Imaging molecular interactions in living cells by FRET microscopy

Current Opinion in Chemical Biology

Volumn 10, Issue 5, 2006, Pages 409-416

  Jares Erijman, Elizabeth A ^a   Jovin, Thomas M ^b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTION; CONFORMATIONAL TRANSITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR INTERACTION; PROTEIN MODIFICATION; PROTEIN TRANSPORT; REVIEW;

CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROTEINS; QUANTUM DOTS; QUANTUM THEORY; SENSITIVITY AND SPECIFICITY;

EID: 33748545640     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2006.08.021     Document Type: Review

References (98)

1. Jares-Erijman E.A., and Jovin T.M. FRET imaging. Nat Biotechnol 21 (2003) 1387-1395
2. Giepmans B.N., Adams S.R., Ellisman M.H., and Tsien R.Y. The fluorescent toolbox for assessing protein location and function. Science 312 (2006) 217-224. A comprehensive outline of molecular design platforms for assessing structure and function. It runs the probe gamut from organic dyes through fluorescent proteins to quantum dots. FRET is, in many cases, the underlying detection principle.
3. De Schryver F.C., Vosch T., Cotlet M., van der Auweraer M., Mülen K., and Hofkens J. Energy dissipation in multichromophoric single dendrimers. Acc Chem Res 38 (2005) 514-522
4. In: Periasamy A., and Day R.N. (Eds). Molecular Imaging: FRET Microscopy and Spectroscopy (2005), Oxford University Press. A compendium of excellent chapters by FRET experts, which we do not cite individually because of space limitations. Most of the topics of the present review are covered. Co-edited by one of the most prolific writers in the FRET field.
5. Bunt G., and Wouters F.S. Visualization of molecular activities inside living cells with fluorescent labels. Int Rev Cytol 237 (2004) 205-277
6. Spector D.L., and Goldman R.D. Live Cell Imaging: A Laboratory Manual (2004), Cold Spring Harbor Laboratory Press
7. Chapman S., Oparka K.J., and Roberts A.G. New tools for in vivo fluorescence tagging. Curr Opin Plant Biol 8 (2005) 565-573
8. Nagy P., Vereb G., Post J.N., Friedländer E., and Szöllösi J. Novel single cell fluorescence approaches in the investigation of signaling at the cellular level. In: Damjanovich S. (Ed). Biophysical Aspects of Transmembrane Signaling. Springer Series in Biophysics, vol 8 (2005), Springer 33-70. An excellent review on all quantitative methodologies available for studying cellular signaling from one of the laboratories most active in this area.
9. Ballou B., Ernst L.A., and Waggoner A.S. Fluorescence imaging of tumors in vivo. Curr Med Chem 12 (2005) 795-805
10. Zimmermann T. Spectral imaging and linear unmixing in light microscopy. Adv Biochem Eng Biotechnol 95 (2005) 245-265
11. Tsien R.Y. Building and breeding molecules to spy on cells and tumors. FEBS Lett 579 (2005) 927-932
12. Majoul I., Jia Y., and Duden R. Practical fluorescence resonance energy transfer or molecular nanobioscopy of living cells. In: Pawley J.B. (Ed). Handbook of Biological Confocal Microscopy, 3rd Ed (2006), Springer Science & Business Media 788-808
13. Kiyokawa E., Hara S., Nakamura T., and Matsuda M. Fluorescence (Forster) resonance energy transfer imaging of oncogene activity in living cells. Cancer Sci 97 (2006) 8-15
14. Yan Y., and Marriott G. Analysis of protein interactions using fluorescence technologies. Curr Opin Chem Biol 7 (2003) 635-640
15. Fan C., Plaxco K.W., and Heeger A.J. Biosensors based on binding-modulated donor-acceptor distances. Trends Biotechnol 23 (2005) 186-192
16. Zal T., and Gascoigne N.R. Photobleaching-corrected FRET efficiency imaging of live cells. Biophys J 86 (2004) 3923-3939
17. Mattheyses A.L., Hoppe A.D., and Axelrod D. Polarized fluorescence resonance energy transfer microscopy. Biophys J 87 (2004) 2787-2797
18. Muller B.K., Zaychikov E., Brauchle C., and Lamb D.C. Pulsed interleaved excitation. Biophys J 89 (2005) 3508-3522
19. Lee N.K., Kapanidis A.N., Wang Y., Michalet X., Mukhopadhyay J., Ebright R.H., and Weiss S. Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. Biophys J 88 (2005) 2939-2953. ALEX provides the means for extracting a full parametric data set for 'FRETing' fluorophores. The donor and acceptor are excited with alternating pulses.
