New red-fluorescent calcium indicators for optogenetics, photoactivation and multi-color imaging

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 10, 2014, Pages 2284-2306

  Oheim, Martin ^a,b,c   van 't Hoff, Marcel ^a,b,c,d   Feltz, Anne ^b,e   Zamaleeva, Alsu ^b,e   Mallet, Jean Maurice ^f,g   Collot, Mayeul ^f,g  

^a CNRS   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY OF FLORENCE   (Italy)

^e PSL RESEARCH UNIVERSITY   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g Centre National de la Recherche Scientifique   (France)

Author keywords

Calcium; Fluorescence; Genetically encoded calcium indicator (GECI); Nanobiosensor; Spectral cross talk

Indexed keywords

BUFFER; CALCIUM CRIMSON; CALCIUM ION; CALCIUM ORANGE; CALCIUM RUBY; FLUORESCENT DYE; FURA RED FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; INDICATOR; MACROGOL; PYRONINE; RED FLUORESCENT PROTEIN; RHODAMINE; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

BINDING AFFINITY; CALCIUM BINDING; CALCIUM IMAGING; CALCIUM SIGNALING; CHEMICAL PARAMETERS; CHEMICAL STRUCTURE; ELECTRON TRANSPORT; EXCITATION; FLUORESCENCE; GENETICALLY ENCODED CALCIUM INDICATOR; IMAGING; IN VITRO STUDY; MOLECULAR BIOLOGY; NONHUMAN; OPTOGENETICS; PHOTOACTIVATION; PHOTOINDUCED CHARGE TRANSFER; PHOTOINDUCED ELECTRON TRANSFER; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; QUANTUM YIELD; REVIEW; SPECTRAL SEPARABILITY INDEX; THERMOSTABILITY;

ANIMALIA;

CALCIUM; FLUORESCENCE; GENETICALLY ENCODED CALCIUM INDICATOR (GECI); NANOBIOSENSOR; SPECTRAL CROSS-TALK;

ANIMALS; BACTERIAL PROTEINS; BENZOFURANS; BORON COMPOUNDS; CALCIUM; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HUMANS; IMIDAZOLES; LUMINESCENT PROTEINS; MOLECULAR IMAGING; OPTOGENETICS; PHOTOCHEMISTRY; RHODAMINES; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

EID: 84904969407     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.03.010     Document Type: Review

References (181)

1. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
2. Takahashi A., Camacho P., Lechleiter J.D., Herman B. Measurement of intracellular calcium. Physiol. Rev. 1999, 79:1089-1125.
3. Hyrc K., Bownik J., Goldberg M. Ionic selectivity of low-affinity ratiometric calcium indicators: mag-Fura-2, Fura-2FF and BTC. Cell Calcium 2000, 27:75-86.
4. 2+ signals. Cell Calcium 2000, 28:213-223.
5. Poenie M. Fluorescent calcium indicators based on BAPTA. Calcium Signalling 2005, Taylor & Francis CRC Press, Boca Raton. 2nd ed. J.W. Putney (Ed.).
6. Paredes R.M., Etzler J.C., Watts L.T., Zheng W., Lechleiter J.D. Chemical calcium indicators. Methods 2008, 46:143-151.
7. c: basic practical considerations. Calcium Signalling Protocols 2013, vol. 937:3-36. Springer, Berlin, Heidelberg, New York. D.G. Lambert, R.D. Rainbow (Eds.).
8. 2+ imaging. Cold Spring Harb. Protoc. 2013, 2013. (pdb. top066050).
9. Tsien R.Y. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 1981, 290:527-528.
10. 2+ signal from fura-2 loaded mast cells depends strongly on the method of dye-loading. FEBS Lett. 1985, 192:13-18.
11. Bright G.R., Fisher G.W., Rogowska J., Taylor D.L. Fluorescence ratio imaging microscopy. Methods Cell Biol. 1989, 30:157-192.
12. Silver R.B. Ratio imaging: practical considerations for measuring intracellular calcium and pH in living tissue. Methods Cell Biol. 1998, 56:237-251.
13. Demchenko A.P. The concept of λ-ratiometry in fluorescence sensing and imaging. J. Fluoresc. 2010, 20:1099-1128.
14. Oheim M., Naraghi M., Müller T.H., Neher E. Two dye two wavelength excitation calcium imaging: results from bovine adrenal chromaffin cells. Cell Calcium 1998, 24:71-84.
15. 2+] signals from calcium-indicator dyes. News Physiol. Sci. 2000, 15:19-26.
16. Neher E. Quantitative aspects of calcium fluorimetry. Cold Spring Harb. Protoc. October 1, 2013, 2013. (pdb.top078204).
17. Molecular Fluorescence 2002, Wiley-VCH, Weinheim. B. Valeur (Ed.).
18. Tsien R.Y. Monitoring cell calcium. Calcium as a Cellular Regulator 1999, 28-54. Oxford University Press, New York. E. Carfoli, C. Klee (Eds.).
19. Harrison S.M., Bers D.M. Correction of proton and Ca association constants of EGTA for temperature and ionic strength. Am. J. Physiol. Cell Physiol. 1989, 256:C1250-C1256.
20. Pethig R., Kuhn M., Payne R., Adler E., Chen T.-H., Jaffe L. On the dissociation constants of BAPTA-type calcium buffers. Cell Calcium 1989, 10:491-498.
21. Oliver A.E., Baker G.A., Fugate R.D., Tablin F., Crowe J.H. Effects of temperature on calcium-sensitive fluorescent probes. Biophys. J. 2000, 78:2116-2126.
22. Messler P., Harz H., Uhl R. Instrumentation for multiwavelengths excitation imaging. J. Neurosci. Methods 1996, 69:137-147.
23. Dunn K., Maxfield F.R. Ratio imaging instrumentation. Methods Cell Biol. 2003, 72:389-413.
24. Uhl R. Arc lamps and monochromators for fluorescence microscopy. Cold Spring Harb. Protoc. 2012, 2012. (pdb. top071001).
25. Becker P., Fay F. Photobleaching of fura-2 and its effect on determination of calcium concentrations. Am. J. Physiol. Cell Physiol. 1987, 253:C613-C618.
26. Roe M., Lemasters J., Herman B. Assessment of Fura-2 for measurements of cytosolic free calcium. Cell Calcium 1990, 11:63-73.
27. Di Virgilio F., Steinberg T., Silverstein S. Inhibition of Fura-2 sequestration and secretion with organic anion transport blockers. Cell Calcium 1990, 11:57-62.
28. 2+ concentrations. Cell Calcium 1991, 12:29-37.
29. Gilabert J.A. Cytoplasmic calcium buffering. Calcium Signalling 2012, vol. 740:483-498. Springer, Dordrecht. M.S. Islam (Ed.).
30. 2+ binding in bovine chromaffin cells. Biophys. J. 1998, 75:1635-1647.
31. Tsien R.Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 1980, 19:2396-2404.
