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Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain
Open accessAbstract
Proinflammatory agents trypsin and mast cell tryptase cleave and activate PAR2, which is expressed on sensory nerves to cause neurogenic inflammation. Transient receptor potential A1 (TRPA1) is an excitatory ion channel on primary sensory nerves of pain pathway. Here, we show that a functional interaction of PAR2 and TRPA1 in dorsal root ganglion (DRG) neurons could contribute to the sensation of inflammatory pain. Frequent colocalization of TRPA1 with PAR2 was found in rat DRG neurons. PAR2 activation increased the TRPA1 currents evoked by its agonists in HEK293 cells transfected with TRPA1, as well as DRG neurons. Application of phospholipase C (PLC) inhibitors or phosphatidylinositol-4,5-bisphosphate (PIP(2)) suppressed this potentiation. Decrease of plasma membrane PIP(2) levels through antibody sequestration or PLC-mediated hydrolysis mimicked the potentiating effects of PAR2 activation at the cellular level. Thus, the increased TRPA1 sensitivity may have been due to activation of PLC, which releases the inhibition of TRPA1 from plasma membrane PIP(2). These results identify for the first time to our knowledge a sensitization mechanism of TRPA1 and a novel mechanism through which trypsin or tryptase released in response to tissue inflammation might trigger the sensation of pain by TRPA1 activation.
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Cites
Protease-activated receptors in inflammation, neuronal signaling and pain
Vergnolle, N., Wallace, J. L., Bunnett, N. W., & Hollenberg, M. D. (2001) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)01634-5 · Cited by 369
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Wilson, S. R., Thé, L., Batia, L. M., Beattie, K., Katibah, G. E., McClain, S. P., Pellegrino, M., Estandian, D. M., & Bautista, D. M. (2013) · Cell · doi:10.1016/j.cell.2013.08.057 · Cited by 987
TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins
Meseguer, V., Alpizar, Y. A., Luis, E., Tajada, S., Denlinger, B., Fajardo, O., Manenschijn, J.-A., Fernández-Peña, C., Talavera, A., Kichko, T., et al. (2014) · Nature Communications · doi:10.1038/ncomms4125 · Cited by 479
Eid, S. R., Crown, E. D., Moore, E. L., Liang, H. A., Choong, K.-C., Dima, S., Henze, D. A., Kane, S. A., & Urban, M. O. (2008) · Molecular Pain · doi:10.1186/1744-8069-4-48 · Cited by 447
Gouin, O., L’Herondelle, K., Lebonvallet, N., Le Gall-Ianotto, C., Sakka, M., Buhé, V., Plée-Gautier, E., Carré, J.-L., Lefeuvre, L., Misery, L., et al. (2017) · Protein & Cell · doi:10.1007/s13238-017-0395-5 · Cited by 425
Metadata
- Authors
- Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Kobayashi, K., Obata, K., Yamanaka, H., & Noguchi, K.
- Venue
- Journal of Clinical Investigation
- Published
- 2007-07-02
- Volume
- 117
- Issue
- 7
- Pages
- 1979-1987
- ISSN
- 0021-9738 (ISSN-L)
- OpenAlex
- W2118612841
- Cited by
- 432
- References
- 1
- FWCI
- 12.01
- Type
- journal article
- Language
- en
- Open access
- bronze
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- Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Kobayashi, K., Obata, K., Yamanaka, H., & Noguchi, K. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. Journal of Clinical Investigation. https://doi.org/10.1172/jci30951
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