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Fluorescence recovery after photobleaching in material and life sciences: putting theory into practice

Published online by Cambridge University Press:  28 August 2015

Niklas Lorén*
Affiliation:
SP Food and Bioscience, PO 5401, SE-402 29, Göteborg, Sweden
Joel Hagman
Affiliation:
SP Food and Bioscience, PO 5401, SE-402 29, Göteborg, Sweden
Jenny K. Jonasson
Affiliation:
Department of Mathematical Sciences, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
Hendrik Deschout
Affiliation:
Biophotonic Imaging Group, Laboratory of General Biochemistry and Physical Pharmacy, Ghent University, 9000 Ghent, Belgium Centre for Nano- and Biophotonics, Ghent University, 9000 Ghent, Belgium
Diana Bernin
Affiliation:
Department of Chemical and Biological Engineering, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
Francesca Cella-Zanacchi
Affiliation:
Nanophysics Department, Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
Alberto Diaspro
Affiliation:
Nanophysics Department, Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
James G. McNally
Affiliation:
Institute for Soft Matter and Functional Materials, Helmholtz Center Berlin, 12489 Berlin, Germany
Marcel Ameloot
Affiliation:
Hasselt University, Campus Diepenbeek, Martelarenlaan 42, 3500 Hasselt, Belgium
Nick Smisdom
Affiliation:
Hasselt University, Campus Diepenbeek, Martelarenlaan 42, 3500 Hasselt, Belgium Environmental Risk and Health Unit, Flemish Institute for Technological Research, Boeretang 200, 2400 Mol, Belgium
Magnus Nydén
Affiliation:
Ian Wark Research Institute, University of South Australia, Adelaide, Australia
Anne-Marie Hermansson
Affiliation:
SP Food and Bioscience, PO 5401, SE-402 29, Göteborg, Sweden Department of Chemical and Biological Engineering, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
Mats Rudemo
Affiliation:
Department of Mathematical Sciences, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
Kevin Braeckmans
Affiliation:
Biophotonic Imaging Group, Laboratory of General Biochemistry and Physical Pharmacy, Ghent University, 9000 Ghent, Belgium Centre for Nano- and Biophotonics, Ghent University, 9000 Ghent, Belgium
*
*Author for correspondence: N. Lorén, Structure and Material Design, SP Food and Bioscience, PO 5401, SE-402 29, Göteborg, Sweden. Tel: +46 10 516 6614; Fax: +46 31 83 37 82; Email: niklas.loren@sp.se

Abstract

Fluorescence recovery after photobleaching (FRAP) is a versatile tool for determining diffusion and interaction/binding properties in biological and material sciences. An understanding of the mechanisms controlling the diffusion requires a deep understanding of structure–interaction–diffusion relationships. In cell biology, for instance, this applies to the movement of proteins and lipids in the plasma membrane, cytoplasm and nucleus. In industrial applications related to pharmaceutics, foods, textiles, hygiene products and cosmetics, the diffusion of solutes and solvent molecules contributes strongly to the properties and functionality of the final product. All these systems are heterogeneous, and accurate quantification of the mass transport processes at the local level is therefore essential to the understanding of the properties of soft (bio)materials. FRAP is a commonly used fluorescence microscopy-based technique to determine local molecular transport at the micrometer scale. A brief high-intensity laser pulse is locally applied to the sample, causing substantial photobleaching of the fluorescent molecules within the illuminated area. This causes a local concentration gradient of fluorescent molecules, leading to diffusional influx of intact fluorophores from the local surroundings into the bleached area. Quantitative information on the molecular transport can be extracted from the time evolution of the fluorescence recovery in the bleached area using a suitable model. A multitude of FRAP models has been developed over the years, each based on specific assumptions. This makes it challenging for the non-specialist to decide which model is best suited for a particular application. Furthermore, there are many subtleties in performing accurate FRAP experiments. For these reasons, this review aims to provide an extensive tutorial covering the essential theoretical and practical aspects so as to enable accurate quantitative FRAP experiments for molecular transport measurements in soft (bio)materials.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2015 

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References

9. References

Al Tanoury, Z., Schaffner-Reckinger, E., Halavatyi, A., Hoffmann, C., Moes, M., Hadzic, E., Catillon, M., Yatskou, M. & Friederich, E. (2010). Quantitative kinetic study of the actin-bundling protein L-plastin and of its impact on actin turn-over. PLoS ONE 5, e9210.Google Scholar
Alvarez-Manceñido, F., Braeckmans, K., De Smedt, S. C., Demeester, J., Landin, M. & Martínez-Pacheco, R. (2006). Characterization of diffusion of macromolecules in konjac glucomannan solutions and gels by fluorescence recovery after photobleaching technique. International Journal of Pharmaceutics 316, 3746.Google Scholar
Arrio-Dupont, M., Foucault, G., Vacher, M., Devaux, P. F. & Cribier, S. (2000). Translational diffusion of globular proteins in the cytoplasm of cultured muscle cells. Biophysical Journal 78, 901907.Google Scholar
Axelrod, D. (1983). Lateral motion of membrane proteins and biological function. Journal of Membrane Biology 75, 110.Google Scholar
Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. & Webb, W. W. (1976a). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophysical Journal 16, 10551069.Google Scholar
Axelrod, D., Ravdin, P., Koppel, D. E., Schlessinger, J., Webb, W. W., Elson, E. L. & Podleski, T. R. (1976b). Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers. Proceedings of the National Academy of Sciences of the United States of America 73, 45944598.Google Scholar
Balakrishnan, G., Nicolai, T. & Durand, D. (2012). Relation between the gel structure and the mobility of tracers in globular protein gels. Journal of Colloid and Interface Science 388, 293299.Google Scholar
Bancaud, A., Huet, S., Daigle, N., Mozziconacci, J., Beaudouin, J. & Ellenberg, J. (2009). Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO Journal 28, 37853798.Google Scholar
Basser, P. J., Mattiello, J. & Lebihan, D. (1994). Estimation of the effective self-diffusion tensor from the NMR spin echo. Journal of Magnetic Resonance Series B 103, 247254.Google Scholar
Beaudouin, J., Mora-Bermudez, F., Klee, T., Daigle, N. & Ellenberg, J. (2006). Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophysical Journal 90, 18781894.Google Scholar
Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, W. O., Olenych, S., Bonifacino, J. S., Davidson, M. W., Lippincott-Schwartz, J. & Hess, H. F. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 16421645.Google Scholar
Black, J. C., Cheney, P. P., Campbell, T. & Knowles, M. K. (2014). Membrane curvature based lipid sorting using a nanoparticle patterned substrate. Soft Matter 10, 20162023.Google Scholar
Blonk, J. C. G., Don, A., Van Aalst, H. & Birmingham, J. J. (1993). Fluorescence photobleaching recovery in the confocal scanning light microscope. Journal of Microscopy 169, 363374.Google Scholar
Born, M. & Wolf, E. (1999). Principles of Optics. 7th edn. Cambridge University Press, Cambridge.Google Scholar
Braeckmans, K., Peeters, L., Sanders, N. N., De Smedt, S. C.& Demeester, J. (2003). Three-dimensional fluorescence recovery after photobleaching with the confocal scanning laser microscope. Biophysical Journal 85, 22402252.Google Scholar
Braeckmans, K., Remaut, K., Vandenbroucke, R. E., Lucas, B., De Smedt, S. C. & Demeester, J. (2007). Line FRAP with the confocal laser scanning microscope for diffusion measurements in small regions of 3-D samples. Biophysical Journal 92, 21722183.Google Scholar
Braeckmans, K., Stubbe, B. G., Remaut, K., Demeester, J. & De Smedt, S. C. (2006). Anomalous photobleaching in fluorescence recovery after photobleaching measurements due to excitation saturation – a case study for fluorescein. Journal of Biomedical Optics 11, 044013.Google Scholar
Braga, J., Desterro, J. M. P. & Carmo-Fonseca, M. (2004). Intracellular macromolecular mobility measured by fluorescence recovery after photobleaching with confocal laser scanning microscopes. Molecular Biology of the Cell 15, 47494760.Google Scholar
Braga, J., McNally, J. G. & Carmo-Fonseca, M. (2007). A reaction-diffusion model to study RNA motion by quantitative fluorescence recovery after photobleaching. Biophysical Journal 92, 26942703.Google Scholar
Branco, M. C., Pochan, D. J., Wagner, N. J. & Schneider, J. P. (2009). Macromolecular diffusion and release from self-assembled β-hairpin peptide hydrogels. Biomaterials 30, 13391347.Google Scholar
Brandl, F., Hammer, N., Blunk, T., Tessmar, J. & Goepferish, A. (2010). Biodegradable hydrogels for time-controlled release of tethered peptides or proteins. Biomacromolecules 11, 496504.Google Scholar
Brown, E. B., Bouchera, Y., Nasser, S. & Jain, R. K. (2004). Measurement of macromolecular diffusion coefficients in human tumors. Microvascular Research 67, 231236.Google Scholar
Brown, E. B., Wu, E. S., Zipfel, W. & Webb, W. W. (1999). Measurement of molecular diffusion in solution by multiphoton fluorescence photobleaching recovery. Biophysical Journal 77, 28372849.Google Scholar
Brown, R. (1828). On the particles contained in the pollen of plants and on the general existence of active molecules in organic and inorganic bodies. Edinburgh New Philosophical Journal July–September, 358371.Google Scholar
Brown, R. (1829). Additional remarks on active molecules. Edinburgh Journal of Science 1, 314319.Google Scholar
Cardarelli, F., Serresi, M., Bizzarri, R., Giacca, M. & Beltram, F. (2007). In vivo study of HIV-1 Tat arginine-rich motif unveils its transport properties. Molecular Therapy 15, 13131322.Google Scholar
Carr, H. & Purcell, E. (1954). Effects of diffusion on free precision in nuclear magnetic resonance experiments. Physical Review 94, 630638.Google Scholar
Carrero, G., Crawford, E., Hendzel, M. J. & de Vries, G. (2004). Characterizing fluorescence recovery curves for nuclear proteins undergoing binding events. Bulletin of Mathematical Biology 66, 15151545.Google Scholar
Carvajal-Rondanelli, P. A. & Lanier, T. C. (2010). Diffusion of active proteins into fish meat to minimize proteolytic degradation. Journal of Agricultural and Food Chemistry 58, 53005307.Google Scholar
Cézanne, L., Lecat, S., Lagane, B., Millot, C., Vollmer, J-Y., Matthes, H., Galzi, J-L. & Lopez, A. (2004). Dynamic confinement of NK2 receptors in the plasma membrane. Improved FRAP analysis and biological relevance. Journal of Biological Chemistry 279, 4505745067.Google Scholar
Chaikin, P. & Lubensky, T. (1995). Principles of Condensed Matter Physics. Cambridge University Press, Cambridge.Google Scholar
Chen, Y., Lagerholm, B. C., Yang, B. & Jacobson, K. (2006). Methods to measure the lateral diffusion of membrane lipids and proteins. Methods 39, 147153.Google Scholar
Cheng, Y., Prud'homme, R. K. & Thomas, J. L. (2002). Diffusion of mesoscopic probes in aqueous polymer solutions measured by fluorescence recovery after photobleaching. Macromolecules 35, 81118121.Google Scholar
Cherry, R. J. (1979). Rotational and lateral diffusion of membrane proteins. Biochimica et Biophysica Acta 559, 289327.Google Scholar
Cherry, R. J., Smith, P. R., Morrison, I. E. & Fernandez, N. (1998). Mobility of cell surface receptors: a re-evaluation. FEBS Letters 430, 8891.Google Scholar
Clark, D. C., Mackie, A. R., Wilde, P. J. & Wilson, D. R. (1994). Differences in the structure and dynamics of adsorbed layers in protein-stabilized model foams and emulsions. Faraday Discussions 98, 253262.Google Scholar
Clark, D. C., Wilde, P. J. & Wilson, D. R. (1990). The effect of pre-isomerised hop extract on the properties of model protein stabilized foams. Journal of the Institute Brewing 97, 169172.Google Scholar
Costantini, L. & Snapp, E. (2013). Probing endoplasmic reticulum dynamics using fluorescence imaging and photobleaching techniques. Current Protocols in Cell Biology 60, Unit 21.7.Google Scholar
Crank, J. (1975). The Mathematics of Diffusion, 2nd edn. Clarendon Press, Oxford.Google Scholar
Cussler, E. (1997). Diffusion Mass Transfer in Fluid Systems, 2nd edn. Cambridge University Press, Cambridge.Google Scholar
Daddysman, M. K. & Fecko, C. J. (2013). Revisiting point FRAP to quantitatively characterize anomalous diffusion in live cells. Journal of Physical Chemistry B 117, 12411251.Google Scholar
Davoust, J., Devaux, P. F. & Leger, L. (1982). Fringe pattern photobleaching, a new method for the measurement of transport coefficients of biological macromolecules. EMBO Journal 1, 12331238.Google Scholar
Dayel, M. J., Hom, E. F. & Verkman, A. S. (1999). Diffusion of green fluorescent protein in the aqueous-phase lumen of endoplasmic reticulum. Biophysical Journal 76, 28432851.Google Scholar
De Clercq, B., Cleuren, B., Deschout, H., Braeckmans, K. & Ameloot, M. (2013). Distinguishing free and anomalous diffusion by rectangular fluorescence recovery after photobleaching: a Monte Carlo study. Journal of Biomedical Optics 18, 076012.Google Scholar
de Gennes, P.-G. (1992). Simple Views on Condensed Matter. World Scientific, Singapore.Google Scholar
