Optogenetic reporters: Fluorescent protein-based genetically encoded indicators of signaling and metabolism in the brain.

Progress in Brain Research

Volumn 196, Issue , 2012, Pages 235-263

  Tantama, Mathew ^a   Hung, Yin Pun ^a   Yellen, Gary ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Biosensor; Circularly permuted; Fluorescent protein; FRET; Genetically encoded; Live cell microscopy; Resonance energy transfer

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE; CHLORIDE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FLUORESCENT DYE; G PROTEIN COUPLED RECEPTOR; GLUCOSE; GLUTAMIC ACID; PROTEINASE; REACTIVE OXYGEN METABOLITE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ZINC;

ARTICLE; BIOSENSOR; BRAIN METABOLISM; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC MARKER; GENETIC PARAMETERS; HUMAN; NERVE FIBER GROWTH; NEUROIMAGING; NEUROPATHOLOGY; OPTOGENETIC REPORTER; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84857076245     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-59426-6.00012-4     Document Type: Chapter

References (184)

1. Agbulut O., Coirault C., Niederlander N., Huet A., Vicart P., Hagege A., et al. GFP expression in muscle cells impairs actin-myosin interactions: Implications for cell therapy. Nature Methods 2006, 3:331.
2. Akerboom J., Rivera J.D., Guilbe M.M., Malave E.C., Hernandez H.H., Tian L., et al. Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. The Journal of Biological Chemistry 2009, 284:6455-6464.
3. Aoki K., Kiyokawa E., Nakamura T., Matsuda M. Visualization of growth signal transduction cascades in living cells with genetically encoded probes based on Forster resonance energy transfer. Philosophical Transactions of the Royal Society of London B: Biological Sciences 2008, 363:2143-2151.
4. Aoki K., Nakamura T., Fujikawa K., Matsuda M. Local phosphatidylinositol 3,4,5-trisphosphate accumulation recruits Vav2 and Vav3 to activate Rac1/Cdc42 and initiate neurite outgrowth in nerve growth factor-stimulated PC12 cells. Molecular Biology of the Cell 2005, 16:2207-2217.
5. Aoki K., Nakamura T., Inoue T., Meyer T., Matsuda M. An essential role for the SHIP2-dependent negative feedback loop in neuritogenesis of nerve growth factor-stimulated PC12 cells. The Journal of Cell Biology 2007, 177:817-827.
6. Aoki K., Nakamura T., Matsuda M. Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in PC12 cells. The Journal of Biological Chemistry 2004, 279:713-719.
7. Azarias G., Perreten H., Lengacher S., Poburko D., Demaurex N., Magistretti P.J., et al. Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes. The Journal of Neuroscience 2011, 31:3550-3559.
8. Baens M., Noels H., Broeckx V., Hagens S., Fevery S., Billiau A.D., et al. The dark side of EGFP: Defective polyubiquitination. PLoS One 2006, 1:e54.
9. Baird G.S., Zacharias D.A., Tsien R.Y. Circular permutation and receptor insertion within green fluorescent proteins. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:11241-11246.
10. Belousov V.V., Fradkov A.F., Lukyanov K.A., Staroverov D.B., Shakhbazov K.S., Terskikh A.V., et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nature Methods 2006, 3:281-286.
11. Berg J., Hung Y.P., Yellen G. A genetically encoded fluorescent reporter of ATP:ADP ratio. Nature Methods 2009, 6:161-166.
12. Berglund K., Schleich W., Krieger P., Loo L.S., Wang D., Cant N.B., et al. Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon. Brain Cell Biology 2006, 35:207-228.
13. Berglund K., Schleich W., Wang H., Feng G., Hall W.C., Kuner T., et al. Imaging synaptic inhibition throughout the brain via genetically targeted Clomeleon. Brain Cell Biology 2008, 36:101-118.
14. Billups D., Billups B., Challiss R.A., Nahorski S.R. Modulation of Gq-protein-coupled inositol trisphosphate and Ca2+ signaling by the membrane potential. The Journal of Neuroscience 2006, 26:9983-9995.
15. Bittner C.X., Loaiza A., Ruminot I., Larenas V., Sotelo-Hitschfeld T., Gutierrez R., et al. High resolution measurement of the glycolytic rate. Frontiers in Neuroenergetics 2010, 2:26.
16. Bittner C.X., Valdebenito R., Ruminot I., Loaiza A., Larenas V., Sotelo-Hitschfeld T., et al. Fast and reversible stimulation of astrocytic glycolysis by k+ and a delayed and persistent effect of glutamate. The Journal of Neuroscience 2011, 31:4709-4713.
