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Effects of Food Components That Activate TRPA1 Receptors on Mucosal Ion Transport in the Mouse Intestine

Identifieur interne : 003D02 ( Ncbi/Curation ); précédent : 003D01; suivant : 003D03

Effects of Food Components That Activate TRPA1 Receptors on Mucosal Ion Transport in the Mouse Intestine

Auteurs : Linda J. Fothergill ; Brid Callaghan ; Leni R. Rivera [Australie] ; Tinamarie Lieu ; Daniel P. Poole ; Hyun-Jung Cho ; David M. Bravo ; John B. Furness [Australie]

Source :

RBID : PMC:5084011

Descripteurs français

English descriptors

Abstract

TRPA1 is a ligand-activated cation channel found in the intestine and other tissues. Components of food that stimulate TRPA1 receptors (phytonutrients) include allyl isothiocyanate, cinnamaldehyde and linalool, but these may also act at other receptors. Cells lining the intestinal mucosa are immunoreactive for TRPA1 and Trpa1 mRNA occurs in mucosal extracts, suggesting that the TRPA1 receptor is the target for these agonists. However, in situ hybridisation reveals Trpa1 expression in 5-HT containing enteroendocrine cells, not enterocytes. TRPA1 agonists evoke mucosal secretion, which may be indirect (through release of 5-HT) or direct by activation of enterocytes. We investigated effects of the phytonutrients on transmucosal ion currents in mouse duodenum and colon, and the specificity of the phytonutrients in cells transfected with Trpa1, and in Trpa1-deficient mice. The phytonutrients increased currents in the duodenum with the relative potencies: allyl isothiocyanate (AITC) > cinnamaldehyde > linalool (0.1 to 300 μM). The rank order was similar in the colon, but linalool was ineffective. Responses to AITC were reduced by the TRPA1 antagonist HC-030031 (100 μM), and were greatly diminished in Trpa1−/− duodenum and colon. Responses were not reduced by tetrodotoxin, 5-HT receptor antagonists, or atropine, but inhibition of prostaglandin synthesis reduced responses. Thus, functional TRPA1 channels are expressed by enterocytes of the duodenum and colon. Activation of enterocyte TRPA1 by food components has the potential to facilitate nutrient absorption.


