Fluorescent proteins and fluorescence resonance energy transfer (FRET) as tools in signaling research

Johannes A. Schmid; Andreas Birbach

doi:10.1160/TH06-08-0472

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2007; 97(03): 378-384
DOI: 10.1160/TH06-08-0472

Theme Issue Article

Schattauer GmbH

Fluorescent proteins and fluorescence resonance energy transfer (FRET) as tools in signaling research

Johannes A. Schmid

¹Center for Biomolecular Medicine and Pharmacology, Department for Vascular Biology and Thrombosis Research, Medical University of Vienna, Austria

²Ludwig Boltzmann Institute for Cancer Research, Vienna, Austria

,

Andreas Birbach

²Ludwig Boltzmann Institute for Cancer Research, Vienna, Austria

› Institutsangaben

Abstract

Summary

The advent of fluorescent proteins has revolutionized signaling research, shifting focus from biochemical assays to analysis of live cells, organized tissues and even entire organisms. Modern applications of fluorescent proteins go beyond their use as specific markers of cells or tissues, allowing the researcher to visualize intracellular translocations as well as biochemical reactions. In this mini-review, we summarize the properties of a variety of fluorescent proteins, their detection using fluorescence microscopy and flow analysis, as well as their basic and more advanced applications, including fluorescence resonance energy transfer (FRET) to study signaling dynamics.