Derichs, N., Jin, B-J., Song, Y., Finkbeiner, W. E. & Verkman, A. S. (2011). Hyperviscous airway periciliary and mucous liquid layers in cystic fibrosis measured by confocal fluorescence photobleaching. FASEB Journal 25, 23252332.Google Scholar
Deschout, H., Cella Zanacchi, F., Mlodzianoski, M., Diaspro, A., Bewersdorf, J., Hess, S. T. & Braeckmans, K. (2014). Precisely and accurately localizing single emitters in fluorescence microscopy. Nature Methods 11, 253266.Google Scholar
Deschout, H., Hagman, J., Fransson, S., Jonasson, J., Rudemo, M., Lorén, N. & Braeckmans, K. (2010). Straightforward FRAP for quantitative diffusion measurements with a laser scanning microscope. Optics Express 18, 2288622905.Google Scholar
Deschout, H., Raemdonck, K., Demeester, J., De Smedt, S. C. & Braeckmans, K. (2013). FRAP in pharmaceutical research: practical guidelines and applications in drug delivery. Pharmaceutical Research 31, 255270.Google Scholar
De Smedt, S. C., Remaut, K., Lucas, B., Braeckmans, K., Sanders, N. N. & Demeester, J. (2005). Studying biophysical barriers to DNA delivery by advanced light microscopy. Advanced Drug Delivery Reviews 57, 191210.Google Scholar
Dhitala, S., Shelata, K. J., Shrestha, A. K. & Gidleya, M. J. (2013). Heterogeneity in maize starch granule internal architecture deduced from diffusion of fluorescent dextran probes. Carbohydrate Polymers 93, 365373.Google Scholar
Diaspro, A. (2010). Nanoscopy and Multidimensional Optical Fluorescence Microscopy, Chapter 8. Chapman & Hall/CRC, Boca Raton, Florida.Google Scholar
Digman, M. A., Brown, C. M., Sengupta, P., Wiseman, P. W., Horwitz, A. R. & Gratton, E. (2005a). Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophysical Journal 89, 13171327.Google Scholar
Digman, M. A. & Gratton, E. (2009). Analysis of diffusion and binding in cells using the RICS approach. Microscopy Research and Technique 72, 323332.Google Scholar
Digman, M. A., Sengupta, P., Wiseman, P. W., Brown, C. M., Horwitz, A. R. & Gratton, E. (2005b). Fluctuation correlation spectroscopy with a laser-scanning microscope: exploiting the hidden time structure. Biophysical Journal 88, L33L36.Google Scholar
Dill, K. & Bromberg, S. (2003). Molecular Driving Forces. Garland Science, London.Google Scholar
Dix, J. A. & Verkman, A. S. (2008). Crowding effects on diffusion in solutions and cells. Annual Review in Biophysics 37, 247263.Google Scholar
Dushek, O., Das, R. & Coombs, D. (2008). Analysis of membrane-localized binding kinetics with FRAP. European Biophysics Journal 37, 627638.Google Scholar
Edward, J. (1970). Molecular volumes and the Stokes-Einstein equation. Journal of Chemical Education 47, 261270.Google Scholar
Einstein, A. (1905). Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen. Annalen der Physik 17, 549560.Google Scholar
Endress, E., Wiegelt, S., Reents, G. & Bayer, T. M. (2005). Derivation of a closed form analytical expression for fluorescence recovery after photobleaching in the case of continuous bleaching during readout. The European Physics Journal E 16, 8187.Google Scholar
Erdel, F. & Rippe, K. (2012). Quantifying transient binding of ISWI chromatin remodelers in living cells by pixel-wise photobleaching profile evolution analysis. Proceedings of the National Academy of Sciences of the United States of America 109, E3221E3230.Google Scholar
Feder, T. J., Brust-Mascher, I., Slattery, J. P., Baird, B. & Webb, W. W. (1996). Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophysical Journal 70, 27672773.Google Scholar
Fick, A. (1855). Über diffusion. Annalen der Physik und Chemie 94, 5986.Google Scholar
Floury, J., Madec, M.-N., Waharte, F., Jeanson, S. & Lortal, S. (2012). First assessment of diffusion coefficients in model cheese by fluorescence recovery after photobleaching (FRAP). Food Chemistry 133, 551556.Google Scholar
Frye, L. D. & Edidin, M. (1970). The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons. Journal of Cell Science 7, 319335.Google Scholar
García-Sáez, A. J. & Schwille, P. (2010). Surface analysis of membrane dynamics. Biochimica et Biophysica Acta 1798, 766776.Google Scholar
Ghosh, V., Ziegler, G. R. & Anantheswaran, R. C. (2002). Fat, moisture and ethanol migration through chocolates and confectionary coatings. Critical Reviews in Food Science and Nutrition 42, 583626.Google Scholar
Gonzalez-Gonzalez, I. M., Jaskolski, F., Goldberg, Y., Ashby, M. C. & Henley, J. M. (2012). Measuring membrane protein dynamics in neurons using fluorescence recovery after photobleach. Methods in Enzymology 504, 127146.Google Scholar
González-Pérez, V., Schmierer, B., Hill, C. S. & Sear, R. P. (2011). Studying Smad2 intranuclear diffusion dynamics by mathematical modelling of FRAP experiments. Integrative Biology 3, 197207.Google Scholar
Gordon, G., Chazotte, B., Wang, X. F. & Herman, B. (1995). Analysis of simulated and experimental fluorescence recovery after photobleaching data for two diffusing components. Biophysical Journal 68, 766778.Google Scholar
Green, P. (2005). Kinetics, Transport and Structure in Hard and Soft Materials. CRC Press, New York.Google Scholar
Groeneweg, F. L., van Royen, M. E., Fenz, S., Keizer, V. I., Geverts, B., Prins, J., de Kloet, E. R., Houtsmuller, A. B., Schmidt, T. S. & Schaaf, M. J. (2014). Quantitation of glucocorticoid receptor DNA-binding dynamics by single-molecule microscopy and FRAP. PLoS ONE 9(3): e90532.Google Scholar
Guizar-Sicairos, M. & Gutierrez-Vega, J. C. (2004). Computation of quasi-discrete Hankel transforms of integer order for propagating optical wave fields. Journal of Optical Society of America A 21, 5358.Google Scholar
Hager, G. L., McNally, J. G. & Misteli, T. (2009). Transcription dynamics. Molecular Cell 35, 741753.Google Scholar
Hagman, J., Lorén, N. & Hermansson, A.-M. (2010). Effect of gelatin gelation kinetics on probe diffusion determined by FRAP and rheology. Biomacromolecules 11, 33593366.Google Scholar
Hagman, J., Lorén, N. & Hermansson, A.-M. (2012). Probe diffusion in κ-carrageenan gels determined by fluorescence recovery after photobleaching. Food Hydrocolloids 29, 106115.Google Scholar
Haj, F. G., Sabet, O., Kinkhabwala, A., Wimmer-Kleikamp, S., Roukos, V., Han, H. M., Grabenbauer, M., Bierbaum, M., Antony, C., Neel, B. G. & Bastiaens, P. I. (2012). Regulation of signaling at regions of cell-cell contact by endoplasmic reticulum-bound protein-tyrosine phosphatase 1B. PLoS ONE 7, e36633.Google Scholar
Hallen, M. A., Ho, J., Yankel, C. D. & Endow, S. A. (2008a). Fluorescence recovery kinetic analysis of gamma-tubulin binding to the mitotic spindle. Biophysical Journal 95, 30483058.Google Scholar