20. Enderlein J., Gregor I., Patra D., Dertinger T., and Kaupp U.B. Performance of fluorescence correlation spectroscopy for measuring diffusion and concentration. ChemPhysChem 6 (2005) 2324-2336
21. Eggeling C., Widengren J., Brand L., Schaffer J., Felekyan S., and Seidel C.A. Analysis of photobleaching in single-molecule multicolor excitation and Forster resonance energy transfer measurements. J Phys Chem A 110 (2006) 2979-2995
22. Clayton A.H., Klonis N., Cody S.H., and Nice E.C. Dual-channel photobleaching FRET microscopy for improved resolution of protein association states in living cells. Eur Biophys J 34 (2005) 82-90
23. Horváth G., Petrás M., Szentesi G., Fábián A., Park J.W., Vereb G., and Szöllösi J. Selecting the right fluorophores and flow cytometer for fluorescence resonance energy transfer measurements. Cytometry A 65 (2005) 148-157
24. Waggoner A. Fluorescent labels for proteomics and genomics. Curr Opin Chem Biol 10 (2006) 62-66
25. Salama G., Choi B.R., Azour G., Lavasani M., Tumbev V., Salzberg B.M., Patrick M.J., Ernst L.A., and Waggoner A.S. Properties of new, long-wavelength, voltage-sensitive dyes in the heart. J Membr Biol 208 (2005) 125-140. The latest contribution from a laboratory pioneering the synthesis and use of new fluorophores, in this case showing improved voltage sensitivity for studies of cardiac function. This special issues of J Membr Biol has other articles on neuronal imaging.
26. Kogure T., Karasawa S., Araki T., Saito K., Kinjo M., and Miyawaki A. A fluorescent variant of a protein from the stony coral Montipora facilitates dual-color single-laser fluorescence cross-correlation spectroscopy. Nat Biotechnol 24 (2006) 577-581
27. Jovin T.M., Lidke D.S., and Post J.N. Dynamic and static fluorescence anisotropy in biological microscopy (rFLIM and emFRET). Proc SPIE 5323 (2004) 1-12
28. Marushchak D., and Johansson L.B.-A. On the quantitative treatment of donor-donor energy migration in regularly aggregated proteins. J Fluoresc 15 (2005) 797-803
29. Leif RC, Vallarino LM, Becker MC, Yang S: Review: increasing the luminescence of lanthanide complexes. Cytometry A 2006, in press. A comprehensive review of current knowledge and exploitation of lanthanide probes.
30. Ganesan S., Ameerbeg S.M., Ng T.T.C., Vojnovic B., and Wouters F.S. A dark yellow fluorescent protein (YFP)-based Resonance Energy Accepting Chromoprotein (REACh) for FRET with GFP. Proc Natl Acad Sci USA 103 (2006) 4089-4094
31. Sauer M. Reversible molecular photoswitches: a key technology for nanoscience and fluorescence imaging. Proc Natl Acad Sci USA 102 (2005) 9433-9434
32. Patterson G.H., and Lippincott-Schwartz J. Selective photolabeling of proteins using photoactivatable GFP. Methods 32 (2004) 445-450
33. Ando R., Mizuno H., and Miyawaki A. Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306 (2004) 1370-1373. A tour de force of molecular engineering resulting in a visible fluorescent protein that can undergo repeated cycles of photochromic interconversion between dark and emitting states. Predestined for pcFRET applications.
