Photobleaching kinetics and time-integrated emission of fluorescent probes in cellular membranes

Molecules

Volumn 19, Issue 8, 2014, Pages 11096-11130

  Wüstner, Daniel ^a   Christensen, Tanja ^a   Solanko, Lukasz M ^a   Sage, Daniel ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b EPFL   (Switzerland)

Author keywords

Autofluorescence correction; BODIPY; Cholesterol; Kinetics; Photophysics; Transport

Indexed keywords

FLUORESCENT DYE;

ALGORITHM; BLEACHING; CELL MEMBRANE; CELL TRACKING; CHEMISTRY; FIBROBLAST; FLUORESCENCE MICROSCOPY; KINETICS; METABOLISM; PHOTOCHEMISTRY; REPRODUCIBILITY; THEORETICAL MODEL;

ALGORITHMS; CELL MEMBRANE; CELL TRACKING; FIBROBLASTS; FLUORESCENT DYES; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, THEORETICAL; PHOTOBLEACHING; PHOTOCHEMISTRY; REPRODUCIBILITY OF RESULTS;

EID: 84906711859     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules190811096     Document Type: Article

References (99)

1. Sönnichsen, B.; de Renzis, S.; Nielsen, E.; Rietdorf, J.; Zerial, M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol 2000, 149, 901-914.
2. Grant, B.; Hirsh, D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol. Cell 1999, 10, 4311-4326.
3. Ghosh, R.N.; Mallet, W.G.; Soe, T.T.; McGraw, T.E.; Maxfield, F.R. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol 1998, 142, 923-936.
4. Chen, I.; Ting, A.Y. Site-specific labeling of proteins with small molecules in live cells. Curr. Opin. Biotechnol 2005, 16, 35-40.
5. Ghosh, R.N.; Gelman, D.L.; Maxfield, F.R. Quantification of low density lipoprotein and transferrin endocytic sorting in HEp2 cells using confocal microscopy. J. Cell Sci. 1994, 107, 2177-2189.
6. Lipsky, N.G.; Pagano, R.E. A vital stain for the Golgi apparatus. Science 1989, 228, 745-747.
7. Pagano, RE.; Sepanski, M.A.; Martin, O.C. Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: Interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy. J. Cell Biol 1989, 109, 2067-2079.
8. Hao, M.; Lin, S.X.; Karylowski, O.J.; Wüstner, D.; McGraw, T.E.; Maxfield, F.R. Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J. Biol Chem. 2002, 277, 609-617.
9. Wüstner, D.; Mondal, M.; Tabas, I.; Maxfield, F.R. Direct observation of rapid internalization and intracellular transport of sterol by macrophage foam cells. Traffic 2005, 6, 396-412.
10. Wüstner, D.; Herrmann, A.; Hao, M.; Maxfield, F.R. Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells. J. Biol Chem. 2002, 277, 30325-30336.
11. Mayor, S.; Presley, J.F.; Maxfield, F.R. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol 1993, 121, 1257-1269.
12. Presley, J.F.; Mayor, S.; McGraw, T.E.; Dunn, K.W.; Maxfield, F.R. Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J. Biol Chem. 1997, 272, 13929-13936.
13. Hao, M.; Maxfield, F.R. Characterization of rapid membrane internalization and recycling. J. Biol Chem. 2000, 275, 15279-15286.
14. Van der Sijs, D.A.; van Faassen, E.E.; Levine, Y.K. The interpretation of fluorescence anisotropy decays of probe molecules in membrane systems. Chem. Phys. Lett. 1993, 216, 559-565.
15. Illinger, D.; Kuhry, J.-G. The kinetic aspects of intracellular fluorescence labeling with TMA-DPH support the maturation model for endocytosis in L929 cells. J. Cell Biol 1994, 125, 783-794.
16. Florine-Casteel, K. Phospholipid order in gel- and fluid phase cell-size liposomes measured by digitized video fluorescence polarization microscopy. Biophys. J. 1990, 57, 1199-1215.
17. Florine-Casteel, K.; Lemasters, J.J.; Herman, B. Lipid order in hepatocyte plasma membrane blebs during ATP-depletion measured by digitized video fluorescence polarization microscopy. FASEB J. 1991, 5, 2078-2084.
