Synthesis and properties of Asante Calcium Red-A novel family of long excitation wavelength calcium indicators

Cell Calcium

Volumn 54, Issue 4, 2013, Pages 320-333

  Hyrc, Krzysztof L ^a   Minta, Akwasi ^b   Escamilla, P Rogelio ^b   Chan, Patrick P L ^a   Meshik, Xenia A ^a   Goldberg, Mark P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEF Labs Inc   (United States)

Author keywords

Confocal microscopy; Dissociation constant; Emission spectra; Excitation spectra; Fluorescence; Intracellular free calcium concentration; Magnesium ions; Multiphoton microscopy; Neurons; Ratio imaging; Zinc ions

Indexed keywords

ASANTE CALCIUM RED 1; ASANTE CALCIUM RED 1 LOW AFFINITY; CALCIUM ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GREEN FLUORESCENT PROTEIN; INDICATOR; MAGNESIUM ION; UNCLASSIFIED DRUG; ZINC ION;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BLEACHING; BRAIN NERVE CELL; CALCIUM BINDING; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; LIGHT; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNTHESIS;

CONFOCAL MICROSCOPY; DISSOCIATION CONSTANT; EMISSION SPECTRA; EXCITATION SPECTRA; FLUORESCENCE; INTRACELLULAR FREE CALCIUM CONCENTRATION; MAGNESIUM IONS; MULTIPHOTON MICROSCOPY; NEURONS; RATIO IMAGING; ZINC IONS;

ANILINE COMPOUNDS; ANIMALS; CALCIUM; CALIBRATION; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; HYDROGEN-ION CONCENTRATION; INDICATORS AND REAGENTS; IONS; LIGHT; MICE; MICROSCOPY, CONFOCAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, FLUORESCENCE;

EID: 84884280124     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2013.08.001     Document Type: Article

References (100)

1. Takahashi A., Camacho P., Lechleiter J.D., Herman B. Measurement of intracellular calcium. Physiol. Rev. 1999, 79:1089-1125.
2. 2+ imaging of organelles, cells, tissues, and organ. Methods Enzymol. 1999, 307:441-469.
3. 2+ concentration. Methods Cell Biol. 2002, 70:453-474.
4. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
5. Minta A., Kao J.P., Tsien R.Y. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 1989, 264:8171-8178.
6. Iatridou H., Foukaraki E., Kuhn M.A., Marcus E.M., Haugland R.P., Katerinopoulos H.E. The development of a new family of intracellular calcium probes. Cell. Calcium 1994, 15:190-198.
7. Gee K.R., Archer E.A., Lapham L.A., et al. New ratiometric fluorescent calcium indicators with moderately attenuated binding affinities. Bioorg. Med. Chem. Lett. 2000, 10:1515-1518.
8. 2+ and other metal ions. Handbook of Fluorescent Probes and Research Products 2002, 767-817. Molecular Probes, Eugene. R.P. Haugland (Ed.).
9. 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.
10. Paredes R.M., Etzler J.C., Watts L.T., Zheng W., Lechleiter J.D. Chemical calcium indicators. Methods 2008, 46:143-151.
11. 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.
12. Sako Y., Sekihata A., Yanagisawa Y., et al. Comparison of two-photon excitation laser scanning microscopy with UV-confocal laser scanning microscopy in three-dimensional calcium imaging using the fluorescence indicator Indo-1. J. Microsc. 1997, 185:9-20.
13. Knight M.M., Roberts S.R., Lee D.A., Bader D.L. Live cell imaging using confocal microscopy induces intracellular calcium transients and cell death. Am. J. Physiol. Cell Physiol. 2003, 284:C1083-C1089.
14. Nishigaki T., Wood C.D., Shiba K., Baba S.A., Darszon A. Stroboscopic illumination using light-emitting diodes reduces phototoxicity in fluorescence cell imaging. BioTechniques 2006, 41:191-197.
15. 2+ clearance and its influence on secretory responses in stimulated chromaffin cells. Cell Calcium 2006, 39:35-46.
16. Asai M., Takeuchi K., Uchida S., et al. Misinterpretation of the effect of amlodipine on cytosolic calcium concentration with fura-2 fluorospectrometry. Naunyn Schmiedebergs Arch. Pharmacol. 2008, 377:423-427.
17. Wokosin D.L., Loughrey C.M., Smith G.L. Characterization of a range of fura dyes with two-photon excitation. Biophys. J. 2004, 86:1726-1738.
18. Kim E., Hyrc K.L., Speck J., et al. Missense mutations in Otopetrin 1 affect subcellular localization and inhibition of purinergic signaling in vestibular supporting cells. Mol. Cell. Neurosci. 2011, 46:655-661.
19. Berkova Z., Morris A.P., Estes M.K. Cytoplasmic calcium measurement in rotavirus enterotoxin-enhanced green fluorescent protein (NSP4-EGFP) expressing cells loaded with Fura-2. Cell Calcium 2003, 34:55-68.
20. 2+ dyes with green fluorescent protein and its variants: problems and solutions. Biochemistry 2001, 356:345-352.
21. Gee K.R., Brown K.A., Chen W.N., Bishop-Stewart J., Gray D., Johnson I. Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes. Cell Calcium 2000, 27:97-106.
22. Trollinger D.R., Cascio W.E., Lemasters J.J. Selective loading of Rhod 2 into mitochondria shows mitochondrial Ca2+ transients during the contractile cycle in adult rabbit cardiac myocytes. Biochem. Biophys. Res. Commun. 1997, 236:738-742.
23. Gerencser A.A., Adam-Vizi V. Selective, high-resolution fluorescence imaging of mitochondrial Ca2+ concentration. Cell Calcium 2001, 30:311-321.
24. Lipp P., Niggli E. Ratiometric confocal Ca(2+)-measurements with visible wavelength indicators in isolated cardiac myocytes. Cell Calcium 1993, 14:359-372.
25. 2+ indicators excited with visible light. Cell Calcium 2006, 39:3-11.
26. 2+ indicator, calcium ruby. Org. Lett. 2007, 9:2629-2632.
27. 2+ imaging. J. Am. Chem. Soc. 2012, 134:14923-14931.
28. Egawa T., Hanaoka K., Koide 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.
29. 2+ imaging. Chem. Commun. (Camb.) 2011, 47:10407-10409.
30. 2+ in EGFP expressing cells with a low-affinity calcium Ruby and its dextran conjugate. Cell Calcium 2009, 45:275-283.
31. A. Minta, P. Escamilla, Cytosolic FluoresentIion Indicators, US Patent WO2012040204, USA, 2012.
32. Meshik X.A., Hyrc K.L., Goldberg M.P. Properties of Asante Calcium Red - a Npvel Ratiometric indicator with long excitation wavelengths. 40th SFN Annual Meeting, San Diego 2010, 611-615.
33. 2+ with Quin2. Methods Enzymol. 1989, 172:230-262.
34. 2+ buffers. Methods Cell Biol. 1994, 40:3-29.
35. Bers D.M., Patton C.W., Nuccitelli R. A practical guide to the preparation of Ca(2+) buffers. Methods Cell Biol. 2010, 99:1-26.
36. Hyrc K.L., Bownik J.M., Goldberg M.P. Ionic selectivity of low-affinity ratiometric calcium indicators: mag-Fura-2, Fura-2FF and BTC. Cell Calcium 2000, 27:75-86.
37. Bancel F., Salmon J.M., Vigo J., Vo-Dinh T., Viallet P. Investigation of noncalcium interactions of fura-2 by classical and synchronous fluorescence spectroscopy. Anal. Biochem. 1992, 204:231-238.
38. Mennerick S., Que J., Benz A., Zorumski C.F. Passive and synaptic properties of hippocampal neurons grown in microcultures and in mass cultures. J. Neurophysiol. 1995, 73:320-332.
39. Colosimo A., Goncz K.K., Holmes A.R., et al. Transfer and expression of foreign genes in mammalian cells. Biotechniques 2000, 29:314-318.
40. 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.
41. M.W. Reed, S.J. Geelhood, P.C. Harris, L.M. Barker, P. Hargrave, O. Nanassy, Fluorescent detector systems for the detection of chemical perturbations in sterile storage devices, US Patent 2007/0251337, USA, 2007.
42. Tsien R.Y. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 1981, 290:527-528.
43. 2+/cAMP fluorescence ratio imaging. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4577-4582.
44. i signaling dynamics and metabolism by perinuclear mitochondria in mouse parotid acinar cells. J. Biol. Chem. 2004, 279:12909-12917.
45. Murphy E., Steenbergen C., Levy L.A., Raju B., London R.E. Cytosolic free magnesium levels in ischemic rat heart. J. Biol. Chem. 1989, 264:5622-5627.
46. Rotevatn S., Murphy E., Levy L.A., Raju B., Lieberman M., London R.E. Cytosolic free magnesium concentration in cultured chick heart cells. Am. J. Physiol. 1989, 257:C141-C146.
47. Freudenrich C.C., Murphy E., Levy L.A., London R.E., Lieberman M. Intracellular pH modulates cytosolic free magnesium in cultured chicken heart cells. Am. J. Physiol. 1992, 262:C1024-C1030.
48. 2+ Concentration. Photochem. Photobiol. 1993, 58:795-802.
49. Morelle B., Salmon J.M., Vigo J., Viallet P. Measurement of intracellular magnesium concentration in 3T3 fibroblasts with the fluorescent indicator Mag-indo-1. Anal. Biochem. 1994, 218:170-176.
50. 2+ in skeletal muscle fibers at rest and during contraction. Jpn. J. Physiol. 1998, 48:421-438.
51. 19F-NMR spectroscopy. Biochem. J. 1997, 322(Pt 3):793-799.
52. Sensi S.L., Canzoniero L.M., Yu S.P., et al. Measurement of intracellular free zinc in living cortical neurons: routes of entry. J. Neurosci. 1997, 17:9554-9564.
53. 2+ homeostasis in neurons from experimental and modeling studies. Am. J. Physiol. Cell Physiol. 2008, 294:C726-C742.
54. Dittmer P.J., Miranda J.G., Gorski J.A., Palmer A.E. Genetically encoded sensors to elucidate spatial distribution of cellular zinc. J. Biol. Chem. 2009, 284:16289-16297.
55. Colvin R.A., Holmes W.R., Fontaine C.P., Maret W. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics 2010, 2:306-317.
56. 2+. Biochem. J. 1990, 269:513-519.
57. Roe M.W., Lemasters J.J., Herman B. Assessment of Fura-2 for measurements of cytosolic free calcium. Cell Calcium 1990, 11:63-73.
58. Haworth R.A., Redon D. Calibration of intracellular Ca transients of isolated adult heart cells labelled with fura-2 by acetoxymethyl ester loading. Cell Calcium 1998, 24:263-273.
59. Merritt J.E., Jacob R., Hallam T.J. Use of manganese to discriminate between calcium influx and mobilization from internal stores in stimulated human neutrophils. J. Biol. Chem. 1989, 264:1522-1527.
60. Hopf F.W., Turner P.R., Denetclaw W.F., Reddy P., Steinhardt R.A. A critical evaluation of resting intracellular free calcium regulation in dystrophic mdx muscle. Am. J. Physiol. 1996, 271:C1325-C1339.
61. Hyrc K.L., Bownik J.M., Goldberg M.P. Neuronal free calcium measurement using BTC/AM, a low affinity calcium indicator. Cell Calcium 1998, 24:165-175.
62. Du C., MacGowan G.A., Farkas D.L., Koretsky A.P. Calibration of the calcium dissociation constant of Rhod(2)in the perfused mouse heart using manganese quenching. Cell Calcium 2001, 29:217-227.
63. Bancel F., Vigo J., Salmon J.M., Viallet P., Acid-Base Calcium-binding properties of the fluorescent calcium indicator Indo-1. J. Photochem. Photobiol. A 1990, 53:397-409.
64. 2+ imaging in single living cells: theoretical and practical issues. Cell Calcium 1990, 11:157-179.
65. i in individual cells undergoing apoptosis. Cell Calcium 1999, 25:19-28.
66. Dineley K.E., Malaiyandi L.M., Reynolds I.J. A reevaluation of neuronal zinc measurements: artifacts associated with high intracellular dye concentration. Mol. Pharmacol. 2002, 62:618-627.
67. Becker P.L., Fay F.S. Photobleaching of fura-2 and its effect on determination of calcium concentrations. Am. J. Physiol. 1987, 253:C613-C618.
68. 2+ concentrations. Chem. Biol. 1996, 3:765-774.
69. Bassnett S., Reinisch L., Beebe D.C. Intracellular pH measurement using single excitation-dual emission fluorescence ratios. Am. J. Physiol. 1990, 258:C171-C178.
70. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 1993, 13:1993-2000.
71. Hyrc K., Handran S.D., Rothman S.M., Goldberg M.P. Ionized intracellular calcium concentration predicts excitotoxic neuronal death: observations with low-affinity fluorescent calcium indicators. J. Neurosci. 1997, 17:6669-6677.
72. Stanika R.I., Villanueva I., Kazanina G., Andrews S.B., Pivovarova N.B. Comparative impact of voltage-gated calcium channels and NMDA receptors on mitochondria-mediated neuronal injury. J. Neurosci. 2012, 32:6642-6650.
73. Stout A.K., Reynolds I.J. High-affinity calcium indicators underestimate increases in intracellular calcium concentrations associated with excitotoxic glutamate stimulations. Neuroscience 1999, 89:91-100.
74. Hyrc K.L., Rzeszotnik Z., Kennedy B.R., Goldberg M.P. Determining calcium concentration in heterogeneous model systems using multiple indicators. Cell Calcium 2007, 42:576-589.
75. 2+ indicators in frog skeletal muscle fibers. Biophys. J. 1996, 70:896-916.
76. Spergel D.J., Kruth U., Shimshek D.R., Sprengel R., Seeburg P.H. Using reporter genes to label selected neuronal populations in transgenic mice for gene promoter, anatomical, and physiological studies. Prog. Neurobiol. 2001, 63:673-686.
77. Shaner N.C., Patterson G.H., Davidson M.W. Advances in fluorescent protein technology. J. Cell Sci. 2007, 120:4247-4260.
78. van den Pol A.N., Ozduman K., Wollmann G., et al. Viral strategies for studying the brain, including a replication-restricted self-amplifying delta-G vesicular stomatis virus that rapidly expresses transgenes in brain and can generate a multicolor golgi-like expression. J. Comp. Neurol. 2009, 516:456-481.
79. Kurebayashi N., Harkins A.B., Baylor S.M. Use of fura red as an intracellular calcium indicator in frog skeletal muscle fibers. Biophys. J. 1993, 64:1934-1960.
80. Rubart M. Two-photon microscopy of cells and tissue. Circ. Res. 2004, 95:1154-1166.
81. Weissleder R. A clearer vision for in vivo imaging. Nat. Biotechnol. 2001, 19:316-317.
82. Denk W., Delaney K.R., Gelperin A., et al. Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy. J. Neurosci. Methods 1994, 54:151-162.
83. Helmchen F., Denk W. Deep tissue two-photon microscopy. Nat. Methods 2005, 2:932-940.
84. Bush P.G., Wokosin D.L., Hall A.C. Two-versus one photon excitation laser scanning microscopy: critical importance of excitation wavelength. Front. Biosci. 2007, 12:2646-2657.
85. 2+-indicator dyes suitable for two-photon fluorescence-lifetime recordings. J. Microsc. 2007, 225:209-213.
86. 2+ ion concentration with the fluorescent probe mag-fura-2 (furaptra). J. Biochem. Biophys. Methods 1993, 27:25-37.
87. Thompson R.B., Peterson D., Mahoney W., et al. Fluorescent zinc indicators for neurobiology. J. Neurosci. Methods 2002, 118:63-75.
88. 2+ pools. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:6157-6162.
89. 2+ -dependent reactive oxygen species accumulation. J. Neurochem. 2008, 106:2184-2193.
90. Kiedrowski L. Cytosolic zinc release and clearance in hippocampal neurons exposed to glutamate-the role of pH and sodium. J. Neurochem. 2011, 117:231-243.
91. Martin J.L., Stork C.J., Li Y.V. Determining zinc with commonly used calcium and zinc fluorescent indicators, a question on calcium signals. Cell Calcium 2006, 40:393-402.
92. Stork C.J., Li Y.V. Intracellular zinc elevation measured with a calcium-specific indicator during ischemia and reperfusion in rat hippocampus: a question on calcium overload. J. Neurosci. 2006, 26:10430-10437.
93. Abdel-Hamid K.M., Baimbridge K.G. The effects of artificial calcium buffers on calcium responses and glutamate-mediated excitotoxicity in cultured hippocampal neurons. Neuroscience 1997, 81:673-687.
94. 2+ concentrations. Chem. Biol. 1996, 3:765-774.
95. Carpenter-Deyo L., Duimstra J.R., Hedstrom O., Reed D.J. Toxicity to isolated hepatocytes caused by the intracellular calcium indicator, Quin 2. J. Pharmacol. Exp. Ther. 1991, 258:739-746.
96. Hartley Z., Dubinsky J.M. Changes in intracellular pH associated with glutamate excitotoxicity. J. Neurosci. 1993, 13:4690-4699.
97. Koch R.A., Barish M.E. Perturbation of intracellular calcium and hydrogen ion regulation in cultured mouse hippocampal neurons by reduction of the sodium ion concentration gradient. J. Neurosci. 1994, 14:2585-2593.
98. 2+ loads. J. Neurophysiol. 1994, 72:2563-2569.
99. + channel in cultured rat hippocampal neurones. J. Physiol. 1998, 511:119-132.
100. 2+ concentration changes in cultured postnatal rat hippocampal neurons. Neuroscience 1999, 93:1003-1016.