Targeting TRPM2 in ROS-Coupled Diseases
<p>ROS production during inflammation and ischemia-reperfusion. (<b>A</b>) In resting state, cytosolic activators such as p40<sup>phox</sup>, p47<sup>phox</sup>, p67<sup>phox</sup> and small G protein RAC do not interact with NOX2-p22<sup>phox</sup> complex. These activators translocate to the plasma membrane during phagocytosis and interact with the NOX2-p22<sup>phox</sup> complex. Electrons derived from NADPH are transferred through the complex to molecular oxygen, leading to <sup>·</sup>O<sub>2</sub><sup>−</sup> production; (<b>B</b>) Oxidative phosphorylation is initiated by electron transport from NADH and/or FADH<sub>2</sub> to the electron transport chain in the mitochondrial inner membrane. The electron transport chain is composed of complexes I–IV. Electrons derived from NADH and FADH<sub>2</sub> are fed to complex I and complex II, respectively. They are then transferred to complexes in ascending order of the redox potential, which release free energy. Molecular oxygen accepts electrons for the formation of H<sub>2</sub>O. On the other hand, the electron transport chain uses free energy derived from electron transport to pump H<sup>+</sup> out of the matrix, thereby creating proton gradient across the mitochondrial inner membrane. By utilizing energy released by the influx of H<sup>+</sup> into the matrix, ADP is phosphorylated, resulting in the generation of ATP. <sup>·</sup>O<sub>2</sub><sup>−</sup> is generated by the leakage of electrons from complexes I and III in the electron transport chain. The activity of the electron transport chain generates a relatively small amount of <sup>·</sup>O<sub>2</sub><sup>−</sup> under normal conditions, but its production may be greatly magnified by events occurring during ischemia-reperfusion. The expression of NOX isoforms is up-regulated by HIF1α during ischemia, and then NADPH oxidase then generates large amounts of ROS by reoxygenation during reperfusion. During ischemia, ATP is catabolized into hypoxanthine.</p> "> Figure 2
<p>Does administration with TRPM2 inhibitors during ROS-coupled disease development improve the grade of these diseases? Pathological mouse model studies have been performed under <span class="html-italic">Trpm2</span>-disrupted conditions, and suggested that <span class="html-italic">Trpm2</span> KO mice are protected from ROS-coupled diseases. However, in terms of cure, it is important that the grade of these diseases is improved by the inhibition of TRPM2 during disease development. Therefore, the studies whether the inhibition of TRPM2 during ROS-coupled disease development has curative effects on the diseases should be done in the future.</p> ">
Abstract
:1. Introduction
2. TRPM2 Activators and Inhibitors
3. ROS Production under Pathological Conditions
3.1. Inflammation
3.2. Ischemia-Reperfusion
4. ROS-Coupled Diseases and TRPM2
4.1. Inflammatory Diseases
4.1.1. TRPM2-Mediated Chemokine Production
4.1.2. LPS-Induced Inflammatory Responses and TRPM2
4.1.3. Functional Roles of TRPM2 during Infection
4.1.4. NLRP3 Inflammasome and TRPM2
4.2. Ischemia-Reperfusion Injury
4.2.1. Brain
4.2.2. Heart
4.2.3. Kidneys
4.3. Other Diseases and Injuries
4.3.1. Acetaminophen-Induced Liver Injury
4.3.2. Radiation-Induced Tissue Damage
4.3.3. Alzheimer’s Disease
5. Conclusions
Acknowledgments
Conflicts of Interest
References
- Clapham, D.E. Calcium signaling. Cell 1995, 80, 259–268. [Google Scholar] [CrossRef]
