Optimization of a GCaMP calcium indicator for neural activity imaging

Journal of Neuroscience

Volumn 32, Issue 40, 2012, Pages 13819-13840

  Akerboom, Jasper ^a   Chen, Tsai Wen ^a   Wardill, Trevor J ^a,l   Tian, Lin ^a,m   Marvin, Jonathan S ^a   Mutlu, Sevinç ^a,b   Calderón, Nicole Carreras ^a,c,d   Esposti, Federico ^c   Borghuis, Bart G ^a,e   Sun, Xiaonan Richard ^f   Gordus, Andrew ^g   Orger, Michael B ^b,h   Portugues, Ruben ^h   Engert, Florian ^h   Macklin, John J ^a   Filosa, Alessandro ⁱ   Aggarwal, Aman ^a,j   Kerr, Rex A ^a   Takagi, Ryousuke ^k   Kracun, Sebastian ^k   Shigetomi, Eiji ^k   Khakh, Baljit S ^k   Baier, Herwig ⁱ   Lagnado, Leon ^c   Wang, Samuel S H ^f   Bargmann, Cornelia I ^g   Kimmel, Bruce E ^a   Jayaraman, Vivek ^a   Svoboda, Karel ^a   Kim, Douglas S ^a   Schreiter, Eric R ^a,d   Looger, Loren L ^a   more..

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d UNIVERSITY OF PUERTO RICO RIO PIEDRAS   (Puerto Rico)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f PRINCETON UNIVERSITY   (United States)

^g ROCKEFELLER UNIVERSITY   (United States)

^h HARVARD UNIVERSITY   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l MARINE BIOLOGICAL LABORATORY   (United States)

^m UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GCAMP PROTEIN; NEURONAL CALCIUM SENSOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CAENORHABDITIS; CALCIUM BINDING; CALCIUM CURRENT; CHROMATOPHORE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DROSOPHILA; ELECTROPHYSIOLOGY; EMBRYO; FEMALE; FLAME PHOTOMETRY; FLUORESCENCE; HUMAN; HUMAN CELL; MOUSE; NEUROIMAGING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; RETINA; SIGNAL NOISE RATIO; TECTUM; VISUAL CORTEX; ZEBRA FISH;

ANIMALS; ASTROCYTES; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA MELANOGASTER; FEMALE; FLUORESCENT DYES; FLUOROMETRY; GENES, SYNTHETIC; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; LARVA; LASERS; MICE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NEUROIMAGING; NEUROMUSCULAR JUNCTION; NEURONS; NEUROPIL; OLFACTORY RECEPTOR NEURONS; PEPTIDES; PHOTIC STIMULATION; PROTEIN CONFORMATION; RATS; RECOMBINANT FUSION PROTEINS; RETINAL BIPOLAR CELLS; SYNAPTIC TRANSMISSION; ZEBRAFISH;

EID: 84867026349     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2601-12.2012     Document Type: Article