17. Bizzarri R., Serresi M., Luin S., Beltram F. Green fluorescent protein based pH indicators for in vivo use: A review. Analytical and Bioanalytical Chemistry 2009, 393:1107-1122.
18. Bunemann M., Frank M., Lohse M.J. Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:16077-16082.
19. Butcher A.J., Torrecilla I., Young K.W., Kong K.C., Mistry S.C., Bottrill A.R., et al. N-methyl-D-aspartate receptors mediate the phosphorylation and desensitization of muscarinic receptors in cerebellar granule neurons. The Journal of Biological Chemistry 2009, 284:17147-17156.
20. Casey J.R., Grinstein S., Orlowski J. Sensors and regulators of intracellular pH. Nature Reviews Molecular Cell Biology 2010, 11:50-61.
21. Chesler M., Kaila K. Modulation of pH by neuronal activity. Trends in Neurosciences 1992, 15:396-402.
22. Chudakov D.M., Matz M.V., Lukyanov S., Lukyanov K.A. Fluorescent proteins and their applications in imaging living cells and tissues. Physiological Reviews 2010, 90:1103-1163.
23. Ciruela F., Vilardaga J.P., Fernandez-Duenas V. Lighting up multiprotein complexes: Lessons from GPCR oligomerization. Trends in Biotechnology 2010, 28:407-415.
24. Citro S., Malik S., Oestreich E.A., Radeff-Huang J., Kelley G.G., Smrcka A.V., et al. Phospholipase Cepsilon is a nexus for Rho and Rap-mediated G protein-coupled receptor-induced astrocyte proliferation. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15543-15548.
25. Comley L.H., Wishart T.M., Baxter B., Murray L.M., Nimmo A., Thomson D., et al. Induction of cell stress in neurons from transgenic mice expressing yellow fluorescent protein: Implications for neurodegeneration research. PLoS One 2011, 6:e17639.
26. Day R.N., Davidson M.W. The fluorescent protein palette: Tools for cellular imaging. Chemical Society Reviews 2009, 38:2887-2921.
27. Deuschle K., Okumoto S., Fehr M., Looger L.L., Kozhukh L., Frommer W.B. Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Science 2005, 14:2304-2314.
28. Dickson B.J. Rho GTPases in growth cone guidance. Current Opinion in Neurobiology 2001, 11:103-110.
29. DiPilato L.M., Cheng X., Zhang J. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16513-16518.
30. Dittmer P.J., Miranda J.G., Gorski J.A., Palmer A.E. Genetically encoded sensors to elucidate spatial distribution of cellular zinc. The Journal of Biological Chemistry 2009, 284:16289-16297.
31. Dooley C.T., Dore T.M., Hanson G.T., Jackson W.C., Remington S.J., Tsien R.Y. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. The Journal of Biological Chemistry 2004, 279:22284-22293.
32. Drobizhev M., Makarov N.S., Tillo S.E., Hughes T.E., Rebane A. Two-photon absorption properties of fluorescent proteins. Nature Methods 2011, 8:393-399.
33. Duebel J., Haverkamp S., Schleich W., Feng G., Augustine G.J., Kuner T., et al. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon. Neuron 2006, 49:81-94.
34. Dulla C., Tani H., Okumoto S., Frommer W.B., Reimer R.J., Huguenard J.R. Imaging of glutamate in brain slices using FRET sensors. Journal of Neuroscience Methods 2008, 168:306-319.
35. Dunn T.A., Wang C.T., Colicos M.A., Zaccolo M., DiPilato L.M., Zhang J., et al. Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. The Journal of Neuroscience 2006, 26:12807-12815.
36. Dzhala V.I., Kuchibhotla K.V., Glykys J.C., Kahle K.T., Swiercz W.B., Feng G., et al. Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. The Journal of Neuroscience 2010, 30:11745-11761.
37. Falkenburger B.H., Jensen J.B., Hille B. Kinetics of M1 muscarinic receptor and G protein signaling to phospholipase C in living cells. The Journal of General Physiology 2010, 135:81-97.
38. Fehr M., Lalonde S., Lager I., Wolff M.W., Frommer W.B. In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. The Journal of Biological Chemistry 2003, 278:19127-19133.
39. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
40. Fernandez-Alfonso T., Ryan T.A. The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 2004, 41:943-953.
41. Frederickson C.J., Koh J.Y., Bush A.I. The neurobiology of zinc in health and disease. Nature Reviews Neuroscience 2005, 6:449-462.
