Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling

EMBO Journal

Volumn 30, Issue 6, 2011, Pages 1110-1122

  Ezcurra, Marina ^a,b   Tanizawa, Yoshinori ^a   Swoboda, Peter ^b   Schafer, William R ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

C. elegans; dopamine; modulation; neuropeptide; nociception

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR;

ANIMAL CELL; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR CHANGE; CAENORHABDITIS ELEGANS; CELL ACTIVATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FOOD; IN VIVO STUDY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TASTE;

ANIMALS; AVOIDANCE LEARNING; BACTERIA; CAENORHABDITIS ELEGANS; DOPAMINE; FEEDING BEHAVIOR; NOCICEPTORS; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS;

EID: 79952763572     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.22     Document Type: Article

References (57)

1. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR (2005) Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46: 247-260 (Pubitemid 40545780)
2. Avery L, Horvitz HR (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253: 263-270 (Pubitemid 20271941)
3. Bargmann CI, Mori I (1997) Chemotaxis and thermotaxis. In C. elegans II, Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds), pp 717-737. Cold Spring Harbor: Cold Spring Harbor Laboratory Press
4. 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
5. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94
6. Carnell L, Illi J, Hong SW, McIntire SL (2005) The G-protein-coupled serotonin receptor SER-1 regulates egg laying and male mating behaviors in Caenorhabditis elegans. J Neurosci 25: 10671-10681 (Pubitemid 41681915)
7. Chao MY, Komatsu H, Fukuto HS, Dionne HM, Hart AC (2004) Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc Natl Acad Sci USA 101: 15512-15517 (Pubitemid 39441572)
8. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC, Kindt KS, Hwang SW, Miller DM 3rd, Treinin M, Driscoll M, Schafer WR (2010) Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 13: 861-868
9. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7: 1096-1103 (Pubitemid 41184450)
10. Davis MW, Morton JJ, Carroll D, Jorgensen EM (2008) Gene activation using FLP recombinase in C. elegans. PLoS Genet 4: e1000028
11. Dernovici S, Starc T, Dent JA, Ribeiro P (2007) The serotonin receptor SER-1 (5HT2ce) contributes to the regulation of locomotion in Caenorhabditis elegans. Dev Neurobiol 67: 189-204
12. Edwards SL, Charlie NK, Milfort MC, Brown BS, Gravlin CN, Knecht JE, Miller KG (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 6: e198
13. Esposito G, Di Schiavi E, Bergamasco C, Bazzicalupo P (2007) Efficient and cell specific knock-down of gene function in targeted C. elegans neurons. Gene 395: 170-176 (Pubitemid 46670643)
14. Etchberger JF, Lorch A, Sleumer MC, Zapf R, Jones SJ, Marra MA, Holt RA, Moerman DG, Hobert O (2007) The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev 21: 1653-1674 (Pubitemid 47026369)
15. Ezak MJ, Ferkey DM (2010) The C. elegans D2-like dopamine receptor DOP-3 decreases behavioral sensitivity to the olfactory stimulus 1-octanol. PLoS One 5: e9487
16. Faumont S, Lockery SR (2006) The awake behaving worm: simultaneous imaging of neuronal activity and behavior in intact animals at millimeter scale. J Neurophysiol 95: 1976-1981
17. Guo ZV, Hart AC, Ramanathan S (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods 6: 891-896
18. Harris G, Mills H, Wragg R, Hapiak V, Castelletto M, Korchnak A, Komuniecki RW (2010) The monoaminergic modulation of sensory-mediated aversive responses in Caenorhabditis elegans requires glutamatergic/peptidergic cotransmission. J Neurosci 30: 7889-7899
19. Harris GP, Hapiak VM, Wragg RT, Miller SB, Hughes LJ, Hobson RJ, Steven R, Bamber B, Komuniecki RW (2009) Three distinct amine receptors operating at different levels within the locomotory circuit are each essential for the serotonergic modulation of chemosensa-tion in Caenorhabditis elegans. J Neurosci 29: 1446-1456
20. Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, Schafer WR (2005) In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J 24: 63-72 (Pubitemid 40188464)
21. 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 (Pubitemid 34455426)
22. 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 (Pubitemid 38436874)
23. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24: 1217-1225 (Pubitemid 38177028)
24. Hobson RJ, Hapiak VM, Xiao H, Buehrer KL, Komuniecki PR, Komuniecki RW (2006) SER-7, a Caenorhabditis elegans 5-HT7-like receptor, is essential for the 5-HT stimulation of pharyngeal pumping and egg laying. Genetics 172: 159-169 (Pubitemid 43345480)
25. Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216: 1012-1014 (Pubitemid 12025047)
26. Jose AM, Smith JJ, Hunter CP (2009) Export of RNA silencing from C. elegans tissues does not require the RNA channel SID-1. Proc Natl Acad Sci USA 106: 2283-2288
27. Kang L, Gao J, Schafer WR, Xie Z, Xu XZ (2010) C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67: 381-391
28. Keating CD, Kriek N, Daniels M, Ashcroft NR, Hopper NA, Siney EJ, Holden-Dye L, Burke JF (2003) Whole-genome analysis of 60 G protein-coupled receptors in Caenorhabditis elegans by gene knockout with RNAi. Curr Biol 13: 1715-1720 (Pubitemid 37216250)
29. Kindt KS, Quast KB, Giles AC, De S, Hendrey D, Nicastro I, Rankin CH, Schafer WR (2007) Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 55: 662-676 (Pubitemid 47223641)
30. Kodama E, Kuhara A, Mohri-Shiomi A, Kimura KD, Okumura M, Tomioka M, Iino Y, Mori I (2006) Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev 20: 2955-2960 (Pubitemid 44771730)
31. Lints R, Emmons SW (1999) Patterning of dopaminergic neuro-transmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFB family signaling pathway and a Hox gene. Development 126: 5819-5831 (Pubitemid 30035028)
32. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970 (Pubitemid 21905425)
33. Mohri A, Kodama E, Kimura KD, Koike M, Mizuno T, Mori I (2005) Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 169: 1437-1450 (Pubitemid 40547455)
34. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A (2005a) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15: 2279-2284 (Pubitemid 41790623)
35. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100: 13940-13945 (Pubitemid 37499170)
36. Nagel G, Szellas T, Kateriya S, Adeishvili N, Hegemann P, Bamberg E (2005b) Channelrhodopsins: directly light-gated cation channels. Biochem Soc Trans 33: 863-866 (Pubitemid 41160880)
37. Ramot D, Johnson BE, Berry Jr 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
38. Rand JB, Nonet ML (1997) Neurotransmitter assignments for specific neurons. In C. elegans II, Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
39. Rex E, Hapiak V, Hobson R, Smith K, Xiao H, Komuniecki R (2005) TYRA-2 (F01E11.5): a Caenorhabditis elegans tyramine receptor expressed in the MC and NSM pharyngeal neurons. J Neurochem 94: 181-191 (Pubitemid 40911404)
40. Rex E, Molitor SC, Hapiak V, Xiao H, Henderson M, Komuniecki R (2004) Tyramine receptor (SER-2) isoforms are involved in the regulation of pharyngeal pumping and foraging behavior in Caenorhabditis elegans. J Neurochem 91 : 1104-1115 (Pubitemid 39587449)
41. Saeki S, Yamamoto M, Iino Y (2001) Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 204: 1757-1764 (Pubitemid 34861421)
42. Sambongi Y, Nagae T, Liu Y, Yoshimizu T, Takeda K, Wada Y, Futai M (1999) Sensing of cadmium and copper ions by externally exposed ADL, ASE, and ASH neurons elicits avoidance response in Caenorhabditis elegans. Neuroreport 10 : 753-757
43. Sanyal S, Wintle RF, Kindt KS, Nuttley WM, Arvan R, Fitzmaurice P, Bigras E, Merz DC, Hebert TE, van der Kooy D, Schafer WR, Culotti JG, Van Tol HH (2004) Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J 23: 473-482 (Pubitemid 38294511)
44. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomo-tory rate is modulated by the environment through a dopaminer-gic pathway and by experience through a serotonergic pathway. Neuron 26: 619-631
45. Schafer WR, Kenyon CJ (1995) A calcium channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375: 73-78
46. Senti G, Ezcurra M, Lobner J, Schafer WR, Swoboda P (2009) Worms with a single functional sensory cilium generate proper neuron-specific behavioral output. Genetics 183: 595-605
47. Sugiura M, Fuke S, Suo S, Sasagawa N, Van Tol HH, Ishiura S (2005) Characterization of a novel D2-like dopamine receptor with a truncated splice variant and a D1-like dopamine receptor unique to invertebrates from Caenorhabditis elegans. J Neurochem 94: 1146-1157 (Pubitemid 41170601)
48. Sulston J, Dew M, Brenner S (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 163: 215-226
49. Suo S, Culotti JG, Van Tol HH (2009) Dopamine counteracts octopamine signalling in a neural circuit mediating food response in C. elegans. EMBO J 28: 2437-2448
50. Suo S, Kimura Y, Van Tol HH (2006) Starvation induces cAMP response element-binding protein-dependent gene expression through octopamine-Gq signaling in Caenorhabditis elegans. J Neurosci 26: 10082-10090 (Pubitemid 44527402)
51. Suo S, Sasagawa N, Ishiura S (2003) Cloning and characterization of a Caenorhabditis elegans D2-like dopamine receptor. J Neurochem 86: 869-878 (Pubitemid 36988799)
52. Swoboda P, Adler HT, Thomas JH (2000) The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 5: 411-421
53. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y (2006) The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51: 613-625 (Pubitemid 44301825)
54. Trent C, Tsung N, Horvitz HR (1983) Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104: 619-647
55. Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O (2003) LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev Biol 263: 81-102 (Pubitemid 37268005)
56. Waggoner LE, Hardaker LA, Golik S, Schafer WR (2000) Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying. Genetics 154: 1181-1192 (Pubitemid 30140704)
57. Xiao H, Hapiak VM, Smith KA, Lin L, Hobson RJ, Plenefisch J, Komuniecki R (2006) SER-1, a Caenorhabditis elegans 5-HT2-like receptor, and a multi-PDZ domain containing protein (MPZ-1) interact in vulval muscle to facilitate serotonin-stimulated egg-laying. Dev Biol 298: 379-391 (Pubitemid 44441182)