32. He Z.H., Lei L., Li J.L., Shi Z. Synthesis of new BAPTA calcium chelators. Synth. Commun. 2009, 39:2074-2081.
33. Levy L.A., Murphy E., Raju B., London R.E. Measurement of cytosolic free magnesium ion concentration by fluorine-19 NMR. Biochemistry 1988, 27:4041-4048.
34. ® based fluorescent off-on indicators with low affinity for calcium. Org. Biomol. Chem. 2005, 3:2755-2761.
35. Kim H.J., Han J.H., Kim M.K., Lim C.S., Kim H.M., Cho B.R. Dual-color imaging of sodium/calcium ion activities with two-photon fluorescent probes. Angew. Chem. Int. Ed. 2010, 49:6786-6789.
36. Yan S. Photoaktivierungsfähige Rhodamine als Bio-Calcium-Sensoren und Markierungen für Tetracystein-Tags in Proteinen 2010, Ph. D., Max-Planck-Institut für biophysikalische Chemie, Georg-August Universität Göttingen, Göttingen.
37. 2+ fluorescent sensor: signaling by conformationally induced PET suppression in a bichromophoric acridinedione. Eur. J. Org. Chem. 2009, 2009:5941-5947.
38. 2+ indicator, Calcium Ruby. Org. Lett. 2007, 9:2629-2632.
39. 2+ dyes with green flent protein and its variants: problems and solutions. Biochem. J. 2001, 356:345-352.
40. 2+ in EGFP expressing cells with a low-affinity Calcium Ruby and its dextran conjugate. Cell Calcium 2009, 45:275-283.
41. 2+ imaging. J. Am. Chem. Soc. 2012, 134:14923-14931.
42. Berridge M.J. Calcium microdomains: organization and function. Cell Calcium 2006, 40:405-412.
43. Maravall M., Mainen Z., Sabatini B., Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 2000, 78:2655-2667.
44. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
45. Ellis-Davies G.C. Are caged compounds still useful?. Photosensitive Molecules for Controlling Biological Function 2011, 39-56. Springer.
46. Fenno L.E., Deisseroth K. Optogenetic tools for control of neural activity. Optical Imaging of Neocortical Dynamics 2014, 73-86. Springer.
47. Bernardinelli Y., Salmon C., Jones E.V., Farmer W.T., Stellwagen D., Murai K.K. Astrocytes display complex and localized calcium responses to single-neuron stimulation in the hippocampus. J. Neurosci. 2011, 31:8905-8919.
48. Mohanty S.K., Reinscheid R.K., Liu X., Okamura N., Krasieva T.B., Berns M.W. In-depth activation of channelrhodopsin 2-sensitized excitable cells with high spatial resolution using two-photon excitation with a near-infrared laser microbeam. Biophys. J. 2008, 95:3916-3926.
49. 2+ indicators and photophysical considerations for optogenetic applications. ACS Chem. Neurosci. 2013, 4:963-972.
50. Buschmann V., Weston K.D., Sauer M. Spectroscopic study and evaluation of red-absorbing fluorescent dyes. Bioconjug. Chem. 2003, 14:195-204.
51. Tsien R.Y., Ernst L., Waggoner A. Fluorophores for confocal microscopy: photophysics and photochemistry. Handbook of Biological Confocal Microscopy 2006, 338-352. Springer, New York. 3rd ed. J.B. Pawley (Ed.).
52. Minta A., Kao J., Tsien R.Y. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 1989, 264:8171-8178.
53. Strickler S., Berg R.A. Relationship between absorption intensity and fluorescence lifetime of molecules. J. Chem. Phys. 1962, 37:814.
54. Oheim M., Li D. Quantitative colocalisation imaging: concepts, measurements, and pitfalls. Imaging Cellular and Molecular Biological Functions 2007, 117-155. Springer, Berlin Heidelberg. S.L. Shorte, F. Frischknecht (Eds.).
55. ijk. Biophys. J. 2009, 96:31a-32a.
56. Lohr C. Monitoring neuronal calcium signalling using a new method for ratiometric confocal calcium imaging. Cell Calcium 2003, 34:295-303.
57. 2+-measurements with visible wavelength indicators in isolated cardiac myocytes. Cell Calcium 1993, 14:359-372.
58. 2+ signal transduction. J. Biol. Chem. 2002, 277:14227-14237.
59. Morris G.E., Nelson C.P., Standen N.B., Challiss R.A., Willets J.M. Endothelin signalling in arterial smooth muscle is tightly regulated by G protein-coupled receptor kinase 2. Cardiovasc. Res. 2010, 85:424-433.