42. Frommer W.B., Davidson M.W., Campbell R.E. Genetically encoded biosensors based on engineered fluorescent proteins. Chemical Society Reviews 2009, 38:2833-2841.
43. Gandhi S.P., Stevens C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 2003, 423:607-613.
44. Gerencser A.A., Mark K.A., Hubbard A.E., Divakaruni A.S., Mehrabian Z., Nicholls D.G., et al. Real-time visualization of cytoplasmic calpain activation and calcium deregulation in acute glutamate excitotoxicity. Journal of Neurochemistry 2009, 110:990-1004.
45. Gervasi N., Hepp R., Tricoire L., Zhang J., Lambolez B., Paupardin-Tritsch D., et al. Dynamics of protein kinase A signaling at the membrane, in the cytosol, and in the nucleus of neurons in mouse brain slices. The Journal of Neuroscience 2007, 27:2744-2750.
46. Glykys J., Dzhala V.I., Kuchibhotla K.V., Feng G., Kuner T., Augustine G., et al. Differences in cortical versus subcortical GABAergic signaling: A candidate mechanism of electroclinical uncoupling of neonatal seizures. Neuron 2009, 63:657-672.
47. Goto A., Hoshino M., Matsuda M., Nakamura T. Phosphorylation of STEF/Tiam2 by protein kinase a is critical for Rac1 activation and neurite outgrowth in dibutyryl cAMP-treated PC12D cells. Molecular Biology of the Cell 2011, 22:1780-1790.
48. Granseth B., Odermatt B., Royle S.J., Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 2006, 51:773-786.
49. Griesbeck O., Baird G.S., Campbell R.E., Zacharias D.A., Tsien R.Y. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. The Journal of Biological Chemistry 2001, 276:29188-29194.
50. Gutscher M., Pauleau A.L., Marty L., Brach T., Wabnitz G.H., Samstag Y., et al. Real-time imaging of the intracellular glutathione redox potential. Nature Methods 2008, 5:553-559.
51. Gutscher M., Sobotta M.C., Wabnitz G.H., Ballikaya S., Meyer A.J., Samstag Y., et al. Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. The Journal of Biological Chemistry 2009, 284:31532-31540.
52. Guzman J.N., Sanchez-Padilla J., Wokosin D., Kondapalli J., Ilijic E., Schumacker P.T., et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 2010, 468:696-700.
53. Hanazono Y., Yu J.M., Dunbar C.E., Emmons R.V. Green fluorescent protein retroviral vectors: Low titer and high recombination frequency suggest a selective disadvantage. Human Gene Therapy 1997, 8:1313-1319.
54. Hanson G.T., Aggeler R., Oglesbee D., Cannon M., Capaldi R.A., Tsien R.Y., et al. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. The Journal of Biological Chemistry 2004, 279:13044-13053.
55. Hanson G.T., McAnaney T.B., Park E.S., Rendell M.E., Yarbrough D.K., Chu S., et al. Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminary application. Biochemistry 2002, 41:15477-15488.
56. Hein P., Frank M., Hoffmann C., Lohse M.J., Bunemann M. Dynamics of receptor/G protein coupling in living cells. The EMBO Journal 2005, 24:4106-4114.
57. Hemmings H.C., Yan W., Westphalen R.I., Ryan T.A. The general anesthetic isoflurane depresses synaptic vesicle exocytosis. Molecular Pharmacology 2005, 67:1591-1599.
58. Hires S.A., Zhu Y., 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.
59. Hirose K., Kadowaki S., Tanabe M., Takeshima H., Iino M. Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns. Science 1999, 284:1527-1530.
60. Hommers L.G., Klenk C., Dees C., Bunemann M. G proteins in reverse mode: Receptor-mediated GTP release inhibits G protein and effector function. The Journal of Biological Chemistry 2010, 285:8227-8233.
61. Honda A., Adams S.R., Sawyer C.L., Lev-Ram V., Tsien R.Y., Dostmann W.R. Spatiotemporal dynamics of guanosine 3',5'-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:2437-2442.
62. Horowitz L.F., Hirdes W., Suh B.C., Hilgemann D.W., Mackie K., Hille B. Phospholipase C in living cells: Activation, inhibition, Ca2+ requirement, and regulation of M current. The Journal of General Physiology 2005, 126:243-262.
63. Huang W.Y., Aramburu J., Douglas P.S., Izumo S. Transgenic expression of green fluorescence protein can cause dilated cardiomyopathy. Nature Medicine 2000, 6:482-483.
64. Imamura H., Nhat K.P., Togawa H., Saito K., Iino R., Kato-Yamada Y., et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:15651-15656.
