Genetically Encoded Fluorescent Sensors of Membrane Potential

Overview

Journal Brain Cell Biol

Publisher Springer

Specialties Cell Biology
Neurology

Date 2008 Aug 6

PMID 18679801

Citations 52

Authors

B J Baker

H Mutoh

D Dimitrov

W Akemann

A Perron

Y Iwamoto

L Jin

L B Cohen

E Y Isacoff

V A Pieribone

T Hughes

T Knopfel

Affiliations

Soon will be listed here.

Abstract

Imaging activity of neurons in intact brain tissue was conceived several decades ago and, after many years of development, voltage-sensitive dyes now offer the highest spatial and temporal resolution for imaging neuronal functions in the living brain. Further progress in this field is expected from the emergent development of genetically encoded fluorescent sensors of membrane potential. These fluorescent protein (FP) voltage sensors overcome the drawbacks of organic voltage sensitive dyes such as non-specificity of cell staining and the low accessibility of the dye to some cell types. In a transgenic animal, a genetically encoded sensor could in principle be expressed specifically in any cell type and would have the advantage of staining only the cell population determined by the specificity of the promoter used to drive expression. Here we critically review the current status of these developments.

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References

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(6):e2514. PMC: 2429971. DOI: 10.1371/journal.pone.0002514. View

Long S, Campbell E, MacKinnon R . Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 2005; 309(5736):897-903. DOI: 10.1126/science.1116269. View

Kalyanaraman B, Feix J, Sieber F, Thomas J, Girotti A . Photodynamic action of merocyanine 540 on artificial and natural cell membranes: involvement of singlet molecular oxygen. Proc Natl Acad Sci U S A. 1987; 84(9):2999-3003. PMC: 304788. DOI: 10.1073/pnas.84.9.2999. View

Pathak M, Yarov-Yarovoy V, Agarwal G, Roux B, Barth P, Kohout S . Closing in on the resting state of the Shaker K(+) channel. Neuron. 2007; 56(1):124-40. DOI: 10.1016/j.neuron.2007.09.023. View

Jiang Y, Ruta V, Chen J, Lee A, MacKinnon R . The principle of gating charge movement in a voltage-dependent K+ channel. Nature. 2003; 423(6935):42-8. DOI: 10.1038/nature01581. View

Boyden E, Zhang F, Bamberg E, Nagel G, Deisseroth K . Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005; 8(9):1263-8. DOI: 10.1038/nn1525. View

Baird G, Zacharias D, Tsien R . Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A. 1999; 96(20):11241-6. PMC: 18018. DOI: 10.1073/pnas.96.20.11241. View

Yaksi E, Friedrich R . Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nat Methods. 2006; 3(5):377-83. DOI: 10.1038/nmeth874. View

Brown J, Cohen L, De Weer P, Pinto L, Ross W, Salzberg B . Rapid changes in intracellular free calcium concentration. Detection by metallochromic indicator dyes in squid giant axon. Biophys J. 1975; 15(11):1155-60. PMC: 1334796. DOI: 10.1016/S0006-3495(75)85891-7. View

10.

Qiu D, Knopfel T . An NMDA receptor/nitric oxide cascade in presynaptic parallel fiber-Purkinje neuron long-term potentiation. J Neurosci. 2007; 27(13):3408-15. PMC: 6672131. DOI: 10.1523/JNEUROSCI.4831-06.2007. View

11.

Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y . Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature. 2005; 435(7046):1239-43. DOI: 10.1038/nature03650. View

12.

Miesenbock G, Kevrekidis I . Optical imaging and control of genetically designated neurons in functioning circuits. Annu Rev Neurosci. 2005; 28:533-63. DOI: 10.1146/annurev.neuro.28.051804.101610. View

13.

Grinvald A, Hildesheim R . VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci. 2004; 5(11):874-85. DOI: 10.1038/nrn1536. View

14.

Chanda B, Blunck R, Faria L, Schweizer F, Mody I, Bezanilla F . A hybrid approach to measuring electrical activity in genetically specified neurons. Nat Neurosci. 2005; 8(11):1619-26. DOI: 10.1038/nn1558. View

15.

Ramsey I, Moran M, Chong J, Clapham D . A voltage-gated proton-selective channel lacking the pore domain. Nature. 2006; 440(7088):1213-6. PMC: 4084761. DOI: 10.1038/nature04700. View

16.

Macdonald V, JOBSIS F . Spectrophotometric studies on the pH of frog skeletal muscle. PH change during and after contractile activity. J Gen Physiol. 1976; 68(2):179-95. PMC: 2228422. DOI: 10.1085/jgp.68.2.179. View

17.

Vranesic I, Iijima T, Ichikawa M, Matsumoto G, Knopfel T . Signal transmission in the parallel fiber-Purkinje cell system visualized by high-resolution imaging. Proc Natl Acad Sci U S A. 1994; 91(26):13014-7. PMC: 45571. DOI: 10.1073/pnas.91.26.13014. View

18.

Knopfel T, Tomita K, Shimazaki R, Sakai R . Optical recordings of membrane potential using genetically targeted voltage-sensitive fluorescent proteins. Methods. 2003; 30(1):42-8. DOI: 10.1016/s1046-2023(03)00006-9. View

19.

Davila H, Salzberg B, Cohen L, Waggoner A . A large change in axon fluorescence that provides a promising method for measuring membrane potential. Nat New Biol. 1973; 241(109):159-60. DOI: 10.1038/newbio241159a0. View

20.

Diez-Garcia J, Akemann W, Knopfel T . In vivo calcium imaging from genetically specified target cells in mouse cerebellum. Neuroimage. 2006; 34(3):859-69. DOI: 10.1016/j.neuroimage.2006.10.021. View