60. Kawai T., Lee J.M., Nagata K., Matsumoto S., Tanokura M., Nagasawa H. The arginine residue within the C-terminal active core of Bombyx mori pheromone biosynthesis-activating neuropeptide is essential for receptor binding and activation. Front. Endocrinol. 2012, 3:42.
61. Schauer C., Leinders-Zufall T. Imaging calcium responses in GFP-tagged neurons of hypothalamic mouse brain slices. J. Vis. Exp. 2012, 66:e4213.
62. Fu M., Xiao Y., Qian X., Zhao D., Xu Y. A design concept of long-wavelength fluorescent analogs of rhodamine dyes: replacement of oxygen with silicon atom. Chem. Commun. 2008, 1780-1782.
63. Egawa T., Koide Y., Hanaoka K., Komatsu T., Terai T., Nagano T. Development of a fluorescein analogue, TokyoMagenta, as a novel scaffold for fluorescence probes in red region. Chem. Commun. 2011, 47:4162-4164.
64. Egawa T., Hanaoka K., Koide Y., Ujita S., Takahashi N., Ikegaya Y., et al. Development of a far-red to near-infrared fluorescence probe for calcium ion and its application to multicolor neuronal imaging. J. Am. Chem. Soc. 2011, 133:14157-14159.
65. Egawa T., Hirbayashi K., Koide Y., Kobayashi C., Takahashi N., Mineno T., et al. Red fluorescent probe for monitoring the dynamics of cytoplasmic calcium ions. Angew. Chem. Int. Ed. 2013, 52:3874-3877.
66. Hyrc K.L., Minta A., Escamilla P.R., Chan P.P., Meshik X.A., Goldberg M.P. Synthesis and properties of Asante Calcium Red-a novel family of long excitation wavelength calcium indicators. Cell Calcium 2013, 54:320-333.
67. Irion G., Ochsenfeld L., Naujok A., Zimmermann H.W. The concentration jump method. Kinetics of vital staining of mitochondria in HeLa cells with lipophilic cationic fluorescent dyes. Histochemistry Jan 1993, 99:75-83.
68. Eberhard M., Erne P. Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochem. Biophys. Res. Commun. 1991, 180:209-215.
69. Ranganathan R., Bacskai B.J., Tsien R.Y., Zuker C.S. Cytosolic calcium transients: spatial localization and role in Drosophila photoreceptor cell function. Neuron 1994, 13:837-848.
70. 2+ network. J. Cell Biol. 1997, 136:833-844.
71. Hoth M., Fanger C.M., Lewis R.S. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 1997, 137:633-648.
72. Hajnóczky G., Robb-Gaspers L.D., Seitz M.B., Thomas A.P. Decoding of cytosolic calcium oscillations in the mitochondria. Cell 1995, 82:415-424.
73. Ward S.M., Ordog T., Koh S.D., Baker S.A., Jun J.Y., Amberg G., et al. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J. Physiol. 2000, 525(Pt. 2):355-361.
74. Del Nido P.J., Glynn P., Buenaventura P., Salama G., Koretsky A.P. Fluorescence measurement of calcium transients in perfused rabbit heart using rhod 2. Am. J. Physiol. 1998, 274:H728-H741.
75. Soibinet M., Souchon V., Leray I., Valeur B. Rhod-5N as a fluorescent molecular sensor of cadmium (II) ion. J. Fluoresc. 2008, 18:1077-1082.
76. Cooley L.A., Martin V.V., Gee K.R. Development and in vitro characterization of ratiometric and intensity-based fluorescent ion sensors. Methods Mol. Biol. 2013, 995:133-145.
77. Hsyu P.H., Gisclon L.G., Hui A.C., Giacomini K.M. Interactions of organic anions with the organic cation transporter in renal BBMV. Am. J. Physiol. 1988, 254:F56-F61.
78. Silverman W., Locovei S., Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 2008, 295:C761-C767.
79. Wang T., Kumada T., Morishima T., Iwata S., Kaneko T., Yanagawa Y., et al. Accumulation of GABAergic neurons, causing a focal ambient GABA gradient, and downregulation of KCC2 are induced during microgyrus formation in a mouse model of polymicrogyria. Cereb. Cortex 2014, 24(4):1088-1101.
80. Hashimoto M., Enomoto M., Morales J., Kurebayashi N., Sakurai T., Hashimoto T., et al. Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi. Mol. Microbiol. 2013, 87:1133-1150.