18. Gasecka, A.; Han, T.J.; Favard, C.; Cho, B.R.; Brasselet, S. Quantitative imaging of molecular order in lipid membranes using two-photon fluorescence polarimetry. Biophys. J. 2009, 97, 2854-2862.
19. Mukherjee, S.; Soe, T.T.; Maxfield, F.R. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol 1999, 144, 1271-1284.
20. Van Genderen, I.; van Meer, G. Differential targeting of glucosylceramide and galactosylceramide analogues after synthesis but not during transcytosis in Madin-Darby canine kidney cells. J. Cell Biol 1995, 131, 645-6554.
21. Van IJzendoorn, S.C.; Zegers, M.M.; Kok, J.W.; Hoekstra, D. Segregation of glucosylceramide and sphingomyelin occurs in the apical to basolateral transcytotic route in HepG2 cells. J. Cell Biol 1997, 137, 347-357.
22. Wüstner, D.; Mukherjee, S.; Maxfield, F.R.; Müller, P.; Hermann, A. Vesicular and nonvesicular transport of phosphatidylcholine in polarized HepG2 cells. Traffic 2001, 2, 277-296.
23. Wüstner, D. Fluorescent sterols as tools in membrane biophysics and cell biology. Chem. Phys. Lipids 2007, 146, 1-25.
24. Maxfield, F.R.; Wüstner, D. Analysis of cholesterol trafficking with fluorescent probes. Methods Cell Biol. 2012, 108, 367-393.
25. 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 2008, 9, 1839-1849.
26. Wüstner, D.; Solanko, L.M.; Sokol, E.; Lund, F.W.; Garvik, O.; Li, Z.; Bittman, R; Korte, T.; Herrmann, A. Quantitative assessment of sterol traffic in living cells by dual labeling with dehydroergosterol and BODIPY-cholesterol. Chem. Phys. Lipids 2011, 164, 221-235.
27. Wüstner, D. Following intracellular cholesterol transport by linear and non-linear optical microscopy of intrinsically fluorescent sterols. Curr. Pharm. Biotechnol. 2012, 13, 303-318.
28. Gimpl, G. Cholesterol-protein interaction: Methods and cholesterol reporter molecules. Subcell. Biochem. 2010, 51, 1-45.
29. Solanko, L.M.; Honigmann, A.; Midtiby, H.S.; Lund, F.W.; Brewer, J.R.; Dekaris, V.; Bittman, R; Eggeling, C.; Wüstner, D. Membrane orientation and lateral diffusion of BODIPY-cholesterol as a function of probe structure. Biophys. J. 2013, 105, 2082-2092.
30. Hiramoto-Yamaki, N.; Tanaka, K.A.; Suzuki, K.G.; Hirosawa, K.M.; Miyahara, M.S.; Kalay, Z.; Tanaka, K; Kasai, R.S.; Kusumi, A.; Fujiwara, T.K. Ultrafast diffusion of a fluorescent cholesterol analog in compartmentalized plasma membranes. Traffic 2014, 15, 583-612.
31. Mazères, S.; Schram, V.; Tocanne, J.F.; Lopez, A. 7-nitrobenz-2-oxa-1,3-diazole-4-yl-labeled phospholipids in lipid membranes: Differences in fluorescence behavior. Biophys. J. 1996, 71, 327-335.
32. Benson, D.M.; Bryan, J.; Plant, A.L.; Gotto, A.M.J.; Smith, L.C. Digital imaging fluorescence microscopy: Spatial heterogeneity of photobleaching rate constants in individual cells. J. Cell Biol. 1985, 100, 1309-1323.
33. Pagano, R.E.; Longmuir, K.J.; Martin, O.C. Intracellular translocation and metabolism of a fluorescent phosphatidic acid in cultured fibroblasts. J. Biol. Chem. 1983, 258, 2034-2040.
34. Martin, O.C.; Comly, M.E.; Blanchette-Mackie, E.J.; Pentchev, P.G.; Pagano, R.E. Cholesterol deprivation affects the fluorescence properties of a ceramide analog at the Golgi apparatus of living cells. Proc. Natl. Acad. Sci. USA 1993, 90, 2661-2665.
35. Hirschfeld, T. Quantum efficiency independence of the time integrated emission from a fluorescent molecule. Appl. Opt. 1976, 15, 3135-3139.
36. Wüstner, D.; Landt Larsen, A.; Færgeman, N.J.; Brewer, J.R.; Sage, D. Selective visualization of fluorescent sterols in Caenorhabditis elegans by bleach-rate based image segmentation. Traffic 2010, 11, 440-454.
37. ImageJ RSB Home Page-Image Processing and Analysis in Java. Available online: http://imagej.nih.gov/ij/ (accessed on 1 January 2014).