References (88)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545-558.
2. Akerboom J, Rivera JD, Guilbe MM, Malave EC, Hernandez HH, Tian L, Hires SA, Marvin JS, Looger LL, Schreiter ER (2009) Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. J Biol Chem 284:6455-6464.
3. Alicea I, Marvin JS, Miklos AE, Ellington AD, Looger LL, Schreiter ER (2011) Structure of the Escherichia coli phosphonate binding protein PhnD and rationally optimized phosphonate biosensors. J Mol Biol 414:356-369.
4. Borghuis BG, Tian L, Xu Y, Nikonov SS, Vardi N, Zemelman BV, Looger LL (2011) Imaging light responses of targeted neuron populations in the rodent retina. J Neurosci 31:2855-2867.
5. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10:433-436.
6. Brand AH, Manoukian AS, Perrimon N (1994) Ectopic expression in Drosophila. Methods Cell Biol 44:635-654.
7. Brenner JF, Dew BS, Horton JB, King T, Neurath PW, Selles WD (1976) An automated microscope for cytologic research a preliminary evaluation. J Histochem Cytochem 24:100-111.
8. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 14:1030-1037.
9. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V (2010) Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol 20:1470-1475.
10. 2+ buffers at nerve firing rates in situ. J Neurosci 30:1869-1881.
11. Cobbold PH, Rink TJ (1987) Fluorescence and bioluminescence measurement of cytoplasmic free calcium. Biochem J 248:313-328.
12. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Ada Crystallogr D Biol Crystallogr 50:760-763.
13. Del Bene F, Wyart C, Robles E, Tran A, Looger L, Scott EK, Isacoff EY, Baier H (2010) Filtering of visual information in the tectum by an identified neural circuit. Science 330:669-673.
14. Dombeck DA, Khabbaz AN, Collman F, Adelman TL, Tank DW (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56:43-57.
15. Dombeck DA, Harvey CD, Tian L, Looger LL, Tank DW (2010) Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat Neurosci 13:1433-1440.
16. Dorostkar MM, Dreosti E, Odermatt B, Lagnado L (2010) Computational processing of optical measurements of neuronal and synaptic activity in networks. J Neurosci Methods 188:141-150.
17. Dreosti E, Odermatt B, Dorostkar MM, Lagnado L (2009) A genetically encoded reporter of synaptic activity in vivo. Nat Methods 6:883-889.
18. Dreosti E, Esposti F, Baden T, Lagnado L (2011) In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat Neurosci 14:951-952.
19. Drobizhev M, Makarov NS, Tillo SE, Hughes TE, Rebane A (2011) Two-photon absorption properties of fluorescent proteins. Nat Methods 8:393-399.
20. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Ada Crystallogr D Biol Crystallogr 60:2126-2132.
21. Greenberg DS, Kerr JN (2009) Automated correction of fast motion artifacts for two-photon imaging of awake animals. J Neurosci Methods 176: 1-15.
22. Grewe BF, Langer D, Kasper H, Kampa BM, Helmchen F (2010) High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat Methods 7:399-405.
23. Guizar-Sicairos M, Thurman ST, Fienup JR (2008) Efficient subpixel image registration algorithms. Opt Lett 33:156-158.
24. Horikawa K, Yamada Y, Matsuda T, Kobayashi K, Hashimoto M, Matsuura T, Miyawaki A, Michikawa T, Mikoshiba K, Nagai T (2010) Spontaneous network activity visualized by ultrasensitive Ca(2+) indicators, yellow Cameleon-Nano. Nat Methods 7:729-732.
25. Huber D, Gutnisky DA, Peron S, O'Connor DH, Wiegert JS, Tian L, Oertner TG, Looger LL, Svoboda K (2012) Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484:473-478.
26. Hultschig C, Hecht HJ, Frank R (2004) Systematic delineation of a calmod-ulin peptide interaction. J Mol Biol 343:559-568.
27. Jan LY, Jan YN (1976) Properties of larval neuromuscular junction in Drosophila melanogaster. J Physiol 262:189-214.
28. Jayaraman V, Laurent G (2007) Evaluating a genetically encoded optical sensor of neural activity using eledrophysiology in intact adult fruit flies. Front Neural Circuits 1:3.
29. Kerlin AM, Andermann ML, Berezovskii VK, Reid RC (2010) Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67:858-871.
