Molecular mechanism for trimetric G protein-coupled thermosensation and synaptic regulation in the temperature response circuit of Caenorhabditis elegans

Neuroscience Research

Volumn 76, Issue 3, 2013, Pages 119-124

  Ohta, Akane ^a   Kuhara, Atsushi ^a  

^a KONAN UNIVERSITY   (Japan)

Author keywords

C. elegans; Calcium imaging; Neural circuit; Temperature response

Indexed keywords

CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CHLORIDE CHANNEL; CHLORIDE ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC GMP; DIACYLGLYCEROL KINASE; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; GUANYLATE CYCLASE; HALORHODOPSIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; VESICULAR GLUTAMATE TRANSPORTER;

ADAPTATION; ARTICLE; CAENORHABDITIS ELEGANS; HEAT SENSATION; INTERNEURON; MEMORY CONSOLIDATION; MOLECULAR BIOLOGY; MOLECULAR GENETICS; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; REGULATORY MECHANISM; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; TEMPERATURE SENSE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GTP-BINDING PROTEINS; MEMORY; NEURAL PATHWAYS; SENSORY RECEPTOR CELLS; SYNAPTIC TRANSMISSION; THERMOSENSING;

EID: 84879016217     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2013.03.008     Document Type: Article

References (41)

1. Bargmann C.I., Hartwieg E., Horvitz H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 1993, 74:515-527.
2. Bargmann C.I., Kaplan J.M. Signal transduction in the Caenorhabditis elegans nervous system. Annu. Rev. Neurosci. 1998, 21:279-308.
3. Beverly M., Anbil S., Sengupta P. Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans. J. Neurosci. 2011, 31:11718-11727.
4. Biron D., Shibuya M., Gabel C., Wasserman S.M., Clark D.A., Brown A., Sengupta P., Samuel A.D. A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nat. Neurosci. 2006, 9:1499-1505.
5. Biron D., Wasserman S., Thomas J.H., Samuel A.D., Sengupta P. An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:11002-11007.
6. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
7. Chatzigeorgiou M., Yoo S., Watson J.D., Lee W.H., Spencer W.C., Kindt K.S., Hwang S.W., Miller D.M., Treinin M., Driscoll M., Schafer W.R. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 2010, 13:861-868.
8. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426:517-524.
9. Clark D.A., Biron D., Sengupta P., Samuel A.D. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J. Neurosci. 2006, 26:7444-7451.
10. de Bono M., Maricq A.V. Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 2005, 28:451-501.
11. Dhaka A., Viswanath V., Patapoutian A. Trp ion channels and temperature sensation. Annu. Rev. Neurosci. 2006, 29:135-161.
12. Greer P.L., Greenberg M.E. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 2008, 59:846-860.
13. Han X., Boyden E.S. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PloS ONE 2007, 2:e299.
14. Han X., Qian X., Stern P., Chuong A.S., Boyden E.S. Informational lesions: optical perturbation of spike timing and neural synchrony via microbial opsin gene fusions. Front. Mol. Neurosci. 2009, 2:12.
15. Hedgecock E.M., Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:4061-4065.
16. Inada H., Ito H., Satterlee J., Sengupta P., Matsumoto K., Mori I. Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 2006, 172:2239-2252.
17. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science (New York, NY) 2001, 294:1030-1038.
18. Kimata T., Sasakura H., Ohnishi N., Nishio N., Mori I. Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity. Worm 2012, 1:31-41.
19. Kimura K.D., Miyawaki A., Matsumoto K., Mori I. The C. elegans thermosensory neuron AFD responds to warming. Curr. Biol. 2004, 14:1291-1295.
20. Komatsu H., Mori I., Rhee J.S., Akaike N., Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 1996, 17:707-718.
21. Kuhara A., Inada H., Katsura I., Mori I. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 2002, 33:751-763.
22. Kuhara A., Mori I. Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. J. Neurosci. 2006, 26:9355-9364.
23. Kuhara A., Ohnishi N., Shimowada T., Mori I. Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans. Nat. Commun. 2011, 2:355.
24. Kuhara A., Okumura M., Kimata T., Tanizawa Y., Takano R., Kimura K.D., Inada H., Matsumoto K., Mori I. Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science (New York, NY) 2008, 320:803-807.
25. Mori I. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans [In Process Citation]. Annu. Rev. Genet. 1999, 33:399-422.
26. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
27. Mori I., Sasakura H., Kuhara A. Worm thermotaxis: a model system for analyzing thermosensation and neural plasticity. Curr. Opin. Neurobiol. 2007, 17:712-719.
28. Morimoto R.I. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 1998, 12:3788-3796.
29. Narayan A., Laurent G., Sternberg P.W. Transfer characteristics of a thermosensory synapse in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9667-9672.
30. Nishida Y., Sugi T., Nonomura M., Mori I. Identification of the AFD neuron as the site of action of the CREB protein in Caenorhabditis elegans thermotaxis. EMBO Rep. 2011, 12:855-862.
31. Ohnishi N., Kuhara A., Nakamura F., Okochi Y., Mori I. Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO J. 2011, 30:1376-1388.
32. Okochi Y., Kimura K.D., Ohta A., Mori I. Diverse regulation of sensory signaling by C. elegans nPKC-epsilon/eta TTX-4. EMBO J. 2005, 24:2127-2137.
33. Patapoutian A., Peier A.M., Story G.M., Viswanath V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat. Rev. Neurosci. 2003, 4:529-539.
34. Ramot D., MacInnis B.L., Goodman M.B. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat. Neurosci. 2008, 11:908-915.
35. Sasakura H., Mori I. Behavioral plasticity, learning, and memory in C. elegans. Curr. Opin. Neurobiol. 2013, 23:92-99.
36. Satterlee J.S., Ryu W.S., Sengupta P. The CMK-1 CaMKI and the TAX-4 cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans. Curr. Biol. 2004, 14:62-68.
37. Satterlee J.S., Sasakura H., Kuhara A., Berkeley M., Mori I., Sengupta P. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 2001, 31:943-956.
38. Sugi T., Nishida Y., Mori I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat. Neurosci. 2011, 14:984-992.
39. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
40. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1986, 314:1-340.
41. Zhang F., Wang L.P., Brauner M., Liewald J.F., Kay K., Watzke N., Wood P.G., Bamberg E., Nagel G., Gottschalk A., Deisseroth K. Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446:633-639.