Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Husson, Steven J ^a,c   Liewald, Jana F ^a   Schultheis, Christian ^a   Stirman, Jeffrey N ^b   Lu, Hang ^b   Gottschalk, Alexander ^a  

^a GOETHE UNIVERSITY   (Germany)

^b Georgia Institute of Technology   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAERHODOPSIN; PROTON PUMP; RHODOPSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL SUBPOPULATION; CHOLINERGIC NERVE CELL; FUNGUS; HALORUBRUM SODOMENSE; ILLUMINATION; INHIBITION KINETICS; INTERNEURON; LEPTOSPHAERIA MACULANS; MOTONEURON; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PHOTOSTIMULATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TOUCH RECEPTOR NERVE CELL;

ANIMALS; ARCHAEAL PROTEINS; CAENORHABDITIS ELEGANS; CHOLINERGIC NEURONS; FUNGAL PROTEINS; HALORHODOPSINS; LIGHT; LOCOMOTION; MOTOR NEURONS; MUSCLE CELLS; NERVE NET; NEURONS; NOCICEPTION; OPTOGENETICS; PROTON PUMPS; SIGNAL TRANSDUCTION; TOUCH;

ANIMALIA; CAENORHABDITIS ELEGANS; FUNGI; HALORUBRUM SODOMENSE; LEPTOSPHAERIA MACULANS; NATRONOMONAS PHARAONIS;

EID: 84864005208     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040937     Document Type: Article

References (39)

1. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K, (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
2. Deisseroth K, (2011) Optogenetics. Nat Methods 8: 26-29.
3. Liewald JF, Brauner M, Stephens GJ, Bouhours M, Schultheis C, et al. (2008) Optogenetic analysis of synaptic function. Nat Methods 5: 895-902.
4. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, et al. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100: 13940-13945.
5. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A, (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15: 2279-2284.
6. Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C, et al. (2011) Real-time multimodal optical control of individual neurons and muscles in freely behaving Caenorhabditis elegans. Nat Meth 8: 153-158.
7. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, et al. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639.
8. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, et al. (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463: 98-102.
9. Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, et al. (1999) Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J Mol Biol 285: 163-174.
10. Waschuk SA, Bezerra AG, Shi L, Brown LS, (2005) Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci U S A 102: 6879-6883.
11. 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: 1-340.
12. Guo ZV, Hart AC, Ramanathan S, (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods 6: 891-896.
13. Leifer AM, Fang-Yen C, Gershow M, Alkema MJ, Samuel AD, (2011) Optogenetic manipulation of neuroal activitgy in freely moving Caenorhabditis elegans. Nat Meth 8: 147-152.
14. Mahoney TR, Luo S, Round EK, Brauner M, Gottschalk A, et al. (2008) Intestinal signaling to GABAergic neurons regulates a rhythmic behavior in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 16350-16355.
15. Kuhara A, Ohnishi N, Shimowada T, Mori I, (2011) Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans. Nat Commun 2: 355.
16. Liu Q, Hollopeter G, Jorgensen EM, (2009) Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc Natl Acad Sci U S A 106: 10823-10828.
17. Gradinaru V, Thompson KR, Deisseroth K, (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol 36: 129-139.
18. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, et al. (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141: 154-165.
19. Stirman JN, Crane MM, Husson SJ, Gottschalk A, Lu H, (2012) Assembly of a multispectral optical illumination system with precise spatiotemporal control for the manipulation of optogenetic reagents. Nature Protocols 7: 207-220.
20. Kaplan JM, Horvitz HR, (1993) A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci U S A 90: 2227-2231.
21. Hilliard MA, Bergamasco C, Arbucci S, Plasterk RH, Bazzicalupo P, (2004) Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. EMBO J 23: 1101-1111.
22. Hilliard MA, Bargmann CI, Bazzicalupo P, (2002) C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Curr Biol 12: 730-734.
23. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI, (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207-218.
24. Bermak JC, Li M, Bullock C, Zhou QY, (2001) Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat Cell Biol 3: 492-498.
25. Ramot D, Johnson BE, Berry TL, Carnell L, Goodman MB, (2008) The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 3: e2208.
26. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S, (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5: 956-964.
27. Wicks SR, Roehrig CJ, Rankin CH, (1996) A dynamic network simulation of the nematode tap withdrawal circuit: predictions concerning synaptic function using behavioral criteria. J Neurosci 16: 4017-4031.
28. Maricq AV, Peckol E, Driscoll M, Bargmann CI, (1995) Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378: 78-81.
29. Bargmann CI, Thomas JH, Horvitz HR, (1990) Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 55: 529-538.
30. Gray JM, Hill JJ, Bargmann CI, (2005) A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A 102: 3184-3191.
31. Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, et al. (2005) In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J 24: 63-72.
32. Geffeney SL, Cueva JG, Glauser DA, Doll JC, Lee THJ-C, et al. (2011) DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 71: 1-13.
33. Mellem JE, Brockie PJ, Zheng Y, Madsen DM, et al. (2002) Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36: 933-944.
34. 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.
35. Chatzigeorgiou M, Schafer WR, (2011) Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 70: 299-309.
36. Ezcurra M, Tanizawa Y, Swoboda P, Schafer WR, (2011) Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling. EMBO J 30: 1110-1122.
37. Chronis N, Zimmer M, Bargmann CI, (2007) Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4: 727-731.
38. Ben AJ, Tanizawa Y, Rabinowitch I, Chatenay D, Schafer WR, (2010) Automated imaging of neuronal activity in freely behaving Caenorhabditis elegans. J Neurosci Methods 187: 229-234.
39. Bargmann CI, (2006) Chemosensation in C. elegans. In: The C. elegans Research Community, editors. editors. WormBook. doi/10.1895/wormbook.1.123.1.