Genetically encoded neural activity indicators

Current Opinion in Neurobiology

Volumn 22, Issue 1, 2012, Pages 18-23

  Looger, Loren L ^a   Griesbeck, Oliver ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CALCIUM ION; GREEN FLUORESCENT PROTEIN; NEUROTRANSMITTER;

CALCIUM SIGNALING; CALCIUM TRANSPORT; EVOKED RESPONSE; FLUORESCENCE ANALYSIS; GENETIC ENGINEERING; IMAGE ANALYSIS; IMAGING SYSTEM; INTRACELLULAR RECORDING; MOLECULAR IMAGING; MOLECULAR PROBE; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE FUNCTION; NERVE POTENTIAL; NEUROIMAGING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROCESS OPTIMIZATION; REVIEW; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; VOLTAGE SENSITIVE DYE IMAGING;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NEURONS; VOLTAGE-SENSITIVE DYE IMAGING;

EID: 84857690012     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2011.10.024     Document Type: Review

References (57)

1. Shimomura O., Johnson F.H., Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from luminous hydromedusan, aequorea. Journal of Cellular and Comparative Physiology 1962, 59:223-239.
2. Ashley C.C., Ridgway E.B. Simultaneous recording of membrane potential calcium transient and tension in single muscle fibres. Nature 1968, 219:1168-1169.
3. Miyawaki A., Llopis J., Heim R., McCaffery J.M., Adams J.A., Ikura M., Tsien R.Y. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
4. Persechini A., Lynch J.A., Romoser V.A. Novel fluorescent indicator proteins for monitoring free intracellular Ca2+. Cell Calcium 1997, 22:209-216.
5. Helmchen F., Denk W. Deep tissue two-photon microscopy. Nature Methods 2005, 2:932-940.
6. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
7. Homma R., Baker B.J., Jin L., Garaschuk O., Konnerth A., Cohen L.B., Zecevic D. Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Philosophical Transactions of the Royal Society B-Biological Sciences 2009, 364:2453-2467.
8. Siegel M.S., Isacoff E.Y. A genetically encoded optical probe of membrane voltage. Neuron 1997, 19:735-741.
9. Ataka K., Pieribone V.A. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophysical Journal 2002, 82:509-516.
10. Sakai R., Repunte-Canonigo V., Raj C.D., Knopfel T. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. European Journal of Neuroscience 2001, 13:2314-2318.
11. Baker B.J., Lee H., Pieribone V.A., Cohen L.B., Isacoff E.Y., Knopfel T., Kosmidis E.K. Three fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells. Journal of Neuroscience Methods 2007, 161:32-38.
12. Murata Y., Iwasaki H., Sasaki M., Inaba K., Okamura Y. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 2005, 435:1239-1243.
13. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nature Methods 2008, 5:683-685.
14. Lundby A., Mutoh H., Dimitrov D., Akemann W., Knopfel T. Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS ONE 2008, 3.
15. Akemann W., Mutoh H., Perron A., Rossier J., Knopfel T. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nature Methods 2010, 7:643-664.
16. Chanda B., Blunck R., Faria L.C., Schweizer F.E., Mody I., Bezanilla F. A hybrid approach to measuring electrical activity in genetically specified neurons. Nature Neuroscience 2005, 8:1619-1626.
17. Kralj J.M., Hochbaum D.R., Douglass A.D., Cohen A.E. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 2011, 333:345-348.
18. Kralj JM, et al. Optical recording of action potentials in mammalian neurons with a voltage indicating protein. Nature Methods (in press).
19. Jaffe D.B., Johnston D., Lasserross N., Lisman J.E., Miyakawa H., Ross W.N. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal-neurons. Nature 1992, 357:244-246.
20. Muller W., Connor J.A. Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 1991, 354:73-76.
21. Hille B. Ionic Channels of Excitable Membranes 1992, Sinauer Associates, Sunderland, MA, USA. edn 2.
22. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnology 2001, 19:137-141.
23. Ohkura M., Matsuzaki M., Kasai H., Imoto K., Nakai J. Genetically encoded bright Ca-2+ probe applicable for dynamic Ca-2+ imaging of dendritic spines. Analytical Chemistry 2005, 77:5861-5869.
24. Tallini Y.N., Ohkura M., Choi B.R., Ji G.J., Imoto K., Doran R., Lee J., Plan P., Wilson J., Xin H.B., et al. Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4753-4758.
25. Wang Q., Shui B., Kotlikoff M.I., Sondermann H. Structural basis for calcium sensing by GCaMP2. Structure 2008, 16:1817-1827.
26. Akerboom J., Rivera J.D.V., Guilbe M.M.R., Malave E.C.A., Hernandez H.H., Tian L., Hires S.A., Marvin J.S., Looger L.L., Schreiter E.R. Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. Journal of Biological Chemistry 2009, 284:6455-6464.
27. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 2009, 6. 875-U113.
