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PMID: 22952643 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Specific expression of channelrhodopsin-2 in single neurons of Caenorhabditis elegans.

PloS one ·Vol. 7 ·No. 8 ·2012-00-00 ·Pages e43164

Schmitt C, Schultheis C, Pokala N, Husson SJ, Liewald JF, Bargmann CI, Gottschalk A

Abstract

Optogenetic approaches using light-activated proteins like Channelrhodopsin-2 (ChR2) enable investigating the function of populations of neurons in live Caenorhabditis elegans (and other) animals, as ChR2 expression can be targeted to these cells using specific promoters. Sub-populations of these neurons, or even single cells, can be further addressed by restricting the illumination to the cell of interest. However, this is technically demanding, particularly in free moving animals. Thus, it would be helpful if expression of ChR2 could be restricted to single neurons or neuron pairs, as even wide-field illumination would photostimulate only this particular cell. To this end we adopted the use of Cre or FLP recombinases and conditional ChR2 expression at the intersection of two promoter expression domains, i.e. in the cell of interest only. Success of this method depends on precise knowledge of the individual promoters' expression patterns and on relative expression levels of recombinase and ChR2. A bicistronic expression cassette with GFP helps to identify the correct expression pattern. Here we show specific expression in the AVA reverse command neurons and the aversive polymodal sensory ASH neurons. This approach shall enable to generate strains for optogenetic manipulation of each of the 302 C. elegans neurons. This may eventually allow to model the C. elegans nervous system in its entirety, based on functional data for each neuron.

