Inducible and titratable silencing of Caenorhabditis elegans neurons in vivo with histamine-gated chloride channels

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 7, 2014, Pages 2770-2775

  Pokala, Navin ^a   Liu, Qiang ^a   Gordus, Andrew ^a   Bargmann, Cornelia I ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Avoidance behavior; Chemical genetics; Neural circuits; Neuronal silencing

Indexed keywords

AVOIDANCE BEHAVIOR; CHEMICAL GENETICS; NEURAL CIRCUITS; NEURONAL SILENCING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CHLORIDE CHANNELS; DROSOPHILA; DROSOPHILA PROTEINS; HISTAMINE; MICROFLUIDIC ANALYTICAL TECHNIQUES; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; NEURONS; PATCH-CLAMP TECHNIQUES;

EID: 84894325541     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400615111     Document Type: Article

References (45)

1. Fang-Yen C, Gabel CV, Samuel AD, Bargmann CI, Avery L (2012) Laser microsurgery in Caenorhabditis elegans. Methods Cell Biol 107:177-206.
2. Zheng Y, Brockie PJ, Mellem JE, Madsen DM, Maricq AV (1999) Neuronal control of locomotion in C. Elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24(2):347-361.
3. Qi YB, Garren EJ, Shu X, Tsien RY, Jin Y (2012) Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proc Natl Acad Sci USA 109(19):7499-7504.
4. Kobayashi J, et al. (2013) A method for selective ablation of neurons in C. Elegans using the phototoxic fluorescent protein, KillerRed. Neurosci Lett 548:261-264.
5. Williams DC, et al. (2013) Rapid and permanent neuronal inactivation in vivo via subcellular generation of reactive oxygen with the use of KillerRed. Cell Rep 5(2): 553-563.
6. Husson SJ, et al. (2012) Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. Elegans. PLoS ONE 7(7): E40937.
7. Edwards SL, et al. (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 6(8):e198.
8. Mori I, Ohshima Y (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376(6538):344-348.
9. Tan EM, et al. (2006) Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. Neuron 51(2):157-170.
10. Conklin BR, et al. (2008) Engineering GPCR signaling pathways with RASSLs. Nat Methods 5(8):673-678.
11. LerchnerW, et al. (2007) Reversible silencing of neuronal excitability in behaving mice by a genetically targeted, ivermectin-gated Cl-channel. Neuron 54(1):35-49.
12. Magnus CJ, et al. (2011) Chemical and genetic engineering of selective ion channelligand interactions. Science 333(6047):1292-1296.
13. Haas HL, Sergeeva OA, Selbach O (2008) Histamine in the nervous system. Physiol Rev 88(3):1183-1241.
14. Gisselmann G, Pusch H, Hovemann BT, Hatt H (2002) Two cDNAs coding for histaminegated ion channels in D. melanogaster. Nat Neurosci 5(1):11-12.
15. Zheng Y, et al. (2002) Identification of two novel Drosophila melanogaster histaminegated chloride channel subunits expressed in the eye. J Biol Chem 277(3):2000-2005.
16. Gengs C, et al. (2002) The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). J Biol Chem 277(44): 42113-42120.
17. Pantazis A, et al. (2008) Distinct roles for two histamine receptors (hclA and hclB) at the Drosophila photoreceptor synapse. J Neurosci 28(29):7250-7259.
18. Liu WW, Wilson RI (2013) Transient and specific inactivation of Drosophila neurons in vivo using a native ligand-gated ion channel. Curr Biol 23(13):1202-1208.
19. Chase DL, Koelle MR (2007) Biogenic amine neurotransmitters in C. Elegans (February 20, 2007). WormBook, ed. The C. Elegans Research Community, WormBook, doi/10.1895/wormbook.1.132.1.
20. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR (2005) Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46(2):247-260.
21. Albrecht DR, Bargmann CI (2011) High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments. Nat Methods 8(7):599-605.
22. Gisselmann G, Plonka J, Pusch H, Hatt H (2004) Unusual functional properties of homo-and heteromultimeric histamine-gated chloride channels of Drosophila melanogaster: Spontaneous currents and dual gating by GABA and histamine. Neurosci Lett 372(1-2):151-156.
23. Pirri JK, McPherson AD, Donnelly JL, Francis MM, Alkema MJ (2009) A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response. Neuron 62(4):526-538.
24. Hilliard MA, et al. (2005) In vivo imaging of C. Elegans ASH neurons: Cellular response and adaptation to chemical repellents. EMBO J 24(1):63-72.
25. Kahn-Kirby AH, et al. (2004) Specific polyunsaturated fatty acids drive TRPVdependent sensory signaling in vivo. Cell 119(6):889-900.
26. Chronis N, Zimmer M, Bargmann CI (2007) Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4(9):727-731.
27. Tian L, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875-881.
28. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314(1165):1-340.
29. Chalfie M, et al. (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5(4):956-964.
30. Gray JM, Hill JJ, Bargmann CI (2005) A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 102(9):3184-3191.
31. Piggott BJ, Liu J, Feng Z, Wescott SA, Xu XZ (2011) The neural circuits and synaptic mechanisms underlying motor initiation in C. Elegans. Cell 147(4):922-933.
32. Miller DM, et al. (1992) C. Elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons. Nature 355(6363): 841-845.
33. Kawano T, et al. (2011) An imbalancing act: Gap junctions reduce the backward motor circuit activity to bias C. Elegans for forward locomotion. Neuron 72(4): 572-586.
34. Mellem JE, Brockie PJ, Zheng Y, Madsen DM, Maricq AV (2002) Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. Elegans. Neuron 36(5):933-944.
35. Lindsay TH, Thiele TR, Lockery SR (2011) Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans. Nat Commun 2:306.
36. Liu Q, Hollopeter G, Jorgensen EM (2009) Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc Natl Acad Sci USA 106(26):10823-10828.
37. Battle A, Jonikas MC, Walter P, Weissman JS, Koller D (2010) Automated identification of pathways from quantitative genetic interaction data. Mol Syst Biol 6:379.
38. Lin JY, Lin MZ, Steinbach P, Tsien RY (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys J 96(5):1803-1814.
39. Raimondo JV, Kay L, Ellender TJ, Akerman CJ (2012) Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat Neurosci 15(8):1102-1104.
40. Ben-Ari Y (2002) Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 3(9):728-739.
41. Lockery SR, Wittenberg G, Kristan WB, Jr., Cottrell GW (1989) Function of identified interneurons in the leech elucidated using neural networks trained by back-propagation. Nature 340(6233):468-471.
42. Bargmann CI (2012) Beyond the connectome: How neuromodulators shape neural circuits. Bioessays 34(6):458-465.
43. Menard C, Horvitz HR, Cannon S (2005) Chimeric mutations in the M2 segment of the 5-hydroxytryptamine-gated chloride channel MOD-1 define a minimal determinant of anion/cation permeability. J Biol Chem 280(30):27502-27507.
44. Sato K, et al. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452(7190):1002-1006.
45. Benjamani Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc, B 57(1):289-300.