30. Kerr JN, Greenberg D, Helmchen F (2005) Imaging input and output of neocortical networks in vivo. Proc Natl Acad Sci U S A 102:14063-14068.
31. Komiyama T, Sato TR, O'Connor DH, Zhang YX, Huber D, Hooks BM, Gabitto M, Svoboda K (2010) Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464:1182-1186.
32. Kunkel TA, Bebenek K, McClary J (1991) Efficient site-directed mutagene-sis using uracil-containing DNA. Methods Enzymol 204:125-139.
33. Leslie AGW (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography.
34. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757-3767.
35. Macleod GT, Hegstrom-Wojtowicz M, Charlton MP, Atwood HL (2002) Fast calcium signals in Drosophila motor neuron terminals. J Neuro-physiol 88:2659-2663.
36. Macleod GT, Marin L, Charlton MP, Atwood HL (2004) Synaptic vesicles: test for a role in presynaptic calcium regulation. J Neurosci 24:2496-2505.
37. Magde D, Wong R, Seybold PG (2002) Fluorescence quantum yields and their relation to lifetimes of rhodamine 6G and fluorescein in nine solvents: improved absolute standards for quantum yields. Photochem Pho-tobiol 75:327-334.
38. Mangini NJ, Pearlman AL (1980) Laminar distribution of receptive field properties in the primary visual cortex of the mouse. J Comp Neurol 193:203-222.
39. Mank M, Griesbeck O (2008) Genetically encoded calcium indicators. Chem Rev 108:1550-1564.
40. Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hiibener M, Griesbeck O (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5:805-811.
41. Mao T, O'Connor DH, Scheuss V, Nakai J, Svoboda K (2008) Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS ONE 3:el796.
42. Marvin JS, Schreiter ER, Echevarria IM, Looger LL (2011) A genetically encoded, high-signal-to-noise maltose sensor. Proteins 79:3025-3036.
43. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40:658-674.
44. Mittmann W, Wallace DJ, Czubayko U, Herb JT, Schaefer AT, Looger LL, Denk W, Kerr JN (2011) Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat Neurosci 14:1089-1093.
45. Muto A, Ohkura M, Kotani T, Higashijima S, Nakai J, Kawakami K (2011) Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish. Proc Natl Acad Sci U S A 108:5425-5430.
46. Miitze J, Iyer V, Macklin JJ, Colonell J, Karsh B, Petrasek Z, Schwille P, Looger LL, Lavis LD, Harris TD (2012) Excitation spectra and brightness optimization of two-photon excited probes. Biophys J 102:934-944.
47. 2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci USA 101: 10554-10559.
48. 2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141.
49. Nevin LM, Robles E, Baier H, Scott EK (2010) Focusing on optic tectum circuitry through the lens of genetics. BMC Biol 8:126.
50. Niell CM, Stryker MP (2008) Highly selective receptive fields in mouse visual cortex. J Neurosci 28:7520-7536.
51. O'Connor DH, Peron SP, Huber D, Svoboda K (2010) Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67:1048-1061.
52. 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.
53. Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J (2005) Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem 77:5861-5869.
54. Osakada F, Mori T, Cetin AH, Marshel JH, Virgen B, Callaway EM (2011) New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. Neuron 71:617-631.
55. 2+indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13:521-530.
56. Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24:79-88.
57. Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437-442.
58. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186:735-755.
59. Pflugrath JW (1999) The finer things in X-ray diffraction data collection. Ada Crystallogr D Biol Crystallogr 55:1718-1725.
60. Pologruto TA, Sabatini BL, Svoboda K (2003) Scanlmage: flexible software for operating laser-scanning microscopes. Biomed Eng Online 2:13.
61. Rodriguez Guilbe MM, Alfaro Malave EC, Akerboom J, Marvin JS, Looger LL, Schreiter ER (2008) Crystallization and preliminary X-ray characterization of the genetically encoded fluorescent calcium indicator protein GCaMP2. Ada Crystallogr Sect F Struct Biol Cryst Commun 64:629-631.