Url:
DOI: 10.3390/nu8100623
PubMed: 27735854
PubMed Central: 5084011

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PMC:5084011

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<name sortKey="Bravo, David M" sort="Bravo, David M" uniqKey="Bravo D" first="David M." last="Bravo">David M. Bravo</name>
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<name sortKey="Lieu, Tinamarie" sort="Lieu, Tinamarie" uniqKey="Lieu T" first="Tinamarie" last="Lieu">Tinamarie Lieu</name>
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<name sortKey="Poole, Daniel P" sort="Poole, Daniel P" uniqKey="Poole D" first="Daniel P." last="Poole">Daniel P. Poole</name>
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<nlm:aff id="af1-nutrients-08-00623">Department of Anatomy & Neuroscience, University of Melbourne, Parkville VIC 3010, Australia;
<email>b.callaghan@unimelb.edu.ac</email>
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<name sortKey="Cho, Hyun Jung" sort="Cho, Hyun Jung" uniqKey="Cho H" first="Hyun-Jung" last="Cho">Hyun-Jung Cho</name>
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<nlm:aff id="af4-nutrients-08-00623">Biological Optical Microscopy Platform, University of Melbourne, Parkville VIC 3010, Australia;
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<name sortKey="Bravo, David M" sort="Bravo, David M" uniqKey="Bravo D" first="David M." last="Bravo">David M. Bravo</name>
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<nlm:aff id="af5-nutrients-08-00623">In Vivo Animal Nutrition & Health, Talhouët, Saint-Nolff 56250, France;
<email>david.bravo@pancosma.ch</email>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Furness, John B" sort="Furness, John B" uniqKey="Furness J" first="John B." last="Furness">John B. Furness</name>
<affiliation>
<nlm:aff id="af1-nutrients-08-00623">Department of Anatomy & Neuroscience, University of Melbourne, Parkville VIC 3010, Australia;
<email>b.callaghan@unimelb.edu.ac</email>
(B.C.);
<email>leni.rivera@deakin.edu.au</email>
(L.R.R.);
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<series>
<title level="j">Nutrients</title>
<idno type="eISSN">2072-6643</idno>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Acrolein (analogs & derivatives)</term>
<term>Acrolein (pharmacology)</term>
<term>Animals</term>
<term>Calcium (metabolism)</term>
<term>Colon (physiology)</term>
<term>Duodenum (physiology)</term>
<term>Electrophysiological Phenomena</term>
<term>Enterocytes (drug effects)</term>
<term>Enterocytes (metabolism)</term>
<term>Food</term>
<term>Gene Expression</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Intestinal Mucosa (chemistry)</term>
<term>Intestinal Mucosa (physiology)</term>
<term>Isothiocyanates (pharmacology)</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
<term>Monoterpenes (pharmacology)</term>
<term>Phytochemicals (pharmacology)</term>
<term>Serotonin 5-HT3 Receptor Antagonists (pharmacology)</term>
<term>Transfection</term>
<term>Transient Receptor Potential Channels (deficiency)</term>
<term>Transient Receptor Potential Channels (drug effects)</term>
<term>Transient Receptor Potential Channels (genetics)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acroléine (analogues et dérivés)</term>
<term>Acroléine (pharmacologie)</term>
<term>Aliments</term>
<term>Animaux</term>
<term>Antagonistes des récepteurs 5-HT3 de la sérotonine (pharmacologie)</term>
<term>Calcium (métabolisme)</term>
<term>Canaux cationiques TRP ()</term>
<term>Canaux cationiques TRP (déficit)</term>
<term>Canaux cationiques TRP (génétique)</term>
<term>Cellules HEK293</term>
<term>Composés phytochimiques (pharmacologie)</term>
<term>Côlon (physiologie)</term>
<term>Duodénum (physiologie)</term>
<term>Entérocytes ()</term>
<term>Entérocytes (métabolisme)</term>
<term>Expression des gènes</term>
<term>Humains</term>
<term>Isothiocyanates (pharmacologie)</term>
<term>Monoterpènes (pharmacologie)</term>
<term>Muqueuse intestinale ()</term>
<term>Muqueuse intestinale (physiologie)</term>
<term>Mâle</term>
<term>Phénomènes électrophysiologiques</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris knockout</term>
<term>Transfection</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en">
<term>Acrolein</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="deficiency" xml:lang="en">
<term>Transient Receptor Potential Channels</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="drug effects" xml:lang="en">
<term>Transient Receptor Potential Channels</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Transient Receptor Potential Channels</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Calcium</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Acrolein</term>
<term>Isothiocyanates</term>
<term>Monoterpenes</term>
<term>Phytochemicals</term>
<term>Serotonin 5-HT3 Receptor Antagonists</term>
</keywords>
<keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr">
<term>Acroléine</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en">
<term>Intestinal Mucosa</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Enterocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="déficit" xml:lang="fr">
<term>Canaux cationiques TRP</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Canaux cationiques TRP</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Enterocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Calcium</term>
<term>Entérocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acroléine</term>
<term>Antagonistes des récepteurs 5-HT3 de la sérotonine</term>
<term>Composés phytochimiques</term>
<term>Isothiocyanates</term>
<term>Monoterpènes</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Côlon</term>
<term>Duodénum</term>
<term>Muqueuse intestinale</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Colon</term>
<term>Duodenum</term>
<term>Intestinal Mucosa</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Electrophysiological Phenomena</term>
<term>Food</term>
<term>Gene Expression</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
<term>Transfection</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Aliments</term>
<term>Animaux</term>
<term>Canaux cationiques TRP</term>
<term>Cellules HEK293</term>
<term>Entérocytes</term>
<term>Expression des gènes</term>
<term>Humains</term>
<term>Muqueuse intestinale</term>
<term>Mâle</term>
<term>Phénomènes électrophysiologiques</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris knockout</term>
<term>Transfection</term>
</keywords>
</textClass>
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<front>
<div type="abstract" xml:lang="en">
<p>TRPA1 is a ligand-activated cation channel found in the intestine and other tissues. Components of food that stimulate TRPA1 receptors (phytonutrients) include allyl isothiocyanate, cinnamaldehyde and linalool, but these may also act at other receptors. Cells lining the intestinal mucosa are immunoreactive for TRPA1 and
<italic>Trpa1</italic>
mRNA occurs in mucosal extracts, suggesting that the TRPA1 receptor is the target for these agonists. However, in situ hybridisation reveals
<italic>Trpa1</italic>
expression in 5-HT containing enteroendocrine cells, not enterocytes. TRPA1 agonists evoke mucosal secretion, which may be indirect (through release of 5-HT) or direct by activation of enterocytes. We investigated effects of the phytonutrients on transmucosal ion currents in mouse duodenum and colon, and the specificity of the phytonutrients in cells transfected with
<italic>Trpa1</italic>
, and in
<italic>Trpa1</italic>
-deficient mice. The phytonutrients increased currents in the duodenum with the relative potencies: allyl isothiocyanate (AITC) > cinnamaldehyde > linalool (0.1 to 300 μM). The rank order was similar in the colon, but linalool was ineffective. Responses to AITC were reduced by the TRPA1 antagonist HC-030031 (100 μM), and were greatly diminished in
<italic>Trpa1</italic>
−/− duodenum and colon. Responses were not reduced by tetrodotoxin, 5-HT receptor antagonists, or atropine, but inhibition of prostaglandin synthesis reduced responses. Thus, functional TRPA1 channels are expressed by enterocytes of the duodenum and colon. Activation of enterocyte TRPA1 by food components has the potential to facilitate nutrient absorption.</p>
</div>
</front>
<back>
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