28. Pedelacq J.D., Cabantous S., Tran T., Terwilliger T.C., Waldo G.S. Engineering and characterization of a superfolder green fluorescent protein (vol 24, pg 79, 2005). Nature Biotechnology 2006, 24:1170.
29. Muto A., Ohkura M., Kotani T., Higashijima S., Nakai J., Kawakami K. Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:5425-5430.
30. Souslova E.A., Belousov V.V., Lock J.G., Stromblad S., Kasparov S., Bolshakov A.P., Pinelis V.G., Labas Y.A., Lukyanov S., Mayr L.M., Chudakov D.M. Single fluorescent protein-based Ca2+ sensors with increased dynamic range. BMC Biotechnology 2007, 7.
31. 2+ Indicators. Science 2011, 333:1888-1891.
32. Nagai T., Yamada S., Tominaga T., Ichikawa M., Miyawaki A. Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:10554-10559.
33. Palmer A.E., Giacomello M., Kortemme T., Hires S.A., Lev-Ram V., Baker D., Tsien R.Y. Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chemistry & Biology 2006, 13:521-530.
34. Horikawa K., Yamada Y., Matsuda T., Kobayashi K., Hashimoto M., Matsu-ura T., Miyawaki A., Michikawa T., Mikoshiba K., Nagai T. Spontaneous network activity visualized by ultrasensitive Ca(2+) indicators, yellow Cameleon-Nano. Nature Methods 2010, 7:729-788.
35. Heim N., Griesbeck O. Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. Journal of Biological Chemistry 2004, 279:14280-14286.
36. Mank M., Santos A.F., Direnberger S., Mrsic-Flogel T.D., Hofer S.B., Stein V., Hendel T., Reiff D.F., Levelt C., Borst A., et al. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nature Methods 2008, 5:805-811.
37. Liu S., He J., Jin H.L., Yang F., Lu J.L., Yang J. Enhanced dynamic range in a genetically encoded Ca(2+) sensor. Biochemical and Biophysical Research Communications 2011, 412:155-159.
38. Kotera I., Iwasaki T., Imamura H., Noji H., Nagai T. Reversible dimerization of aequorea victoria fluorescent proteins increases the dynamic range of FRET-based indicators. ACS Chemical Biology 2010, 5:215-222.
39. Piljic A., de Diego I., Wilmanns M., Schultz C. Rapid development of genetically encoded FRET reporters. ACS Chemical Biology 2011, 6:685-691.
40. Reiff D.F., Plett J., Mank M., Griesbeck O., Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nature Neuroscience 2010, 13:973-992.
41. Clark D.A., Bursztyn L., Horowitz M.A., Schnitzer M.J., Clandinin T.R. Defining the computational structure of the motion detector in Drosophila. Neuron 2011, 70:1165-1177.
42. Mittmann W., Wallace D.J., Czubayko U., Herb J.T., Schaefer A.T., Looger L.L., Denk W., Kerr J.N.D. Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nature Neuroscience 2011, 14:1089-1195.
43. Borghuis B.G., Tian L., Xu Y., Nikonov S.S., Vardi N., Zemelman B.V., Looger L.L. Imaging light responses of targeted neuron populations in the rodent retina. Journal of Neuroscience 2011, 31:2855-2867.
44. Dreosti E., Odermatt B., Dorostkar M.M., Lagnado L. A genetically encoded reporter of synaptic activity in vivo. Nature Methods 2009, 6. 883-U122.
45. Shigetomi E., Kracun S., Sofroniew M.V., Khakh B.S. A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nature Neuroscience 2010, 13. 759-U143.
46. Andermann M.L., Kerlin A.M., Reid R.C. Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing. Frontiers in Cellular Neuroscience 2010, 4.
47. Lutcke H., Murayama M., Hahn T., Margolis D.J., Astori S., Borgloh S.M.Z., Gobel W., Yang Y., Tang W.N., Kugler S., et al. Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Frontiers in Neural Circuits 2010, 4.
48. Dombeck D.A., Harvey C.D., Tian L., Looger L.L., Tank D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nature Neuroscience 2010, 13:1433-2180.
49. Miesenbock G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
50. Li H., Foss S.M., Dobryy Y.L., Park C.K., Hires S.A., Shaner N.C., Tsien R.Y., Osborne L.C., Voglmaier S.M. Concurrent imaging of synaptic vesicle recycling and calcium dynamics. Frontiers Mol Neurosci 2011, 4:34.
51. Okumoto S., Looger L.L., Micheva K.D., Reimer R.J., Smith S.J., Frommer W.B. Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:8740-8745.
52. Tsien R.Y. Building and breeding molecules to spy on cells and tumors. FEBS Letters 2005, 579:927-932.
53. Hires S.A., Zhu Y.L., Tsien R.Y. Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:4411-4416.
54. Nguyen Q.T., Schroeder L.F., Mank M., Muller A., Taylor P., Griesbeck O., Kleinfeld D. An in vivo biosensor for neurotransmitter release and in situ receptor activity. Nature Neuroscience 2010, 13. 127-U301.
55. Yamauchi J.G., Nemecz A., Quoc T.N., Muller A., Schroeder L.F., Talley T.T., Lindstrom J., Kleinfeld D., Taylor P. Characterizing ligand-gated ion channel receptors with genetically encoded Ca(++) sensors. PLoS ONE 2011, 6.
56. Keller P.J., Schmidt A.D., Wittbrodt J., Stelzer E.H.K. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 2008, 322:1065-1069.
57. Shepherd G.M.G., Pologruto T.A., Svoboda K. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 2003, 38:277-289.