Molecular biology of thermosensory transduction in C. elegans

Current Opinion in Neurobiology

Volumn 34, Issue , 2015, Pages 117-124

  Aoki, Ichiro ^a   Mori, Ikue ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; CAENORHABDITIS ELEGANS PROTEIN;

CAENORHABDITIS ELEGANS; DOWNSTREAM PROCESSING; ENVIRONMENTAL TEMPERATURE; GENETIC ANALYSIS; INTERNEURON; LOCOMOTION; MOLECULAR BIOLOGY; MOLECULAR GENETICS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STORAGE TEMPERATURE; TEMPERATURE SENSE; ANIMAL; GENETICS; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; MOLECULAR BIOLOGY; SIGNAL TRANSDUCTION; THERMOSENSING;

EID: 84925938397     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2015.03.011     Document Type: Review

References (56)

1. 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.
2. 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.
3. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
4. Kimura K.D., Miyawaki A., Matsumoto K., Mori I. The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 2004, 14:1291-1295.
5. Wasserman S., Beverly M., Bell H., Sengupta P. Regulation of response properties and operating range of the AFD thermosensory neurons by cGMP signaling. Curr Biol 2011, 21:353-362.
6. 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.
7. Clark D.A., Gabel C.V., Gabel H., Samuel A.D. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 2007, 27:6083-6090.
8. Yu Y.V., Bell H.W., Glauser D.A., Van Hooser S.D., Goodman M.B., Sengupta P. CaMKI-dependent regulation of sensory gene expression mediates experience-dependent plasticity in the operating range of a thermosensory neuron. Neuron 2014. 10.1016/j.neuron.2014.10.046.
9. Luo L., Cook N., Venkatachalam V., Martinez-Velazquez L.A., Zhang X., Calvo A.C., Hawk J., MacInnis B.L., Frank M., Ng J.H., et al. Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proc Natl Acad Sci U S A 2014, 111:2776-2781.
10. 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.
11. 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.
12. Wang D., O'Halloran D., Goodman M.B. GCY-8, PDE-2, and NCS-1 are critical elements of the cGMP-dependent thermotransduction cascade in the AFD neurons responsible for C. elegans thermotaxis. J Gen Physiol 2013, 142:437-449.
13. Satterlee J., 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.
14. Bacaj T., Tevlin M., Lu Y., Shaham S. Glia are essential for sensory organ function in C. elegans. Science 2008, 322:744-747.
15. 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.
16. Talavera K., Nilius B., Voets T. Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci 2008, 31:287-295.
17. Fu Y., Yau K.-W.W. Phototransduction in mouse rods and cones. Pflugers Arch 2007, 454:805-819.
18. Xiong W.H., Solessio E.C., Yau K.W. An unusual cGMP pathway underlying depolarizing light response of the vertebrate parietal-eye photoreceptor. Nat Neurosci 1998, 1:359-365.
19. 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.
20. Coburn C.M., Bargmann C.I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 1996, 17:695-706.
21. Smith H., Luo L., O'Halloran D., Guo D., Huang X.-Y., Samuel A., Hobert O. Defining specificity determinants of cGMP mediated gustatory sensory transduction in Caenorhabditis elegans. Genetics 2013, 194:885-901.
22. Komatsu H., Jin Y.H., L'Etoile N., Mori I., Bargmann C.I., Akaike N., Ohshima Y. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res 1999, 821:160-168.
23. 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.
24. 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.
25. 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.
26. Benito E., Barco A. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 2010, 33:230-240.
27. 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.
28. Russell J., Vidal-Gadea A., Makay A., Lanam C., Pierce-Shimomura J. Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2014. 10.1073/pnas.1322512111.