34. Valentin G., Verheggen C., Piolot T., Neel H., Coppey-Moisan M., and Bertrand E. Photoconversion of YFP into a CFP-like species during acceptor photobleaching FRET experiments. Nat Methods 2 (2005) 801
35. Tsutsui H., Karasawa S., Shimizu H., Nukina N., and Miyawaki A. Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep 6 (2005) 233-238
36. Sinnecker D., Voigt P., Hellwig N., and Schaefer M. Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 44 (2005) 7085-7094
37. Post J.N., Lidke K.A., Rieger B., and Arndt-Jovin D.J. One- and two-photon photoactivation of a paGFP-fusion protein, a phototoxicity study in live Drosophila embryos. FEBS Lett 579 (2005) 325-330
38. Souslova E.A., and Chudakov D.M. Photoswitchable cyan fluorescent protein as a FRET donor. Microsc Res Tech 69 (2006) 207-209
39. Mutoh T., Miyata T., Kashiwagi S., Miyawaki A., and Ogawa M. Dynamic behavior of individual cells in developing organotypic brain slices revealed by the photoconvertable protein Kaede. Exp Neurol 200 (2006) 430-437
40. Takakusa H., Kikuchi K., Urano Y., Kojima H., and Nagano T. A novel design method of ratiometric fluorescent probes based on fluorescence resonance energy transfer switching by spectral overlap integral. Chemistry 9 (2003) 1479-1485
41. Jares-Erijman E.A., Giordano L., Spagnuolo C., Kawior J., Vermeij R.J., and Jovin T.M. Photochromic Fluorescence Resonance Energy Transfer (pcFRET): formalism, implementation, and perspectives. Proc SPIE 5323 (2004) 13-26
42. Jares-Erijman E.A., Giordano L., Spagnuolo C., Lidke K.A., and Jovin T.M. Imaging quantum dots switched on and off by photochromic Fluorescence Resonance Energy Transfer (pcFRET). Mol Cryst Liq Cryst 430 (2005) 257-265
43. Miskoski S, Giordano L, Etchehon MH, Menendez G, Lidke KA, Hagen GM, Jovin TM, Jares-Erijman EA: Spectroscopic modulation of multifunctionalized quantum dots for use as biological probes and effectors. Proc SPIE 2006, 6096:60960X1-7.
44. Sakata T., Yan Y., and Marriott G. Family of site-selective molecular optical switches. J Org Chem 70 (2005) 2009-2013
45. Hofmann M., Eggeling C., Jakobs S., and Hell S.W. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci USA 102 (2005) 17565-17569
46. Medintz I.L., Uyeda H.T., Goldman E.R., and Mattoussi H. Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater 4 (2005) 435-446
47. Michalet X., Pinaud F.F., Bentolila L.A., Tsay J.M., Doose S., Li J.J., Sundaresan G., Wu A.M., Gambhir S.S., and Weiss S. Quantum dots for live cells, in vivo imaging, and diagnostics. Science 307 (2005) 538-544. A broad-ranging coverage of QD properties and applications by pioneers in the field.
48. Pinaud F., Michalet X., Bentolila L.A., Tsay J.M., Doose S., Li J.J., Iyer G., and Weiss S. Advances in fluorescence imaging with quantum dot bio-probes. Biomaterials 27 (2006) 1679-1687
49. Arndt-Jovin D.J., Lopez-Quintela M.A., Lidke D.S., Rodriguez M.J., Santos F.M., Lidke K.A., Hagen G.M., and Jovin T.M. In vivo cell imaging with semiconductor quantum dots and noble-metal nanodots. Proc SPIE 6096 (2006) 60960P1-60960P10
50. Lidke K.A., Rieger B., Jovin T.M., and Heintzmann R. Superresolution by localization of quantum dots using blinking statistics. Opt Express 13 (2005) 7052-7062
51. Hohng S., and Ha T. Single-molecule quantum-dot fluorescence resonance energy transfer. ChemPhysChem 6 (2005) 956-960
52. Clapp A.R., Medintz I.L., and Mattoussi H. Forster resonance energy transfer investigations using quantum-dot fluorophores. ChemPhysChem 7 (2006) 47-57. This group has generated numerous ingenious bioassays based on QDs as FRET donors.
53. Wang L., and Tan W. Multicolor FRET silica nanoparticles by single wavelength excitation. Nano Lett 6 (2006) 84-88
54. Bene L., Szentesi G., Mátyus L., Gáspár R., and Damjanovich S. Nanoparticle energy transfer on the cell surface. J Mol Recognit 18 (2005) 236-253
55. Steinmeyer R., Noskov A., Krasel C., Weber I., Dees C., and Harms G.S. Improved fluorescent proteins for single-molecule research in molecular tracking and co-localization. J Fluoresc 15 (2005) 707-721
56. Shaner N.C., Steinbach P.A., and Tsien R.Y. A guide to choosing fluorescent proteins. Nat Methods 2 (2005) 905-909
57. Ward T.H., and Lippincott-Schwartz J. The uses of green fluorescent protein in mammalian cells. Methods Biochem Anal 47 (2006) 305-337
58. Shimozono S., Hosoi H., Mizuno H., Fukano T., Tahara T., and Miyawaki A. Concatenation of cyan and yellow fluorescent proteins for efficient resonance energy transfer. Biochemistry 45 (2006) 6267-6271
59. Miller L.W., and Cornish V.W. Selective chemical labeling of proteins in living cells. Curr Opin Chem Biol 9 (2005) 56-61
60. Martin B.R., Giepmans B.N., Adams S.R., and Tsien R.Y. Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity. Nat Biotechnol 23 (2005) 1308-1314. Optimization of peptide sequences for biarsenicals targeted to a tetracysteine core. This expression system is gaining in favor due to these improvements as well as those in the biarsenical probes.