38. Bright, G.R.; Fisher, G.W.; Rogowska, J.; Taylor, D.L. Fluorescence ratio imaging microscopy. Methods Cell Biol. 1989, 30, 157-192.
39. Jovin, T.M.; Arndt-Jovin, D.J. FRET Microscopy: Digital imaging of fluorescence resonance energy transfer. Applications in cell biology. In Cell Structure and Function by Microspectrofluorometry; Kohen, E., Hirschberg, J.G., Eds.; Academic Press: Waltham, MA, USA, 1989; pp. 99-117.
40. White, J.C.; Stryer, L. Photostability studies of phycobiliprotein fluorescent labels. Anal. Biochem. 1987, 161, 442-452.
41. Ariola, F.S.; Li, Z.; Cornejo, C.; Bittman, R.; Heikal, A.A. Membrane fluidity and lipid order in ternary giant unilamellar vesicles using a new bodipy-cholesterol derivative. Biophys. J. 2009, 96, 2696-2708.
42. Chattopadhyay, A. Chemistry and biology of N-(7-nitrobenz-2-oxa-1,3- diazol-4-yl)-labeled lipids: Fluorescent probes of biological and model membranes. Chem. Phys. Lipids 1990, 53, 1-15.
43. Marks, D.L.; Bittman, R.; Pagano, R.E. Use of Bodipy-labeled sphingolipid and cholesterol analogs to examine membrane microdomains in cells. Histochem. Cell Biol. 2008, 130, 819-832.
44. MacDonald, R.I. Characteristics of self-quenching of the fluorescence of lipid-conjugated rhodamine in membranes. J. Biol. Chem. 1990, 265, 13533-13539.
45. Ghauharali, R.I.; Müller, M.; Buist, A.H.; Sosnowski, T.S.; Norris, T.B.; Squier, J.; Brakenhoff, G.J. Optical saturation measurements of fluorophores in solution with pulsed femtosecond excitation and two-dimensional CCD camera detection. Appl. Opt. 1997, 36, 4320-4328.
46. Lund, F.W.; Wüstner, D. A comparison of single particle tracking and temporal image correlation spectroscopy for quantitative analysis of endosome motility. J. Microsc. 2013, 252, 169-188.
47. Dulin, D.; le Gali, A.; Perronet, K.; Soler, N.; Fourmy, D.; Yoshizawa, S.; Bouyer, P.; Westbrook, N. Reduced photobleaching of BODIPY-FL. Phys. Procedia 2010, 3, 1563-1567.
48. Deschenes, L.A.; Vanden Bout, D.A. Single molecule photobleaching: Increased photon yield and survival time through suppression of two-step photolysis. Chem. Phys. Lett. 2002, 365, 387-395.
49. Kubitscheck, U.; Kircheis, M.; Schweitzer-Stenner, R.; Dreybrodt, W.; Jovin, T.M.; Pecht, I. Fluorescence resonance energy transfer on single living cells. Biophys. J. 1991, 60, 307-318.
50. Young, R.M.; Arnette, K.; Roess, D.A.; Barisas, B.G. Quantitation of fluorescence energy transfer between cell surface proteins via fluorescence donor photobleaching kinetics. Biophys. J. 1994, 67, 881-888.
51. Szabo, G.; Pine, P.S.; Weaver, J.L.; Kasari, M.; Aszalos, A. Epitope mapping by photobleaching fluorescence resonance energy-transfer measurements using a laser scanning microscope system. Biophys. J. 1992, 61, 661-670.
52. Wüstner, D.; Brewer, J.R.; Bagatolli, L.A.; Sage, D. Potential of ultraviolet widefield imaging and multiphoton microscopy for analysis of dehydroergosterol in cellular membranes. Microsc. Res. Tech. 2011, 74, 92-108.
53. Brandt, S. Datenanalyse; Spektrum Verlag: Heidelberg, Berlin, Germany, 1999.
54. Wüstner, D.; Solanko, L.M.; Lund, F.W.; Sage, D.; Schroll, J.A.; Lomholt, M.A. Quantitative fluorescence loss in photobleaching for analysis of protein transport and aggregation. BMC Bioinform. 2012, 13, 296.
55. Pourmousa, M.; Róg, T.; Mikkeli, R.; Vattulainen, I.; Solanko, L.; Wüstner, D.; List, N.; Kongsted, J.; Karttunen, M. Dehydroergosterol as an analogue for cholesterol: Why it mimics cholesterol so well or does It? J. Phys. Chem. B 2014, 118, 7345-7357.
56. Stöckl, M.; Plazzo, A.P.; Korte, T.; Herrmann, A. Detection of lipid domains in model and cell membranes by fluorescence lifetime imaging microscopy of fluorescent lipid analogues. J. Biol. Chem. 2008, 283, 30828-30837.