62. Sato TR, Svoboda K (2010) The functional properties of barrel cortex neurons projecting to the primary motor cortex. J Neurosci 30:4256-4260.
63. Sato TR, Gray NW, Mainen ZF, Svoboda K (2007) The functional microarchitecture of the mouse barrel cortex. PLoS Biol 5:el89.
64. Schwille P, Haupts U, Maiti S, Webb WW (1999) Molecular dynamics in living cells observed by fluorescence correlation spedroscopy with one-and two-photon excitation. Biophys J 77:2251-2265.
65. Seelig JD, Chiappe ME, Lott GK, Dutta A, Osborne JE, Reiser MB, Jayaraman V (2010) Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat Methods 7:535-540.
66. Shigetomi E, Kracun S, Khakh BS (2010a) Monitoring astrocyte calcium microdomains with improved membrane targeted GCaMP reporters. Neuron Glia Biol 16:1-9.
67. Shigetomi E, Kracun S, Sofroniew MV, Khakh BS (2010b) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat Neurosci 13:759-766.
68. Shindo A, Hara Y, Yamamoto TS, Ohkura M, Nakai J, Ueno N (2010) Tissue-tissue interaction-triggered calcium elevation is required for cell polarization during Xenopus gastrulation. PLoS One 5:e8897.
69. Sohya K, Kameyama K, Yanagawa Y, Obata K, Tsumoto T (2007) GABAe-rgic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2 + imaging in transgenic mice. J Neurosci 27:2145-2149.
70. Sorensen BR, Shea MA (1996) Calcium binding decreases the stokes radius of calmodulin and mutants R74A, R90A, and R90G. Biophys J 71:3407-3420.
71. Souslova EA, Belousov W, Lock JG, Stromblad S, Kasparov S, Bolshakov AP, Pinelis VG, Labas YA, Lukyanov S, Mayr LM, Chudakov DM (2007) Single fluorescent protein-based Ca2 + sensors with increased dynamic range. BMC Biotechnol 7:37.
72. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100: 7319-7324.
73. Straw AD (2008) Vision egg: an open-source library for realtime visual stimulus generation. Front Neuroinform 2:4.
74. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234.
75. Suter BA, O'Connor T, Iyer V, Petreanu LT, Hooks BM, Kiritani T, Svoboda K, Shepherd GMG (2010) Ephus: multipurpose data acquisition software for neuroscience experiments. Front Neurosci Methods 4:1-12.
76. Tallini YN, Ohkura M, Choi BR, Ji G, Imoto K, Doran R, Lee J, Plan P, Wilson J, Xin HB, Sanbe A, Gulick J, Mathai J, Robbins J, Salama G, Nakai J, Kotlikoff MI (2006) Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc Natl Acad Sci U S A 103:4753-4758.
77. Thevenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to sub-pixel registration based on intensity. IEEE Trans Image Process 7:27-41.
78. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6:875-881.
79. Venken KJ, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: a BAC transgenie platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747-1751.
80. Wang Q, Shui B, Kotlikoff MI, Sondermann H (2008) Structural basis for calcium sensing by GCaMP2. Structure 16:1817-1827.
81. Ward WW (2005) Biochemical and physical properties of green fluorescent protein. In: Methods of biochemical analysis, green fluorescent protein: properties, applications, and protocols, Ed 2 (Chalfie M, Kain SR, eds), p 56. Hoboken, NJ: Wiley.
82. Xu C, Webb WW (1996) Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm. J Opt Soc AiriB 13:481-491.
83. Xu N, O'Connor DH, Clack NG, Tian L, Myers EW, Looger L, Svoboda K, Magee JC (2010) Distal dendritic activity of layer 5 pyramidal neurons in awake behaving animals signals active tactile object detection. Soc Neurosci Abstracts 36:587.1.
84. 2+ imaging. Nat Methods 3:377-383.
85. 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:pl5.
86. Zariwala HA, Madisen L, Ahrens KF, Bernard A, Lein ES, Jones AR, Zeng H (2011) Visual tuning properties of genetically identified layer 2/3 neuronal types in the primary visual cortex of cre-transgenic mice. Front Syst Neurosci 4:162.
87. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW (2012) A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32:3131-3141.
88. 2+ indicators. Science 333:1888-1891.