Reporting neural activity with genetically encoded calcium indicators

Brain Cell Biology

Volumn 36, Issue 1-4, 2008, Pages 69-86

  Hires, S Andrew ^a   Tian, Lin ^a   Looger, Loren L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FLUORESCENT DYE;

ACTION POTENTIAL; ANALYTIC METHOD; CALCIUM TRANSPORT; CELL ACTIVITY; COMPUTER MODEL; GENETICALLY ENCODED CALCIUM INDICATOR; IMAGING SYSTEM; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; ELECTROPHYSIOLOGY; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; NEURONS; SIGNAL TRANSDUCTION;

EID: 57049110387     PISSN: 15597105     EISSN: 15597113     Source Type: Journal    
DOI: 10.1007/s11068-008-9029-4     Document Type: Review

References (81)

1. H. W. Ai S. G. Olenych P. Wong M. W. Davidson R. E. Campbell 2008 Hue-shifted monomeric variants of Clavularia cyan fluorescent protein: identification of the molecular determinants of color and applications in fluorescence imaging BMC Biol. 6 13
2. G. S. Baird D. A. Zacharias R. Y. Tsien 1999 Circular permutation and receptor insertion within green fluorescent proteins Proc. Natl Acad. Sci. USA 96 11241 11246
3. R. D. Burgoyne 2007 Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling Nat. Rev. Neurosci. 8 182 193
4. N. Chronis M. Zimmer C. I. Bargmann 2007 Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans Nat. Method. 4 727 731
5. D. A. Clark C. V. Gabel H. Gabel A. D. Samuel 2007 Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients J. Neurosci. 27 6083 6090
6. W. Denk R. Yuste K. Svoboda D. W. Tank 1996 Imaging calcium dynamics in dendritic spines Curr. Opin. Neurobiol. 6 372 378
7. F. Di Virgilio T. H. Steinberg J. A. Swanson S. C. Silverstein 1988 Fura-2 secretion and sequestration in macrophages. A blocker of organic anion transport reveals that these processes occur via a membrane transport system for organic anions J. Immunol. 140 915 920
8. 2+ indicator protein Eur. J. Neurosci. 22 627 635
9. D. M. Ferkey R. Hyde G. Haspel H. M. Dionne H. A. Hess H. Suzuki 2007 C. elegans G protein regulator RGS-3 controls sensitivity to sensory stimuli Neuron 53 39 52
10. A. Fiala T. Spall S. Diegelmann B. Eisermann S. Sachse J. M. Devaud 2002 Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons Curr. Biol. 12 1877 1884
11. S. Furler J. C. Paterna M. Weibel H. Bueler 2001 Recombinant AAV vectors containing the foot and mouth disease virus 2A sequence confer efficient bicistronic gene expression in cultured cells and rat substantia nigra neurons Gene Ther. 8 864 873
12. O. Garaschuk O. Griesbeck A. Konnerth 2007 Troponin C-based biosensors: a new family of genetically encoded indicators for in vivo calcium imaging in the nervous system Cell Calcium 42 351 361
13. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 3440 3450
14. X. Han E. S. Boyden 2007 Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution PLoS ONE 2 e299
15. 2+ indicator proteins in transgenic mice under TET control PLoS Biol. 2 e163
16. Haugland, R. P., Spence, M. T. Z., Johnson, I. D., and Basey, A. (2005). The Handbook: A Guide to Fluorescent Probes and Labeling Technologies, 10th ed., Molecular Probes, Eugene, OR
17. N. Heim O. Griesbeck 2004 Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein J. Biol. Chem. 279 14280 14286
18. N. Heim O. Garaschuk M. W. Friedrich M. Mank R. I. Milos Y. Kovalchuk 2007 Improved calcium imaging in transgenic mice expressing a troponin C-based biosensor Nat. Method 4 127 129
19. 2+ signaling in dendrites of pyramidal neurons Biophys. J. 70 1069 1081
20. S. Higashijima M. A. Masino G. Mandel J. R. Fetcho 2003 Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator J. Neurophysiol. 90 3986 3997
21. Hille, B. (1992). Ionic Channels of Excitable Membranes, 2nd edn. Sinauer Associates, Sunderland, MA.
22. Hires, S. A., Zhu, Y., and Tsien, R. Y. (2008). Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc. Natl. Acad. Sci. USA 105, 4411-4416
23. 2+ entry into hippocampal neurons Nature 357 244 246
24. Jayaraman, V., and Laurent, G. (2007). Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Front. Neural Circ. 1. doi: 10.3389/neuro.04.003.2007
25. 2+ in biological systems Nat. New. Biol. 237 287 288
26. J. N. Kerr W. Denk 2008 Imaging in vivo: watching the brain in action Nat. Rev. Neurosci. 9 195 205
27. R. Kerr V. Lev-Ram G. Baird P. Vincent R. Y. Tsien W. R. Schafer 2000 Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans Neuron 26 583 594
28. 2+ imaging in C. elegans Method. Mol. Biol. 351 253 264
29. K. S. Kindt K. B. Quast A. C. Giles S. De D. Hendrey I. Nicastro 2007 Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans Neuron 55 662 676
30. 2+ indicators: using genetics and molecular design to understand complex physiology J. Physiol. 578 55 67
31. S. Linse A. Helmersson S. Forsen 1991 Calcium binding to calmodulin and its globular domains J. Biol. Chem. 266 8050 8054
32. R. Llinas M. Sugimori S. M. Simon 1982 Transmission by presynaptic spike-like depolarization in the squid giant synapse Proc. Natl. Acad. Sci. USA 79 2415 2419
33. Mank, M., and Griesbeck, O. (2008). Genetically encoded calcium indicators. Chem. Rev. 108, 1550-1564
34. M. Mank D. F. Reiff N. Heim M. W. Friedrich A. Borst O. Griesbeck 2006 A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change Biophys. J. 90 1790 1796
35. T. Mao D. H. O'Connor V. Scheuss J. Nakai K. Svoboda 2008 Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators PLoS ONE 3 e1796
36. H. Markram B. Sakmann 1994 Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels Proc. Natl. Acad. Sci. USA 91 5207 5211
37. H. Markram P. J. Helm B. Sakmann 1995 Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons J. Physiol. 485 1 20
38. A. Minta J. P. Kao R. Y. Tsien 1989 Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores J. Biol. Chem. 264 8171 8178
39. A. Miyawaki R. Y. Tsien 2000 Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein Method. Enzymol. 327 472 500
40. 2+ based on green fluorescent proteins and calmodulin Nature 388 882 887
41. 2+ measurements using improved cameleons Proc. Natl. Acad. Sci. USA 96 2135 2140
42. 2+ responses Nature 354 73 76
43. 2+ Proc. Natl. Acad. Sci. USA 98 3197 3202
44. 2+ by circularly permuted yellow fluorescent proteins Proc. Natl. Acad. Sci. USA 101 10554 10559
45. J. Nakai M. Ohkura K. Imoto 2001 A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein Nat. Biotechnol. 19 137 141
46. E. Neher 1995 The use of fura-2 for estimating Ca buffers and Ca fluxes Neuropharmacology 34 1423 1442
47. ++ signals Cell Calcium 24 345 357
48. Y. Ogawa M. Tanokura 1984 Calcium binding to calmodulin: effects of ionic strength, Mg2+, pH and temperature J. Biochem. 95 19 28
49. 2+ imaging of dendritic spines Anal. Chem. 77 5861 5869
50. A. E. Palmer R. Y. Tsien 2006 Measuring calcium signaling using genetically targetable fluorescent indicators Nat. Protoc. 1 1057 1065
51. 2+ indicators based on computationally redesigned calmodulin-peptide pairs Chem. Biol. 13 521 530
52. J. Pelletier N. Sonenberg 1988 Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA Nature 334 320 325
53. 2+ indicators J. Neurosci. 24 9572 9579