61. Hoffmann C., Gaietta G., Bunemann M., Adams S.R., Oberdorff-Maass S., Behr B., Vilardaga J.P., Tsien R.Y., Ellisman M.H., and Lohse M.J. A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat Methods 2 (2005) 171-176
62. Geho D.H., Jones C.D., Petricoin E.F., and Liotta L.A. Nanoparticles: potential biomarker harvesters. Curr Opin Chem Biol 10 (2006) 56-61
63. Howarth M., Takao K., Hayashi Y., and Ting A.Y. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc Natl Acad Sci USA 102 (2005) 7583-7588
64. Juillerat A., Heinis C., Sielaff I., Barnikow J., Jaccard H., Kunz B., Terskikh A., and Johnsson K. Engineering substrate specificity of O6-alkylguanine-DNA alkyltransferase for specific protein labeling in living cells. ChemBioChem 6 (2005) 1263-1269
65. Meyer B.H., Martinez K.L., Segura J.M., Pascoal P., Hovius R., George N., Johnsson K., and Vogel H. Covalent labeling of cell-surface proteins for in-vivo FRET studies. FEBS Lett 580 (2006) 1654-1658
66. Lamla T., and Erdmann V.A. The Nano-tag, a streptavidin-binding peptide for the purification and detection of recombinant proteins. Protein Expr Purif 33 (2004) 39-47
67. Chen I., Howarth M., Lin W., and Ting A.Y. Site-specific labeling of cell surface proteins with biophysical probes using biotin ligase. Nat Methods 2 (2005) 99-104
68. Jäger M., Nir E., and Weiss S. Site-specific labeling of proteins for single-molecule FRET by combining chemical and enzymatic modification. Protein Sci 15 (2006) 640-646
69. Lin C.W., and Ting A.Y. Transglutaminase-catalyzed site-specific conjugation of small-molecule probes to proteins in vitro and on the surface of living cells. J Am Chem Soc 128 (2006) 4542-4543
70. Meredith G.D., Wu H.Y., and Allbritton N.L. Targetted protein functionalization using his-tags. Bioconjug Chem 15 (2004) 969-982
71. Yeo D.S., Srinivasan R., Chen G.Y., and Yao S.Q. Expanded utility of the native chemical ligation reaction. Chemistry 10 (2004) 4664-4672
72. Jovin T.M., Lidke D.S., and Jares-Erijman E.A. Fluorescence resonance energy transfer (FRET) and fluorescence lifetime imaging microscopy (FLIM). In: Evangelista V., Barsanti L., Passarelli V., and Gualteri P. (Eds). From Cells to Proteins: Imaging Nature Across Dimensions. Proc NATO ASI (2005), Springer 209-216
73. Thaler C., Koushik S.V., Blank P.S., and Vogel S.S. Quantitative multiphoton spectral imaging and its use for measuring resonance energy transfer. Biophys J 89 (2005) 2736-2749
74. Wallrabe H., and Periasamy A. Imaging protein molecules using FRET and FLIM microscopy. Curr Opin Biotechnol 16 (2005) 19-27
75. van Munster E.B., Kremers G.J., Adjobo-Hermans M.J., and Gadella Jr. T.W.J. Fluorescence resonance energy transfer (FRET) measurement by gradual acceptor photobleaching. J Microsc 218 (2005) 253-262
76. Hanley QS, Murray PI, Forde TS: Microspectroscopic fluorescence analysis with prism-based imaging spectrometers: Review and current studies. Cytometry A 2006, 69:10.1002/cyto.a.20265.
77. Pfleger K.D.G., and Eidne K.A. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat Methods 3 (2006) 165
78. Esposito A., and Wouters F.S. Fluorescence Lifetime Imaging Microscopy. Curr Protocols Cell Biol (2004) 4.14.11-14.14.30
79. Duncan R.R., Bergmann A., Cousin M.A., Apps D.K., and Shipston M.J. Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells. J Microsc 215 (2004) 1-12
80. Esposito A., Gerritsen H.C., Oggier T., Lustenberger F., and Wouters F.S. Innovating lifetime microscopy: a compact and simple tool for life sciences, screening, and diagnostics. J Biomed Opt 11 (2006) 034016. A significant breakthrough in widefield detectors and other technology for FLIM.
