Significance of TRP channels in oxidative stress

Significance of TRP channels in oxidative stress

European Journal of Pharmacology xx (xxxx) xxxx–xxxx Contents lists available at ScienceDirect European Journal of Pharmacology journal homepage: ww...

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European Journal of Pharmacology xx (xxxx) xxxx–xxxx

Contents lists available at ScienceDirect

European Journal of Pharmacology journal homepage: www.elsevier.com/locate/ejphar

Perspective

Significance of TRP channels in oxidative stress Shinichiro Yamamoto, Shunichi Shimizu



Division of Pharmacology, Faculty of Pharmaceutical Sciences, Teikyo Heisei University, Tokyo, Japan

A R T I C L E I N F O

A BS T RAC T

Keywords: TRP channels TRPM2 TRPA1 Reactive oxygen species Oxidative stress

Reactive oxygen species induce oxidative stress, leading to cell damage, but also function as signal transduction molecules. Transient receptor potential (TRP) channels have been attracting increasing attention as Ca2+permeable channels that sense environmental changes. The members of one class of TRP channels have emerged as reactive oxygen species sensors. The significance of Ca2+ signaling induced by the activation of reactive oxygen species-sensitive TRP channels under pathological conditions is currently being elucidated. The selective inhibition of reactive oxygen species-sensitive TRP channels represents a future challenge that may lead to new therapeutic strategies for the suppression of reactive oxygen species-related diseases.

1. Reactive oxygen species-sensitive TRP channels Transient receptor potential (TRP) channels have been divided into six subfamilies (C, V, M, P, ML, and A) (Clapham, 2003). TRPM2, TRPC5, TRPV1, and TRPA1 have been identified as reactive oxygen species-sensitive Ca2+-permeable channels. The activation of TRPM2 is triggered by ADP-ribose binding to the NudT9-H domain in its Cterminus (Perraud et al., 2001). We previously reported that the activation of TRPM2 is triggered by reactive oxygen species such as hydrogen peroxide (H2O2) (Hara et al., 2002). Reactive oxygen speciesinduced TRPM2 activation was also found to be triggered by the production of ADP-ribose in nuclei via poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase pathways (Fonfria et al., 2004) (Fig. 1). We recently demonstrated that H2O2-induced TRPM2 activation was mediated through the hydroxyl radical, which is produced by the reaction of H2O2 with intracellular Fe2+ (Fenton reaction) (Ishii et al., 2006; Shimizu et al., 2015). On the other hand, TRPC5, TRPV1, and TRPA1 are activated by reactive oxygen species through oxidative modifications to cysteine residues (Yoshida et al., 2006; Takahashi et al., 2008). The sensitivity of TRPA1 to reactive oxygen species is the greatest among the TRP channels. Cysteine residues on the poreforming region located within the plasma membrane and cytoplasmic N-terminal region are considered to be essential for the reactive oxygen species-induced activation of TRPC5/TRPV1 and TRPA1, respectively (Fig. 1). The activation of TRPA1 by H2O2 appears to be mediated by H2O2-derived hydroxyl radicals (Andersson et al., 2008) (Fig. 1). Since the hydroxyl radical is membrane impermeable, the activation of TRPV1 and TRPC5 may be triggered by H2O2 rather than the hydroxyl radical. The hydroxyl radical is more reactive than H2O2. TRPA1 rather



than TRPC5 and TRPV1 has been suggested to function as an oxidative stress sensor. Under pathological conditions such as inflammatory diseases and ischemia-reperfusion, various cells produce a large amount of reactive oxygen species (Dröge, 2002; Lambeth, 2004). Ca2+ influx via reactive oxygen species-sensitive TRP channels under pathological conditions has been shown to contribute to the aggravation of these diseases. 2. Pathological roles of TRPA1 Pungent compounds such as allyl isothiocyanate in mustard oil and noxious cold stimuli trigger the activation of TRPA1 (Story et al., 2003; Jordt et al., 2004), suggesting that TRPA1 functions as a nociceptive receptor. TRPA1 also functions as an O2 sensor, which plays an important role in maintaining O2 homeostasis (Takahashi et al., 2011). A previous study demonstrated that TRPA1 expressed in sensory neurons mediated neuropeptide release and chemokine production in the airways, and these are responsible for the aggravation of asthma (Caceres et al., 2009). Asthma is an inflammatory disease, and reactive oxygen species also function as mediators for the aggravation of symptoms (Henricks and Nijkamp, 2001). Therefore, TRPA1 is considered to be a sensor of oxidative stress and has been implicated in inflammatory diseases. 3. Pathological roles of TRPM2 Previous studies have indicated that the activation of TRPM2 in response to reactive oxygen species participates in the aggravation of inflammatory diseases. Ca2+ influxes through TRPM2 in monocytes/

Corresponding author. E-mail address: [email protected] (S. Shimizu).

http://dx.doi.org/10.1016/j.ejphar.2016.11.007 Received 22 August 2016; Received in revised form 20 October 2016; Accepted 2 November 2016 Available online xxxx 0014-2999/ © 2016 Elsevier B.V. All rights reserved.

Please cite this article as: Yamamoto, S., European Journal of Pharmacology (2016), http://dx.doi.org/10.1016/j.ejphar.2016.11.007

European Journal of Pharmacology xx (xxxx) xxxx–xxxx

S. Yamamoto, S. Shimizu

TRPM2

TRPA1

TRPV1 TRPC5 SH HS

NudT9-H

NudT9-H

HS

ADP-ribose NAD+ PARP PARG poly(ADP-ribose) neucleus

trans membrane

SH

OH fenton reaction

H2O2

PARG: poly(ADP-ribose) glycohydrolase PARP: poly(ADP-ribose) polymerase

Fig. 1. Differences in reactive oxygen species-induced activation mechanisms among reactive oxygen species-sensitive TRP channels.

References

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4. General conclusions and future perspectives Since TRPM2 is important for host defense responses to bacterial infections, its inhibition during infections may exacerbate symptoms. However, a number of studies using mouse disease models have suggested that TRPM2 contributes to the aggravation of various reactive oxygen species-related diseases. TRPM2 is attracting interest as a new target for suppressing various reactive oxygen species-related diseases; however, specific inhibitors are not yet available. In contrast, TRPA1 functions as a nociceptive receptor and O2 sensor. Therefore, direct TRPA1 channel blockers are considered to disrupt the physiological functions of TRPA1. We recently found that AG-related compounds blocked the H2O2-induced activation of TRPM2 and TRPA1 by scavenging the intracellular hydroxyl radical (Shimizu et al., 2014; Toda et al., 2016). Membrane-permeable hydroxyl radical scavengers represent one of the candidates to attenuate reactive oxygen species-related diseases through the blockage of TRPM2 and TRPA1. Curcumin ((1E,6E)-1,7-bis-(4-hy- droxy-3-methoxyphenyl)-1,6-heptadien-3,5-dione), which is the main natural polyphenol in Curcuma longa (turmeric root), has been shown to exert strong inhibitory effects on H2O2-induced TRPM2 activation (Kheradpezhouh et al., 2016). On the other hand, curcumin activates and subsequently desensitizes TRPA1 (Leamy et al., 2011). Curcumin has been shown to exert beneficial effects on various diseases including inflammatory diseases (Pulido-Moran et al., 2016). The actions of curcumin described above have prompted us to speculate that TRPM2 inhibitors have clinically beneficial effects against reactive oxygen species-related diseases. 2

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