn, and M. J. Hinner. 2008. ANNINE-6plus, a voltage-sensitive dye with good solubility, strong membrane binding and high sensitivity. Eur. Biophys. J. 37:509-514.