65. Itoh R.E., Kurokawa K., Ohba Y., Yoshizaki H., Mochizuki N., Matsuda M. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Molecular and Cellular Biology 2002, 22:6582-6591.
66. Janetopoulos C., Jin T., Devreotes P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 2001, 291:2408-2411.
67. Jayaraman S., Haggie P., Wachter R.M., Remington S.J., Verkman A.S. Mechanism and cellular applications of a green fluorescent protein-based halide sensor. The Journal of Biological Chemistry 2000, 275:6047-6050.
68. Jensen J.B., Lyssand J.S., Hague C., Hille B. Fluorescence changes reveal kinetic steps of muscarinic receptor-mediated modulation of phosphoinositides and Kv7.2/7.3 K+ channels. The Journal of General Physiology 2009, 133:347-359.
69. Klein R.L., Dayton R.D., Leidenheimer N.J., Jansen K., Golde T.E., Zweig R.M. Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Molecular Therapy 2006, 13:517-527.
70. Knopfel T., Lin M.Z., Levskaya A., Tian L., Lin J.Y., Boyden E.S. Toward the second generation of optogenetic tools. The Journal of Neuroscience 2010, 30:14998-15004.
71. Kraynov V.S., Chamberlain C., Bokoch G.M., Schwartz M.A., Slabaugh S., Hahn K.M. Localized Rac activation dynamics visualized in living cells. Science 2000, 290:333-337.
72. Krestel H.E., Mihaljevic A.L., Hoffman D.A., Schneider A. Neuronal co-expression of EGFP and beta-galactosidase in mice causes neuropathology and premature death. Neurobiology of Disease 2004, 17:310-318.
73. Kumar V., Jong Y.J., O'Malley K.L. Activated nuclear metabotropic glutamate receptor mGlu5 couples to nuclear Gq/11 proteins to generate inositol 1,4,5-trisphosphate-mediated nuclear Ca2+ release. The Journal of Biological Chemistry 2008, 283:14072-14083.
74. Kuner T., Augustine G.J. A genetically encoded ratiometric indicator for chloride: Capturing chloride transients in cultured hippocampal neurons. Neuron 2000, 27:447-459.
75. Kunishima N., Shimada Y., Tsuji Y., Sato T., Yamamoto M., Kumasaka T., et al. Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 2000, 407:971-977.
76. Lee S., Yoon B.E., Berglund K., Oh S.J., Park H., Shin H.S., et al. Channel-mediated tonic GABA release from glia. Science 2010, 330:790-796.
77. Li Z., Burrone J., Tyler W.J., Hartman K.N., Albeanu D.F., Murthy V.N. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:6131-6136.
78. Liu H.S., Jan M.S., Chou C.K., Chen P.H., Ke N.J. Is green fluorescent protein toxic to the living cells?. Biochemical and Biophysical Research Communications 1999, 260:712-717.
79. Lohse M.J., Bunemann M., Hoffmann C., Vilardaga J.P., Nikolaev V.O. Monitoring receptor signaling by intramolecular FRET. Current Opinion in Pharmacology 2007, 7:547-553.
80. Lohse M.J., Nikolaev V.O., Hein P., Hoffmann C., Vilardaga J.P., Bunemann M. Optical techniques to analyze real-time activation and signaling of G-protein-coupled receptors. Trends in Pharmacological Sciences 2008, 29:159-165.
81. Marcaggi P., Mutoh H., Dimitrov D., Beato M., Knopfel T. Optical measurement of mGluR1 conformational changes reveals fast activation, slow deactivation, and sensitization. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:11388-11393.
82. Markova O., Mukhtarov M., Real E., Jacob Y., Bregestovski P. Genetically encoded chloride indicator with improved sensitivity. Journal of Neuroscience Methods 2008, 170:67-76.
83. Matsushita S., Nakata H., Kubo Y., Tateyama M. Ligand-induced rearrangements of the GABA(B) receptor revealed by fluorescence resonance energy transfer. The Journal of Biological Chemistry 2010, 285:10291-10299.
84. Matsu-ura T., Michikawa T., Inoue T., Miyawaki A., Yoshida M., Mikoshiba K. Cytosolic inositol 1,4,5-trisphosphate dynamics during intracellular calcium oscillations in living cells. The Journal of Cell Biology 2006, 173:755-765.
85. McGann J.P., Pirez N., Gainey M.A., Muratore C., Elias A.S., Wachowiak M. Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 2005, 48:1039-1053.
