Enhancement of odor avoidance regulated by dopamine signaling in Caenorhabditis elegans

Journal of Neuroscience

Volumn 30, Issue 48, 2010, Pages 16365-16375

  Kimura, Koutarou D ^a,b,c   Fujita, Kosuke ^b   Katsura, Isao ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 NONANONE; DEODORANT AGENT; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR DOP3; OCTANOL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CAENORHABDITIS ELEGANS; CONDITIONING; CONTROLLED STUDY; FOOD INTAKE; INTERNEURON; MEMORY; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; STATE DEPENDENT LEARNING;

1-OCTANOL; ANIMALS; AVOIDANCE LEARNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DOPAMINE; GENE KNOCKOUT TECHNIQUES; KETONES; ODORS; RECEPTORS, DOPAMINE D2; SIGNAL TRANSDUCTION;

EID: 78649732415     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6023-09.2010     Document Type: Article

References (74)

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.
2. Avery L, Horvitz HR (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253:263-270.
3. Bargmann CI (2006) Chemosensation in C. elegans. In: WormBook (The C. elegans Research Community, ed), doi/10.1895/wormbook.1.123.1, http://www.wormbook.org.
4. Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-527.
5. Basbaum AI, Jessell TM (2000) The perception of pain. In: Principles of neural science, Ed 4 (Kandel ER, Schwartz JH, Jessell TM, eds), pp 472-491. New York: McGraw-Hill.
6. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
7. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV (2001) Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 21:1510-1522.
8. Chalasani SH, Kato S, Albrecht DR, Nakagawa T, Abbott LF, Bargmann CI (2010) Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nat Neurosci 13:615-621.
9. 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 U S A 101:15512-15517.
10. Chase DL, Koelle MR (2007) Biogenic amine neurotransmitters in C. elegans. In: WormBook (The C. elegans Research Community, ed), doi/10.1895/wormbook.1.132.1, http://www.wormbook.org.
11. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7:1096-1103.
12. Chou JH, Bargmann CI, Sengupta P (2001) The Caenorhabditis elegans odr-2 gene encodes a novel Ly-6-related protein required for olfaction. Genetics 157:211-224.
13. Coburn CM, Bargmann CI (1996) A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17:695-706.
14. Colbert HA, Bargmann CI (1995) Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803-812.
15. Colosimo ME, Brown A, Mukhopadhyay S, Gabel C, Lanjuin AE, Samuel AD, Sengupta P (2004) Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr Biol 14:2245-2251.
16. Dalton P, Doolittle N, Breslin PA (2002) Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci 5:199-200.
17. DeZazzo J, Tully T (1995) Dissection of memory formation: from behavioral pharmacology to molecular genetics. Trends Neurosci 18:212-218.
18. Driscoll M, Chalfie M (1991) The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349:588-593.
19. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE, Rand JB (1999) The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 19:72-84.
20. Eastman C, Horvitz HR, Jin Y (1999) Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the Caenorhabditis elegans UNC-30 homeodomain protein. J Neurosci 19:6225-6234.
21. 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.
22. 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.
23. Feng Z, Cronin CJ, Wittig JH Jr, Sternberg PW, Schafer WR (2004) An imaging system for standardized quantitative analysis of C. elegans behavior. BMC Bioinformatics 5:115.
24. Finney M, Ruvkun G (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895-905.
25. Giles AC, Rose JK, Rankin CH (2006) Investigations of learning and memory in Caenorhabditis elegans. Int Rev Neurobiol 69:37-71.
26. Gray JM, Hill JJ, Bargmann CI (2005) Acircuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A 102:3184-3191.
27. Hallam S, Singer E, Waring D, Jin Y (2000) The C. elegans NeuroD homolog cnd-1 functions in multiple aspects of motor neuron fate specification. Development 127:4239-4252.
28. Hawkins RD, Kandel ER, Siegelbaum SA (1993) Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu Rev Neurosci 16:625-665.
29. 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.
30. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24:1217-1225.
31. Hobert O, D'Alberti T, Liu Y, Ruvkun G (1998) Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J Neurosci 18:2084-2096.
32. Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216:1012-1014.
33. Hukema RK, Rademakers S, Jansen G (2008) Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine, and glutamate. Learn Mem 15:829-836.
34. Kandel ER, Kupfermann I, Iversen S (2000) Learning and memory. In: Principles of neural science, Ed 4 (Kandel ER, Schwartz JH, Jessell TM, eds), pp 1227-1246. New York: McGraw-Hill.
35. Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8:341-354.
36. 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.
37. Kuhara A, Okumura M, Kimata T, Tanizawa Y, Takano R, Kimura KD, Inada H, Matsumoto K, Mori I (2008) Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320:803-807.
38. Lee J, Jee C, McIntire SL (2009) Ethanol preference in C. elegans. Genes Brain Behav 8:578-585.
39. Lints R, Emmons SW (1999) Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene. Development 126:5819-5831.
40. Liu DW, Thomas JH (1994) Regulation of a periodic motor program in C. elegans. J Neurosci 14:1953-1962.
41. Loer CM, Kenyon CJ (1993) Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13:5407-5417.
42. 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.
43. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
44. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189-225.
45. Morrison GE, Wen JY, Runciman S, van der Kooy D (1999) Olfactory associative learning in Caenorhabditis elegans is impaired in lrn-1 and lrn-2 mutants. Behav Neurosci 113:358-367.
46. Pezze MA, Feldon J (2004) Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 74:301-320.
47. Pierce-Shimomura JT, Morse TM, Lockery SR (1999) The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19:9557-9569.
48. Ranganathan R, Sawin ER, Trent C, Horvitz HR (2001) Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. J Neurosci 21:5871-5884.
49. Rankin CH, Beck CD, Chiba CM (1990) Caenorhabditis elegans: a new model system for the study of learning and memory. Behav Brain Res 37:89-92.
50. Rose JK, Rankin CH (2001) Analyses of habituation in Caenorhabditis elegans. Learn Mem 8:63-69.
51. Sahley CL (1995) What we have learned from the study of learning in the leech. J Neurobiol 27:434-445.
52. Sanyal S, Wintle RF, Kindt KS, Nuttley WM, Arvan R, Fitzmaurice P, Bigras E, Merz DC, Hébert 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.
53. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619-631.
54. Schafer WR, Kenyon CJ (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375:73-78.
55. 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.
56. Sulston J, Hodgkin J (1988) Methods. In: The nematode Caenorhabditis elegans (Wood WB, ed), pp 587-606. Plainview, NY: Cold Spring Harbor Laboratory.
57. 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.
58. Suzuki H, Kerr R, Bianchi L, Frøkjaer-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M, Schafer WR (2003) In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39:1005-1017.
59. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403:560-564.
60. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16-43.
61. 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.
62. Torayama I, Ishihara T, Katsura I (2007) Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. J Neurosci 27:741-750.
63. Troemel ER, Kimmel BE, Bargmann CI (1997) Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91:161-169.
64. Unoki S, Matsumoto Y, Mizunami M (2006) Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur J Neurosci 24:2031-2038.
65. Voglis G, Tavernarakis N (2008) A synaptic DEG/ENaC ion channel mediates learning in C. elegans by facilitating dopamine signalling. EMBO J 27:3288-3299.
66. Waddington JL, O'Boyle KM (1989) Drugs acting on brain dopamine receptors: a conceptual re-evaluation five years after the first selective D-1 antagonist. Pharmacol Ther 43:1-52.
67. Wang HW, Wysocki CJ, Gold GH (1993) Induction of olfactory receptor sensitivity in mice. Science 260:998-1000.
68. Weinshenker D, Garriga G, Thomas JH (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15:6975-6985.
69. 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.
70. Wicks SR, de Vries CJ, van Luenen HG, Plasterk RH (2000) CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev Biol 221:295-307.
71. Woolf CJ, Walters ET (1991) Commonpatterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia. Trends Neurosci 14:74-78.
72. Wysocki CJ, Dorries KM, Beauchamp GK (1989) Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc Natl Acad Sci U S A 86:7976-7978.
73. Yee KK, Wysocki CJ (2001) Odorant exposure increases olfactory sensitivity: olfactory epithelium is implicated. Physiol Behav 72:705-711.
74. 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 24:347-361.