Random insertion of split-cans of the fluorescent protein venus into Shaker channels yields voltage sensitive probes with improved membrane localization in mammalian cells

Journal of Neuroscience Methods

Volumn 199, Issue 1, 2011, Pages 1-9

  Jin, Lei ^a   Baker, Bradley ^a   Mealer, Robbie ^b   Cohen, Lawrence ^a   Pieribone, Vincent ^a,c   Pralle, Arnd ^d,e   Hughes, Thomas ^b  

^a YALE UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c JOHN B PIERCE LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY AT BUFFALO   (United States)

Author keywords

FP voltage sensor; Genetically encoded voltage sensor; Membrane localization; Shaker; Split can; Transposon; Venus

Indexed keywords

SHAKER POTASSIUM CHANNEL; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONJUGATION; ENDOPLASMIC RETICULUM; FLUORESCENCE; HUMAN; HUMAN CELL; MAMMAL CELL; MEMBRANE POTENTIAL; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSPOSON;

BACTERIAL PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CYTOSOL; DNA TRANSPOSABLE ELEMENTS; FLUORESCENT DYES; HUMANS; KIDNEY; LUMINESCENT PROTEINS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTATION, MISSENSE; NEUROBLASTOMA; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; TRANSFECTION;

EID: 79958140367     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2011.03.028     Document Type: Article

References (41)