- Montell, C.; Rubin, G.M. Molecular characterization of the Drosophila trp locus: A putative integral membrane protein required for phototransduction. Neuron 1989, 2, 1313–1323. [Google Scholar] [CrossRef]
- Clapham, D.E. TRP channels as cellular sensors. Nature 2003, 426, 517–524. [Google Scholar] [CrossRef] [PubMed]
- Goel, M.; Sinkins, W.G.; Schilling, W.P. Selective Association of TRPC Channel Subunits in Rat Brain Synaptosomes. J. Biol. Chem. 2002, 277, 48303–48310. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, T.; Schaefer, M.; Schultz, G.; Sudermann, T. Subunit composition of mammalian transient receptor potential channels in living cells. Proc. Natl. Acad. Sci. USA 2002, 99, 7461–7466. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Jiang, M.; Peyton, M.; Boulay, G.; Hurst, R.; Stefani, E.; Birnbaumer, L. trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell 1996, 85, 661–671. [Google Scholar] [CrossRef]
- Hofmann, T.; Obukhov, A.G.; Schaefer, M.; Harteneck, C.; Gudermann, T.; Schultz, G. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 1999, 397, 259–263. [Google Scholar] [PubMed]
- Okada, T.; Inoue, R.; Yamazaki, K.; Maeda, A.; Kurosaki, T.; Yamakuni, T.; Tanaka, I.; Shimizu, S.; Ikenaka, K.; Imoto, K.; et al. Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. J. Biol. Chem. 1999, 274, 27359–27370. [Google Scholar] [CrossRef] [PubMed]
- Inoue, R.; Okada, T.; Onoue, H.; Hara, Y.; Shimizu, S.; Naitoh, S.; Ito, Y.; Mori, Y. The transient receptor potential protein homologue TRP6 is the essential component of vascular α1-adrenoceptor-activated Ca2+-permeable cation channel. Circ. Res. 2001, 88, 325–332. [Google Scholar] [CrossRef] [PubMed]
- Caterina, M.J.; Schumacher, M.A.; Tominaga, M.; Rosen, T.A.; Levine, J.D.; Julius, D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997, 389, 816–824. [Google Scholar] [PubMed]
- Caterina, M.J.; Rosen, T.A.; Tominaga, M.; Brake, A.J.; Julius, D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 1999, 398, 436–441. [Google Scholar] [PubMed]
- Güler, A.D.; Lee, H.; Iida, T.; Shimizu, I.; Tominaga, M.; Caterina, M. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 2002, 22, 6408–6414. [Google Scholar] [PubMed]
- Peier, A.M.; Reeve, A.J.; Andersson, D.A.; Moqrich, A.; Earley, T.J.; Hergarden, A.C.; Story, G.M.; Colley, S.; Hogenesch, J.B.; McIntyre, P.; et al. A heat-sensitive TRP channel expressed in keratinocytes. Science 2002, 296, 2046–2049. [Google Scholar] [CrossRef] [PubMed]
- Smith, G.D.; Gunthorpe, M.J.; Kelsell, R.E.; Hayes, P.D.; Reilly, P.; Facer, P.; Wright, J.E.; Jerman, J.C.; Walhin, J.P.; Ooi, L.; et al. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 2002, 418, 186–190. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, H.; Vriens, J.; Suh, S.H.; Benham, C.D.; Droogmans, G.; Nilius, B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J. Biol. Chem. 2002, 277, 47044–47051. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Ramsey, I.S.; Kotecha, S.A.; Moran, M.M.; Chong, J.A.; Lawson, D.; Ge, P.; Lilly, J.; Silos-Santiago, I.; Xie, Y.; et al. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 2002, 418, 181–186. [Google Scholar] [CrossRef] [PubMed]
- Tominaga, M.; Caterina, M.J.; Malmberg, A.B.; Rosen, T.A.; Gilbert, H.; Skinner, K.; Raumann, B.E.; Basbaum, A.I.; Julius, D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21, 531–543. [Google Scholar] [CrossRef]