86. Mercado J., Gordon-Shaag A., Zagotta W.N., Gordon S.E. Ca2+-dependent desensitization of TRPV2 channels is mediated by hydrolysis of phosphatidylinositol 4,5-bisphosphate. The Journal of Neuroscience 2010, 30:13338-13347.
87. Merksamer P.I., Trusina A., Papa F.R. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 2008, 135:933-947.
88. Metzger F., Repunte-Canonigo V., Matsushita S., Akemann W., Diez-Garcia J., Ho C.S., et al. Transgenic mice expressing a pH and Cl-sensing yellow-fluorescent protein under the control of a potassium channel promoter. The European Journal of Neuroscience 2002, 15:40-50.
89. Meyer A.J., Dick T.P. Fluorescent protein-based redox probes. Antioxidants & Redox Signaling 2010, 13:621-650.
90. Micheva K.D., Holz R.W., Smith S.J. Regulation of presynaptic phosphatidylinositol 4,5-biphosphate by neuronal activity. The Journal of Cell Biology 2001, 154:355-368.
91. 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.
92. Miyawaki A., Llopis J., Heim R., McCaffery J.M., Adams J.A., Ikura M., et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
93. Mochizuki N., Yamashita S., Kurokawa K., Ohba Y., Nagai T., Miyawaki A., et al. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 2001, 411:1065-1068.
94. Mukhtarov M., Markova O., Real E., Jacob Y., Buldakova S., Bregestovski P. Monitoring of chloride and activity of glycine receptor channels using genetically encoded fluorescent sensors. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences 2008, 366:3445-3462.
95. Muller F.L. A critical evaluation of cpYFP as a probe for superoxide. Free Radical Biology & Medicine 2009, 47:1779-1780.
96. Murakoshi H., Lee S.J., Yasuda R. Highly sensitive and quantitative FRET-FLIM imaging in single dendritic spines using improved non-radiative YFP. Brain Cell Biology 2008, 36:31-42.
97. Nagai Y., Miyazaki M., Aoki R., Zama T., Inouye S., Hirose K., et al. A fluorescent indicator for visualizing cAMP-induced phosphorylation in vivo. Nature Biotechnology 2000, 18:313-316.
98. Nagai T., Sawano A., Park E.S., Miyawaki A. Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3197-3202.
99. Nagai T., Yamada S., Tominaga T., Ichikawa M., Miyawaki A. Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:10554-10559.
100. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nature Biotechnology 2001, 19:137-141.
101. Nakamura T., Aoki K., Matsuda M. FRET imaging and in silico simulation: Analysis of the signaling network of nerve growth factor-induced neuritogenesis. Brain Cell Biology 2008, 36:19-30.
102. Nausch L.W., Ledoux J., Bonev A.D., Nelson M.T., Dostmann W.R. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:365-370.
103. Nelson C.P., Nahorski S.R., Challiss R.A. Temporal profiling of changes in phosphatidylinositol 4,5-bisphosphate, inositol 1,4,5-trisphosphate and diacylglycerol allows comprehensive analysis of phospholipase C-initiated signalling in single neurons. Journal of Neurochemistry 2008, 107:602-615.
104. Nemani V.M., Lu W., Berge V., Nakamura K., Onoa B., Lee M.K., et al. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 2010, 65:66-79.
105. Newman R.H., Fosbrink M.D., Zhang J. Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chemistry Review 2011, 111:3614-3666.
106. Nikolaev V.O., Bunemann M., Hein L., Hannawacker A., Lohse M.J. Novel single chain cAMP sensors for receptor-induced signal propagation. The Journal of Biological Chemistry 2004, 279:37215-37218.
107. Nishioka T., Aoki K., Hikake K., Yoshizaki H., Kiyokawa E., Matsuda M. Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells. Molecular Biology of the Cell 2008, 19:4213-4223.
108. Nobles M., Benians A., Tinker A. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:18706-18711.
109. Oancea E., Teruel M.N., Quest A.F., Meyer T. Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. The Journal of Cell Biology 1998, 140:485-498.
110. Okubo Y., Kakizawa S., Hirose K., Iino M. Visualization of IP(3) dynamics reveals a novel AMPA receptor-triggered IP(3) production pathway mediated by voltage-dependent Ca(2+) influx in Purkinje cells. Neuron 2001, 32:113-122.
111. 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.
112. Okumoto S., Takanaga H., Frommer W.B. Quantitative imaging for discovery and assembly of the metabo-regulome. New Phytologist 2008, 180:271-295.
113. Ostergaard H., Henriksen A., Hansen F.G., Winther J.R. Shedding light on disulfide bond formation: Engineering a redox switch in green fluorescent protein. The EMBO Journal 2001, 20:5853-5862.
