Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal.
Plants produce insect repellents, such as citronellal, which is the main component of citronellal oil. However, the molecular pathways through which insects sense botanical repellents are unknown. Here, we show that Drosophila use two pathways for direct avoidance of citronellal. The olfactory coreceptor OR83b contributes to citronellal repulsion and is essential for citronellal-evoked action potentials. Mutations affecting the Ca(2+)-permeable cation channel TRPA1 result in a comparable defect in avoiding citronellal vapor. The TRPA1-dependent aversion to citronellal relies on a G protein (Gq)/phospholipase C (PLC) signaling cascade rather than direct detection of citronellal by TRPA1. Loss of TRPA1, Gq, or PLC causes an increase in the frequency of citronellal-evoked action potentials in olfactory receptor neurons. Absence of the Ca(2+)-activated K(+) channel (BK channel) Slowpoke results in a similar impairment in citronellal avoidance and an increase in the frequency of action potentials. These results suggest that TRPA1 is required for activation of a BK channel to modulate citronellal-evoked action potentials and for aversion to citronellal. In contrast to Drosophila TRPA1, Anopheles gambiae TRPA1 is directly and potently activated by citronellal, thereby raising the possibility that mosquito TRPA1 may be a target for developing improved repellents to reduce insect-borne diseases such as malaria.
Kwon
Young
Y
Department of Biological Chemistry, Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Kim
Sang Hoon
SH
Ronderos
David S
DS
Lee
Youngseok
Y
Akitake
Bradley
B
Woodward
Owen M
OM
Guggino
William B
WB
Smith
Dean P
DP
Montell
Craig
C
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000080462:Acyclic Monoterpenes; D000447:Aldehydes / Q000494:pharmacology*; D000818:Animals; D000852:Anopheles / Q000187:drug effects / Q000378:metabolism; D001522:Behavior, Animal; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000187:drug effects / Q000378:metabolism; D005260:Female; D007302:Insect Repellents / Q000494:pharmacology*; D007473:Ion Channels; D051036:Large-Conductance Calcium-Activated Potassium Channels / Q000378:metabolism; D008297:Male; D039821:Monoterpenes / Q000494:pharmacology*; D000074025:TRPA1 Cation Channel; D050052:TRPC Cation Channels / Q000235:genetics / Q000378:metabolism*
D000080462:Acyclic Monoterpenes; D000447:Aldehydes; D029721:Drosophila Proteins; D007302:Insect Repellents; D007473:Ion Channels; D051036:Large-Conductance Calcium-Activated Potassium Channels; D039821:Monoterpenes; D000074025:TRPA1 Cation Channel; D050052:TRPC Cation Channels; C475684:TrpA1 protein, Drosophila; C108217:citronellal
Front Cell Neurosci. 2009 Sep 09;3:10
19826623
Cell. 2002 Mar 8;108(5):705-15
11893340
Fly (Austin). 2009 Oct-Dec;3(4):290-7
19786837
Curr Biol. 2005 May 24;15(10):929-34
15916949
Handb Exp Pharmacol. 2009;(194):563-87
19655118
Eur J Neurosci. 2009 Sep;30(6):967-74
19735290
Nature. 2010 Mar 25;464(7288):597-600
20237474
Proc Natl Acad Sci U S A. 2010 May 4;107(18):8440-5
20404155
Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12248-52
16103371
Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17542-7
17956991
Annu Rev Biochem. 2007;76:387-417
17579562
J Econ Entomol. 2001 Dec;94(6):1584-8
11777068
J Neurosci. 2003 Oct 29;23(30):9906-12
14586020
Nat Neurosci. 2008 Aug;11(8):871-3
18660806
J Cell Physiol. 2007 Aug;212(2):348-57
17523149
Cell. 2003 Dec 12;115(6):655-66
14675531
Annu Rev Neurosci. 2007;30:505-33
17506643
Cell Calcium. 2009 Mar;45(3):300-9
19135721
Science. 2008 Mar 28;319(5871):1838-42
18339904
Nature. 2008 Jul 10;454(7201):217-20
18548007
Crit Rev Oral Biol Med. 2000;11(1):4-25
10682899
Nature. 1997 Oct 23;389(6653):816-24
9349813
Pflugers Arch. 2007 Aug;454(5):749-58
17205355
Nature. 2004 Jan 15;427(6971):260-5
14712238
Neuron. 2004 Sep 2;43(5):703-14
15339651
J Am Acad Dermatol. 2008 May;58(5):865-71
18272250
Curr Opin Neurobiol. 2007 Aug;17(4):490-7
17706410
Nature. 2003 Jun 19;423(6942):822-3
12815418
Curr Biol. 1999 Nov 4;9(21):1267-70
10556094
Neuron. 2001 May;30(2):537-52
11395013
Nature. 2002 Mar 7;416(6876):52-8
11882888
PLoS One. 2008 May 07;3(5):e2082
18461159
J Neurosci. 2001 Mar 1;21(5):1523-31
11222642