- Liedtke, W.; Choe, Y.; Marti-Renom, M.A.; Bell, A.M.; Denis, C.S.; Sali, A.; Hudspeth, A.J.; Friedman, J.M.; Heller, S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 2000, 103, 525–535. [Google Scholar] [CrossRef]
- Strotmann, R.; Harteneck, C.; Nunnenmacher, K.; Schultz, G.; Plant, T.D. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat. Cell Biol. 2000, 2, 695–702. [Google Scholar] [PubMed]
- McKemy, D.D.; Neuhausser, W.M.; Julius, D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416, 52–58. [Google Scholar] [CrossRef] [PubMed]
- Peier, A.M.; Moqrich, A.; Hergarden, A.C.; Reeve, A.J.; Andersson, D.A.; Story, G.M.; Earley, T.J.; Dragoni, I.; McIntyre, P.; Bevan, S.; et al. A TRP channel that senses cold stimuli and menthol. Cell 2002, 108, 705–715. [Google Scholar] [CrossRef]
- Nauli, S.M.; Alenghat, F.J.; Luo, Y.; Williams, E.; Vassilev, P.; Li, X.; Elia, A.E.; Lu, W.; Brown, E.M.; Quinn, S.J.; et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33, 129–137. [Google Scholar] [CrossRef] [PubMed]
- Mochizuki, T.; Tsuchiya, K.; Nitta, K. Autosomal dominant polycystic kidney disease: Recent advances in pathogenesis and potential therapies. Clin. Exp. Nephrol. 2013, 17, 317–326. [Google Scholar] [CrossRef] [PubMed]
- Jefferies, H.B.; Cooke, F.T.; Jat, P.; Boucheron, C.; Koizumi, T.; Hayakawa, M.; Kaizawa, H.; Ohishi, T.; Workman, P.; Waterfield, M.D.; et al. A selective PIKfyve inhibitor blocks PtdIns(3,5)P2 production and disrupts endomembrane transport and retroviral budding. EMBO Rep. 2008, 9, 164–170. [Google Scholar] [CrossRef] [PubMed]
- Dong, X.P.; Shen, D.; Wang, X.; Dawson, T.; Li, X.; Zhang, Q.; Cheng, X.; Zhang, Y.; Weisman, L.S.; Delling, M.; et al. PI(3,5)P2 controls membrane trafficking by direct activation of mucolipin Ca2+ release channels in the endolysosome. Nat. Commun. 2010, 1, 38. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, N.; Mizuno, Y.; Kozai, D.; Yamamoto, S.; Kiyonaka, S.; Shibata, T.; Uchida, K.; Mori, Y. Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators. Channels 2008, 2, 287–298. [Google Scholar] [CrossRef] [PubMed]
- Macpherson, L.J.; Geierstanger, B.H.; Viswanath, V.; Bandell, M.; Eid, S.R.; Hwang, S.; Patapoutian, A. The pungency of garlic: Activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 2005, 15, 929–934. [Google Scholar] [CrossRef] [PubMed]
- Jordt, S.E.; Bautista, D.M.; Chuang, H.H.; McKemy, D.D.; Zygmunt, P.M.; Hogestatt, E.D.; Meng, I.D.; Julius, D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004, 427, 260–265. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, N.; Kuwaki, T.; Kiyonaka, S.; Numata, T.; Kozai, D.; Mizuno, Y.; Yamamoto, S.; Naito, S.; Knevels, E.; Carmeliet, P.; et al. TRPA1 underlies a sensing mechanism for O2. Nat. Chem. Biol. 2011, 10, 701–711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henricks, P.A.; Nijkamp, F.P. Reactive oxygen species as mediators in asthma. Pulm. Pharmacol. Ther. 2001, 14, 409–420. [Google Scholar] [CrossRef] [PubMed]
- Dröge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82, 47–95. [Google Scholar] [CrossRef] [PubMed]
- Taguchi, K.; Motohashi, H.; Yamamoto, M. Molecular mechanisms of Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011, 16, 123–140. [Google Scholar] [CrossRef] [PubMed]