Keywords

Endothelial cells - signal transduction - protein trafficking

Volltext

Referenzen

References
1 Prasher DC, Eckenrode VK, Ward WW. et al. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 1992; 111: 229-233.
2 Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 1962; 59: 223-239.
3 Tsien RY. The green fluorescent protein. Annu Rev Biochem 1998; 67: 509-544.
4 Matz MV, Fradkov AF, Labas YA. et al. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 1999; 17: 969-973.
5 Baird GS, Zacharias DA, Tsien RY. Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA 2000; 97: 11984-11989.
6 Gurskaya NG, Fradkov AF, Terskikh A. et al. GFPlike chromoproteins as a source of far-red fluorescent proteins. FEBS Lett 2001; 507: 16-20.
7 Campbell RE, Tour O, Palmer AE. et al. A monomeric red fluorescent protein. Proc Natl Acad Sci USA 2002; 99: 7877-7882.
8 Shaner NC, Campbell RE, Steinbach PA. et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004; 22: 1567-1572.
9 Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Meth 2005; 2: 905-909.
10 Terskikh A, Fradkov A, Ermakova G. et al. „Fluorescent timer“: protein that changes color with time. Science 2000; 290: 1585-1588.
11 Patterson GH, Lippincott-Schwartz J. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 2002; 297: 1873-1877.
12 Chudakov DM, Verkhusha VV, Staroverov DB. et al. Photoswitchable cyan fluorescent protein for protein tracking. Nat Biotechnol 2004; 22: 1435-1439.
13 Miyawaki A. Fluorescent proteins in a new light. Nat Biotechnol 2004; 22: 1374-1376.
14 Wiedenmann J, Ivanchenko S, Oswald F. et al. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci USA 2004; 101: 15905-15910.
15 Valentin G, Verheggen C, Piolot T. et al. Photoconversion of YFP into a CFP-like species during acceptor photobleaching FRET experiments. Nat Methods 2005; 2: 801
16 Ormo M, Cubitt AB, Kallio K. et al. Crystal structure of the Aequorea victoria green fluorescent protein. Science 1996; 273: 1392-1395.
17 Rosenow MA, Huffman HA, Phail ME. et al. The crystal structure of the Y66L variant of green fluorescent protein supports a cyclization-oxidation-dehydration mechanism for chromophore maturation. Biochemistry 2004; 43: 4464-4472.
18 Yang F, Moss LG, Phillips Jr GN. The molecular structure of green fluorescent protein. Nat Biotechnol 1996; 14: 1246-1251.
19 Yarbrough D, Wachter RM, Kallio K. et al. Refined crystal structure of DsRed, a red fluorescent protein from coral, at 2.0-A resolution. Proc Natl Acad Sci USA 2001; 98: 462-467.
20 van Haperen R, Cheng C, Mees BM. et al. Functional expression of endothelial nitric oxide synthase fused to green fluorescent protein in transgenic mice. Am J Pathol 2003; 163: 1677-1686.
21 Schmid JA, Birbach A, Hofer-Warbinek R. et al. Dynamics of NF kappa B and Ikappa Balpha studied with green fluorescent protein (GFP) fusion proteins. Investigation of GFP-p65 binding to DNa by fluorescence resonance energy transfer. J Biol Chem 2000; 275: 17035-17042.
22 Kearney JB, Kappas NC, Ellerstrom C. et al. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood 2004; 03: 4527-4535.
23 Chan FK, Siegel RM, Zacharias D. et al. Fluorescence resonance energy transfer analysis of cell surface receptor interactions and signaling using spectral variants of the green fluorescent protein. Cytometry 2001; 44: 361-368.
24 Zhang F, Hackett NR, Lam G. et al. Green fluorescent protein selectively induces HSP70-mediated upregulation of COX-2 expression in endothelial cells. Blood 2003; 102: 2115-2121.
25 Meyer-Ficca ML, Meyer RG, Kaiser H. et al. Comparative analysis of inducible expression systems in transient transfection studies. Anal Biochem 2004; 334: 9-19.
26 Giaretta I, Madeo D, Bonaguro R. et al. A comparative evaluation of gene transfer into blood cells using the same retroviral backbone for independent expression of the EGFP and deltaLNGFR marker genes. Haematologica 2000; 85: 680-689.
27 Motoike T, Loughna S, Perens E. et al. Universal GFP reporter for the study of vascular development. Genesis 2000; 28: 75-81.
28 Eslami MH, Gangadharan SP, Sui X. et al. Gene delivery to in situ veins: differential effects of adenovirus and adeno-associated viral vectors. J Vasc Surg 2000; 31: 1149-1159.
29 Garton KJ, Ferri N, Raines EW. Efficient expression of exogenous genes in primary vascular cells using IRES-based retroviral vectors. Biotechniques. 2002 32: 830, 832, 834
30 Lamfers ML, Wijnberg MJ, Grimbergen JM. et al. Adenoviral gene transfer of a u-PA receptor-binding plasmin inhibitor and green fluorescent protein: inhibition of migration and visualization of expression. Thromb Haemost 2000; 84: 460-467.
31 Breuss JM, Cejna M, Bergmeister H. et al. Activation of nuclear factor-kappa B significantly contributes to lumen loss in a rabbit iliac artery balloon angioplasty model. Circulation 2002; 105: 633-638.
32 Amoh Y, Yang M, Li L. et al. Nestin-linked green fluorescent protein transgenic nude mouse for imaging human tumor angiogenesis. Cancer Res 2005; 65: 5352-5357.
33 Zentilin L, Tafuro S, Zacchigna S. et al. Bone marrow mononuclear cells are recruited to the sites of VEGF-induced neovascularization but are not incorporated into the newly formed vessels. Blood 2006; 107: 3546-3554.
34 White J, Stelzer E. Photobleaching GFP reveals protein dynamics inside live cells. Trends Cell Biol 1999; 9: 61-65.
35 Maiti S, Haupts U, Webb WW. Fluorescence correlation spectroscopy: diagnostics for sparse molecules. Proc Natl Acad Sci USA 1997; 94: 11753-11757.
36 Medina MA, Schwille P. Fluorescence correlation spectroscopy for the detection and study of single molecules in biology. Bioessays 2002; 24: 758-764.
37 Maddox PS, Moree B, Canman JC. et al. Spinning disk confocal microscope system for rapid high-resolution, multimode, fluorescence speckle microscopy and green fluorescent protein imaging in living cells. Methods Enzymol 2003; 360: 597-617.
38 Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 1990; 248: 73-76.
39 Denk W, Svoboda K. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 1997; 18: 351-357.
40 White N, Errington R. Multi-photon microscopy: seeing more by imaging less. Biotechniques 2002; 33: 298-295.
41 Tozer GM, Ameer-Beg SM, Baker J. et al. Intravital imaging of tumour vascular networks using multiphoton fluorescence microscopy. Adv Drug Deliv Rev 2005; 57: 135-152.
42 Galbraith DW, Anderson MT, Herzenberg LA. Flow cytometric analysis and FACS sorting of cells based on GFP accumulation. Methods Cell Biol 1999; 58: 315-341.
43 Jares-Erijman EA, Jovin TM. FRET imaging. Nat Biotechnol 2003; 21: 1387-1395.
44 Schmid JA, Sitte HH. Fluorescence resonance energy transfer in the study of cancer pathways. Curr Opin Oncol 2003; 15: 55-64.
45 Förster T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys 1948; 2: 57-75.
46 Wallrabe H, Periasamy A. Imaging protein molecules using FRET and FLIM microscopy. Curr Opin Biotechnol 2005; 16: 19-27.
47 Tzima E, Del Pozo MA, Kiosses WB. et al. Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J 2002; 21: 6791-6800.
48 Jobin CM, Chen H, Lin AJ. et al. Receptor-regulated dynamic interaction between endothelial nitric oxide synthase and calmodulin revealed by fluorescence resonance energy transfer in living cells. Biochemistry 2003; 42: 11716-11725.
49 Sato M, Ozawa T, Inukai K. et al. Fluorescent indicators for imaging protein phosphorylation in single living cells. Nat Biotechnol 2002; 20: 287-294.
50 Zhang J, Ma Y, Taylor SS. et al. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Natl Acad Sci USA 2001; 98: 14997-15002.
51 Sasaki K, Sato M, Umezawa Y. Fluorescent indicators for Akt/protein kinase B and dynamics of Akt activity visualized in living cells. J Biol Chem 2003; 278: 30945-30951.
52 van der Wal J, Habets R, Varnai P. et al. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J Biol Chem 2001; 276: 15337-15344.
53 Violin JD, Zhang J, Tsien RY. et al. A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J Cell Biol 2003; 161: 899-909.
54 Mochizuki N, Yamashita S, Kurokawa K. et al. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 2001; 411: 1065-1068.
55 Pertz O, Hahn KM. Designing biosensors for Rho family proteins--deciphering the dynamics of Rho family GTPase activation in living cells. J Cell Sci 2004; 117: 1313-1318.
56 Zaccolo M. Use of chimeric fluorescent proteins and fluorescence resonance energy transfer to monitor cellular responses. Circ Res 2004; 94: 866-873.
57 Hoffmann C, Gaietta G, Bunemann M. et al. A FlAsH-based FRET approach to determine G proteincoupled receptor activation in living cells. Nat Methods 2005; 2: 171-176.
58 Vilardaga JP, Bunemann M, Krasel C. et al. Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat Biotechnol 2003; 21: 807-812.
59 Nobles M, Benians A, Tinker A. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc Natl Acad Sci USA 2005; 102: 18706-18711.
60 Gales C, Rebois RV, Hogue M. et al. Real-time monitoring of receptor and G-protein interactions in living cells. Nat Methods 2005; 2: 177-184.
61 Hein P, Frank M, Hoffmann C. et al. Dynamics of receptor/G protein coupling in living cells. EMBO J 2005; 24: 4106-4114.
62 Bunemann M, Frank M, Lohse MJ. Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc Natl Acad Sci USA 2003; 100: 16077-16082.
63 Gibson SK, Gilman AG. Gialpha and Gbeta subunits both define selectivity of G protein activation by alpha2-adrenergic receptors. Proc Natl Acad Sci USA 2006; 103: 212-217.
64 Janetopoulos C, Jin T, Devreotes P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 2001; 291: 2408-2411.
65 Sato M, Ueda Y, Takagi T. et al. Production of PtdInsP3 at endomembranes is triggered by receptor endocytosis. Nat Cell Biol 2003; 5: 1016-1022.
66 Tanimura A, Nezu A, Morita T. et al. Fluorescent biosensor for quantitative real-time measurements of inositol 1,4,5-trisphosphate in single living cells. J Biol Chem 2004; 279: 38095-38098.
67 Zaccolo M, De Giorgi F, Cho CY. et al. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol 2000; 2: 25-29.
68 Honda A, Adams SR, Sawyer CL. et al. Spatiotemporal dynamics of guanosine 3',5'-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci USA 2001; 98: 2437-2442.
69 Sato M, Hida N, Ozawa T. et al. Fluorescent indicators for cyclic GMP based on cyclic GMP-dependent protein kinase Ialpha and green fluorescent proteins. Anal Chem 2000; 72: 5918-5924.
70 Zaccolo M, Pozzan T. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 2002; 295: 1711-1715.
71 Ponsioen B, Zhao J, Riedl J. et al. Detecting cAMPinduced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 2004; 5: 1176-1180.
72 Nikolaev VO, Gambaryan S, Lohse MJ. Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 2006; 3: 23-25.
73 Wouters FS, Verveer PJ, Bastiaens PI. Imaging biochemistry inside cells. Trends Cell Biol 2001; 11: 203-211.
74 Verveer PJ, Wouters FS, Reynolds AR. et al. Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. Science 2000; 290: 1567-1570.
75 Patterson G, Day RN, Piston D. Fluorescent protein spectra. Journal of Cell Science 2001; 114: 837-838.
76 Rizzo MA, Springer GH, Granada B. et al. An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 2004; 22: 445-449.
77 Griesbeck O, Baird GS, Campbell RE. et al. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 2001; 276: 29188-29194.
78 Bevis BJ, Glick BS. Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat Biotechnol 2002; 20: 83-87.
79 Fradkov AF, Verkhusha VV, Staroverov DB. et al. Far-red fluorescent tag for protein labelling. Biochem J 2002; 368: 17-21.
80 Youvan DC, Coleman WJ, Silva CM. et al. Calibration of fluorescence resonance energy transfer in microscopy using genetically engineered GFP derivatives on nickel chelating beads. Biotechnology et alia 1997; 3: 1-18.