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Genetic and pharmacological evidence for low-abundance TRPV3 expression in primary vagal afferent neurons.
Am J Physiol Regul Integr Comp Physiol. 2016 05 01; 310(9):R794-805.AJ

Abstract

Primary vagal afferent neurons express a multitude of thermosensitive ion channels. Within this family of ion channels, the heat-sensitive capsaicin receptor (TRPV1) greatly influences vagal afferent signaling by determining the threshold for action-potential initiation at the peripheral endings, while controlling temperature-sensitive forms of glutamate release at central vagal terminals. Genetic deletion of TRPV1 does not completely eliminate these temperature-dependent effects, suggesting involvement of additional thermosensitive ion channels. The warm-sensitive, calcium-permeable, ion channel TRPV3 is commonly expressed with TRPV1; however, the extent to which TRPV3 is found in vagal afferent neurons is unknown. Here, we begin to characterize the genetic and functional expression of TRPV3 in vagal afferent neurons using molecular biology (RT-PCR and RT-quantitative PCR) in whole nodose and isolated neurons and fluorescent calcium imaging on primary cultures of nodose ganglia neurons. We confirmed low-level TRPV3 expression in vagal afferent neurons and observed direct activation with putative TRPV3 agonists eugenol, ethyl vanillin (EVA), and farnesyl pyrophosphate (FPP). Agonist activation stimulated neurons also containing TRPV1 and was blocked by ruthenium red. FPP sensitivity overlapped with EVA and eugenol but represented the smallest percentage of vagal afferent neurons, and it was the only agonist that did not stimulate neurons from TRPV3(-/-1) mice, suggesting FPP has the highest selectivity. Further, FPP was predictive of enhanced responses to capsaicin, EVA, and eugenol in rats. From our results, we conclude TRPV3 is expressed in a discrete subpopulation of vagal afferent neurons and may contribute to vagal afferent signaling either directly or in combination with TRPV1.

Authors+Show Affiliations

Department of Integrative Physiology and Neuroscience, Washington State University, Pullman, Washington.Department of Integrative Physiology and Neuroscience, Washington State University, Pullman, Washington.Department of Integrative Physiology and Neuroscience, Washington State University, Pullman, Washington jamespeters@vetmed.wsu.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

26843581

Citation

Wu, Shaw-Wen, et al. "Genetic and Pharmacological Evidence for Low-abundance TRPV3 Expression in Primary Vagal Afferent Neurons." American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 310, no. 9, 2016, pp. R794-805.
Wu SW, Lindberg JE, Peters JH. Genetic and pharmacological evidence for low-abundance TRPV3 expression in primary vagal afferent neurons. Am J Physiol Regul Integr Comp Physiol. 2016;310(9):R794-805.
Wu, S. W., Lindberg, J. E., & Peters, J. H. (2016). Genetic and pharmacological evidence for low-abundance TRPV3 expression in primary vagal afferent neurons. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 310(9), R794-805. https://doi.org/10.1152/ajpregu.00366.2015
Wu SW, Lindberg JE, Peters JH. Genetic and Pharmacological Evidence for Low-abundance TRPV3 Expression in Primary Vagal Afferent Neurons. Am J Physiol Regul Integr Comp Physiol. 2016 05 1;310(9):R794-805. PubMed PMID: 26843581.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genetic and pharmacological evidence for low-abundance TRPV3 expression in primary vagal afferent neurons. AU - Wu,Shaw-Wen, AU - Lindberg,Jonathan E M, AU - Peters,James H, Y1 - 2016/02/03/ PY - 2015/08/20/received PY - 2016/01/28/accepted PY - 2016/2/5/entrez PY - 2016/2/5/pubmed PY - 2017/6/28/medline KW - autonomic reflexes KW - calcium KW - nodose ganglion KW - satiety KW - vagus SP - R794 EP - 805 JF - American journal of physiology. Regulatory, integrative and comparative physiology JO - Am J Physiol Regul Integr Comp Physiol VL - 310 IS - 9 N2 - Primary vagal afferent neurons express a multitude of thermosensitive ion channels. Within this family of ion channels, the heat-sensitive capsaicin receptor (TRPV1) greatly influences vagal afferent signaling by determining the threshold for action-potential initiation at the peripheral endings, while controlling temperature-sensitive forms of glutamate release at central vagal terminals. Genetic deletion of TRPV1 does not completely eliminate these temperature-dependent effects, suggesting involvement of additional thermosensitive ion channels. The warm-sensitive, calcium-permeable, ion channel TRPV3 is commonly expressed with TRPV1; however, the extent to which TRPV3 is found in vagal afferent neurons is unknown. Here, we begin to characterize the genetic and functional expression of TRPV3 in vagal afferent neurons using molecular biology (RT-PCR and RT-quantitative PCR) in whole nodose and isolated neurons and fluorescent calcium imaging on primary cultures of nodose ganglia neurons. We confirmed low-level TRPV3 expression in vagal afferent neurons and observed direct activation with putative TRPV3 agonists eugenol, ethyl vanillin (EVA), and farnesyl pyrophosphate (FPP). Agonist activation stimulated neurons also containing TRPV1 and was blocked by ruthenium red. FPP sensitivity overlapped with EVA and eugenol but represented the smallest percentage of vagal afferent neurons, and it was the only agonist that did not stimulate neurons from TRPV3(-/-1) mice, suggesting FPP has the highest selectivity. Further, FPP was predictive of enhanced responses to capsaicin, EVA, and eugenol in rats. From our results, we conclude TRPV3 is expressed in a discrete subpopulation of vagal afferent neurons and may contribute to vagal afferent signaling either directly or in combination with TRPV1. SN - 1522-1490 UR - https://www.unboundmedicine.com/medline/citation/26843581/Genetic_and_pharmacological_evidence_for_low_abundance_TRPV3_expression_in_primary_vagal_afferent_neurons_ L2 - https://journals.physiology.org/doi/10.1152/ajpregu.00366.2015?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -