In vivo performance of genetically encoded indicators of neural activity in flies

Journal of Neuroscience

Volumn 25, Issue 19, 2005, Pages 4766-4778

  Reiff, Dierk F ^a   Ihring, Alexandra ^a   Guerrero, Giovanna ^b   Isacoff, Ehud Y ^b   Joesch, Maximilian ^a   Nakai, Junichi ^c   Borst, Alexander ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b University of California Berkeley   (United States)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Calcium; Genetic indicators; GFP; Neural activity; Optical imaging; Transgenic animals

Indexed keywords

CAMGAROO 1; CAMGAROO 2; COMPLEMENTARY DNA; FLASH PERICAM; GCAMP 1.3; GCAMP 1.6; GENETICALLY ENCODED CALCIUM INDICATOR; INVERSE PERICAM; PEPTIDES AND PROTEINS; RECOMBINANT DNA; TROPONEON L15; UNCLASSIFIED DRUG; YELLOW CAMELEON 2.0; YELLOW CAMELEON 2.3; YELLOW CAMLEON 3.3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEACHING; CELL ACTIVITY; CHROMATOPHORE; CONTROLLED STUDY; DNA PROBE; FLUORESCENCE ANALYSIS; GENETIC CODE; IN VIVO STUDY; NERVE CELL; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL NOISE RATIO;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DOSE-RESPONSE RELATIONSHIP, RADIATION; DROSOPHILA; ELECTRIC STIMULATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; IMMUNOHISTOCHEMISTRY; LARVA; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR PROBE TECHNIQUES; NEUROMUSCULAR JUNCTION; NEURONS; PRESYNAPTIC TERMINALS; REPRODUCIBILITY OF RESULTS; TIME FACTORS;

EID: 18644370150     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4900-04.2005     Document Type: Article

References (79)

1. Abeles M (1991) Corticonics. Cambridge, MA: Cambridge UP.
2. Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci USA 96:11241-11246.
3. Barclay JW, Atwood HL, Robertson RM (2002) Impairment of central pattern generation in Drosophila cystein string protein mutants. J Comp Physiol [A] 188:71-78.
4. Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208-214.
5. i in intact rabbit cardiac myocytes. Biophys J 68:1453-1460.
6. 2+] signals from calcium-indicator dyes. News Physiol Sci 15:19-26.
7. Benaim G, Villalobo A (2002) Phosphorylation of calmodulin. Functional implications. Eur J Biochem 269:3619-3725.
8. Borst A, Theunissen FE (1999) Information theory and neural coding. Nat Neurosci 11:947-957.
9. Bozza T, McGann JP, Mombaerts P, Wachowiak M (2004) In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42:9-21.
10. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
11. Cattaert D, Birman S (2001) Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. J Neurobiol 48:58-73.
12. Cohen LB, Salzberg BM, Grinvald A (1978) Optical methods for monitoring neuron activity. Annu Rev Neurosci 1:171-182.
13. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73-76.
14. de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, Bialek W (1997) Reproducibility and variability in neural spike trains. Science 5307:1805-1808.
15. Fernandez-Alfonso T, Ryan TA (2004) The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41:943-953.
16. Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud J-M, Buchner E, Galizia CG (2002) Genetically expressed Cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 12:1877-1884.
17. Filippin L, Magalhaes PJ, Di Benedetto G, Pozzan T (2003) Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 278:39224-39234.
18. Gossen M, Bujard H (2002) Studying gene function in eukaryotes by conditional gene inactivation. Annu Rev Genet 36:153-173.
19. Griesbeck O (2004) Fluorescent proteins as sensors for cellular function. Curr Opin Neurobiol 14:636-641.
20. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 276:29188-29194.
21. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
22. Guerrero G, Isacoff EY (2001) Genetically encoded optical sensors of neuronal activity and cellular function. Curr Opin Neurobiol 11:601-607.
23. Habuchi S, Cotlet M, Hofkens J, Dirix G, Michiels J, Vanderleyden J, Subramaniam V, De Schryver FC (2002) Resonance energy transfer in a calcium concentration-dependent cameleon protein. J Biophys 8:3499-3506.
24. 2+ indicator proteins in transgenic mice under TET control. PLoS Biol 2:763-775.
25. Heim N, Griesbeck O (2004) Genetically encoded indicators of cellular calcium dynamics based on Troponin C and green fluorescent protein. J Biol Chem 279:14280-14286.
26. Higashijima S, Masino MA, Mandel G, Fetcho JR (2003) Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 6:3986-3997.
27. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D, Yuste R (2004) Synfire chains and cortical songs: temporal modules of cortical activity. Science 5670:559-564.
28. Jares-Erijman E, Jovin TM (2003) FRET imaging. Nat Biotechnol 21:1387-1395.
29. Jurado LA, Chockalingam PS, Jarrett HW (1999) Apocalmodulin. Physiol Rev 79:661-682.
30. Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR (2000) Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26:583-594.
31. Kimura KD, Miyawaki A, Matsumoto K, Mori I (2004) The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14:1291-1295.
32. Kurebayashi N, Harkins AB, Baylor SM (1993) Use of Fura red as an intracellular calcium indicator in frog skeletal muscle fibers. Biophys J 64:1934-1960.
33. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
34. Lin DM, Goodman CS (1994) Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13:507-523.
35. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ (2003) Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 6:267-273.
36. Macleod GT, Hegstrom-Wojtowicz M, Charlton MP, Atwood HL (2002) Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88:2659-2663.
37. Macleod GT, Marin L, Charlton MP, Atwood HL (2004) Synaptic vesicles: test fora role in presynaptic calcium regulation. J Neurosci 24:2496-2505.
38. Miesenboeck G (2004) Genetic methods for illuminating the function of neural circuits. Curr Opin Neurobiol 14:395-402.
39. Miesenboeck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
40. Miyawaki A (2003a) Fluorescence imaging of physiological activity in complex systems using GFP-based probes. Curr Opin Neurobiol 13:591-596.
41. Miyawaki A (2003b) Visualization of the spatial and temporal dynamics of intracellular signaling. Dev Cell 4:295-305.
42. 2+ based on green fluorescent proteins and calmodulin. Nature 388:882-887.
43. 2+ measurements using improved cameleons. Proc Natl Acad Sci USA 96:2135-2140.
44. Mizuno H, Sawano A, Eli P, Hama H, Miyawaki A (2001) Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry 40:2502-2510.
45. 2+. Proc Natl Acad Sci USA 98:3197-3202.
46. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90.
47. 2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci USA 29:10554-10559.
48. 2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141.
49. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenbock G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463-474.
50. Nicholson-Tomishima K, Ryan TA (2004) Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc Natl Acad Sci USA 101:16648-16652.
51. 2+. Cell Calcium 22:209-216.
52. 2+ indicators. J Neurosci 24:9572-9579.
53. Reiff DF, Thiel PR, Schuster CM (2002) Differential regulation of active zone density during long-term strengthening of Drosophila neuromuscular junctions. J Neurosci 22:9399-9409.
54. Rieke F, Warland D, de Ruyter van Steveninck RR, Bialek W (1997) Spikes - exploring the neural code. Cambridge, MA: MIT.
55. 2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators. J Biol Chem 272:13270-13274.
56. Rudolf R, Mongillo M, Rizzuto R, Pozzan T (2003) Looking forward to seeing calcium. Nat Rev Mol Cell Biol 4:579-586.
57. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4:569-579.
58. Shyn SI, Kerr R, Schafer WR (2003) Serotonin and Go modulate functional states of neurons and muscles controlling C. elegans egg-laying behavior. Curr Biol 21:1910-1915.
59. Spradling AC, Rubin GM (1982) Transposition of cloned P-elements into Drosophila germ line chromosomes. Science 218:341-347.
60. Spradling AC, Rubin GM (1983) The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 1:47-57.
61. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol [A] 175:179-191.
62. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA 12:7319-7324.
63. Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854-859.
64. Suzuki H, Kerr R, Bianchi L, Frokjaer-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M, Schafer WR (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.
65. Svoboda K, Denk W, Kleinfeld D, Tank DW (1997) In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165.
66. Tank DW, Sugimori M, Connor JA, Llinás RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242:773-777.
67. Tank DW, Regehr WG, Delany KR (1995) A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. J Neurosci 15:7940-7952.
68. 2+ imaging by a new calmodulin-GFP fusion molecule. Nat Struct Biol 8:1069-1073.
69. Tsien RY, Miyawaki A (1998) Seeing the machinery of live cells. Science 280:1954-1955.
70. 2+ loads. J Neurophysiol 72:2563-2569.
71. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
72. 2+ imaging. J Neurosci 24:6507-6514.
73. Wilson RI, Turner GC, Laurant G (2004) Transformation of olfactory representation in the Drosophila antennal lobe. Science 5656:366-370.
74. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
75. Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K (2004) Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE 2004:p15.
76. Yu D, Baird GS, Tsien RY, Davis RL (2003) Detection of calcium transients in Drosophila mushroom body neurons with Camgaroo reporters. J Neurosci 23:64-72.
77. Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42:437-449.
78. Zemelman BV, Miesenboeck G (2001) Genetic schemes and schemata in neurophysiology. Curr Opin Neurobiol 11:409-414.
79. Zhang J, Campbell RE, Ting AY, Tsien RY (2002) Creating new fluorescent probes for cell biology. Nat Rev Mol Cell Biol 3:907-918.