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Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons.
J Appl Physiol (1985). 2015 Jun 15; 118(12):1533-43.JA

Abstract

Both transient receptor potential ankyrin 1 (TRPA1) and vanilloid 1 (TRPV1) receptors are abundantly expressed in bronchopulmonary C-fiber sensory nerves and can be activated by a number of endogenous inflammatory mediators. A recent study has reported a synergistic effect of simultaneous TRPA1 and TRPV1 activations in vagal pulmonary C-fiber afferents in anesthetized rats, but its underlying mechanism was not known. This study aimed to characterize a possible interaction between these two TRP channels and to investigate the potential role of Ca(2+) as a mediator of this interaction in isolated rat vagal pulmonary sensory neurons. Using the perforated patch-clamp recording technique, our study demonstrated a distinct positive interaction occurring abruptly between TRPA1 and TRPV1 when they were activated simultaneously by their respective agonists, capsaicin (Cap) and allyl isothiocyanate (AITC), at near-threshold concentrations in these neurons. AITC at this low concentration evoked only minimal or undetectable responses, but it markedly amplified the Cap-evoked current in the same neurons. This potentiating effect was eliminated when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, when Ca(2+) was removed from the extracellular solution, the synergistic effect of Cap and AITC on pulmonary sensory neurons was completely abrogated, clearly indicating a critical role of Ca(2+) in mediating the action. These results suggest that this TRPA1-TRPV1 interaction may play a part in regulating the sensitivity of pulmonary sensory neurons during airway inflammatory reaction.

Authors+Show Affiliations

Department of Physiology, University of Kentucky Medical Center, Lexington, Kentucky.Department of Physiology, University of Kentucky Medical Center, Lexington, Kentucky lylee@uky.edu.

Pub Type(s)

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

Language

eng

PubMed ID

25858491

Citation

Hsu, Chun-Chun, and Lu-Yuan Lee. "Role of Calcium Ions in the Positive Interaction Between TRPA1 and TRPV1 Channels in Bronchopulmonary Sensory Neurons." Journal of Applied Physiology (Bethesda, Md. : 1985), vol. 118, no. 12, 2015, pp. 1533-43.
Hsu CC, Lee LY. Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons. J Appl Physiol (1985). 2015;118(12):1533-43.
Hsu, C. C., & Lee, L. Y. (2015). Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons. Journal of Applied Physiology (Bethesda, Md. : 1985), 118(12), 1533-43. https://doi.org/10.1152/japplphysiol.00043.2015
Hsu CC, Lee LY. Role of Calcium Ions in the Positive Interaction Between TRPA1 and TRPV1 Channels in Bronchopulmonary Sensory Neurons. J Appl Physiol (1985). 2015 Jun 15;118(12):1533-43. PubMed PMID: 25858491.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons. AU - Hsu,Chun-Chun, AU - Lee,Lu-Yuan, Y1 - 2015/04/09/ PY - 2015/01/16/received PY - 2015/04/05/accepted PY - 2015/4/11/entrez PY - 2015/4/11/pubmed PY - 2016/3/12/medline KW - airway KW - inflammation KW - sensory nerve KW - transient receptor potential ankyrin 1 KW - transient receptor potential vanilloid 1 SP - 1533 EP - 43 JF - Journal of applied physiology (Bethesda, Md. : 1985) JO - J Appl Physiol (1985) VL - 118 IS - 12 N2 - Both transient receptor potential ankyrin 1 (TRPA1) and vanilloid 1 (TRPV1) receptors are abundantly expressed in bronchopulmonary C-fiber sensory nerves and can be activated by a number of endogenous inflammatory mediators. A recent study has reported a synergistic effect of simultaneous TRPA1 and TRPV1 activations in vagal pulmonary C-fiber afferents in anesthetized rats, but its underlying mechanism was not known. This study aimed to characterize a possible interaction between these two TRP channels and to investigate the potential role of Ca(2+) as a mediator of this interaction in isolated rat vagal pulmonary sensory neurons. Using the perforated patch-clamp recording technique, our study demonstrated a distinct positive interaction occurring abruptly between TRPA1 and TRPV1 when they were activated simultaneously by their respective agonists, capsaicin (Cap) and allyl isothiocyanate (AITC), at near-threshold concentrations in these neurons. AITC at this low concentration evoked only minimal or undetectable responses, but it markedly amplified the Cap-evoked current in the same neurons. This potentiating effect was eliminated when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, when Ca(2+) was removed from the extracellular solution, the synergistic effect of Cap and AITC on pulmonary sensory neurons was completely abrogated, clearly indicating a critical role of Ca(2+) in mediating the action. These results suggest that this TRPA1-TRPV1 interaction may play a part in regulating the sensitivity of pulmonary sensory neurons during airway inflammatory reaction. SN - 1522-1601 UR - https://www.unboundmedicine.com/medline/citation/25858491/Role_of_calcium_ions_in_the_positive_interaction_between_TRPA1_and_TRPV1_channels_in_bronchopulmonary_sensory_neurons_ L2 - https://journals.physiology.org/doi/10.1152/japplphysiol.00043.2015?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -