CaRuby-Nano: A novel high affinity calcium probe for dual color imaging

eLife

Volumn 2015, Issue 4, 2015, Pages

  Collot, Mayeul ^a   Wilms, Christian D ^b   Bentkhayet, Asma ^a   Marcaggi, Païkan ^c   Couchman, Kiri ^d,e   Charpak, Serge ^d,e   Dieudonné, Stéphane ^c   Häusser, Michael ^b   Feltz, Anne ^c   Mallet, Jean Maurice ^a  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLUTAMIC ACID; RED FLUORESCENT PROTEIN; ALEXA FLUOR 488 C5-MALEIMIDE; BACTERIAL PROTEIN; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; FLUORESCENT DYE; MALEIMIDE DERIVATIVE; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CEREBELLUM; CRANIOTOMY; ELECTROPHYSIOLOGY; ION CURRENT; MOUSE; NEOCORTEX; NONHUMAN; OLFACTORY NERVE; PURKINJE CELL; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COLOR; GENETICS; LUMINESCENCE; MEMBRANE POTENTIAL; METABOLISM; MULTIPHOTON MICROSCOPY; NERVE CELL; PHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SYNTHESIS; TRANSGENIC MOUSE;

ANIMALS; BACTERIAL PROTEINS; CALCIUM; CALCIUM SIGNALING; COLOR; FLUORESCENT DYES; INDICATORS AND REAGENTS; LUMINESCENT MEASUREMENTS; LUMINESCENT PROTEINS; MALEIMIDES; MEMBRANE POTENTIALS; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MODELS, CHEMICAL; MOLECULAR STRUCTURE; NEURONS; REPRODUCIBILITY OF RESULTS;

EID: 84926500475     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05808     Document Type: Article

References (35)