Hallen, M. A. & Layton, A. T. (2010). Expanding the scope of quantitative FRAP analysis. Journal of Theoretical Biology 262, 295305.Google Scholar
Hallen, M. A., Liang, Z. Y. & Endow, S. A. (2008b). Ncd motor binding and transport in the spindle. Journal of Cell Science 121, 38343841.Google Scholar
Hansen, J.-P. & McDonald, R. (2006). Theory of Simple Liquids, 3rd edn. Elsevier, Amsterdam.Google Scholar
Hardy, L. R. (2012). Fluorescence recovery after photobleaching (FRAP) with a focus on F-actin. Current Protocol in Neurosciences, Chapter 2: Unit 2.17.Google Scholar
Hawlicka, E. (1995). Self-diffusion in multicomponent liquid systems. Chemical Society Reviews 24, 367377.Google Scholar
Hebert, B., Costantino, S. & Wiseman, P. W. (2005). Spatiotemporal image correlation spectroscopy (STICS) theory, verification, and application to protein velocity mapping in living CHO cells. Biophysical Journal 88, 36013614.Google Scholar
Heitjans, P. & Kärger, J. (2005). Diffusion in Condensed Matter. Berlin, Heidelberg: Springer-Verlag.Google Scholar
Hell, S. W. & Wichmann, J. (1994). Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Optics Letters 19, 780782.Google Scholar
Hellriegel, C., Kirstein, J., Brauchle, C., Latour, V., Pigot, T., Olivier, R., Lacombe, S., Brown, R., Guieu, V. & Payrastre, C. (2004). Diffusion of single streptocyanine molecules in the nanoporous network of sol–gel glasses. Journal of Physical Chemistry B 108, 1469914709.Google Scholar
Hellriegel, C., Kirstein, J. & Brauchle, C. (2005). Tracking of single molecules as a powerful method to characterize diffusivity of organic species in mesoporous materials. New Journal of Physics 7(23): 114.Google Scholar
Herman, B. (1998). Fluorescence Microscopy. UK: BIOS Scientific Publishers, Royal Microscopical Society.Google Scholar
Hermansson, A.-M., Lorén, N. & Nydén, M. (2006). The importance of microstructure for solvent and solute diffusion on the micro and nano length scales. In Water Properties of Food, Pharmaceutical, and Biological Materials (eds. del Pilar Buera, M., Welti-Chanes, J., Lillford, P. J. & Corti, H. R.), p. 79. CRC Taylor and Francis, Boca Raton.Google Scholar
Hinow, P., Rogers, C. E., Barbieri, C. E., Pietenpol, J. A., Kenworthy, A. K. & DiBenedetto, E. (2006). The DNA binding activity of p53 displays reaction-diffusion kinetics. Biophysical Journal 91, 330342.Google Scholar
Holmberg, C. I., Staniszewski, K. E., Mensah, K. N., Matouschek, A. & Morimoto, R. I. (2004). Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO Journal 23, 43074318.Google Scholar
Houtsmuller, A. B. (2005). Fluorescence recovery after photobleaching: application to nuclear proteins. Advances in Biochemical Engineering/Biotechnology 95, 177199.Google Scholar
Inoué, S. (2006). Foundations of confocal scanned imaging in light microscopy. In Biological Confocal Microscopy, Chapter 1 (ed. Pawley, J. B.), pp. 119. Springer Science+Business Media, New York.Google Scholar
Jensen, S., Rolin, C. & Ipsen, R. (2010). Stabilisation of acidified skimmed milk with HM pectin. Food Hydrocolloids 24, 291299.Google Scholar
Jonasson, J. K., Hagman, J., Lorén, N., Bernin, D., Nydén, M. & Rudemo, M. (2010). Pixel-based analysis of FRAP data with a general initial bleaching profile. Journal of Microscopy 239, 142153.Google Scholar
Jonasson, J. K., Lorén, N., Olofsson, P., Nydén, M. & Rudemo, M. (2008). A pixel-based likelihood framework for analysis of fluorescence recovery after photobleaching data. Journal of Microscopy 232, 260269.Google Scholar
Jonkman, J. E. N. & Stelzer, E. H. K. (2002). Resolution and contrast in confocal and two-photon microscopy. In Confocal and Two-Photon Microscopy, Chapter 5 (ed. Diaspro, A.), pp. 101125. New York, USA: Wiley-Liss, Inc.Google Scholar
Jönsson, B., Wennerström, H., Nilsson, P. G. & Linse, P. (1986). Self-diffusion of small molecules in colloidal systems. Colloid and Polymer Science 264, 7788.Google Scholar
Jönsson, P., Jonsson, M. P., Tegenfeldt, J. O. & Höök, F. (2008). A method improving the accuracy of fluorescence recovery after photobleaching analysis. Biophysical Journal 95, 53345348.Google Scholar
Kang, M., Day, C. A., DiBenedetto, E. & Kenworthy, A. K. (2010). A quantitative approach to analyze binding diffusion kinetics by confocal FRAP. Biophysical Journal 99, 27372747.Google Scholar
Kang, M., Day, C. A., Drake, K., Kenworthy, A. K. & DiBenedetto, E. A. (2009). A generalization of theory for two-dimensional fluorescence recovery after photobleaching applicable to confocal laser scanning microscopy. Biophysical Journal 97, 15011511.Google Scholar
Kang, M., DiBenedetto, E. & Kenworthy, A. K. (2011). Proposed correction to Feder's anomalous diffusion FRAP equations. Biophysical Journal 100, 791792.Google Scholar
Kapitza, H. G., Mcgregor, G. & Jacobson, K. A. (1985). Direct measurement of lateral transport in membranes by using time-resolved spatial photometry. Proceedings of the National Academy of Sciences of the United States of America 82, 41224126.Google Scholar
Karbowiak, T., Debeaufort, F., Voilley, A. & Trystram, G. (2009). From macroscopic to molecular scale investigations of mass transfer of small molecules through edible packaging applied at interfaces of multiphase food products. Innovative Food Science and Emerging Technologies 10, 116127.Google Scholar
Karbowiak, T., Hervet, H., Léger, L., Champion, D., Debeaufort, F. & Voilley, A. (2006). Effect of plasticizers (water and glycerol) on the diffusion of a small molecule in iota-carrageenan biopolymer films for edible coating application. Biomacromolecules 7, 20112019.Google Scholar
Kaufman, E. N. & Jain, R. K. (1990). Quantification of transport and binding parameters using fluorescence recovery after photobleaching. Potential for in vivo applications. Biophysical Journal 58, 873885.Google Scholar
Kenworthy, A. K. (2007). Fluorescence recovery after photobleaching studies of lipid rafts. Methods in Molecular Biology 398, 179192.Google Scholar
Kenworthy, A. K., Nichols, B. J., Remmert, C. L., Hendrix, G. M., Kumar, M., Zimmerberg, J. & Lippincott-Schwartz, J. (2004). Dynamics of putative raft-associated proteins at the cell surface. Journal of Cell Biology 165, 735746.Google Scholar
Kolin, D. L. & Wiseman, P. V. (2007). Advances in image correlation spectroscopy: measuring number densities, aggregation states, and dynamics of fluorescently labeled macromolecules in cells. Cell Biochemistry and Biophysics 49, 141164.Google Scholar
Koppel, D. E., Axelrod, D., Schlessinger, J., Elson, E. L. & Webb, W. W. (1976). Dynamics of fluorescence marker concentration as a probe of mobility. Biophysical Journal 16, 13151329.Google Scholar
Koster, M., Frahm, T. & Hauser, H. (2005). Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Current Opinion in Biotechnology 16, 2834.Google Scholar
Kubitscheck, U., Wedekind, P. & Peters, R. (1994). Lateral diffusion measurement at high spatial resolution by scanning microphotolysis in a confocal microscope. Biophysical Journal 67, 948956.Google Scholar
Kubitscheck, U., Wedekind, P. & Peters, R. (1998). Three-dimensional diffusion measurements by scanning microphotolysis. Journal of Microscopy 192, 126138.Google Scholar
Kusto, K. B. & Deen, W. M. (2004). Diffusivities of macromolecules in composite hydrogels. AiChe Journal 50, 26482658.Google Scholar
Kusumi, A., Koyama-Honda, I. & Suzuki, K. (2004). Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5, 213230.Google Scholar
Latour, L. L., Mitra, P. P., Kleinberg, R. L. & Sotak, C. H. (1993). Time-dependent diffusion coefficient of fluids in porous media as a probe of surface-to-volume ratio. J. Magn. Reson. Series A 101, 342346.Google Scholar
Lele, T., Oh, P., Nickerson, J. A. & Ingber, D. E. (2004). An improved mathematical approach for determination of molecular kinetics in living cells with FRAP. Mechanics & Chemistry of Biosystems 1, 181190.Google Scholar
Lenk, R. (1986). Fluctuations, Diffusion and Spin Relaxation. Elsevier, New York.Google Scholar
Levi, V. & Gratton, E. (2007). Exploring dynamics in living cells by tracking single particles. Cell Biochemistry and Biophysics 48, 115.Google Scholar
Lin, C. C. & Metters, A. T. (2006). Hydrogels in controlled release formulations: network design and mathematical modeling. Advanced Drug Delivery Reviews 58, 13791408.Google Scholar
Lippincott-Schwartz, J., Altan-Bonnet, N. & Patterson, G. H. (2003). Photobleaching and photoactivation: following protein dynamics in living cells. Nature Cell Biology 5, S7S14.Google Scholar
Lippincott-Schwartz, J. & Patterson, G. H. (2003). Development and use of fluorescent protein markers in living cells. Science 300, 8791.Google Scholar
Lorén, N., Nydén, M. & Hermasson, A-M. (2009). Determination of local diffusion properties in heterogeneous biomaterials. Advances in Colloidal and Interface Science 150, 515.Google Scholar
Lubelski, A. & Klafter, J. (2008). Fluorescence recovery after photobleaching: the case of anomalous diffusion. Biophysical Journal 94, 46464653.Google Scholar
Lukacs, G. L., Haggie, P., Seksek, O., Lechardeur, D., Freedman, N. & Verkman, A. S. (2000). Size-dependent DNA mobility in cytoplasm and nucleus. Journal of Biological Chemistry 275, 16251629.Google Scholar
Lukyanov, K. A., Chudakov, D. M., Lukyanov, S. & Verkhusha, V. V. (2005). Innovation: photoactivatable fluorescent proteins. Nature Reviews Molecular Cell Biology 6, 88589.Google Scholar
Luu, D. T. & Maurel, C. (2013). Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic 14, 629635.Google Scholar
Mackie, A. R., Nativel, S., Wilson, D. R., Ladha, S. & Clark, D. C. (1996). Process-induced changes in molecular structure that alter adsorbed layer properties in oil-in-water emulsions stabilised by β-Casein/Tween20 mixtures. Journal of the Science of Food and Agriculture 70, 413421.Google Scholar
Marguet, D., Lenne, P. F., Rigneault, H. & He, H. T. (2006). Dynamics in the plasma membrane: how to combine fluidity and order. EMBO Journal 25, 34463457.Google Scholar
Marty, S., Schroeder, M., Baker, K. W., Mazzanti, G. & Marangoni, A. G. (2009). Small molecule diffusion through polycrystalline triglyceride networks quantified using fluorescent recovery after photobleaching. Langmuir 25, 87808785.Google Scholar
Maru, B. S., Tobias, J. H., Rivers, C., Caunt, C. J., Normana, M. R. & McArdlea, C. A. (2009). Potential use of an estrogen–glucocorticoid receptor chimera as a drug screen for tissue selective estrogenic activity. Bone 44, 102112.Google Scholar
Maxfield, F. R., Willingham, M. C., Pastan, I., Dragsten, P. & Cheng, S. Y. (1981). Binding and mobility of the cell surface receptors for 3,3′,5-triiodo-L-thyronine. Science 211, 6365.Google Scholar
Mazza, D., Abernathy, A., Golob, N., Morisaki, T. & McNally, J. G. (2012). A benchmark for chromatin binding measurements in live cells. Nucleic Acids Research 40, e119.Google Scholar
Mazza, D., Braeckmans, K., Cella, F., Testa, I., Vercauteren, D., Demeester, J., De Smedt, S. S. & Diaspro, A. (2008). A new FRAP/FRAPa method for three-dimensional diffusion measurements based on multiphoton excitation microscopy. Biophysical Journal 95, 34573469.Google Scholar
Mazza, D., Cella, F., Vicidomini, G., Krol, S. & Diaspro, A. (2007). Role of three-dimensional bleach distribution in confocal and two-photon fluorescence recovery after photobleaching experiments. Applied Optics 46, 74017411.Google Scholar
McGrath, J. L., Tardy, Y., Dewey, C. F., Meister, J. J. & Hartwig, J. H. (1998). Simultaneous measurements of actin filament turnover, filament fraction, and monomer diffusion in endothelial cells. Biophysical Journal 75, 20702078.Google Scholar
Meder, D., Moreno, M. J., Verkade, P., Vaz, W. L. & Simons, K. (2006). Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 103, 329334.Google Scholar
Meyvis, T. K., De Smedt, S. C., Van Oostveldt, P. & Demeester, J. (1999). Fluorescence recovery after photobleaching: a versatile tool for mobility and interaction measurements in pharmaceutical research. Pharmaceutical Research 16, 11531162.Google Scholar
Michelman-Ribeiro, A., Mazza, D., Rosales, T., Stasevich, T. J., Boukari, H., Rishi, V., Vinson, C., Knutson, J. R. & McNally, J. G. (2009). Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. Biophysical Journal 97, 337346.Google Scholar
Minati, L. & Weglarz, W. (2007). Physical foundations, models, and methods of diffusion magnetic resonance imaging of the brain: a review. Concepts in Magnetic Resonance 30A, 278307.Google Scholar
Montero Llopis, P., Sliusarenko, O., Heinritz, J. & Jacobs-Wagner, C. (2012). In vivo biochemistry in bacterial cells using FRAP: insight into the translation cycle. Biophysical Journal 103, 18481859.Google Scholar
Mori, S. (2007). Introduction to Diffusion Tensor Imaging. Oxford: Elsevier.Google Scholar
Morisaki, T. & McNally, J. G. (2014). Photoswitching-free FRAP analysis with a genetically encoded fluorescent tag. PLoS ONE 18, 9(9), e107730.Google Scholar
Mueller, F., Mazza, D., Stasevich, T. J. & McNally, J. G. (2010). FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know? Current Opinion in Cell Biology 22, 403411.Google Scholar
Mueller, F., Morisaki, T., Mazza, D. & McNally, J. G. (2012). Minimizing the impact of photoswitching of fluorescent proteins on FRAP analysis. Biophysical Journal 102, 16561665.Google Scholar
Mueller, F., Wach, P. & McNally, J. G. (2008). Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophysical Journal 94, 33233339.Google Scholar
Müller, K. P., Erdel, F., Caudron-Herger, M., Marth, C., Fodor, B. D., Richter, M., Scaranaro, M., Beaudouin, J., Wachsmuth, M. & Rippe, K. (2009). Multiscale analysis of dynamics and interactions of heterochromatin protein 1 by fluorescence fluctuation microscopy. Biophysical Journal 97, 28762885.Google Scholar
Nickerson, J. A. (2009). The biochemistry of RNA metabolism studied in situ. RNA Biology 6, 2530.Google Scholar
Netti, P. A., Berk, D. A., Swartz, M. A., Grodzinsky, A. J. & Jain, R. K. (2000). Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Research 60, 24972503.Google Scholar
Norris, S. C., Humpolíčková, J., Amler, E., Huranová, M., Buzgo, M., Macháň, R., Lukáš, D. & Hof, M. (2011). Raster image correlation spectroscopy as a novel tool to study interactions of macromolecules with nanofiber scaffolds. Acta Biomaterialia 7, 41954203.Google Scholar
Notelaers, K., Smisdom, N., Rocha, S., Janssen, D., Meier, J. C., Rigo, J. M., Hofkens, J. & Ameloot, M. (2012). Ensemble and single particle fluorimetric techniques in concerted action to study the diffusion and aggregation of the glycine receptor α3 isoforms in the cell plasma membrane. Biochimica et Biophysica Acta 1818, 31313140.Google Scholar
Orlova, D. Y., Bartova, E., Maltsev, V. P., Kozubek, S. & Chernyshev, A. V. (2011). A nonfitting method using a spatial sine window transform for inhomogeneous effective-diffusion measurements by FRAP. Biophysical Journal 100, 507516.Google Scholar
Packer, K. J., Rees, C. & Tomlinson, D. J. (1972). Studies of diffusion and flow by pulsed NMR techniques. Advances in Molecular Relaxation Processes 3, 119131.Google Scholar
Papadopoulos, M. C., Binder, D. K. & Verkman, A. S. (2005). Enhanced macromolecular diffusion in brain extracellular space in mouse models of vasogenic edema measured by cortical surface photobleaching. FASEB Journal 19, 425427.Google Scholar
Pastor, I., Vilaseca, E., Madurga, S., Lluís Garcés, J., Cascante, M. & Mas, F. (2010). Diffusion of α-Chymotrypsin in solution-crowded media. A fluorescence recovery after photobleaching study. Journal of Physical Chemistry B 114, 40284034.Google Scholar
Patterson, G. H. & Piston, D. W. (2000). Photobleaching in two-photon excitation microscopy. Biophysical Journal 78, 21592162.Google Scholar
Pawley, J. B. (2006). Handbook of Biological Confocal Microscopy, 3rd edn. New York: Springer.Google Scholar
Payet, L., Ponton, A., Léger, L., Hervet, H., Grossiord, J. L. & Agnely, F. (2008). Self-diffusion in chitosan networks: from a gel-gel method to fluorescence recovery after photobleaching by fringe pattern. Macromolecules 41, 93769381.Google Scholar
Periasamy, N. & Verkman, A. S. (1998). Analysis of fluorophore diffusion by continuous distributions of diffusion coefficients: application to photobleaching measurements of multicomponent and anomalous diffusion. Biophysical Journal 75, 557567.Google Scholar
Peters, R., Peters, J., Tews, K. H. & Bähr, W. (1974). A microfluorimetric study of translational diffusion in erythrocyte membranes. Biochimica et Biophysica Acta 367, 282294.Google Scholar
Petersen, N. O., Hoddelius, P. L., Wiseman, P. W., Seger, O. & Magnusson, K. E. (1993). Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application. Biophysical Journal 65, 11351146.Google Scholar
Phair, R. D. & Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604609.Google Scholar
Phair, R. D. & Misteli, T. (2001). Kinetic modelling approaches to in vivo imaging. Nature Reviews Molecular Cell Biology 2, 898907.Google Scholar
Pike, L. J. (2006). Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. Journal of Lipid Research 47, 15971598.Google Scholar
Pinte, J., Joly, C., Plé, K., Dole, P. & Feigenbaum, A. (2008). Proposal of a set of model polymer additives designed for confocal FRAP diffusion experiments. Journal of Agricultural and Food Chemistry 56, 1000310011.Google Scholar
Pluen, A., Boucher, Y., Ramanujan, S., McKee, T. D., Gohongi, T., di Tomaso, E., Brown, E. B., Izumi, Y., Campbell, R. B., Berk, D. A. & Jain, R. K. (2001). Role of tumor–host interactions in interstitial diffusion of macromolecules: cranial vs. subcutaneous tumors. Proceedings of the National Academy of Sciences of the United States of America 98, 46224633.Google Scholar
Price, W. (1997). Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part 1. Basic theory. Concepts in Magnetic Resonance 9, 299336.Google Scholar
Price, W. (2009). NMR Studies of Translational Motion. Cambridge University Press, Cambridge.Google Scholar
Raghuram, N., Carrero, G., Th'ng, J. & Hendzel, M. J. (2009). Molecular dynamics of histone H1. Biochemistry and Cell Biology 87, 189206.Google Scholar
Reits, E., Griekspoor, A., Neijssen, J., Groothuis, T., Jalink, K., van Veelen, P., Janssen, H., Calafat, J., Drijfhout, J. W. & Neefjes, J. (2003). Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18, 97108.Google Scholar
Remaut, K., Sanders, N. N., De Geest, B. G., Braeckmans, K., Demeester, J. & De Smedt, S. C. (2007). Nucleic acid delivery: where material sciences and bio-sciences meet. Materials Science & Engineering R – Reports 58, 117161.Google Scholar
Renz, M. & Langowski, J. (2008). Dynamics of the CapG actin-binding protein in the cell nucleus studied by FRAP and FCS. Chromosome Research 16, 427437.Google Scholar
Ritchie, K., Shan, X. Y., Kondo, J., Iwasawa, K., Fujiwara, T. & Kusumi, A. (2005). Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophysical Journal 88, 22662277.Google Scholar
Rossow, M. J., Sasaki, J. M., Digman, M. A. & Gratton, E. (2010). Raster image correlation spectroscopy in live cells. Nature Protocols 5, 17611774.Google Scholar
Ruthardt, N., Lamb, D. C. & Brauchle, C. (2011). Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles. Molecular Therapy: The Journal of the American Society of Gene Therapy 19, 11991211.Google Scholar
Sadegh, Z. K. & Montas, H. J. (2010). A class of exact solutions for biomacromolecule diffusion-reaction in live cells. Journal of Theoretical Biology 264, 914933.Google Scholar
Saffman, P. G. & Delbruck, M. (1975). Brownian motion in biological membranes. Proceedings of the National Academy of Sciences of the United States of America 72, 31113113.Google Scholar
Salinas, D., Haggie, P. M., Thiagarajah, J. R., Song, Y., Rosbe, K., Finkbeiner, W. E., Nielson, D. W. & Verkman, A. S. (2005). Submucosal gland dysfunction as a primary defect in cystic fibrosis. FASEB Journal 19, 431433.Google Scholar
Salome, L., Cazeils, J. L., Lopez, A. & Tocanne, J. F. (1998). Characterization of membrane domains by FRAP experiments at variable observation areas. European Biophysical Journal 27, 391402.Google Scholar