114. Pacary E., Heng J., Azzarelli R., Riou P., Castro D., Lebel-Potter M., et al. Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 2011, 69:1069-1084.
115. Palmer A.E., Giacomello M., Kortemme T., Hires S.A., Lev-Ram V., Baker D., et al. Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chemical Biology 2006, 13:521-530.
116. Patterson G.H., Piston D.W., Barisas B.G. Forster distances between green fluorescent protein pairs. Analytical Biochemistry 2000, 284:438-440.
117. Pertz O., Hodgson L., Klemke R.L., Hahn K.M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006, 440:1069-1072.
118. Poburko D., Santo-Domingo J., Demaurex N. Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. The Journal of Biological Chemistry 2011, 286:11672-11684.
119. Pond B.B., Berglund K., Kuner T., Feng G., Augustine G.J., Schwartz-Bloom R.D. The chloride transporter Na(+)-K(+)-Cl- cotransporter isoform-1 contributes to intracellular chloride increases after in vitro ischemia. The Journal of Neuroscience 2006, 26:1396-1406.
120. Prebil M., Chowdhury H.H., Zorec R., Kreft M. Changes in cytosolic glucose level in ATP stimulated live astrocytes. Biochemical and Biophysical Research Communications 2011, 405:308-313.
121. Prebil M., Vardjan N., Jensen J., Zorec R., Kreft M. Dynamic monitoring of cytosolic glucose in single astrocytes. Glia 2011, 59:903-913.
122. Qin Y., Dittmer P.J., Park J.G., Jansen K.B., Palmer A.E. Measuring steady-state and dynamic endoplasmic reticulum and Golgi Zn2+ with genetically encoded sensors. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:7351-7356.
123. Quinn K.V., Behe P., Tinker A. Monitoring changes in membrane phosphatidylinositol 4,5-bisphosphate in living cells using a domain from the transcription factor tubby. The Journal of Physiology 2008, 586:2855-2871.
124. Remus T.P., Zima A.V., Bossuyt J., Bare D.J., Martin J.L., Blatter L.A., et al. Biosensors to measure inositol 1,4,5-trisphosphate concentration in living cells with spatiotemporal resolution. The Journal of Biological Chemistry 2006, 281:608-616.
125. Rochais F., Vilardaga J.P., Nikolaev V.O., Bunemann M., Lohse M.J., Engelhardt S. Real-time optical recording of beta1-adrenergic receptor activation reveals supersensitivity of the Arg389 variant to carvedilol. The Journal of Clinical Investigation 2007, 117:229-235.
126. Romoser V.A., Hinkle P.M., Persechini A. Detection in living cells of Ca2+-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. The Journal of Biological Chemistry 1997, 272:13270-13274.
127. Ryan T.A. Presynaptic imaging techniques. Current Opinion in Neurobiology 2001, 11:544-549.
128. Sabouri-Ghomi M., Wu Y., Hahn K., Danuser G. Visualizing and quantifying adhesive signals. Current Opinion in Cell Biology 2008, 20:541-550.
129. Saneyoshi T., Wayman G., Fortin D., Davare M., Hoshi N., Nozaki N., et al. Activity-dependent synaptogenesis: Regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 2008, 57:94-107.
130. Sankaranarayanan S., De Angelis D., Rothman J.E., Ryan T.A. The use of pHluorins for optical measurements of presynaptic activity. Biophysical Journal 2000, 79:2199-2208.
131. Sankaranarayanan S., Ryan T.A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nature Neuroscience 2001, 4:129-136.
132. Santagata S., Boggon T.J., Baird C.L., Gomez C.A., Zhao J., Shan W.S., et al. G-protein signaling through tubby proteins. Science 2001, 292:2041-2050.
133. Sasaki K., Sato M., Umezawa Y. Fluorescent indicators for Akt/protein kinase B and dynamics of Akt activity visualized in living cells. The Journal of Biological Chemistry 2003, 278:30945-30951.
134. Sato M., Nakajima T., Goto M., Umezawa Y. Cell-based indicator to visualize picomolar dynamics of nitric oxide release from living cells. Analytical Chemistry 2006, 78:8175-8182.
135. Sato M., Ueda Y., Shibuya M., Umezawa Y. Locating inositol 1,4,5-trisphosphate in the nucleus and neuronal dendrites with genetically encoded fluorescent indicators. Analytical Chemistry 2005, 77:4751-4758.