54. D. F. Reiff A. Ihring G. Guerrero E. Y. Isacoff M. Joesch J. Nakai 2005 In vivo performance of genetically encoded indicators of neural activity in flies J. Neurosci. 25 4766 4778
55. T. J. Rink R. Y. Tsien A. E. Warner 1980 Free calcium in Xenopus embryos measured with ion-selective microelectrodes Nature 283 658 660
56. M. A. Rizzo G. H. Springer B. Granada D. W. Piston 2004 An improved cyan fluorescent protein variant useful for FRET Nat. Biotechnol. 22 445 449
57. J. Schiller F. Helmchen B. Sakmann 1995 Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones J. Physiol. 487 583 600
58. N. C. Shaner P. A. Steinbach R. Y. Tsien 2005 A guide to choosing fluorescent proteins Nat. Method. 2 905 909
59. S. Shimozono A. Miyawaki 2008 Engineering FRET constructs using CFP and YFP Method. Cell Biol. 85 381 393
60. 2+ sensors with increased dynamic range BMC Biotechnol. 7 37
61. H. Suzuki R. Kerr L. Bianchi C. Frokjaer-Jensen D. Slone J. Xue 2003 In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation Neuron 39 1005 1017
62. 2+ indicator GCaMP2 Proc. Natl. Acad. Sci. USA 103 4753 4758
63. 2+ sensor Biophys. J. 93 4031 4040
64. O. Tour S. R. Adams R. A. Kerr R. M. Meijer T. J. Sejnowski R. W. Tsien 2007 Calcium Green FlAsH as a genetically targeted small-molecule calcium indicator Nat. Chem. Biol. 3 423 431
65. K. Truong A. Sawano A. Miyawaki M. Ikura 2007 Calcium indicators based on calmodulin-fluorescent protein fusions Methods Mol. Biol. 352 71 82
66. P. S. Tsai B. Friedman A. I. Ifarraguerri B. D. Thompson V. Lev-Ram C. B. Schaffer 2003 All-optical histology using ultrashort laser pulses Neuron 39 27 41
67. R. Y. Tsien 1980 New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures Biochemistry 19 2396 2404
68. R. Y. Tsien 1998 The green fluorescent protein Annu. Rev. Biochem. 67 509 544
69. Tsien, R. Y. (1999). Monitoring cell calcium. In E. Carafoli a C. B. Klee (Eds.), Calcium as a Cellular Regulator. Oxford University Press, USA, pp. 28-54
70. 2+. In J. Barker and J. F. McKelvey (Eds.), Current Methods of Cellular Neurobiology, 3rd edn. Wiley, New York.
71. J. W. Wang A. M. Wong J. Flores L. B. Vosshall R. Axel 2003 Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain Cell 112 271 282
72. M. Willemse E. Janssen F. de Lange B. Wieringa J. Fransen 2007 ATP and FRET-a cautionary note Nat. Biotechnol. 25 170 172
73. 2+ imaging Nat. Method. 3 377 383
74. Y. Yang A. Costa N. Leonhardt R. S. Siegel J. I. Schroeder 2008 Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool Plant Method. 4 6
75. Yasuda, R., Nimchinsky, E. A., Scheuss, V., Pologruto, T. A., Oertner, T. G., Sabatini, B. L., et al. (2004). Imaging calcium concentration dynamics in small neuronal compartments. Sci. STKE 2004, l5
76. R. Yuste W. Denk 1995 Dendritic spines as basic functional units of neuronal integration Nature 375 682 684
77. R. Yuste A. Majewska S. S. Cash W. Denk 1999 Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis J. Neurosci. 19 1976 1987
78. Y. P. Zhang T. G. Oertner 2007 Optical induction of synaptic plasticity using a light-sensitive channel Nat. Method. 4 139 141
79. F. Zhang L. P. Wang E. S. Boyden K. Deisseroth 2006 Channelrhodopsin-2 and optical control of excitable cells Nat. Method. 3 785 792
80. F. Zhang L. P. Wang M. Brauner J. F. Liewald K. Kay N. Watzke 2007 Multimodal fast optical interrogation of neural circuitry Nature 446 633 639
81. F. Zhang M. Prigge F. Beyriere S. P. Tsunoda J. Mattis O. Yizhar 2008 Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri Nat. Neurosci. 11 631 633