Gustatory receptor neurons in manduca sexta contain a TrpA1-dependent signaling pathway that integrates taste and temperature

Chemical Senses

Volumn 38, Issue 7, 2013, Pages 605-617

  Afroz, Anika ^a   Howlett, Natalie ^a   Shukla, Aditi ^a   Ahmad, Farah ^a   Batista, Elizabeth ^a   Bedard, Katie ^a   Payne, Sara ^a   Morton, Brian ^a   Mansfield, Jennifer H ^a   Glendinning, John I ^a  

^a Program on US Russia Relations at Columbia s Harriman Institute   (United States)

Author keywords

Aristolochic acid; Insect; Taste; Temperature; Trpa1

Indexed keywords

ARISTOLOCHIC ACID; CAFFEINE; COMPLEMENTARY DNA; GLUCOSE; INOSITOL; MECAMYLAMINE; N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; SUCROSE; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; DNA SYNTHESIS; EXCITATORY JUNCTION POTENTIAL; GENE IDENTIFICATION; GUSTATORY SYSTEM; INSECT GENETICS; LARVA; MANDUCA SEXTA; MAXILLA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REARING; RNA EXTRACTION; SENSILLUM; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TASTE; TEMPERATURE; TEMPERATURE DEPENDENCE; THERMOREGULATION; THERMOSTABILITY; TRPA1 GENE;

ARISTOLOCHIC ACID; INSECT; TASTE; TEMPERATURE; TRPA1;

ACETANILIDES; ANIMALS; ARISTOLOCHIC ACIDS; CAFFEINE; INSECT PROTEINS; MANDUCA; MAXILLA; NEURONS; PURINES; RECEPTORS, CELL SURFACE; SENSILLA; SIGNAL TRANSDUCTION; TASTE; TEMPERATURE; TRPC CATION CHANNELS;

EID: 84882992512     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjt032     Document Type: Article

References (54)