1. Collot M, Loukou C, Yakovlev AV, Wilms CD, Li D, Evrard A, Zamaleeva A, Bourdieu L, Léger JF, Ropert N, Eilers J, Oheim M, Feltz A, Mallet JM. 2012. Calcium rubies: a family of red-emitting functionalizable indicators suitable for two-photon Ca2+ imaging. Journal of the American Chemical Society 134:14923-14931. doi: 10.1021/ ja304018d.
2. Davie JT, Kole MH, Letzkus JJ, Rancz EA, Spruston N, Stuart GJ, Häusser M. 2006. Dendritic patch-clamp recording. Nature Protocols 1:1235-1247. doi: 10.1038/nprot.2006.164.
3. Dugue GP, Brunel N, Hakim V, Schwartz E, Chat M, Lévesque M, Courtemanche R, Léna C, Dieudonné S. 2009. Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61:126-139. doi: 10.1016/j.neuron.2008.11.028.
4. Eberhard M, Erne P. 1991. Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochemical and Biophysical Research Communications 180:209-215. doi: 10.1016/S0006-291X (05)81278-1.
5. Egawa T, Hanaoka K, Koide Y, Ujita S, Takahashi N, Ikegaya Y, Matsuki N, Terai T, Ueno T, Komatsu T, Nagano T. 2011. Development of a far-red to near-infrared fluorescence probe for calcium ion and its application to multicolor neuronal imaging. Journal of the American Chemical Society 133:14157-14159. doi: 10.1021/ ja205809h.
6. Higley MJ, Sabatini BL. 2008. Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 59:902-913. doi: 10.1016/j.neuron.2008.08.020.
7. Kolb HC, Finn MG, Sharpless KB. 2001. Click chemistry: diverse chemical function from a few good reactions. Angewandte Chemie 40:2004-2021. doi: 10.1002/1521-3773(20010601)40:11<2004::AID-ANIE2004>3.0. CO;2-5.
8. Lecoq J, Tiret P, Charpak S. 2009. Peripheral adaptation codes for high odor concentration in glomeruli. The Journal of Neuroscience 29:3067-3072. doi: 10.1523/JNEUROSCI.6187-08.2009.
9. Lev-Ram V, Miyakawa H, Lasser-Ross N, Ross WN. 1992. Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. Journal of Neurophysiology 68:1167-1177.
10. Looger LL, Griesbeck O. 2012. Genetically encoded neural activity indicators. Current Opinion in Neurobiology 22: 18-23. doi: 10.1016/j.conb.2011.10.024.
11. Maravall M, Mainen ZF, Sabatini BL, Svoboda K. 2000. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophysical Journal 78:2655-2667. doi: 10.1016/S0006-3495(00)76809-3.
12. Markram H, Roth A, Helmchen F. 1998. Competitive calcium binding: implications for dendritic calcium signaling. Journal of Computational Neuroscience 5:331-348. doi: 10.1023/A:1008891229546.
13. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, Gordus A, Renninger SL, Chen TW, Bargmann CI, Orger MB, Schreiter ER, Demb JB, Gan WB, Hires SA, Looger LL. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nature Methods 10:162-170. doi: 10.1038/nmeth.2333.
14. Metzger F, Repunte-Canonigo V, Matsushita S, Akemann W, Diez-Garcia J, Ho CS, Iwasato T, Grandes P, Itohara S, Joho RH, Knöpfel T. 2002. Transgenic mice expressing a pH and Cl- sensing yellow-fluorescent protein under the control of a potassium channel promoter. The European Journal of Neuroscience 15:40-50. doi: 10.1046/j. 0953-816x.2001.01837.x.
15. Miyawaki A. 2011. Development of probes for cellular functions using fluorescent proteins and fluorescence resonance energy transfer. Annual Review of Biochemistry 80:357-373. doi: 10.1146/annurev-biochem-072909-094736.
16. Neher E. 2005. Some quantitative aspects of calcium fluorimetry. Imaging in neuroscience and development: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
17. Nielsen TT, Wintgens V, Amiel C, Wimmer R, Larsen KL. 2010. Facile synthesis of beta-Cyclodextrin-dextran Polymers by 'Click' chemistry. Biomacromolecules 11:1710-1715. doi: 10.1021/bm9013233.
18. Oheim M, van 't Hoff M, Feltz A, Zamaleeva A, Mallet JM, Collot M. 2014. New red-fluorescent calcium indicators for optogenetics, photoactivation and multi-color imaging. Biochimica Et Biophysica Acta 1843:2284-2306. doi: 10.1016/j.bbamcr.2014.03.010.
19. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433:597-603. doi: 10.1038/Nature03274.
20. Otsu Y, Bormuth V, Wong J, Mathieu B, Dugué GP, Feltz A, Dieudonné S. 2008. Optical monitoring of neuronal activity at high frame rate with a digital random-access multiphoton (RAMP) microscope. Journal of Neuroscience Methods 173:259-270. doi: 10.1016/j.jneumeth.2008.06.015.
21. Otsu Y, Marcaggi P, Feltz A, Isope P, Kollo M, Nusser Z, Mathieu B, Kano M, Tsujita M, Sakimura K, Dieudonné S. 2014. Activity-Dependent Gating of calcium spikes by A-type K+ channels controls climbing fiber signaling in purkinje cell dendrites. Neuron 84:137-151. doi: 10.1016/j.neuron.2014.08.035.
22. Ozden I, Sullivan MR, Lee HM, Wang SS. 2009. Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. The Journal of Neuroscience 29:10463-10473. doi: 10.1523/ JNEUROSCI.0967-09.2009.
23. Pawley JB. 2006. Handbook of biological confocal microscopy. New York, NY: Springer.
24. Pologruto TA, Sabatini BL, Svoboda K. 2003. ScanImage: flexible software for operating laser scanning microscopes. Biomedical Engineering Online 2:13. doi: 10.1186/1475-925X-2-13.
25. Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Häusser M. 2009. Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. The Journal of Neuroscience 29:8005-8015. doi: 10.1523/JNEUROSCI.4919-08.2009.
26. Stosiek C, Garaschuk O, Holthoff K, Konnerth A. 2003. In vivo two-photon calcium imaging of neuronal networks. Proceedings of the National Academy of Sciences of USA 100:7319-7324. doi: 10.1073/pnas.1232232100.
27. Sullivan MR, Nimmerjahn A, Sarkisov DV, Helmchen F, Wang SS. 2005. In vivo calcium imaging of circuit activity in cerebellar cortex. Journal of Neurophysiology 94:1636-1644. doi: 10.1152/jn.01013.2004.
28. Svoboda K, Denk W, Kleinfeld D, Tank DW. 1997. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165. doi: 10.1038/385161a0.
29. Tan YP, Llano I, Hopt A, Würriehausen F, Neher E. 1999. Fast scanning and efficient photodetection in a simple two-photon microscope. Journal of Neuroscience Methods 92:123-135. doi: 10.1016/S0165-0270(99)00103-X.
30. Tsien RY. 1981. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290: 527-528. doi: 10.1038/290527a0.
31. Tsien RY. 1980. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19:2396-2404. doi: 10.1021/bi00552a018.
32. WachowiakM, Cohen LB. 2001. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32:723-735. doi: 10.1016/S0896-6273(01)00506-2.
33. Wilt BA, Burns LD, Wei Ho ET, Ghosh KK, Mukamel EA, Schnitzer MJ. 2009. Advances in light microscopy for neuroscience. Annual Review of Neuroscience 32:435-506. doi: 10.1146/annurev.neuro.051508.135540.
34. Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K. 2004. Imaging calcium concentration dynamics in small neuronal compartments. Science's STKE 2004:pl5.
35. Zamaleeva AI, Collot M, Bahembera E, Tisseyre C, Rostaing P, Yakovlev AV, Oheim M, de Waard M, Mallet JM, Feltz A. 2014. Cell-penetrating nanobiosensors for pointillistic intracellular Ca2+-transient detection. Nano Letters 14:2994-3001. doi: 10.1021/Nl500733g.