136. Schwarzlander M., Logan D.C., Fricker M.D., Sweetlove L. The circularly permuted yellow fluorescent protein cpYFP that has been used as a superoxide probe is highly responsive to pH but not superoxide in mitochondria: Implications for the existence of superoxide 'flashes'. The Biochemical Journal 2011, 437:381-387.
137. Shafer O.T., Kim D.J., Dunbar-Yaffe R., Nikolaev V.O., Lohse M.J., Taghert P.H. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 2008, 58:223-237.
138. Shang Y., Claridge-Chang A., Sjulson L., Pypaert M., Miesenbock G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 2007, 128:601-612.
139. Slemmer J.E., Matsushita S., De Zeeuw C.I., Weber J.T., Knopfel T. Glutamate-induced elevations in intracellular chloride concentration in hippocampal cell cultures derived from EYFP-expressing mice. The European Journal of Neuroscience 2004, 19:2915-2922.
140. Srivastava J., Barber D.L., Jacobson M.P. Intracellular pH sensors: Design principles and functional significance. Physiology (Bethesda, MD) 2007, 22:30-39.
141. Stauffer T.P., Ahn S., Meyer T. Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Current Biology 1998, 8:343-346.
142. Suh B.C., Horowitz L.F., Hirdes W., Mackie K., Hille B. Regulation of KCNQ2/KCNQ3 current by G protein cycling: The kinetics of receptor-mediated signaling by Gq. The Journal of General Physiology 2004, 123:663-683.
143. Svoboda K., Yasuda R. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 2006, 50:823-839.
144. Szentpetery Z., Balla A., Kim Y.J., Lemmon M.A., Balla T. Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biology 2009, 10:67.
145. Takanaga H., Chaudhuri B., Frommer W.B. GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochimica et Biophysica Acta 2008, 1778:1091-1099.
146. Tani H., Dulla C.G., Huguenard J.R., Reimer R.J. Glutamine is required for persistent epileptiform activity in the disinhibited neocortical brain slice. The Journal of Neuroscience 2010, 30:1288-1300.
147. Tanimura A., Nezu A., Morita T., Turner R.J., Tojyo Y. Fluorescent biosensor for quantitative real-time measurements of inositol 1,4,5-trisphosphate in single living cells. The Journal of Biological Chemistry 2004, 279:38095-38098.
148. Tateyama M., Abe H., Nakata H., Saito O., Kubo Y. Ligand-induced rearrangement of the dimeric metabotropic glutamate receptor 1alpha. Nature Structural & Molecular Biology 2004, 11:637-642.
149. Thorsen T.S., Madsen K.L., Rebola N., Rathje M., Anggono V., Bach A., et al. Identification of a small-molecule inhibitor of the PICK1 PDZ domain that inhibits hippocampal LTP and LTD. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:413-418.
150. Tsien R.Y. The green fluorescent protein. Annual Review of Biochemistry 1998, 67:509-544.
151. Tsou P., Zheng B., Hsu C.H., Sasaki A.T., Cantley L.C. A fluorescent reporter of AMPK activity and cellular energy stress. Cell Metabolism 2011, 13:476-486.
152. Tuffy L.P., Concannon C.G., D'Orsi B., King M.A., Woods I., Huber H.J., et al. Characterization of Puma-dependent and Puma-independent neuronal cell death pathways following prolonged proteasomal inhibition. Molecular and Cellular Biology 2010, 30:5484-5501.
153. van der Wal J., Habets R., Varnai P., Balla T., Jalink K. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. The Journal of Biological Chemistry 2001, 276:15337-15344.
154. Vanderklish P.W., Krushel L.A., Holst B.H., Gally J.A., Crossin K.L., Edelman G.M. Marking synaptic activity in dendritic spines with a calpain substrate exhibiting fluorescence resonance energy transfer. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:2253-2258.
155. Varnai P., Balla T. Visualization of phosphoinositides that bind pleckstrin homology domains: Calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. The Journal of Cell Biology 1998, 143:501-510.
156. Varnai P., Balla T. Live cell imaging of phosphoinositide dynamics with fluorescent protein domains. Biochimica et Biophysica Acta 2006, 1761:957-967.
157. Vesce S., Jekabsons M.B., Johnson-Cadwell L.I., Nicholls D.G. Acute glutathione depletion restricts mitochondrial ATP export in cerebellar granule neurons. The Journal of Biological Chemistry 2005, 280:38720-38728.
158. Vilardaga J.P., Bunemann M., Krasel C., Castro M., Lohse M.J. Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nature Biotechnology 2003, 21:807-812.
159. Vincent P., Gervasi N., Zhang J. Real-time monitoring of cyclic nucleotide signaling in neurons using genetically encoded FRET probes. Brain Cell Biology 2008, 36:3-17.