Sanchez, S. A. & Gratton, E. (2005). Lipid–protein interactions revealed by two-photon microscopy and fluorescence correlation spectroscopy. Accounts of Chemical Research 38, 469477.Google Scholar
Sanger, J. W., Wang, J., Fan, Y., White, J. & Sanger, J. M. (2010). Assembly and dynamics of myofibrils. Journal of Biomedicine and Biotechnology 2010, 858606.Google Scholar
Saxton, M. J. (1996). Anomalous diffusion due to binding: a Monte Carlo study. Biophysical Journal 70, 12501262.Google Scholar
Saxton, M. J. (1997). Single-particle tracking: the distribution of diffusion coefficients. Biophysical Journal 72, 17441753.Google Scholar
Saxton, M. J. (2001). Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study. Biophysical Journal 81, 22262240.Google Scholar
Saxton, M. J. (2007). A biological interpretation of transient anomalous subdiffusion, I. Qualitative model. Biophysical Journal 92, 11781191.Google Scholar
Saxton, M. J. & Jacobson, K. (1997). Single-particle tracking: applications to membrane dynamics. Annual Review of Biophysics and Biomolecular Structure 26, 373399.Google Scholar
Saxton, W. M., Stemple, D. L., Leslie, R. J., Salmon, E. D., Zavortink, M. & McIntosh, J. R. (1984). Tubulin dynamics in cultured mammalian cells. Journal of Cell Biology 99, 21752186.Google Scholar
Sbalzarini, I. F., Mezzacasa, A., Helenius, A. & Koumoutsakos, P. (2005). Effects of organelle shape on fluorescence recovery after photobleaching. Biophysical Journal 89, 14821492.Google Scholar
Schlessinger, J., Elson, E. L., Webb, W. W., Yahara, I., Rutishauser, U., Edelman, G. M. (1977). Receptor diffusion on cell surfaces modulated by locally bound concanavalin A. Proceedings of the National Academy of Sciences of the United States of America 74, 11101114.Google Scholar
Schlessinger, J., Shechter, Y., Cuatrecasas, P., Willingham, M. C. & Pastan, I. (1978). Quantitative determination of the lateral diffusion coefficients of the hormone-receptor complexes of insulin and epidermal growth factor on the plasma membrane of cultured fibroblasts. Proceedings of the National Academy of Sciences of the United States of America 75, 53535357.Google Scholar
Schlessinger, J., Webb, W. W., Elson, E. L. & Metzger, H. (1976). Lateral motion and valence of Fc receptors on rat peritoneal mast cells. Nature 264, 550552.Google Scholar
Schmiedeberg, L., Weisshart, K., Diekmann, S., Meyer, Z., Hoerste, G. & Hemmerich, P. (2004). High- and low-mobility populations of HP1 in heterochromatin of mammalian cells. Molecular Biology of the Cell 15, 28192833.Google Scholar
Schuster, E., Eckardt, J., Hermansson, A-M., Larsson, A., Lorén, N., Altskär, A. & Ström, A. (2014a). Microstructural, mechanical and mass transport properties of isotropic and capillary alginate gels. Soft Matter 10, 357366.Google Scholar
Schuster, E., Hermansson, A-M., Öhgren, C., Rudemo, M. & Lorén, N. (2014b). Interactions and diffusion in fine-stranded beta-lactoglobulin gels determined via FRAP and binding. Biophysical Journal 106, 253262.Google Scholar
Shaner, N. C., Patterson, G. H. & Davidson, M. W. (2007). Advances in fluorescent protein technology. Journal of Cell Science 120, 42474260.Google Scholar
Shelat, K. J., Vilaplana, F., Nicholson, T. M., Wonga, K. H., Gidley, M. J. & Gilbert, R. G. (2010). Diffusion and viscosity in arabinoxylan solutions: implications for nutrition. Carbohydrate Polymers 82, 4653.Google Scholar
Shen, H., Hu, Y. & Saltzman, W. M. (2006). DNA diffusion in mucus: effect of size, topology of DNAs, and transfection reagents. Biophysical Journal 91, 639644.Google Scholar
Shi, C., Cisewski, S. E., Bell, P. D. & Yao, H. (2014). Measurement of three-dimensional anisotropic diffusion by multiphoton fluorescence recovery after photobleaching. Annals of Biomedical Engineering 42, 555565.Google Scholar
Siggia, E. D., Lippincott-Schwartz, J. & Bekiranov, S. (2000). Diffusion in inhomogeneous media: theory and simulations applied to whole cell photobleach recovery. Biophysical Journal 79, 17611770.Google Scholar
Silva, J. V. C., Peixoto, P. D. S., Lortal, S. & Floury, J. (2013). Transport phenomena in a model cheese: the influence of the charge and shape of solutes on diffusion. Journal of Dairy Science 96, 61866198.Google Scholar
Singer, J. (1978). NMR diffusion and flow measurements and an introduction to spin phase graphing. Journal of Physics E 11, 281291.Google Scholar
Singer, S. J. & Nicolson, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science 175, 720731.Google Scholar
Sinnecker, D., Voigt, P., Hellwig, N. & Schaefer, M. (2005). Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 44, 70857094.Google Scholar
Smisdom, N., Braeckmans, K., Deschout, H., van de Ven, M., Rigo, J.-M., De Smedt, S. C. & Ameloot, M. (2011). Fluorescence recovery after photobleaching on the confocal laser-scanning microscope: generalized model without restriction on the size of the photobleached disk. Journal of Biomedical Optics 16, 046021.Google Scholar
Smith, B. A. & McConnell, H. M. (1978). Determination of molecular motion in membranes using periodic pattern photobleaching. Proceedings of the National Academy of Sciences of the United States of America 75, 27592763.Google Scholar
Smoluchowski, M. (1906). Zur kinetischen Theorie der Brownsche Molekularbewegung und der Suspensionen. Annalen der Physik 21, 756780.Google Scholar
Snieckers, Y. H. & van Donkelaar, C. C. (2005). Determining diffusion coefficients in inhomogeneous tissues using fluorescence recovery after photobleaching. Biophysical Journal 89, 13021307.Google Scholar
Soumpasis, D. M. (1983). Theoretical analysis of fluorescence photobleaching recovery experiments. Biophysical Journal 41, 9597.Google Scholar
Sprague, B. L. & McNally, J. G. (2005). FRAP analysis of binding: proper and fitting. Trends in Cell Biology 15, 8491.Google Scholar
Sprague, B. L., Muller, F., Pego, R. L., Bungay, P. M., Stavreva, D. A. & McNally, J. G. (2006). Analysis of binding at a single spatially localized cluster of binding sites by fluorescence recovery after photobleaching. Biophysical Journal 91, 11691191.Google Scholar
Sprague, B. L., Pego, R. L., Stavreva, D. A. & McNally, J. G. (2004). Analysis of binding reactions by fluorescence recovery after photobleaching. Biophysical Journal 86, 34733495.Google Scholar
Srivastava, M. & Petersen, N. O. (1998). Diffusion of transferrin receptor clusters. Biophysical Chemistry 75, 201211.Google Scholar
Stasevich, T. J., Mueller, F., Brown, D. T. & McNally, J. G. (2010a). Dissecting the binding mechanism of the linker histone in live cells: an integrated FRAP analysis. EMBO Journal 29, 12251234.Google Scholar
