TRPA1 mediates sensation of the rate of temperature change in Drosophila larvae

Nature Neuroscience

Volumn 20, Issue 1, 2017, Pages 34-41

  Luo, Junjie ^a,b   Shen, Wei L ^b,c   Montell, Craig ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHANGHAITECH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; DROSOPHILA PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPA1 PROTEIN, DROSOPHILA;

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ECTOPIC EXPRESSION; FEMALE; LOW TEMPERATURE; MALE; NONHUMAN; OOCYTE; PAIN THRESHOLD; PHENOTYPE; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; TEMPERATURE MEASUREMENT; TEMPERATURE SENSITIVITY; TRANSLATION INITIATION; TRPA1 GENE; VELOCITY; XENOPUS LAEVIS; ADVERSE EFFECTS; ANIMAL; BRAIN; GROWTH, DEVELOPMENT AND AGING; HEAT; LARVA; METABOLISM; NERVE CELL; TEMPERATURE;

ANIMALS; BRAIN; DROSOPHILA; DROSOPHILA PROTEINS; HOT TEMPERATURE; LARVA; NEURONS; TEMPERATURE; TRPC CATION CHANNELS;

EID: 84991574384     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4416     Document Type: Article

References (62)

1. Julius, D. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29, 355-384 (2013).
2. Patapoutian, A., Peier, A.M., Story, G.M. & Viswanath, V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat. Rev. Neurosci. 4, 529-539 (2003).
3. Venkatachalam, K. & Montell, C. TRP channels. Annu. Rev. Biochem. 76, 387-417 (2007).
4. Venkatachalam, K., Luo, J. & Montell, C. Evolutionarily conserved, multitasking TRP channels: lessons from worms and flies. Handb. Exp. Pharmacol. 223, 937-962 (2014).
5. Caterina, M.J. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824 (1997).
6. Caterina, M.J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313 (2000).
7. Bautista, D.M. et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448, 204-208 (2007).
8. McKemy, D.D., Neuhausser, W.M. & Julius, D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52-58 (2002).
9. Peier, A.M. et al. A TRP channel that senses cold stimuli and menthol. Cell 108, 705-715 (2002).
10. Story, G.M. et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819-829 (2003).
11. Xiao, R. et al. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806-817 (2013).
12. Tracey, W.D. Jr., Wilson, R.I., Laurent, G. & Benzer, S. painless, a Drosophila gene essential for nociception. Cell 113, 261-273 (2003).
13. Lee, Y. et al. Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat. Genet. 37, 305-310 (2005).
14. Zhong, L. et al. Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat-sensor domains of a thermoTRP Channel. Cell Rep. 1, 43-55 (2012).
15. Neely, G.G. et al. TrpA1 regulates thermal nociception in Drosophila. PLoS One 6, e24343 (2011).
16. Kwon, Y., Shim, H.S., Wang, X. & Montell, C. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat. Neurosci. 11, 871-873 (2008).
17. Shen, W.L. et al. Function of rhodopsin in temperature discrimination in Drosophila. Science 331, 1333-1336 (2011).
18. Sedgwick, W.T. On variations of reflex-excitability in the frog, induced by changes of temperature. Stud. Biol. Lab., Johns Hopkins University 385 (1882).
19. Clark, D.A., Gabel, C.V., Lee, T.M. & Samuel, A.D. Short-term adaptation and temporal processing in the cryophilic response of Caenorhabditis elegans. J. Neurophysiol. 97, 1903-1910 (2007).
20. Green, B.G. & Akirav, C. Threshold and rate sensitivity of low-threshold thermal nociception. Eur. J. Neurosci. 31, 1637-1645 (2010).
21. Gershow, M. et al. Controlling airborne cues to study small animal navigation. Nat. Methods 9, 290-296 (2012).
22. Mitchell, T.M. Machine Learning (McGraw-Hill, 1997).
23. Manning, C.D., Raghavan, P. & Schütze, H. Introduction to Information Retrieval (Cambridge University Press, Cambridge, 2008).
24. Viswanath, V. et al. Opposite thermosensor in fruitfly and mouse. Nature 423, 822-823 (2003).
25. Sokabe, T., Tsujiuchi, S., Kadowaki, T. & Tominaga, M. Drosophila painless is a Ca2+-requiring channel activated by noxious heat. J. Neurosci. 28, 9929-9938 (2008).
26. Babcock, D.T. et al. Hedgehog signaling regulates nociceptive sensitization. Curr. Biol. 21, 1525-1533 (2011).
27. Oswald, M., Rymarczyk, B., Chatters, A. & Sweeney, S.T. A novel thermosensitive escape behavior in Drosophila larvae. Fly (Austin) 5, 304-306 (2011).
28. Ni, L. et al. A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500, 580-584 (2013).
29. Kang, K. et al. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481, 76-80 (2011).
30. Kim, S.H. et al. Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc. Natl. Acad. Sci. USA 107, 8440-8445 (2010).
31. Kondo, S. & Ueda, R. Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics 195, 715-721 (2013).
32. Yu, Z. et al. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics 195, 289-291 (2013).
33. Gratz, S.J. et al. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194, 1029-1035 (2013).
34. Bassett, A.R., Tibbit, C., Ponting, C.P. & Liu, J.L. Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep. 4, 220-228 (2013).
35. Klapoetke, N.C. et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346 (2014).
36. Gordon, M.D. & Scott, K. Motor control in a Drosophila taste circuit. Neuron 61, 373-384 (2009).
37. Chen, T.W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
38. Wang, Y.Y., Chang, R.B., Waters, H.N., McKemy, D.D. & Liman, E.R. The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J. Biol. Chem. 283, 32691-32703 (2008).
39. Jordt, S.E. et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265 (2004).
40. Nagata, K., Duggan, A., Kumar, G. & García-Añoveros, J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25, 4052-4061 (2005).
41. Zurborg, S., Yurgionas, B., Jira, J.A., Caspani, O. & Heppenstall, P.A. Direct activation of the ion channel TRPA1 by Ca2+. Nat. Neurosci. 10, 277-279 (2007).
42. Stoney, S.D. Jr. & Machne, X. Mechanisms of accommodation in different types of frog neurons. J. Gen. Physiol. 53, 248-262 (1969).
43. Hamada, F.N. et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220 (2008).
44. Kwon, Y. et al. Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr. Biol. 20, 1672-1678 (2010).
45. Bellen, H.J. et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761-781 (2004).
46. Zhong, L., Hwang, R.Y. & Tracey, W.D. Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr. Biol. 20, 429-434 (2010).
47. Baines, R.A., Uhler, J.P., Thompson, A., Sweeney, S.T. & Bate, M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531 (2001).
48. Berni, J., Pulver, S.R., Griffith, L.C. & Bate, M. Autonomous circuitry for substrate exploration in freely moving Drosophila larvae. Curr. Biol. 22, 1861-1870 (2012).
49. Shearin, H.K., Macdonald, I.S., Spector, L.P. & Stowers, R.S. Hexameric GFP and mCherry reporters for the Drosophila GAL4, Q, and LexA transcription systems. Genetics 196, 951-960 (2014).
50. Duffy, J.B., Harrison, D.A. & Perrimon, N. Identifying loci required for follicular patterning using directed mosaics. Development 125, 2263-2271 (1998).
51. Inagaki, H.K. et al. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11, 325-332 (2014).
52. Taghert, P.H. et al. Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J. Neurosci. 21, 6673-6686 (2001).
53. Pfeiffer, B.D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105, 9715-9720 (2008).
54. Ni, J.Q. et al. A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182, 1089-1100 (2009).
55. Ohyama, T. et al. High-throughput analysis of stimulus-evoked behaviors in Drosophila larva reveals multiple modality-specific escape strategies. PLoS One 8, e71706 (2013).
56. Ben-Ialli, A., Bohuon, P., Collignan, A. & Méot, J.-M. Modeling heat transfer for disinfestation and control of insects (larvae and eggs) in date fruits. J. Food Eng. 116, 505-514 (2013).
57. Gong, W.J. & Golic, K.G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 100, 2556-2561 (2003).
58. Moon, S.J., Lee, Y., Jiao, Y. & Montell, C. A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 1623-1627 (2009).
59. DeCoursey, T.E. & Cherny, V.V. Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J. Gen. Physiol. 112, 503-522 (1998).
60. Klein, M. et al. Sensory determinants of behavioral dynamics in Drosophila thermotaxis. Proc. Natl. Acad. Sci. USA 112, E220-E229 (2015).
61. Ohyama, T. et al. A multilevel multimodal circuit enhances action selection in Drosophila. Nature 520, 633-639 (2015).
62. Gracheva, E.O. et al. Molecular basis of infrared detection by snakes. Nature 464, 1006-1011 (2010).