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TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons.
Front Physiol. 2017; 8:272.FP

Abstract

The transient receptor potential vanilloid 1 (TRPV1) channel is highly expressed in a subset of sensory neurons in the dorsal root ganglia (DRG) and trigeminal ganglia of experimental animals, responsible for nociception. Many researches have revealed that some TRPV1-positive neurons co-express the transient receptor potential ankyrin 1 (TRPA1) channel whose activities are closely modulated by TRPV1 channel. However, it is less investigated whether the activities of TRPV1 channel are modulated by the presence of TRPA1 channel in primary sensory neurons. This study clarified the difference in electrophysiological responses induced by TRPV1 channel activation between TRPA1-positive and TRPA1-negative DRG. TRPV1 and TRPA1 channel activations were evoked by capsaicin (1 μM), a TRPV1 agonist, and allyl isothiocyanate (AITC; 500 μM), a TRPA1 agonist, respectively. Capsaicin perfusion for 15 s caused a large inward current without a desensitization phase at a membrane potential of -70 mV in AITC-insensitive DRG (current density; 29.6 ± 5.6 pA/pF, time constant of decay; 12.8 ± 1.8 s). The capsaicin-induced currents in AITC-sensitive DRG had a small current density (12.7 ± 2.9 pA/pF) with a large time constant of decay (24.3 ± 5.4 s). In calcium imaging with Fura-2, the peak response by capsaicin was small and duration reaching the peak response was long in AITC-sensitive neurons. These electrophysiological differences were completely eliminated by HC-030031, a TRPA1 antagonist, in an extracellular solution or 10 mM EGTA, a Ca2+ chelator, in an internal solution. Capsaicin perfusion for 120 s desensitized the inward currents after a transient peak. The decay during capsaicin perfusion was notably slow in AITC-sensitive DRG; ratio of capsaicin-induced current 60 s after the treatment per the peak current in AITC-sensitive neurons (78 ± 9%) was larger than that in AITC-insensitive neurons (48 ± 5%). The capsaicin-induced current in the desensitization phase was attenuated by HC-030031 in AITC-insensitive DRG. These results indicate that (1) TRPV1-mediated currents in TRPA1-positive neurons characterize small current densities with slow decay, which is caused by TRPA1 channel activities and intracellular Ca2+ mobilization and (2) desensitization of TRPV1-mediated current in TRPA1-positive neurons is apparently slow, due to appending TRPA1-mediated current.

Authors+Show Affiliations

Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.Department of Pharmacology, School of Medicine, Kanazawa Medical UniversityUchinada, Japan.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

28515697

Citation

Masuoka, Takayoshi, et al. "TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons." Frontiers in Physiology, vol. 8, 2017, p. 272.
Masuoka T, Kudo M, Yamashita Y, et al. TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons. Front Physiol. 2017;8:272.
Masuoka, T., Kudo, M., Yamashita, Y., Yoshida, J., Imaizumi, N., Muramatsu, I., Nishio, M., & Ishibashi, T. (2017). TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons. Frontiers in Physiology, 8, 272. https://doi.org/10.3389/fphys.2017.00272
Masuoka T, et al. TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons. Front Physiol. 2017;8:272. PubMed PMID: 28515697.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons. AU - Masuoka,Takayoshi, AU - Kudo,Makiko, AU - Yamashita,Yuka, AU - Yoshida,Junko, AU - Imaizumi,Noriko, AU - Muramatsu,Ikunobu, AU - Nishio,Matomo, AU - Ishibashi,Takaharu, Y1 - 2017/05/03/ PY - 2016/12/27/received PY - 2017/04/13/accepted PY - 2017/5/19/entrez PY - 2017/5/19/pubmed PY - 2017/5/19/medline KW - TRPA1 KW - TRPV1 KW - dorsal root ganglion KW - intracellular calcium ion KW - membrane current SP - 272 EP - 272 JF - Frontiers in physiology JO - Front Physiol VL - 8 N2 - The transient receptor potential vanilloid 1 (TRPV1) channel is highly expressed in a subset of sensory neurons in the dorsal root ganglia (DRG) and trigeminal ganglia of experimental animals, responsible for nociception. Many researches have revealed that some TRPV1-positive neurons co-express the transient receptor potential ankyrin 1 (TRPA1) channel whose activities are closely modulated by TRPV1 channel. However, it is less investigated whether the activities of TRPV1 channel are modulated by the presence of TRPA1 channel in primary sensory neurons. This study clarified the difference in electrophysiological responses induced by TRPV1 channel activation between TRPA1-positive and TRPA1-negative DRG. TRPV1 and TRPA1 channel activations were evoked by capsaicin (1 μM), a TRPV1 agonist, and allyl isothiocyanate (AITC; 500 μM), a TRPA1 agonist, respectively. Capsaicin perfusion for 15 s caused a large inward current without a desensitization phase at a membrane potential of -70 mV in AITC-insensitive DRG (current density; 29.6 ± 5.6 pA/pF, time constant of decay; 12.8 ± 1.8 s). The capsaicin-induced currents in AITC-sensitive DRG had a small current density (12.7 ± 2.9 pA/pF) with a large time constant of decay (24.3 ± 5.4 s). In calcium imaging with Fura-2, the peak response by capsaicin was small and duration reaching the peak response was long in AITC-sensitive neurons. These electrophysiological differences were completely eliminated by HC-030031, a TRPA1 antagonist, in an extracellular solution or 10 mM EGTA, a Ca2+ chelator, in an internal solution. Capsaicin perfusion for 120 s desensitized the inward currents after a transient peak. The decay during capsaicin perfusion was notably slow in AITC-sensitive DRG; ratio of capsaicin-induced current 60 s after the treatment per the peak current in AITC-sensitive neurons (78 ± 9%) was larger than that in AITC-insensitive neurons (48 ± 5%). The capsaicin-induced current in the desensitization phase was attenuated by HC-030031 in AITC-insensitive DRG. These results indicate that (1) TRPV1-mediated currents in TRPA1-positive neurons characterize small current densities with slow decay, which is caused by TRPA1 channel activities and intracellular Ca2+ mobilization and (2) desensitization of TRPV1-mediated current in TRPA1-positive neurons is apparently slow, due to appending TRPA1-mediated current. SN - 1664-042X UR - https://www.unboundmedicine.com/medline/citation/28515697/TRPA1_Channels_Modify_TRPV1_Mediated_Current_Responses_in_Dorsal_Root_Ganglion_Neurons_ L2 - https://doi.org/10.3389/fphys.2017.00272 DB - PRIME DP - Unbound Medicine ER -
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