Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila

There has been disagreement over the functional roles of the painless gene product in the detection and subsequent behavioral aversion to the active ingredient in wasabi, allyl isothiocyanate (AITC). Originally, painless was reported to eliminate the behavioral aversion to AITC, although subsequent...

Full description

Bibliographic Details
Main Authors: Samantha J. Mandel, Madison L. Shoaf, Jason T. Braco, Wayne L. Silver, Erik C. Johnson
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncir.2018.00045/full
_version_ 1828832179423019008
author Samantha J. Mandel
Madison L. Shoaf
Jason T. Braco
Wayne L. Silver
Wayne L. Silver
Erik C. Johnson
Erik C. Johnson
author_facet Samantha J. Mandel
Madison L. Shoaf
Jason T. Braco
Wayne L. Silver
Wayne L. Silver
Erik C. Johnson
Erik C. Johnson
author_sort Samantha J. Mandel
collection DOAJ
description There has been disagreement over the functional roles of the painless gene product in the detection and subsequent behavioral aversion to the active ingredient in wasabi, allyl isothiocyanate (AITC). Originally, painless was reported to eliminate the behavioral aversion to AITC, although subsequent reports suggested that another trpA homolog, dTRPA1, was responsible for AITC aversion. We re-evaluated the role of the painless gene in the detection of AITC, employing several different behavioral assays. Using the proboscis extension reflex (PER) assay, we observed that AITC did not reduce PER frequencies in painless or dTRPA1 mutants but did in wild-type genotypes. Quantification of food intake showed a significant decline in food consumption in the presence of AITC in wild-type, but not painless mutants. We adapted an oviposition choice assay and found wild-type oviposit on substrates lacking AITC, in contrast to painless and dTRPA1 mutants. Lastly, tracking individual flies relative to a point source of AITC, showed a consistent clustering of wild-type animals away from the point source, which was absent in painless mutants. We evaluated expression patterns of both dTRPA1 and painless, which showed expression in distinct central and peripheral populations. We identified the transmitter phenotypes of subsets of painless and dTRPA1 neurons and found similar neuropeptides as those expressed by mammalian trpA expressing neurons. Using a calcium reporter, we observed AITC-evoked responses in both painless and dTRPA1 expressing neurons. Collectively, these results reaffirm the necessity of painless in nociceptive behaviors and suggest experiments to further resolve the molecular basis of aversion.
first_indexed 2024-12-12T16:48:49Z
format Article
id doaj.art-53be7bc8b1274904b0f81a67ea94ee95
institution Directory Open Access Journal
issn 1662-5110
language English
last_indexed 2024-12-12T16:48:49Z
publishDate 2018-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neural Circuits
spelling doaj.art-53be7bc8b1274904b0f81a67ea94ee952022-12-22T00:18:25ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102018-07-011210.3389/fncir.2018.00045350327Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in DrosophilaSamantha J. Mandel0Madison L. Shoaf1Jason T. Braco2Wayne L. Silver3Wayne L. Silver4Erik C. Johnson5Erik C. Johnson6Department of Biology, Wake Forest University, Winston-Salem, NC, United StatesDepartment of Biology, Wake Forest University, Winston-Salem, NC, United StatesDepartment of Biology, Wake Forest University, Winston-Salem, NC, United StatesDepartment of Biology, Wake Forest University, Winston-Salem, NC, United StatesCenter for Molecular Communication and Signaling, Wake Forest University, Winston-Salem, NC, United StatesDepartment of Biology, Wake Forest University, Winston-Salem, NC, United StatesCenter for Molecular Communication and Signaling, Wake Forest University, Winston-Salem, NC, United StatesThere has been disagreement over the functional roles of the painless gene product in the detection and subsequent behavioral aversion to the active ingredient in wasabi, allyl isothiocyanate (AITC). Originally, painless was reported to eliminate the behavioral aversion to AITC, although subsequent reports suggested that another trpA homolog, dTRPA1, was responsible for AITC aversion. We re-evaluated the role of the painless gene in the detection of AITC, employing several different behavioral assays. Using the proboscis extension reflex (PER) assay, we observed that AITC did not reduce PER frequencies in painless or dTRPA1 mutants but did in wild-type genotypes. Quantification of food intake showed a significant decline in food consumption in the presence of AITC in wild-type, but not painless mutants. We adapted an oviposition choice assay and found wild-type oviposit on substrates lacking AITC, in contrast to painless and dTRPA1 mutants. Lastly, tracking individual flies relative to a point source of AITC, showed a consistent clustering of wild-type animals away from the point source, which was absent in painless mutants. We evaluated expression patterns of both dTRPA1 and painless, which showed expression in distinct central and peripheral populations. We identified the transmitter phenotypes of subsets of painless and dTRPA1 neurons and found similar neuropeptides as those expressed by mammalian trpA expressing neurons. Using a calcium reporter, we observed AITC-evoked responses in both painless and dTRPA1 expressing neurons. Collectively, these results reaffirm the necessity of painless in nociceptive behaviors and suggest experiments to further resolve the molecular basis of aversion.https://www.frontiersin.org/article/10.3389/fncir.2018.00045/fullnociceptionDrosophilaTRPAallyl isothiocyanateaversion
spellingShingle Samantha J. Mandel
Madison L. Shoaf
Jason T. Braco
Wayne L. Silver
Wayne L. Silver
Erik C. Johnson
Erik C. Johnson
Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
Frontiers in Neural Circuits
nociception
Drosophila
TRPA
allyl isothiocyanate
aversion
title Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
title_full Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
title_fullStr Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
title_full_unstemmed Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
title_short Behavioral Aversion to AITC Requires Both Painless and dTRPA1 in Drosophila
title_sort behavioral aversion to aitc requires both painless and dtrpa1 in drosophila
topic nociception
Drosophila
TRPA
allyl isothiocyanate
aversion
url https://www.frontiersin.org/article/10.3389/fncir.2018.00045/full
work_keys_str_mv AT samanthajmandel behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT madisonlshoaf behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT jasontbraco behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT waynelsilver behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT waynelsilver behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT erikcjohnson behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila
AT erikcjohnson behavioralaversiontoaitcrequiresbothpainlessanddtrpa1indrosophila