1. Adolph AR. 1973. Thermal sensitivity of lateral inhibition in Limulus eye. J Gen Physiol. 62(4):392-406.
2. Aho AC, Donner K, Reuter T. 1993. Retinal origins of the temperature effect on absolute visual sensitivity in frogs. J Physiol. 463:501-521.
3. Bell RA, Joachim FA. 1976. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am. 69:365-373.
4. Bernays EA, Chapman RF. 1994. Host-plant selection by phytophagous insects. New York: Chapman & Hall.
5. Bestmann HJ, Dippold K. 1983. Temperaturabhiingigkeit von elektroantennogrammen bei Lepidopteren. Naturwissensch. 70:47-48.
6. Bestmann HJ, Dippold K. 1989. Temperature dependence of electrophysiological responses of Lepidopteran antennae. Z Naturforsch. 44c:333-344.
7. Breza JM, Curtis KS, Contreras RJ. 2006. Temperature modulates taste responsiveness and stimulates gustatory neurons in the rat geniculate ganglion. J Neurophysiol. 95(2):674-685.
8. Casey TM. 1976. Activity patterns, body temperature and thermal ecology in two desert caterpillars (Lepidoptera: Sphingidae). Ecology. 57:485-497.
9. Cocco N, Glendinning JI. 2012. Not all sugars are created equal: some mask aversive tastes better than others in an herbivorous insect. J Exp Biol. 215(Pt 8):1412-1421.
10. de Boer G. 2006. The role of the antennae and maxillary palps in mediating food preference by larvae of the tobacco hornworm, Manduca sexta. Entomol Exp Appl. 119:29-38.
11. del Campo ML, Miles CI, Schroeder FC, Mueller C, Booker R, Renwick JA. 2001. Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature. 411(6834):186-189.
12. Diamond SE, Kingsolver JG. 2010. Environmental dependence of thermal reaction norms: host plant quality can reverse the temperature-size rule. Am Nat. 175(1):1-10.
13. Eid SR, Crown ED, Moore EL, Liang HA, Choong K, Dima S, Henze DA, Kane SA, Urban MO. 2008. HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity. Mol Pain. 48:1-10.
14. Fonseca PJ, Correia T. 2007. Effects of temperature on tuning of the auditory pathway in the cicada Tettigetta josei (Hemiptera, Tibicinidae). J Exp Biol. 210(Pt 10):1834-1845.
15. George NT, Sponberg S, Daniel TL. 2012. Temperature gradients drive mechanical energy gradients in the flight muscle of Manduca sexta. J Exp Biol. 215(Pt 3):471-479.
16. Gillary HL. 1966. Stimulation of the salt receptor of the blowfly. II. Temperature. J Gen Physiol. 50(2):351-357.
17. Glendinning JI, Davis A, Ramaswamy S. 2002. Contribution of different taste cells and signaling pathways to the discrimination of"bitter" taste stimuli by an insect. J Neurosci. 22(16):7281-7287.
18. Glendinning JI, Foley C, Loncar I, Rai M. 2009. Induced preference for host plant chemicals in the tobacco hornworm: contribution of olfaction and taste. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 195(6):591-601.
19. Glendinning JI, Hills TT. 1997. Electrophysiological evidence for two transduction pathways within a bitter-sensitive taste receptor. J Neurophysiol. 78(2):734-745.
20. Glendinning JI, Jerud A, Reinherz AT. 2007. The hungry caterpillar: an analysis of how carbohydrates stimulate feeding in Manduca sexta. J Exp Biol. 210(Pt 17):3054-3067.
21. Glendinning JI, Tarre M, Asaoka K. 1999. Contribution of different bittersensitive taste cells to feeding inhibition in a caterpillar (Manduca sexta). Behav Neurosci. 113(4):840-854.
22. Gothilf S, Hanson FE. 1994. A technique for electrophysiologically recording from chemosensory organs of intact caterpillars. Entomol Exp Appl. 72:304-310.
23. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA. 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature. 454(7201):217-220.
24. Howlett N, Dauber KL, Shukla A, Morton B, Glendinning JI, Brent E, Gleason C, Islam F, Izquierdo D, Sanghavi S, et al. 2012. Identification of chemosensory receptor genes in Manduca sexta and knockdown by RNA interference. BMC Genomics. 13:211.
25. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MA, Garrity PA. 2012. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature. 481(7379):76-80.
26. Kester KM, Peterson SC, Hanson F, Jackson M, Severson RF. 2002. The roles of nicotine and natural enemies in determining larval feeding site distributions of Manduca sexta L. and Manduca quinquemaculata (Haworth) on tobacco. Chemoecology. 12:1-10.
27. Kim SH, Lee Y, Akitake B, Woodward OM, Guggino WB, Montell C. 2010. Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc Natl Acad Sci USA. 107(18):8440-8445.
28. Kwon Y, Kim SH, Ronderos DS, Lee Y, Akitake B, Woodward OM, Guggino WB, Smith DP, Montell C. 2010. Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr Biol. 20(18):1672-1678.
29. Kwon Y, Shim HS, Wang X, Montell C. 2008. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat Neurosci. 11(8):871-873.
30. Lu B, Breza JM, Nikonov AA, Paedae AB, Contreras RJ. 2012. Leptin increases temperature-dependent chorda tympani nerve responses to sucrose in mice. Physiol Behav. 107(4):533-539.
31. Madden AH, Chamberlin FS. 1945. Biology of the tobacco hornworm in the southern cigar-tobacco district. USDA Technical Bull. 896:1-51.
32. Martin F, Riveron J, Alcorta E. 2011. Environmental temperature modulates olfactory reception in Drosophila melanogaster. J Insect Physiol. 57(12):1631-1642.
33. Matsuura H, Sokabe T, Kohno K, Tominaga M, Kadowaki T. 2009. Evolutionary conservation and changes in insect TRP channels. BMC Evol Biol. 9:228.
34. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, et al. 2007. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA. 104(33):13525-13530.
35. Nagaki J, Yamashita S, Sato M. 1964. Neural response of cat to taste stimuli of varying temperatures. Jpn J Physiol. 14:67-89.
36. Nakamura M, Kurihara K. 1991. Differential temperature dependence of taste nerve responses to various taste stimuli in dogs and rats. Am J Physiol. 261(6 Pt 2):R1402-R1408.
37. Nelson N, Bernays EA. 1998. Inositol in two host plants of Manduca sexta. Entomol Exp Appl. 88:189-191.
38. Ohkuri T, Yasumatsu K, Horio N, Jyotaki M, Margolskee RF, Ninomiya Y. 2009. Multiple sweet receptors and transduction pathways revealed in knockout mice by temperature dependence and gurmarin sensitivity. Am J Physiol Regul Integr Comp Physiol. 296(4):R960-R971.
39. Rall JA, Woledge RC. 1990. Influence of temperature on mechanics and energetics of muscle contraction. Am J Physiol. 259(2 Pt 2):R197-R203.
40. Reynolds SE, Yoemans MR, Timmins WA. 1986. The feeding behavior or caterpillars (Manduca sexta) on tobacco and artificial diet. Physiol Entomol. 11:39-51.
41. Samczynski Z, Dybczynski RS, Polkowska-Motrenko H, Chajduk E, Pyszynska M, Danko B, Czerska E, Kulisa K, Doner K, Kalbarczyk P. 2012. Two new reference materials based on tobacco leaves: certification for over a dozen of toxic and essential elements. ScientificWorld J. 2012:216380.
42. Schoonhoven LM. 1972. Plant recognition by lepidopterous larvae. In: van Emden HF, editors. Insect/plant relationships. Oxford: Blackwell Scientific Publications. p. 87-99.
43. Shoji T, Abe Y, Furihata E, Kurihara K. 1994. High sensitivity of the turtle olfactory system to nonvolatile substances: comparison of response properties with those in gustatory systems. Brain Res. 666(1):68-76.
44. Snyder MJ, Glendinning JI. 1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J Comp Physiol A. 179(2):255-261.
45. Stamp N, Yang Y. 1996. Response of insect herbivores to multiple allelochemicals under different thermal regimes. Ecology. 77:1088-1102.
46. Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, et al. 2009. Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci. 12(10):1293-1299.
47. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B. 2005. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature. 438(7070):1022-1025.
48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28(10):2731-2739.
49. Uehara S, Morita H. 1972. The effects of temperature on the labellar chemoreceptors of the blowfly. J Gen Physiol. 59(2):213-226.
50. Venkatachalam K, Montell C. 2007. TRP channels. Annu Rev Biochem. 76:387-417.
51. Waldbauer GP, Fraenkel G. 1961. Feeding on normally rejected plants by maxillectomized larvae of the tobacco hornworm, Protoparce sexta (Lepidoptera: Sphingidae). Ann Entomol Soc Am. 54:477-485.
52. Yamashita S. 1964. Chemoreceptor response in frog, as modified by temperature change. Jpn J Physiol. 14:488-504.
53. Yamashita S, Ogawa H, Kiyoara T, Sato M. 1970. Modification by temperature change of gustatory impulse discharges in chorda tympani fibres of rats. Jpn J Physiol. 20(3):348-363.
54. Yamashita S, Yamada K, Sato M. 1964. The effect of temperature on neural taste response of cats. Jpn J Physiol. 14:505-514.