160. Vinkenborg J.L., Koay M.S., Merkx M. Fluorescent imaging of transition metal homeostasis using genetically encoded sensors. Current Opinion in Chemical Biology 2010, 14:231-237.
161. Violin J.D., Zhang J., Tsien R.Y., Newton A.C. A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. The Journal of Cell Biology 2003, 161:899-909.
162. Wachter R.M., Elsliger M.A., Kallio K., Hanson G.T., Remington S.J. Structural basis of spectral shifts in the yellow-emission variants of green fluorescent protein. Structure 1998, 6:1267-1277.
163. Wachter R.M., Yarbrough D., Kallio K., Remington S.J. Crystallographic and energetic analysis of binding of selected anions to the yellow variants of green fluorescent protein. Journal of Molecular Biology 2000, 301:157-171.
164. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., et al. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
165. Wang Q., Shui B., Kotlikoff M.I., Sondermann H. Structural basis for calcium sensing by GCaMP2. Structure 2008, 16:1817-1827.
166. Ward M.W., Rehm M., Duessmann H., Kacmar S., Concannon C.G., Prehn J.H. Real time single cell analysis of Bid cleavage and Bid translocation during caspase-dependent and neuronal caspase-independent apoptosis. The Journal of Biological Chemistry 2006, 281:5837-5844.
167. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: Progress, pitfalls, and prospects. Free Radical Biology & Medicine 2007, 43:995-1022.
168. Waseem T., Mukhtarov M., Buldakova S., Medina I., Bregestovski P. Genetically encoded Cl-sensor as a tool for monitoring of Cl-dependent processes in small neuronal compartments. Journal of Neuroscience Methods 2010, 193:14-23.
169. Willemse M., Janssen E., de Lange F., Wieringa B., Fransen J. ATP and FRET-A cautionary note. Nature Biotechnology 2007, 25:170-172.
170. Willets J.M., Nelson C.P., Nahorski S.R., Challiss R.A. The regulation of M1 muscarinic acetylcholine receptor desensitization by synaptic activity in cultured hippocampal neurons. Journal of Neurochemistry 2007, 103:2268-2280.
171. Willoughby D., Cooper D.M. Live-cell imaging of cAMP dynamics. Nature Methods 2008, 5:29-36.
172. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nature Chemical Biology 2008, 4:278-286.
173. Xu X., Gerard A.L., Huang B.C., Anderson D.C., Payan D.G., Luo Y. Detection of programmed cell death using fluorescence energy transfer. Nucleic Acids Research 1998, 26:2034-2035.
174. Xu C., Watras J., Loew L.M. Kinetic analysis of receptor-activated phosphoinositide turnover. The Journal of Cell Biology 2003, 161:779-791.
175. Yan H.D., Villalobos C., Andrade R. TRPC channels mediate a muscarinic receptor-induced afterdepolarization in cerebral cortex. The Journal of Neuroscience 2009, 29:10038-10046.
176. Yoshizaki H., Ohba Y., Kurokawa K., Itoh R.E., Nakamura T., Mochizuki N., et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. The Journal of Cell Biology 2003, 162:223-232.
177. Yu D., Ponomarev A., Davis R.L. Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 2004, 42:437-449.
178. Zaccolo M., De Giorgi F., Cho C.Y., Feng L., Knapp T., Negulescu P.A., et al. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nature Cell Biology 2000, 2:25-29.
179. Zadran S., Jourdi H., Rostamiani K., Qin Q., Bi X., Baudry M. Brain-derived neurotrophic factor and epidermal growth factor activate neuronal m-calpain via mitogen-activated protein kinase-dependent phosphorylation. The Journal of Neuroscience 2010, 30:1086-1095.
180. Zhang Q., Li Y., Tsien R.W. The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 2009, 323:1448-1453.
181. Zhang J., Ma Y., Taylor S.S., Tsien R.Y. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:14997-15002.
182. Zhang H., Macara I.G. The PAR-6 polarity protein regulates dendritic spine morphogenesis through p190 RhoGAP and the Rho GTPase. Developmental Cell 2008, 14:216-226.
183. Zhang J., Wang Y., Chi Z., Keuss M.J., Pai Y.M., Kang H.C., et al. The AAA(+) ATPase thorase regulates AMPA receptor-dependent synaptic plasticity and behavior. Cell 2011, 145:284-299.
184. Zuo Y., Lubischer J.L., Kang H., Tian L., Mikesh M., Marks A., et al. Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. The Journal of Neuroscience 2004, 24:10999-11009.