Stasevich, T. J., Mueller, F., Michelman-Ribeiro, A., Rosales, T., Knutson, J. R. & McNally, J. G. (2010b). Cross-validating FRAP and FCS to quantify the impact of photobleaching on binding measurements in live cells. Biophysical Journal 29, 12251234.Google Scholar
Stenoien, D. L., Mielke, M. & Mancini, M. A. (2002). Intranuclear ataxin1 inclusions contain both fast- and slow-exchanging components. Nature Cell Biology 4, 806810.Google Scholar
Stokes, G. (1856). On the effect of the internal friction of fluids on the motion of pendulums. Transactions of the Cambridge Philosophical Society 9, 8106.Google Scholar
Stylianopoulos, T., Diop-Frimpong, B., Munn, L. L. & Jain, R. K. (2010). Diffusion anisotropy in collagen gels and tumors: the effect of fiber network orientation. Biophysical Journal 99, 31193128.Google Scholar
Suh, J., Dawson, M. & Hanes, J. (2005). Real-time multiple-particle tracking: applications in drug/gene delivery. Advanced Drug Delivery Reviews 57, 6378.Google Scholar
Sullivan, K. D. & Brown, E. B. (2011). Multiphoton fluorescence recovery after photobleaching in bounded systems. Physical Review E 83, 051916.Google Scholar
Sullivan, K, D., Sipprell, W. H., Brown, E. B. Jr. & Brown, E. B. (2009). Improved model of fluorescence recovery expands the application of multiphoton fluorescence recovery after photobleaching in vivo . Biophysical Journal 96, 50825094.Google Scholar
Svanberg, L., Ahrné, L., Lorén, N. & Windhab, E. (2011). Effect of pre-crystallization process and solid particle addition on compactness of structure in chocolate model systems. Food Research International 44, 13391350.Google Scholar
Swaminathan, R., Hoang, C. P. & Verkman, A. S. (1997). Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophysical Journal 72, 19001907.Google Scholar
Travascio, F. & Gu, W. Y. (2011). Simultaneous measurement of anisotropic solute diffusivity and binding reaction rates in biological tissues by FRAP. Annals of Biomedical Engineering 39, 5365.Google Scholar
Trembacka, D. O., Kuzak, M. & Dobrucki, J. W. (2010). Conditions for using FRAP as a quantitative technique – influence of the bleaching protocol. Cytometry A 77A, 366370.Google Scholar
Tsay, T.-T. & Jacobson, K. A. (1991). Spatial Fourier analysis of video photobleaching measurements – principles and optimization. Biophysical Journal 60, 360368.Google Scholar
Tsibidis, G. D. (2009). Quantitative interpretation of binding reactions of rapidly diffusing species using fluorescence recovery after photobleaching. Journal of Microscopy 233, 384390.Google Scholar
Tsibidis, G. D. & Ripoll, J. (2008). Investigation of binding mechanisms of nuclear proteins using confocal scanning laser microscopy and FRAP. Journal of Theoretical Biology 253, 755768.Google Scholar
Tsien, R. Y. (1998). The green fluorecsent protein. Annual Review of Biochemistry 67, 50944.Google Scholar
Van Oostveldt, P. & Bauwens, S. (1990). Quantitative fluorescence in confocal microscopy. The effect of the detection pinhole aperture on the re-absorption and inner filter phenomena. Journal of Microscopy 158, 121132.Google Scholar
van Royen, M. E., Farla, P., Mattern, K. A., Geverts, B., Trapman, J. & Houtsmuller, A. B. (2009). Fluorescence recovery after photobleaching (FRAP) to study nuclear protein dynamics in living cells. Methods in Molecular Biology 464, 363385.Google Scholar
Verheyen, E., van der Wal, S., Deschout, H., Braeckmans, K., de Smedt, S., Barendregt, A., Hennink, W. E. & van Nostrum, C. F. (2011). Protein macromonomers containing reduction-sensitive linkers for covalent immobilization and glutathione triggered release from dextran hydrogels. Journal of Controlled Release 156, 329336.Google Scholar
Videcoq, P., Steenkeste, K., Bonnina, E. & Garnier, C. (2013). A multi-scale study of enzyme diffusion in macromolecular solutions and physical gels of pectin polysaccharides. Soft Matter 9, 5110.Google Scholar
Vinnakota, K. C., Mitchell, D. A., Deschenes, R. J., Wakatsuki, T. & Beard, D. A. (2010). Analysis of diffusion of Ras2 in Saccharomyces cerevisiae using fluorescence recovery after photobleaching. Physical Biology 4, 026011.Google Scholar
Wachsmuth, M. (2014). Molecular diffusion and binding analyzed with FRAP. Protoplasma 251, 373382.Google Scholar
Waharte, F., Brown, C. M., Coscoy, S., Coudrier, E. & Amblard, F. (2005). A two-photon FRAP analysis of the cytoskeleton dynamics in the microvilli of intestinal cells. Biophysical Journal 88, 14671478.Google Scholar
Walczak, C. E., Rizk, R. S., Shaw, S. L. (2010). The use of fluorescence redistribution after photobleaching for analysis of cellular microtubule dynamics. Methods in Cell Biology 97, 3552.Google Scholar
Watanabe, N., Yamashiro, S., Vavylonis, D. & Kiuchi, T. (2013). Molecular viewing of actin polymerizing actions and beyond: combination analysis of single-molecule speckle microscopy with modeling, FRAP and s-FDAP (sequential fluorescence decay after photoactivation). Dev Growth Differ 55(4), 508514.Google Scholar
Webb, W. W. (2006). Commentary on the pleasures of solving impossible problems of experimental physiology. Annual Review of Physiology 68, 128.Google Scholar
Wedekind, P., Kubitscheck, U. & Peters, R. (1994). Scanning microphotolysis: a new photobleaching technique based on fast intensity modulation of a scanned laser beam and confocal imaging. Journal of Microscopy 176, 2333.Google Scholar
Weiss, M. 2004. Challenges and artifacts in quantitative photobleaching experiments. Traffic 5, 662671.Google Scholar
Wiseman, P. W., Squier, J. A., Ellisman, M. H. & Wilson, K. R. (2000). Two-photon image correlation spectroscopy and image cross-correlation spectroscopy. Journal of Microscopy 200, 1425.Google Scholar
Wu, E. S., Jacobson, K. & Papahadjopoulos, D. (1977). Lateral diffusion in phospholipid multibilayers measured by fluorescence recovery after photobleaching. Biochemistry 16, 39363941.Google Scholar
Wu, J., Shekhar, N., Lele, P. P. & Lele, T. P. (2012). FRAP analysis: accounting for bleaching during image capture. PLoS ONE 7, e42854.Google Scholar
Yechiel, E. & Edidin, M. (1987). Micrometer-scale domains in fibroblast plasma membranes. Journal of Cell Biology 105, 755760.Google Scholar
Zagato, E., Forier, K., Martens, T., Neyts, K., Demeester, J., De Smedt, S., Remaut, K. & Braeckmans, K. (2014). Single particle tracking for studying nanomaterial dynamics: applications and fundamentals in drug delivery. Nanomedicine 9, 913927.Google Scholar
Ziv, N. E. & Fisher-Lavie, A. (2014). Presynaptic and postsynaptic scaffolds: dynamics fast and slow. Neuroscientist 20(5), 439452.Google Scholar
Zuleger, N., Kelly, D. A. & Schirmer, E. C. (2013). Considering discrete protein pools when measuring the dynamics of nuclear membrane proteins. Methods in Molecular Biology 1042, 275298.Google Scholar