MeSH Terms
Animals Behavior, Animal Caenorhabditis elegans/metabolism Caenorhabditis elegans Proteins/biosynthesis,genetics Gene Expression Profiling Gene Expression Regulation Green Fluorescent Proteins/metabolism Microscopy, Fluorescence/methods Models, Biological Models, Genetic Neurons/metabolism Plasmids/metabolism Promoter Regions, Genetic Recombinases/metabolism Rhodopsin/biosynthesis,genetics Transgenes
Chemicals
Caenorhabditis elegans Proteins Recombinases Green Fluorescent Proteins Rhodopsin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Schmitt Cornelia
Buchmann Institute for Molecular Life Sciences, Goethe-University, Frankfurt, Germany.
Schultheis Christian
Pokala Navin
Husson Steven J
Liewald Jana F
Bargmann Cornelia I
Gottschalk Alexander
References (66)
66 references, click to expand
  1. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans.
    Neuron. 1991 Nov;7(5):729-42 PMID: 1660283
  2. Light-sensitive neurons and channels mediate phototaxis in C. elegans.
    Nat Neurosci. 2008 Aug;11(8):916-22 PMID: 18604203
  3. Structure of the light-driven chloride pump halorhodopsin at 1.8 A resolution.
    Science. 2000 May 26;288(5470):1390-6 PMID: 10827943
  4. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans.
    Nature. 2009 Apr 30;458(7242):1171-5 PMID: 19349961
  5. Millisecond-timescale, genetically targeted optical control of neural activity.
    Nat Neurosci. 2005 Sep;8(9):1263-8 PMID: 16116447
  6. Cre-loxP biochemistry.
    Methods. 2002 Nov;28(3):374-83 PMID: 12431441
  7. GFP in mammalian cells.
    Trends Genet. 1995 Aug;11(8):326-7 PMID: 8585132
  8. Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling.
    EMBO J. 2011 Mar 16;30(6):1110-22 PMID: 21304491
  9. Neocortical excitation/inhibition balance in information processing and social dysfunction.
    Nature. 2011 Jul 27;477(7363):171-8 PMID: 21796121
  10. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP.
    Nat Genet. 2000 Jun;25(2):139-40 PMID: 10835623
  11. Fast manipulation of cellular cAMP level by light in vivo.
    Nat Methods. 2007 Jan;4(1):39-42 PMID: 17128267
  12. Optogenetic analysis of synaptic function.
    Nat Methods. 2008 Oct;5(10):895-902 PMID: 18794862
  13. Localization, trafficking, and temperature-dependence of the Aequorea green fluorescent protein in cultured vertebrate cells.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11899-903 PMID: 8524871
  14. Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans.
    Dev Biol. 1999 Nov 15;215(2):314-31 PMID: 10545240
  15. Gene activation using FLP recombinase in C. elegans.
    PLoS Genet. 2008 Mar 21;4(3):e1000028 PMID: 18369447
  16. Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans.
    Nat Methods. 2011 Feb;8(2):147-52 PMID: 21240279
  17. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans.
    Cell. 1997 Oct 17;91(2):161-9 PMID: 9346234
  18. A genetically encoded photoactivatable Rac controls the motility of living cells.
    Nature. 2009 Sep 3;461(7260):104-8 PMID: 19693014
  19. Spatiotemporal control of cell signalling using a light-switchable protein interaction.
    Nature. 2009 Oct 15;461(7266):997-1001 PMID: 19749742
  20. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13940-5 PMID: 14615590
  21. Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells.
    Genesis. 2006 Jan;44(1):23-8 PMID: 16400644
  22. Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15492-5 PMID: 9860996
  23. Locating proteins in the cell using TargetP, SignalP and related tools.
    Nat Protoc. 2007;2(4):953-71 PMID: 17446895
  24. The nature of the interaction of the P1 recombinase Cre with the recombining site loxP.
    Cold Spring Harb Symp Quant Biol. 1984;49:761-8 PMID: 6335689
  25. Optogenetic long-term manipulation of behavior and animal development.
    PLoS One. 2011 Apr 20;6(4):e18766 PMID: 21533086
  26. T-Coffee: A novel method for fast and accurate multiple sequence alignment.
    J Mol Biol. 2000 Sep 8;302(1):205-17 PMID: 10964570
  27. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes.
    Dev Biol. 1985 Sep;111(1):158-70 PMID: 3928418
  28. The HMMTOP transmembrane topology prediction server.
    Bioinformatics. 2001 Sep;17(9):849-50 PMID: 11590105
  29. Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42.
    J Neurosci. 2001 Mar 1;21(5):1510-22 PMID: 11222641
  30. Green fluorescent protein: applications in cell biology.
    FEBS Lett. 1996 Jun 24;389(1):44-7 PMID: 8682203
  31. Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor.
    Neuron. 1999 Oct;24(2):347-61 PMID: 10571229
  32. The neural circuit for touch sensitivity in Caenorhabditis elegans.
    J Neurosci. 1985 Apr;5(4):956-64 PMID: 3981252
  33. The complete family of genes encoding G proteins of Caenorhabditis elegans.
    Nat Genet. 1999 Apr;21(4):414-9 PMID: 10192394
  34. Widespread recombinase expression using FLPeR (flipper) mice.
    Genesis. 2000 Nov-Dec;28(3-4):106-10 PMID: 11105051
  35. Orthorhombic crystal form of bacteriorhodopsin nucleated on benzamidine diffracting to 3.6 A resolution.
    J Mol Biol. 1993 Nov 5;234(1):156-64 PMID: 8230195
  36. High-performance genetically targetable optical neural silencing by light-driven proton pumps.
    Nature. 2010 Jan 7;463(7277):98-102 PMID: 20054397
  37. The structure of the nervous system of the nematode Caenorhabditis elegans.
    Philos Trans R Soc Lond B Biol Sci. 1986 Nov 12;314(1165):1-340 PMID: 22462104
  38. Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans.
    Nat Methods. 2011 Feb;8(2):153-8 PMID: 21240278
  39. PACα--an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans.
    J Neurochem. 2011 Feb;116(4):616-25 PMID: 21166803
  40. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.
    EMBO J. 1991 Dec;10(12):3959-70 PMID: 1935914
  41. lin-12 Notch functions in the adult nervous system of C. elegans.
    BMC Neurosci. 2005 Jul 12;6:45 PMID: 16011804
  42. Targeted cell killing by reconstituted caspases.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2283-8 PMID: 17283333
  43. Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors.
    Curr Biol. 2012 May 8;22(9):743-52 PMID: 22483941
  44. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans.
    PLoS Biol. 2008 Aug 5;6(8):e198 PMID: 18687026
  45. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  46. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2227-31 PMID: 8460126
  47. A multispectral optical illumination system with precise spatiotemporal control for the manipulation of optogenetic reagents.
    Nat Protoc. 2012 Jan 12;7(2):207-20 PMID: 22240583
  48. Optical induction of synaptic plasticity using a light-sensitive channel.
    Nat Methods. 2007 Feb;4(2):139-41 PMID: 17195846
  49. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems.
    Neuron. 2008 Feb 7;57(3):353-63 PMID: 18255029
  50. SOSUI: classification and secondary structure prediction system for membrane proteins.
    Bioinformatics. 1998;14(4):378-9 PMID: 9632836
  51. Enhanced efficiency through nuclear localization signal fusion on phage PhiC31-integrase: activity comparison with Cre and FLPe recombinase in mammalian cells.
    Nucleic Acids Res. 2002 Jun 1;30(11):2299-306 PMID: 12034816
  52. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1.
    Nat Neurosci. 2003 Nov;6(11):1178-85 PMID: 14555955
  53. IgCAMs redundantly control axon navigation in Caenorhabditis elegans.
    Neural Dev. 2009 Apr 02;4:13 PMID: 19341471
  54. Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa.
    J Biol Chem. 2011 Jan 14;286(2):1181-8 PMID: 21030594
  55. The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans.
    Cell. 2011 Nov 11;147(4):922-33 PMID: 22078887
  56. Multimodal fast optical interrogation of neural circuitry.
    Nature. 2007 Apr 5;446(7136):633-9 PMID: 17410168
  57. Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron.
    J Neurosci. 1999 Mar 15;19(6):1952-8 PMID: 10066248
  58. Refolding of bacteriorhodopsin from expressed polypeptide fragments.
    J Biol Chem. 1998 Apr 10;273(15):9312-22 PMID: 9535926
  59. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  60. Inducible gene targeting in mice using the Cre/lox system.
    Methods. 1998 Apr;14(4):381-92 PMID: 9608509
  61. Combinatorial marking of cells and organelles with reconstituted fluorescent proteins.
    Cell. 2004 Oct 1;119(1):137-44 PMID: 15454087
  62. Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans.
    PLoS One. 2012;7(7):e40937 PMID: 22815873
  63. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins.
    Nat Methods. 2011 Dec 18;9(2):159-72 PMID: 22179551
  64. Neural regulation of thermotaxis in Caenorhabditis elegans.
    Nature. 1995 Jul 27;376(6538):344-8 PMID: 7630402
  65. Improving the accuracy of transmembrane protein topology prediction using evolutionary information.
    Bioinformatics. 2007 Mar 1;23(5):538-44 PMID: 17237066
  66. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses.
    Curr Biol. 2005 Dec 20;15(24):2279-84 PMID: 16360690
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2012-00-00
Epub
2012-00-30
Pages
e43164
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3431400
Subset
IM
Corrections
ErratumIn
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