Memory in Caenorhabditis elegans Is Mediated by NMDA-Type Ionotropic Glutamate Receptors

Current Biology

Volumn 18, Issue 13, 2008, Pages 1010-1015

  Kano, Takashi ^a   Brockie, Penelope J ^c   Sassa, Toshihiro ^a   Fujimoto, Hiroyuki ^a   Kawahara, Yasushi ^a   Iino, Yuichi ^b   Mellem, Jerry E ^c   Madsen, David M ^c   Hosono, Ryuji ^a   Maricq, Andres V ^c  

^a KANAZAWA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

SYSNEURO

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYLASPARTIC ACID; NMR 1 PROTEIN, C ELEGANS; NMR 2 PROTEIN, C ELEGANS; NMR-1 PROTEIN, C ELEGANS; NMR-2 PROTEIN, C ELEGANS; RIM PROTEIN, C ELEGANS; SODIUM CHLORIDE;

AMINO ACID SEQUENCE; ANIMAL; APPETITE; ARTICLE; AVOIDANCE BEHAVIOR; CAENORHABDITIS ELEGANS; CHEMOTAXIS; DRUG EFFECT; FOOD; GENETICS; INTERNEURON; LEARNING; MEMORY; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; STARVATION;

AMINO ACID SEQUENCE; ANIMALS; APPETITIVE BEHAVIOR; ASSOCIATION LEARNING; AVOIDANCE LEARNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CHEMOTAXIS; FOOD; INTERNEURONS; MEMORY; MOLECULAR SEQUENCE DATA; MUTATION; N-METHYLASPARTATE; RECEPTORS, N-METHYL-D-ASPARTATE; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM CHLORIDE; STARVATION;

ANIMALIA; CAENORHABDITIS ELEGANS; INVERTEBRATA; VERTEBRATA;

EID: 45849113972     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2008.05.051     Document Type: Article

References (47)