57. Smutzer, G.; Crawford, B.F.; Yeagle, P.L. Physical properties of the fluorescent sterol probe dehydroergosterol. Biochim. Biophys. Acta 1986, 862, 361-371.
58. 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.
59. Widengren, J.; Mets, Ü.; Rigler, R. Fluorescence correlation spectroscopy of triplet states in solution: A theoretical and experimental study. J. Phys. Chem. 1995, 99, 13368-13379.
60. Song, L.; Varma, C.A.; Verhoeven, J.W.; Tanke, H.J. Influence of the triplet excited state on the photobleaching kinetics of fluorescein in microscopy. Biophys. J. 1996, 70, 252959-252968.
61. Song, L.; Hennink, E.J.; Young, I.T.; Tanke, H.J. Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy. Biophys. J. 1995, 68, 2588-2600.
62. Song, L.; van Gijlswijk, R.P.M.; Young, I.T.; Tanke, H.J. Influence of fluorochrome labeling density on the photobleaching kinetics of fluorescein in microscopy. Cytometry 1997, 27, 213-223.
63. Boens, N.; Ameloot, M. Compartmental modeling and identifiability analysis in photophysics: Review. Int. J. Quant. Chem. 2005, 106, 300-315.
64. Toptygin, D.; Brand, L. Fluorescence decay of DPH in lipid membranes: Influence of the external refractive index. Biophys. Chem. 1993, 48, 205-220.
65. Krishna, M.M.G.; Periasamy, N. Orientational distribution of linear dye molecules in bilayer membranes. Chem. Phys. Lett. 1998, 298, 359-367.
66. Listenberger, L.L.; Brown, D.A. Fluorescent detection of lipid droplets and associated proteins. Curr. Protoc. Cell Biol. 2007, 24, doi:10.1002/ 0471143030.cb2402s35.
67. Berberan-Santos, M.N.; Bodunov, E.N.; Valeur, B. Mathematical functions for the analysis of luminescence decays with underlying distributions 1. Kohlrausch decay function (stretched exponential). Chem. Phys. 2005, 315, 171-182.
68. Kohlrausch, R. Theorie des elektrischen Rückstandes in der Leidner Flasche. Pogg. Ann. Phys. Chem. 1854, 91, 179-213.
69. Berberan-Santos, M.N. Luminescence decays with underlying distributions: General properties and analysis with mathematical functions. J. Luminesc. 2007, 126, 263-272.
70. Hinkeldey, B.; Schmitt, A.; Jung, G. Comparative photostability studies of BODIPY and fluorescein dyes by using fluorescence correlation spectroscopy. ChemPhysChem 2008, 9, 2019-2027.
71. Berberan-Santos, M.N. Mathematical basis of the integral formalism of chemical kinetics. Compact representation of the general solution of the first-order linear differential equation. J. Math. Chem. 2010, 47, 1184-1188.
72. Greenbaum, L.; Rothmann, Z.; Lavie, R.; Malik, Z. Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen. Biol. Chem. 2000, 381, 1251-1258.
73. Georgakoudi, I.; Foster, T.H. Singlet oxygen-versus nonsinglet oxygen-mediated mechanisms of sensitizer photobleaching and their effects on photodynamic dosimetry. Photochem. Photobiol. 1998, 67, 612-625.
74. Lee, P.C.; Rodgers, M.A.J. Singlet molecular oxygen in micellar systems. 1. Distribution Equilibria between hydrophobic and hydrophilic compartments. J. Phys. Chem. 1983, 87, 4894-4898.
75. Subczynski, W.K.; Hyde, J.S.; Kusumi, A. Oxygen permeability of phosphatidylcholine-Cholesterol membranes. Proc. Natl. Acad. Sci. USA 1989, 86, 4474-4478.
76. Bäumler, W.; Regensburger, J.; Knak, A.; Felgenträger, A.; Maisch, T. UVA and endogeneous photosensitizers - the detection of singlet oxygen by its luminescence. Photochem. Photobiol. Sci. 2012, 11, 107-117.
77. Sikorski, M.; Krystkowiak, E.; Steer, R.P. The kinetics of fast fluorescence quenching processes. J. Photochem. Photobiol. A Chem. 1998, 117, 1-16.
78. Weller, A. Eine verallgemeinerte theorie diffusionsbestimmter reaktionen und ihre anwendung auf die fluoreszenzlöschung. Z. Phys. Chem. 1957, 13, 335-352.