1. Akemann W., Mutoh H., Perron A., Rossier J., Knöpfel T. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat Methods 2010, 7:643-649.
2. Ataka K., Pieribone V. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys J 2002, 82:509-516.
3. Baker B., Lee H., Pieribone V., Cohen L., Isacoff E., Knopfel T., et al. Three fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells. J Neurosci Methods 2007, 161:32-38.
4. Baker B., Mutoh H., Dimitrov D., Akemann W., Perron A., Iwamoto Y., et al. Genetically encoded fluorescent sensors of membrane potential. Brain Cell Biol 2008, 36:53-67.
5. 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, 15:1155-1160.
6. Canepari M., Vogt K., Zecevic D. Combining voltage and calcium imaging from neuronal dendrites. Cell Mol Neurobiol 2008, 28:1079-1093.
7. Carter M., Shieh J.C. Visualizing nervous system function. Guide to research techniques in neuroscience 2010, Academic Press, New York, p. 169-89.
8. Clay J., Kuzirian A. Trafficking of axonal K+ channels: potential role of Hsc70. J Neurosci Res 2002, 67:745-752.
9. 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, 241:159-160.
10. Dimitrov D., He Y., Mutoh H., Baker B.J., Cohen L., Akemann W., et al. Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS One 2007, 2:e440.
11. Grinvald A., Ross W., Farber I. Simultaneous optical measurements of electrical activity from multiple sites on processes of cultured neurons. Proc Natl Acad Sci U S A 1981, 78:3245-3249.
12. Grinvald A., Manker A., Segal M. Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J Physiol 1982, 333:269-291.
13. Grinvald A., Lieke E., Frostig R., Gilbert C., Wiesel T. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 1986, 324:361-364.
14. Guerrero G., Siegel M., Roska B., Loots E., Isacoff E. Tuning FlaSh: redesign of the dynamics, voltage range, and color of the genetically encoded optical sensor of membrane potential. Biophys J 2002, 83:3607-3618.
15. Gupta R., Salzberg B., Grinvald A., Cohen L., Kamino K., Lesher S., et al. Improvements in optical methods for measuring rapid changes in membrane potential. J Membr Biol 1981, 58:123-137.
16. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996, 14(33-8):27-28.
17. Jackrel M., Cortajarena A., Liu T., Regan L. Screening libraries to identify proteins with desired binding activities using a split-GFP reassembly assay. ACS Chem Biol 2010, 5:553-562.
18. Kwong K., Belliveau J., Chesler D., Goldberg I., Weisskoff R., Poncelet B., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci U S A 1992, 89:5675-5679.
19. Lindman S., Johansson I., Thulin E., Linse S. Green fluorescence induced by EF-hand assembly in a split GFP system. Protein Sci 2009, 18:1221-1229.
20. Loew L., Cohen L., Salzberg B., Obaid A., Bezanilla F. Charge-shift probes of membrane potential. Characterization of aminostyrylpyridinium dyes on the squid giant axon. Biophys J 1985, 47:71-77.
21. Lu J., Robinson J., Edwards D., Deutsch C. T1-T1 interactions occur in ER membranes while nascent Kv peptides are still attached to ribosomes. Biochemistry 2001, 40:10934-10946.
22. Mealer R., Pralle A., Isacoff E., Hughes T. Scanning the Shaker channel subunit with fragments of GFP: can complementing fragments on adjacent subunits produce a fluorophore?. Biophysics Annual Conference 2006, [Abstract r 2266].
23. Mealer R., Butler H., Hughes T. Functional fusion proteins by random transposon-based GFP insertion. Methods Cell Biol 2008, 85:23-44.
24. Nagai T., Ibata K., Park E., Kubota M., Mikoshiba K., Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 2002, 20:87-90.
25. Nagaya N., Papazian D. Potassium channel alpha and beta subunits assemble in the endoplasmic reticulum. J Biol Chem 1997, 272:3022-3027.
26. Ozawa T. Designing split reporter proteins for analytical tools. Anal Chim Acta 2006, 556:58-68.
27. Ozawa T. Protein reconstitution methods for visualizing biomolecular function in living cells. Yakugaku Zasshi 2009, 129:289-295.
28. Perozo E., Papazian D., Stefani E., Bezanilla F. Gating currents in Shaker K+ channels. Implications for activation and inactivation models. Biophys J 1992, 62:160-168. [discussion 9-71].
29. Perozo E., MacKinnon R., Bezanilla F., Stefani E. Gating currents from a nonconducting mutant reveal open-closed conformations in Shaker K+ channels. Neuron 1993, 11:353-358.
30. Pralle A., Mealer R., Hughes T., Isacoff E. Optical voltage sensor from random insertion of GFP fragments into the Shaker channel. Biophysics Annual Conference 2006, [Abstract r 2271].
31. Reddy P., Corley R. Assembly, sorting, and exit of oligomeric proteins from the endoplasmic reticulum. Bioessays 1998, 20:546-554.
32. Rekas A., Alattia J., Nagai T., Miyawaki A., Ikura M. Crystal structure of venus, a yellow fluorescent protein with improved maturation and reduced environmental sensitivity. J Biol Chem 2002, 277:50573-50578.
33. Robinson J., Deutsch C. Coupled tertiary folding and oligomerization of the T1 domain of Kv channels. Neuron 2005, 45:223-232.
34. Sakai R., Repunte-Canonigo V., Raj C., Knöpfel T. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur J Neurosci 2001, 13:2314-2318.
35. Salzberg B., Grinvald A., Cohen L., Davila H., Ross W. Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons. J Neurophysiol 1977, 40:1281-1291.
36. Siegel M.S., Isacoff E.Y. A genetically encoded optical probe of membrane voltage. Neuron 1997, 19:735-741.
37. Tolkovsky A., Richards C. Na+/H+ exchange is the major mechanism of pH regulation in cultured sympathetic neurons: measurements in single cell bodies and neurites using a fluorescent pH indicator. Neuroscience 1987, 22:1093-1102.
38. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 2008, 5:683-685.
39. Wilson C., Magliery T., Regan L. Detecting protein-protein interactions with GFP-fragment reassembly. Nat Methods 2004, 1:255-262.
40. Zecević D., Wu J., Cohen L., London J., Höpp H., Falk C. Hundreds of neurons in the Aplysia abdominal ganglion are active during the gill-withdrawal reflex. J Neurosci 1989, 9:3681-3689.
41. Zochowski M., Cohen L. Oscillations in the olfactory bulb carry information about odorant history. J Neurophysiol 2005, 94:2667-2675.