1. Lynch M.A. Long-term potentiation and memory. Physiol. Rev. 84 (2004) 87-136
2. Malenka R.C., and Bear M.F. LTP and LTD: An embarrassment of riches. Neuron 44 (2004) 5-21
3. Brockie P.J., Mellem J.E., Hills T., Madsen D.M., and Maricq A.V. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31 (2001) 617-630
4. Saeki S., Yamamoto M., and Iino Y. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J. Exp. Biol. 204 (2001) 1757-1764
5. de Bono M., and Maricq A.V. Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 28 (2005) 451-501
6. Hedgecock E.M., and Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 72 (1975) 4061-4065
7. Mohri A., Kodama E., Kimura K.D., Koike M., Mizuno T., and Mori I. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 169 (2005) 1437-1450
8. Rankin C.H., Beck C.D., and Chiba C.M. Caenorhabditis elegans: A new model system for the study of learning and memory. Behav. Brain Res. 37 (1990) 89-92
9. Wen J.Y., Kumar N., Morrison G., Rambaldini G., Runciman S., Rousseau J., and van der Kooy D. Mutations that prevent associative learning in C. elegans. Behav. Neurosci. 111 (1997) 354-368
10. Zhang Y., Lu H., and Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438 (2005) 179-184
11. Ishihara T., Iino Y., Mohri A., Mori I., Gengyo-Ando K., Mitani S., and Katsura I. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109 (2002) 639-649
12. Ikeda D.D., Duan Y., Matsuki M., Kunitomo H., Hutter H., Hedgecock E.M., and Iino Y. CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105 (2008) 5260-5265
13. Tomioka M., Adachi T., Suzuki H., Kunitomo H., Schafer W.R., and Iino Y. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51 (2006) 613-625
14. Matsuki M., Kunitomo H., and Iino Y. Goalpha regulates olfactory adaptation by antagonizing Gqalpha-DAG signaling in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 103 (2006) 1112-1117
15. Groc L., and Choquet D. AMPA and NMDA glutamate receptor trafficking: Multiple roads for reaching and leaving the synapse. Cell Tissue Res. 326 (2006) 423-438
16. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25 (2002) 103-126
17. Rose J.K., Kaun K.R., Chen S.H., and Rankin C.H. GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J. Neurosci. 23 (2003) 9595-9599
18. Li Q., Roberts A.C., and Glanzman D.L. Synaptic facilitation and behavioral dishabituation in Aplysia: Dependence on release of Ca2+ from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy. J. Neurosci. 25 (2005) 5623-5637
19. Wu C.L., Xia S., Fu T.F., Wang H., Chen Y.H., Leong D., Chiang A.S., and Tully T. Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat. Neurosci. 10 (2007) 1578-1586
20. Xia S., Miyashita T., Fu T.F., Lin W.Y., Wu C.L., Pyzocha L., Lin I.R., Saitoe M., Tully T., and Chiang A.S. NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15 (2005) 603-615
21. Si A., Helliwell P., and Maleszka R. Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera). Pharmacol. Biochem. Behav. 77 (2004) 191-197
22. Bliss T.V., and Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
23. Morris R.G., Anderson E., Lynch G.S., and Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319 (1986) 774-776
24. Nakazawa K., McHugh T.J., Wilson M.A., and Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 5 (2004) 361-372
25. Ezzeddine Y., and Glanzman D.L. Prolonged habituation of the gill-withdrawal reflex in Aplysia depends on protein synthesis, protein phosphatase activity, and postsynaptic glutamate receptors. J. Neurosci. 23 (2003) 9585-9594
26. Murphy G.G., and Glanzman D.L. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278 (1997) 467-471
27. Hart A.C., Sims S., and Kaplan J.M. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378 (1995) 82-85
28. Maricq A.V., Peckol E., Driscoll M., and Bargmann C.I. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378 (1995) 78-81
29. Mellem J.E., Brockie P.J., Zheng Y., Madsen D.M., and Maricq A.V. Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36 (2002) 933-944
30. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J., et al. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368 (1994) 32-38
31. Sawin E.R., Ranganathan R., and Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26 (2000) 619-631
32. Brockie P.J., Madsen D.M., Zheng Y., Mellem J., and Maricq A.V. 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 (2001) 1510-1522
33. Chalfie M., Sulston J.E., White J.G., Southgate E., Thomson J.N., and Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5 (1985) 956-964
34. Alkema M.J., Hunter-Ensor M., Ringstad N., and Horvitz H.R. Tyramine Functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46 (2005) 247-260
35. Hills T., Brockie P.J., and Maricq A.V. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J. Neurosci. 24 (2004) 1217-1225
36. Gray J.M., Hill J.J., and Bargmann C.I. A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 102 (2005) 3184-3191
37. Pierce-Shimomura J.T., Morse T.M., and Lockery S.R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci. 19 (1999) 9557-9569
38. Ryu W.S., and Samuel A.D. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined Thermal stimuli. J. Neurosci. 22 (2002) 5727-5733
39. Zariwala H.A., Miller A.C., Faumont S., and Lockery S.R. Step response analysis of thermotaxis in Caenorhabditis elegans. J. Neurosci. 23 (2003) 4369-4377
40. Farooqui T., Robinson K., Vaessin H., and Smith B.H. Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neurosci. 23 (2003) 5370-5380
41. Hammer M., and Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5 (1998) 146-156
42. Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., and Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23 (2003) 10495-10502
43. Unoki S., Matsumoto Y., and Mizunami M. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur. J. Neurosci. 22 (2005) 1409-1416
44. Bourne H.R., and Nicoll R. Molecular machines integrate coincident synaptic signals. Cell 72 (1993) 65-75
45. Mello C.C., Kramer J.M., Stinchcomb D., and Ambros V. Efficient gene transfer in C.elegans: Extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10 (1991) 3959-3970
46. Francis M.M., and Maricq A.V. Electrophysiological analysis of neuronal and muscle function in C. elegans. Methods Mol. Biol. 351 (2006) 175-192
47. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., and Bairoch A. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31 (2003) 3784-3788