79. Mondal, M.; Mesmin, B.; Mukherjee, S.; Maxfield, F.R. Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol. Biol. Cell 2009, 20, 581-588.
80. Biomedical Imaging Group. PixBleach - Pixelwise analysis of bleach rate in time-lapse images. Available online: http://bigwww.epfl.ch/algorithms/ pixbleach/ (accessed on 1 June 2014).
81. Ghauharali, R.I.; Hofstraat, J.W.; Brakenhoff, G.J. Fluorescence photobleaching-based shading correction for fluorescence microscopy. J. Microsc. 1998, 192, 99-113.
82. Zwier, J.M.; van Rooij, G.J.; Hofstraat, J.W.; Brakenhoff, G.J. Image calibration in fluorescence microscopy. J. Microsc. 2004, 216, 15-24.
83. Koppel, D.E.; Carlson, C.; Smilowitz, H. Analysis of heterogeneous fluorescence photobleaching by video kinetics imaging: The method of cumulants. J. Microsc. 1989, 155, 199-206.
84. Van Oostveldt, P.; Verhaegen, F.; Messens, K. Heterogeneous photobleaching in confocal microscopy caused by differences in refractive index and excitation mode. Cytometry 1998, 32, 137-146.
85. Kalyansundaram, K.; Thomas, J.K. Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems. J. Am. Chem. Soc. 1977, 99, 2039-2044.
86. Somerharju, P. Pyrene-labeled lipids as tools in membrane biophysics and cell biology. Chem. Phys. Lett. 2002, 116, 57-74.
87. Albro, P.W.; Bilski, P.; Corbett, J.T.; Schroeder, J.L.; Chignell, C.F. Photochemical reactions and phototoxicity of sterols: Novel self-perpetuating mechanisms for lipid photoxidation. Photochem. Photobiol. 1997, 66, 316-325.
88. Eggeling, C.; Widengren, J.; Rigler, R.; Seidel, C.A.M. Photobleaching of fluorescent dyes under conditions used for single-molecule detection: Evidence of two-step photolysis. Anal. Chem. 1998, 70, 2651-2659.
89. Gensch, T.; Böhmer, M.; Aramendia, P.F. Single molecule blinking and photobleaching separated by wide-field fluorescence microscopy. J. Phys. Chem. 2005, 109, 6652-6658.
90. Bernas, T.; Zaresbski, M.; Cook, R.R.; Dobrucki, J.W. Minimizing photobleaching during confocal microscopy of fluorescent probes bound to chromatin: Role of anoxia and photon flux. J. Microscopy 2004, 215, 281-296.
91. Baranyai, P.; Gangl, S.; Grabner, G.; Knapp, M.; Köhler, G.; Vidoczy, T. Using the decay of incorporated photoexcited triplet probes to study unilamellar phospholipid bilayer membranes. Langmuir 1999, 15, 7577-7584.
92. Murray, J.M.; Appleton, P.L.; Swedlow, J.R.; Waters, J.C. Evaluating performance in three-dimensional fluorescence microscopy. J. Microscopy 2007, 228, 390-405.
93. Velez, M.; Axelrod, D. Polarized fluorescence photobleaching recovery for measuring rotational diffusion in solutions and membranes. Biophys. J. 1988, 53, 575-591.
94. Sinnecker, D.; Voigt, P.; Hellwig, N.; Schaefer, M. Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 2005, 44, 7085-7094.
95. Mueller, F.; Morisaki, T.; Mazza, D.; McNally, J.G. Minimizing the impact of photoswitching of fluorescent proteins on FRAP analysis. Biophys. J. 2012, 102, 1656-1665.
96. Daddysman, M.K.; Fecko, C.J. Revisiting point FRAP to quantitatively characterize anomalous diffusion in live cells. J. Phys. Chem. 2013, 117, 1241-1251.
97. Ringemann, C.; Schönle, A.; Giske, A.; von Middendorff, C.; Hell, S.W.; Eggeling, C. Enhancing fluorescence brightness: Effect of reverse intersystem crossing studied by fluorescence fluctuation spectroscopy. ChemPhysChem 2008, 9, 612-624.
98. Füreder-Kitzmüller, E.; Hesse, J.; Ebner, A.; Gruber, H.J.; Schütz, G.J. Non-exponential bleaching of single bioconjugated Cy5 molecules. Chem. Phys. Lett. 2005, 404, 13-18.
99. Levin, P.P.; Costa, S.M.P. Kinetics of oxygen induced delayed fluorescence of eosin adsorbed on alumina. The dependence on dye and oxygen concentrations. Chem. Phys. Lett. 2000, 320, 194-201.