Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons.
Mammalian sweet, bitter, and umami taste is mediated by a single transduction pathway that includes a phospholipase C (PLC)beta and one cation channel, TRPM5. However, in insects such as the fruit fly, Drosophila melanogaster, it is unclear whether different tastants, such as bitter compounds, are sensed in gustatory receptor neurons (GRNs) through one or multiple ion channels, as the cation channels required in insect GRNs are unknown. Here, we set out to explore additional sensory roles for the Drosophila TRPA1 channel, which was known to function in thermosensation. We found that TRPA1 was expressed in GRNs that respond to aversive compounds. Elimination of TRPA1 had no impact on the responses to nearly all bitter compounds tested, including caffeine, quinine, and strychnine. Rather, we found that TRPA1 was required in a subset of avoidance GRNs for the behavioral and electrophysiological responses to aristolochic acid. TRPA1 did not appear to be activated or inhibited directly by aristolochic acid. We found that elimination of the same PLC that leads to activation of TRPA1 in thermosensory neurons was also required in the TRPA1-expressing GRNs for avoiding aristolochic acid. Given that mammalian TRPA1 is required for responding to noxious chemicals, many of which cause pain and injury, our analysis underscores the evolutionarily conserved role for TRPA1 channels in chemical avoidance.
Kim
Sang Hoon
SH
Departmentsof Biological Chemistry and Neuroscience, Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Lee
Youngseok
Y
Akitake
Bradley
B
Woodward
Owen M
OM
Guggino
William B
WB
Montell
Craig
C
D000818:Animals; D030801:Animals, Genetically Modified; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000235:genetics / Q000378:metabolism*; D005260:Female; D007473:Ion Channels; D009474:Neurons / Q000378:metabolism; D009865:Oocytes / Q000378:metabolism; D011956:Receptors, Cell Surface / Q000235:genetics / Q000378:metabolism; D000074025:TRPA1 Cation Channel; D050052:TRPC Cation Channels / Q000235:genetics / Q000378:metabolism*; D013649:Taste; D013696:Temperature; D010738:Type C Phospholipases / Q000378:metabolism; D014982:Xenopus laevis
D029721:Drosophila Proteins; D007473:Ion Channels; D011956:Receptors, Cell Surface; D000074025:TRPA1 Cation Channel; D050052:TRPC Cation Channels; C475684:TrpA1 protein, Drosophila; C405956:gustatory receptor, Drosophila; D010738:Type C Phospholipases
Cell. 1996 May 31;85(5):651-9
8646774
Cell. 2006 Mar 24;124(6):1269-82
16564016
J Neurophysiol. 1997 Aug;78(2):734-45
9307108
J Clin Invest. 2005 Sep;115(9):2393-401
16110328
Curr Biol. 2001 Sep 18;11(18):1451-5
11566105
Nat Neurosci. 2009 Oct;12(10):1293-9
19749751
Curr Biol. 2006 May 23;16(10):1034-40
16647259
Curr Biol. 2006 Sep 19;16(18):1812-7
16979558
J Cell Biol. 2005 Nov 21;171(4):685-94
16301334
Cell. 2003 Mar 21;112(6):819-29
12654248
Curr Biol. 2005 May 24;15(10):929-34
15916949
Pflugers Arch. 2005 Oct;451(1):19-28
15952038
Nat Neurosci. 2002 Nov;5(11):1169-76
12368808
Curr Biol. 2008 Nov 25;18(22):1797-801
19026541
Curr Biol. 2001 Jun 5;11(11):822-35
11516643
Nat Neurosci. 2008 Aug;11(8):871-3
18660806
Cell. 2003 Apr 18;113(2):261-73
12705873
J Neurochem. 2004 May;89(4):998-1008
15140198
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2556-61
12589026
Genes Dev. 2005 Feb 15;19(4):419-24
15681611
J Biol Chem. 1996 Mar 1;271(9):4937-45
8617767
Neuron. 2004 Mar 25;41(6):849-57
15046718
J Neurosci. 2008 Oct 1;28(40):10102-10
18829968
Neuron. 2006 Apr 20;50(2):277-89
16630838
Curr Biol. 2004 Jun 22;14(12):1065-79
15202999
Zoolog Sci. 2002 Sep;19(9):1009-18
12362054
Curr Biol. 2009 Oct 13;19(19):1623-7
19765987
Nature. 2000 May 11;405(6783):183-7
10821274
Annu Rev Neurosci. 2007;30:505-33
17506643
Nature. 2008 Jul 10;454(7201):217-20
18548007
Nature. 2004 Jan 15;427(6971):260-5
14712238
Curr Biol. 2007 Oct 23;17(20):1809-16
17919910
J Neurobiol. 2003 Aug;56(2):139-52
12838579
Nature. 2005 Dec 15;438(7070):1022-5
16355226
Cell. 2003 Feb 7;112(3):293-301
12581520
Nature. 2003 Jun 19;423(6942):822-3
12815418
Cell. 2004 Jun 25;117(7):981-91
15210117
Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12248-52
16103371
Nature. 2006 Nov 16;444(7117):302-7
17108954
J Neurosci. 2002 Aug 15;22(16):7281-7
12177223
Proc Natl Acad Sci U S A. 2009 Jan 27;106(4):1273-8
19144922
Science. 2000 Apr 14;288(5464):306-13
10764638
Nature. 2003 Jul 3;424(6944):81-4
12819662
Nat Neurosci. 2007 May;10(5):568-77
17450139
Annu Rev Biochem. 2007;76:387-417
17579562
Curr Opin Neurobiol. 2009 Aug;19(4):345-53
19660932
Neuron. 2007 Nov 8;56(3):503-16
17988633
Proc Natl Acad Sci U S A. 2007 Aug 28;104(35):14110-5
17715294
Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4495-500
19246397
Nat Neurosci. 2001 Dec;4(12):1182-6
11704765