81. Esposito A., Gerritsen H.C., and Wouters F.S. Fluorescence lifetime heterogeneity resolution in the frequency domain by lifetime moments analysis. Biophys J 89 (2005) 4286-4299
82. Dumas D., and Stoltz J.F. New tool to monitor membrane potential by FRET voltage sensitive dye (FRET-VSD) using spectral and fluorescence lifetime imaging microscopy (FLIM). Interest in cell engineering. Clin Hemorheol Microcirc 33 (2005) 293-302
83. van Munster E.B., and Gadella Jr. T.W.J. Fluorescence lifetime imaging microscopy (FLIM). Adv Biochem Eng Biotechnol 95 (2005) 143-175. An excellent overview of FLIM instrumentation and applications
84. Redford G.I., and Clegg R.M. Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J Fluoresc 15 (2005) 805-815
85. Hanley Q.S., Lidke K.A., Heintzmann R., Arndt-Jovin D.J., and Jovin T.M. Fluorescence lifetime imaging in an optically sectioning programmable array microscope (PAM). Cytometry A 67 (2005) 112-118
86. Hanley Q.S., and Clayton A.H. AB-plot assisted determination of fluorophore mixtures in a fluorescence lifetime microscope using spectra or quenchers. J Microsc 218 (2005) 62-67
87. Matthews D.R., Summers H.D., Njoh K., Errington R.J., Smith P.J., Barber P., Ameer-Beg S., and Vojnovic B. Technique for measurement of fluorescence lifetime by use of stroboscopic excitation and continuous-wave detection. Appl Opt 45 (2006) 2115-2123
88. Waharte F., Spriet C., and Heliot L. Setup and characterization of a multiphoton FLIM instrument for protein-protein interaction measurements in living cells. Cytometry A 69 (2006) 299-306
89. Hanley Q.S., and Ramkumar V. An internal standardization procedure for spectrally resolved fluorescence lifetime imaging. Appl Spectrosc 59 (2005) 261-266
90. Szentesi G., Vereb G., Horváth G., Bodnar A., Fábián A., Matkó J., Gáspár R., Damjanovich S., Mátyus L., and Jenei A. Computer program for analyzing donor photobleaching FRET image series. Cytometry A 67 (2005) 119-128
91. Jares-Erijman E.A., Spagnuolo C., Giordano L., Etchehon M., Kawior J., Mañalich-Arana M., Bossi M., Lidke D.S., Post J.N., Vermeij R.J., et al. Novel (bio)chemical and (photo)physical probes for imaging live cells. In: Pifat-Mrzljak G. (Ed). Supramolecular Structure and Function vol 8 (2004), Kluwer 99-118
92. Lidke K.A., Rieger B., Lidke D.S., and Jovin T.M. The role of photon statistics in fluorescence anisotropy imaging. IEEE Trans Image Process 14 (2005) 1237-1245
93. Cohen-Kashi M., Namer Y., and Deutsch M. Fluorescence resonance energy transfer imaging via fluorescence polarization measurement. J Biomed Opt 11 (2006) 034015
94. Rizzo M.A., and Piston D.W. High-contrast imaging of fluorescent protein FRET by fluorescence polarization microscopy. Biophys J 88 (2005) L14-L16
95. Squire A., Verveer P.J., Rocks O., and Bastiaens P.I. Red-edge anisotropy microscopy enables dynamic imaging of homo-FRET between green fluorescent proteins in cells. J Struct Biol 147 (2004) 62-69
96. Sapsford K.E., Berti L., and Medintz I.L. Materials for fluorescence resonance energy transfer analysis: beyond traditional donor-acceptor combinations. Angew Chem Int Ed Engl 45 (2006) 4562-4589. This survey with over 300 references covers the use of nanocrystals, nanoparticles, polymers and genetically encoded proteins in FRET measurements.
97. Ojida A., Honda K., Shinmi D., Kiyonaka S., Mori Y., and Hamachi I. Oligo-asp tag/Zn(II) complex probe as a new pair for labeling and fluorescence imaging of proteins. J Am Chem Soc (2006) 10.1021/ja061860
98. Spagnuolo CC, Vermeij RJ, Jares-Erijman EA: Improved photostable FRET-competent biarsenical-tetracysteine probes based on fluorinated fluoresceins. J Am Chem Soc 2006, in press. A difluoro-derivative of FlAsH displays higher photostability and quantum yield, and serves as a FRET donor for a tetrafluoro-derivative as acceptor.