81. Qian L., Berry E.C., Fu J.D., Ieda M., Srivastava D. Reprogramming of mouse fibroblasts into cardiomyocyte-like cells in vitro. Nat. Protoc. 2013, 8:1204-1215.
82. Fei B., Yu S., Geahlen R.L. Modulation by Syk of Bcl-2, calcium and the calpain-calpastatin proteolytic system in human breast cancer cells. Biochim. Biophys. Acta 2013, 1833:2153-2164.
83. Mortensen O.V. MKP3 eliminates depolarization-dependent neurotransmitter release through downregulation of L-type calcium channel Cav1.2 expression. Cell Calcium Mar 2013, 53:224-230.
84. Whitaker J.E., Haugland R.P., Ryan D., Hewitt P.C., Haugland R.P., Prendergast F.G. Fluorescent rhodol derivatives: versatile, photostable labels and tracers. Anal. Biochem. 1992, 207:267-279.
85. Rousseau E., Michel P.P., Hirsch E.C. The iron-binding protein lactoferrin protects vulnerable dopamine neurons from degeneration by preserving mitochondrial calcium homeostasis. Mol. Pharmacol. Dec 2013, 84:888-898.
86. Entcheva E. Cardiac optogenetics. Am. J. Physiol. Heart Circ. Physiol. 2013, 304:H1179-H1191.
87. Jia Z., Valiunas V., Lu Z., Bien H., Liu H., Wang H.Z., et al. Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery. Circ. Arrhythm. Electrophysiol. 2011, 4:753-760.
88. Koide Y., Urano Y., Hanaoka K., Terai T., Nagano T. Development of an Si-rhodamine-based far-red to near-infrared fluorescence probe selective for hypochlorous acid and its applications for biological imaging. J. Am. Chem. Soc. 2011, 133:5680-5682.
89. Koide Y., Urano Y., Hanaoka K., Piao W., Kusakabe M., Saito N., et al. Development of NIR fluorescent dyes based on Si-rhodamine for in vivo imaging. J. Am. Chem. Soc. 2012, 134:5029-5031.
90. Wang T., Zhao Q.-J., Hu H.-G., Yu S.-C., Liu X., Liu L., et al. Spirolactonized Si-rhodamine: a novel NIR fluorophore utilized as a platform to construct Si-rhodamine-based probes. Chem. Commun. 2012, 48:8781-8783.
91. Sun Y.-Q., Liu J., Lv X., Liu Y., Zhao Y., Guo W. Rhodamine-inspired far-red to near-infrared dyes and their application as fluorescence probes. Angew. Chem. Int. Ed. 2012, 51:7634-7636.
92. Lemke E.A., Heppenstall P., Eggeling C., Manley S., Johnsson K. A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat. Chem. 2013, 5:132-139.
93. Nimmerjahn A., Kirchhoff F., Kerr J.N., Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 2004, 1:31-37.
94. Wu L., Dai Y., Marriott G. Optical control of calcium affinity in a spiroamido-rhodamine based calcium chelator. Org. Lett. 2011, 13:2018-2021.
95. Wang T., Zhao Q.-J., Hu H.-G., Yu S.-C., Liu X., Liu L., Wu Q.-Y. Spirolactonized Si-rhodamine: a novel NIR fluorophore utilized as a platform to construct Si-rhodamine-based probes. Chem. Comm. 2012, 48:8781-8783.
96. Sorrentino R., Autore G., Cirino G., d'Emmanuele de Villa Bianca R., Calignano A., Vanasia M., et al. Effect of spironolactone and its metabolites on contractile property of isolated rat aorta rings. J. Cardiovasc. Pharmacol. 2000, 36:230-235.
97. 2+ indicators into intact single fibers of frog muscle. Biophys. J. 1997, 72:2736-2747.
98. Tsien R.Y., Minta A. Fluorescent Indicator Dyes for Calcium Working at Long Wavelengths 1994.
99. Li D., Hérault K., Isacoff E.Y., Oheim M., Ropert N. Optogenetic activation of LiGluR-expressing astrocytes evokes anion channel-mediated glutamate release. J. Physiol. 2012, 590:855-873.
100. 2+-regulated exocytosis from cortical astrocytes. J. Neurosci. 2008, 28:7648-7658.
101. Collot M., Wilms C.D., Bentkhayet A., Marcaggi P., Couchman K., Charpak S., et al. Nanomolar affinity Calcium Ruby, a powerful tool forcellular imaging 2014, (submitted).
102. M. Collot and J.-M. Mallet, "Fluorescent red emitting functionalizable calcium indicators," FR Patent, 2013.
103. Schnell C., Shahmoradi A., Wichert S.P., Mayerl S., Hagos Y., Heuer H., et al. The multispecific thyroid hormone transporter OATP1C1 mediates cell-specific sulforhodamine 101-labeling of hippocampal astrocytes. Brain Struct. Funct. 2013, 1-11.
104. Huang S.-T., Jian J.-L., Peng H.-Z., Wang K.-L., Lin C.-M., Huang C.-H., et al. The synthesis and optical characterization of novel iminocoumarin derivatives. Dyes Pigments 2010, 86:6-14.
105. 2+ indicators excited with visible light. Cell Calcium 2006, 39:3-11.
106. 2+ indicators excited with visible light. Cell Calcium 11/2001, 30:331-335.
107. 2+ indicator for in vivo bioimaging. Chin. Chem. Lett. 2013, 24:156-158.
108. 2+ fluoroionophores based on the BODIPY fluorophore. Comb. Chem. High Throughput Screen. 2003, 6:363-366.
109. De Silva A.P., Gunaratne H.N., Gunnlaugsson T., Huxley A.J., McCoy C.P., Rademacher J.T., et al. Signaling recognition events with fluorescent sensors and switches. Chem. Rev. 1997, 97:1515-1566.
110. Loudet A., Burgess K. BODIPY dyes and their derivatives: syntheses and spectroscopic properties. Chem. Rev. 2007, 107:4891-4932.
111. Boens N., Leen V., Dehaen W. Fluorescent indicators based on BODIPY. Chem. Soc. Rev. 2012, 41:1130-1172.
112. Kamiya M., Johnsson K. Localizable and highly sensitive calcium indicator based on a BODIPY fluorophore. Anal. Chem. 2010, 82:6472-6479.
113. Umezawa K., Matsui A., Nakamura Y., Citterio D., Suzuki K. Bright, color-tunable fluorescent dyes in the VIS/NIR region: establishment of new 'tailor-made' multicolor fluorophores based on borondipyrromethene. Chem. Eur. 2009, 15:1096-1106.
114. 2+ imaging. Chem. Commun. 2011, 47:10407-10409.
115. Ozmen B., Akkaya E.U. Infrared fluorescence sensing of submicromolar calcium: pushing the limits of photoinduced electron transfer. Tetrahedron Lett. 11/18/2000, 41:9185-9188.
116. Akkaya E.U., Turkyilmaz S. A squaraine-based near IR fluorescent chemosensor for calcium. Tetrahedron Lett. 1997, 38:4513-4516.
117. Lattanzio F.A., Bartschat D.K. The effect of pH on rate constants, ion selectivity and thermodynamic properties of fluorescent calcium and magnesium indicators. Biochem. Biophys. Res. Commun. 1991, 177:184-191.
118. Zheng Q., Juette M.F., Jockusch S., Wasserman M.R., Zhou Z., Altman R.B., et al. Ultra-stable organic fluorophores for single-molecule research. Chem. Soc. Rev. 2014, 43:1044-1056.
119. Kolmakov K., Wurm C.A., Meineke D.N., Göttfert F., Boyarskiy V.P., Belov V.N., et al. Polar red-emitting rhodamine dyes with reactive groups: synthesis, photophysical properties, and two-color STED nanoscopy applications. Chem. Eur. J. 2014, 20:146-157.
120. 2+ reporters at the single-cell level. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7260-7265.
121. Rogers K.L., Picaud S., Roncali E., Boisgard R., Colasante C., Stinnakre J., et al. Non-invasive in vivo imaging of calcium signaling in mice. PLoS One 2007, 2:e974.
122. 2+ sensitive bioluminescent reporter. Methods Mol. Biol. 2014, 1098:33-45.
123. 2+ reporters in single cells and mice. PLoS One 2011, 6:e19520.
124. Garaschuk O., Milos R.-I., Konnerth A. Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat. Protoc. 2006, 1:380-386.
125. Takahashi N., Oba S., Yukinawa N., Ujita S., Mizunuma M., Matsuki N., et al. High-speed multineuron calcium imaging using Nipkow-type confocal microscopy. Curr Protoc Neurosci 2011, vol. 2:14. (Chapter 2, Unit 2).
126. Li D., Agulhon C., Schmidt E., Oheim M., Ropert N. New tools for investigating astrocyte-to-neuron communication. Front. Cell. Neurosci. 2013, 7:193.
127. Baird G.S., Zacharias D.A., Tsien R.Y. Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11241-11246.
128. 2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 2001, 19:137-141.
129. 2+. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3197-3202.
130. 2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. 1999, 96:2135-2140.
131. 2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
132. Heim N., Griesbeck O. Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J. Biol. Chem. 2004, 279:14280-14286.
133. Mank M., Griesbeck O. Genetically encoded calcium indicators. Chem. Rev. 2008, 108:1550-1564.
134. Chen T.-W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
135. Mishin A.S., Subach F.V., Yampolsky I.V., King W., Lukyanov K.A., Verkhusha V.V. The first mutant of the Aequorea victoria green fluorescent protein that forms a red chromophore. Biochemistry 2008, 47:4666-4673.
136. Matz M.V., Fradkov A.F., Labas Y.A., Savitsky A.P., Zaraisky A.G., Markelov M.L., et al. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 1999, 17:969-973.
137. Fradkov A.F., Chen Y., Ding L., Barsova E.V., Matz M.V., Lukyanov S.A. Novel fluorescent protein from Discosoma coral and its mutants possesses a unique far-red fluorescence. FEBS Lett. 2000, 479:127-130.
138. Wiedenmann J., Schenk A., Röcker C., Girod A., Spindler K.-D., Nienhaus G.U. A far-red fluorescent protein with fast maturation and reduced oligomerization tendency from Entacmaea quadricolor (Anthozoa, Actinaria). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11646-11651.
139. Wiedenmann J., Oswald F., Nienhaus G.U. Fluorescent proteins for live cell imaging: opportunities, limitations, and challenges. IUBMB Life 2009, 61:1029-1042.
140. Müller-Taubenberger A., Anderson K.I. Recent advances using green and red fluorescent protein variants. Appl. Microbiol. Biotechnol. 2007, 77:1-12.
141. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., et al. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:7877-7882.
142. Shaner N.C., Lin M.Z., McKeown M.R., Steinbach P.A., Hazelwood K.L., Davidson M.W., et al. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 2008, 5:545-551.
143. Kredel S., Nienhaus K., Oswald F., Wolff M., Ivanchenko S., Cymer F., et al. Optimized and far-red-emitting variants of fluorescent protein eqFP611. Chem. Biol. 2008, 15:224-233.
144. Kredel S., Oswald F., Nienhaus K., Deuschle K., Röcker C., Wolff M., et al. mRuby, a bright monomeric red fluorescent protein for labeling of subcellular structures. PLoS One 2009, 4:e4391.
145. Remington S.J. Fluorescent proteins: maturation, photochemistry and photophysics. Curr. Opin. Struct. Biol. 2006, 16:714-721.
146. 2+ indicators. Science 2011, 333:1888-1891.
147. 2+ indicators: properties and evaluation. Biochim. Biophys. Acta, Mol. Cell Res. 2013, 1833(7):1787-1797.
148. 2+ indicator for detecting optically evoked action potentials. PLoS One 2012, 7:e39933.
149. Lefort S., Tomm C., Floyd Sarria J.-C., Petersen C.C. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 2009, 61:301-316.
150. Shigetomi E., Kracun S., Khakh B.S. Monitoring astrocyte calcium microdomains with improved membrane targeted GCaMP reporters. Neuron Glia Biol. 2010, 6:183-191.
151. Shigetomi E., Bushong E.A., Haustein M.D., Tong X., Jackson-Weaver O., Kracun S., et al. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J. Gen. Physiol. 2013, 141:633-647.
152. Reeves A.M., Shigetomi E., Khakh B.S. Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps. J. Neurosci. 2011, 31:9353-9358.
153. 2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 2011, 14:1276-1284.
154. Haugh J.M. Live-cell fluorescence microscopy with molecular biosensors: what are we really measuring?. Biophys. J. 2012, 102:2003-2011.
155. Thestrup T., Litzlbauer J., Bartholomäus I., Mues M., Russo L., Dana H., et al. Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat. Methods 2014, 11:175-182.