29. Murayama T., Takayama J., Fujiwara M., Maruyama I. Environmental alkalinity sensing mediated by the transmembrane guanylyl cyclase GCY-14 in C. elegans. Curr Biol 2013, 23:1007-1012.
30. Shen W.L., Kwon Y., Adegbola A.A., Luo J., Chess A., Montell C. Function of rhodopsin in temperature discrimination in Drosophila. Science 2011. 10.1126/science.1198904.
31. 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 2008, 320:803-807.
32. Biron D., Wasserman S., Thomas J., Samuel A., 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.
33. 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.
34. Hobert O., Mori I., Yamashita Y., Honda H., Ohshima Y., Liu Y., Ruvkun G. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 1997, 19:345-357.
35. 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.
36. Speese S., Petrie M., Schuske K., Ailion M., Ann K., Iwasaki K., Jorgensen E., Martin T. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J Neurosci 2007, 27:6150-6162.
37. 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.
38. 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.
39. Morgan A., Burgoyne R., Barclay J., Craig T., Prescott G., Ciufo L., Evans G., Graham M. Regulation of exocytosis by protein kinase C. Biochem Soc Trans 2005, 33:1341.
40. Sieburth D., Madison J., Kaplan J. PKC-1 regulates secretion of neuropeptides. Nat Neurosci 2007, 10:49-57.
41. Edwards M., Johnson J., Rankin K., Jenkins R., Maguire C., Morgan A., Burgoyne R., Barclay J. PKC-2 phosphorylation of UNC-18 Ser322 in AFD neurons regulates temperature dependency of locomotion. J Neurosci 2012, 32:7042-7051.
42. Sugi T., Nishida Y., Mori I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat Neurosci 2011, 14:984-992.
43. Conti B. Considerations on temperature, longevity and aging. Cell Mol Life Sci 2008, 65:1626-1630.
44. Xiao R., Zhang B., Dong Y., Gong J., Xu T., Liu J., Xu X.Z. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 2013, 152:806-817.
45. Wittenburg N., Baumeister R. Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proc Natl Acad Sci U S A 1999, 96:10477-10482.
46. Liu S., Schulze E., Baumeister R. Temperature- and touch-sensitive neurons couple CNG and TRPV channel activities to control heat avoidance in Caenorhabditis elegans. PLoS One 2012, 7.
47. Glauser D., Chen W., Agin R., MacInnis B., Goodman M. Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics 2011. 10.1534/genetics.111.127100.
48. Schild L.C., Zbinden L., Bell H.W., Yu Y.V., Sengupta P., Goodman M.B., Glauser D.A. The balance between cytoplasmic and nuclear CaM kinase-1 signaling controls the operating range of noxious heat avoidance. Neuron 2014. 10.1016/j.neuron.2014.10.039.
49. Chatzigeorgiou M., Yoo S., Watson J., Lee W.-H., Spencer W., Kindt K., Hwang S., Miller D., Treinin M., Driscoll M. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 2010, 13:861-868.
50. Savory F.R., Sait S.M., Hope I.A. DAF-16 and δ9 desaturase genes promote cold tolerance in long-lived Caenorhabditis elegans age-1 mutants. PLoS One 2011. 10.1371/journal.pone.0024550.
51. Murray P., Hayward S.A., Govan G.G., Gracey A.Y., Cossins A.R. An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2007, 104:5489-5494.
52. Ohta A., Ujisawa T., Sonoda S., Kuhara A. Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans. Nat Commun 2014, 5.
53. Julius D. TRP channels and pain. Annu Rev Cell Dev Biol 2013, 29:355-384.
54. Chao Y., Chen C., Lin Y., Breer H., Fleischer J., Yang R. Receptor guanylyl cyclase G is a novel thermosensory protein activated by cool temperatures. EMBO J 2014. 10.15252/embj.201489652.
55. Samuel A.D., Silva R.A., Murthy V.N. Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J Neurosci 2003, 23:373-376.
56. Oda S., Tomioka M., Iino Y. Neuronal plasticity regulated by the insulin-like signaling pathway underlies salt chemotaxis learning in Caenorhabditis elegans. J Neurophysiol 2011, 106:301-308.