156. Akerboom J., Calderón N.C., Tian L., Wabnig S., Prigge M., Tolö J., et al. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 2013, 6.
157. 2+-permeable channelrhodopsin CatCh. Nat. Neurosci. 2011, 14:513-518.
158. Nadrigny F., Li D., Kemnitz K., Ropert N., Koulakoff A., Rudolph S., et al. Systematic colocalization errors between acridine orange and EGFP in astrocyte vesicular organelles. Biophys. J. 2007, 93:969-980.
159. ijk - a figure of merit and software tool for evaluating spectral cross-talk in multi-channel fluorescence 2014, (in preparation).
160. Oheim M. Instrumentation for live-cell imaging and main formats. Live Cell Imaging 2010, 3-16. Springer. D.B. Papkovsky (Ed.).
161. Yuan L., Lin W., Zheng K., He W., Huang W. Far-red to near infrared analyte-responsive probes based on organic fluorophore platforms for fluorescence imaging. Chem. Soc. Rev. 2013, 42:622-661.
162. Shcherbo D., Shemiakina I.I., Ryabova A.V., Luker K.E., Schmidt B.T., Souslova E.A., et al. Near-infrared fluorescent proteins. Nat. Methods 2010, 7:827-829.
163. Llinas R., Sugimori M., Silver R. Microdomains of high calcium concentration in a presynaptic terminal. Science 1992, 256:677-679.
164. Oheim M., Kirchhoff F., Stühmer W. Calcium microdomains in regulated exocytosis. Cell Calcium 2006, 40:423-439.
165. Machleidt T., Robers M., Hanson G.T. Protein labeling with FlAsH and ReAsH. High Content Screening 2006, 209-220. Springer.
166. O'Hare H.M., Johnsson K., Gautier A. Chemical probes shed light on protein function. Curr. Opin. Struct. Biol. 2007, 17:488-494.
167. Martin V.V., Beierlein M., Morgan J.L., Rothe A., Gee K.R. Novel fluo-4 analogs for fluorescent calcium measurements. Cell Calcium 2004, 36:509-514.
168. Beierlein M., Gee K.R., Martin V.V., Regehr W.G. Presynaptic calcium measurements at physiological temperatures using a new class of dextran-conjugated indicators. J. Neurophysiol. 2004, 92:591-599.
169. Prasuhn D.E., Feltz A., Blanco-Canosa J.B., Susumu K., Stewart M.H., Mei B.C., et al. Quantum dot peptide biosensors for monitoring caspase 3 proteolysis and calcium ions. ACS Nano 2010, 4:5487-5497.
170. 2+ indicator to prolong its cytosolic retention. Chem. Commun. 2013, 49:7313-7315.
171. Kamiya M., Johnsson K. Localizable and highly sensitive calcium indicator based on a BODIPY fluorophore. Anal. Chem. 2010, 82:6472-6479.
172. Dahan M., Levi S., Luccardini C., Rostaing P., Riveau B., Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 2003, 302:442-445.
173. Pinaud F., Clarke S., Sittner A., Dahan M. Probing cellular events, one quantum dot at a time. Nat. Methods 2010, 7:275-285.
174. Bruchez M.P. Quantum dots find their stride in single molecule tracking. Curr. Opin. Chem. Biol. 2011, 15:775-780.
175. Chang J.C., Rosenthal S.J. A bright light to reveal mobility: single quantum dot tracking reveals membrane dynamics and cellular mechanisms. J. Phys. Chem. Lett. 2013, 4:2858-2866.
176. Snee P.T., Somers R.C., Nair G., Zimmer J.P., Bawendi M.G., Nocera D.G. A ratiometric CdSe/ZnS nanocrystal pH sensor. J. Am. Chem. Soc. 2006, 128:13320-13321.
177. Medintz I.L., Uyeda H.T., Goldman E.R., Mattoussi H. Quantum dot bioconjugates for imaging, labelling and sensing. Nat. Mater. 2005, 4:435-446.
178. Somers R.C., Bawendi M.G., Nocera D.G. CdSe nanocrystal based chem-/bio-sensors. Chem. Soc. Rev. 2007, 36:579-591.
179. Frasco M.F., Chaniotakis N. Semiconductor quantum dots in chemical sensors and biosensors. Sensors 2009, 9:7266-7286.
180. 2+ and its bioimaging applications. Anal. Bioanal. Chem. 2010, 397:1245-1250.
181. Niswender K.D., Blackman S.M., Rohde L., Magnuson M.A., Piston D.W. Quantitative imaging of green fluorescent protein in cultured cells: comparison of microscopic techniques, use in fusion proteins and detection limits. Journal of Microscopy 1995, 180(2):109-116.