- Soga, M.; Matsuzawa, A.; Ichijo, H. Oxidative stress-induced diseases via the ASK1 signaling pathway. Int. J. Cell Biol. 2012, 2012. article ID 439587. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, S.; Kawakami, S.; Hara, Y.; Wakamori, M.; Itoh, E.; Minami, T.; Takada, Y.; Kume, T.; Katsuki, H.; Mori, Y.; et al. A critical role of TRPM2 in neuronal cell death by hydrogen peroxide. J. Pharmacol. Sci. 2006, 101, 66–76. [Google Scholar] [CrossRef] [PubMed]
- Miller, B.A.; Wang, J.; Hirschler-Laszkiewicz, I.; Gao, E.; Song, J.; Zhang, X.; Koch, W.J.; Madesh, M.; Mallilankaraman, K.; Gu, T.; et al. The second member of transient receptor potential-melastatin channel family protects hearts from ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 2013, 304, H1010–H1022. [Google Scholar] [CrossRef] [PubMed]
- Togashi, K.; Hara, Y.; Tominaga, T.; Higashi, T.; Konishi, Y.; Mori, Y.; Tominaga, M. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J. 2006, 25, 1804–1815. [Google Scholar] [CrossRef] [PubMed]
- Lange, I.; Yamamoto, S.; Partida-Sánchez, S.; Mori, Y.; Fleig, A.; Penner, R. TRPM2 functions as lysosomal Ca2+ release channel in β-cells. Sci. Signal. 2009, 71, ra23. [Google Scholar] [CrossRef] [PubMed]
- Partida-Sánchez, S.; Gasser, A.; Fliegert, R.; Siebrands, C.C.; Dammermann, W.; Shi, G.; Mousseau, B.J.; Sumazo-Toledo, A.; Bhagat, H.; Walseth, T.F.; et al. Chemotaxis of mouse bone marrow neutrophils and dendritic cell is controlled by ADP-ribose, the major product generated by the CD38 enzyme reaction. J. Immunol. 2007, 179, 7827–7839. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Chu, X.; Tong, Q.; Cheung, J.Y.; Conrad, K.; Masker, K.; Miller, B.A. A novel TRPM2 isoform inhibits calcium influx and susceptibility to cell death. J. Biol. Chem. 2003, 278, 16222–16229. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, S.; Shimizu, S.; Kiyonaka, S.; Takahashi, N.; Wajima, T.; Hara, Y.; Negoro, T.; Hiroi, T.; Kiuchi, Y.; Okada, T.; et al. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat. Med. 2008, 14, 738–747. [Google Scholar] [CrossRef] [PubMed]
- Wehage, E.; Eisfeld, J.; Heiner, I.; Jungling, E.; Zitt, C.; Luckhoff, A. Activation of the cation channel long transient receptor potential channel 2 (LTRPC2) by hydrogen peroxide. A splice variant reveals a mode of activation independent of ADP-ribose. J. Biol. Chem. 2002, 277, 23150–23156. [Google Scholar] [CrossRef] [PubMed]
- Sumoza-Toledo, A.; Lange, I.; Cortado, H.; Bhagat, H.; Mori, Y.; Fleig, A.; Penner, R.; Partida-Sánchez, S. Dendritic cell maturation and chemotaxis is regulated by TRPM2-mediated lysosomal Ca2+ release. FASEB J. 2011, 25, 3529–3542. [Google Scholar] [CrossRef] [PubMed]
- Brieger, K.; Schiavone, S.; Miller, F.J.; Krause, K. Reactive oxygen species: From health to disease. Swiss Med. Wkly. 2012, 142, w13659. [Google Scholar] [CrossRef] [PubMed]
- Kühn, F.J.; Lückhoff, A. Sites of the NUDT9-H domain critical for ADP-ribose activation of the cation channel TRPM2. J. Biol. Chem. 2004, 279, 46431–46437. [Google Scholar] [CrossRef] [PubMed]
- Perraud, A.L.; Fleig, A.; Dunn, C.A.; Bagley, L.A.; Launay, P.; Schmitz, C.; Stokes, A.J.; Zhu, Q.; Bessman, M.J.; Penner, R.; et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 2001, 411, 595–599. [Google Scholar] [CrossRef] [PubMed]
- Kolisek, M.; Beck, A.; Fleig, A.; Penner, R. Cyclic ADP-ribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol. Cell 2005, 18, 61–69. [Google Scholar] [CrossRef] [PubMed]
- Starkus, J.; Beck, A.; Fleig, A.; Penner, R. Regulation of TRPM2 by extra- and intracellular calcium. J. Gen. Physiol. 2007, 130, 427–440. [Google Scholar] [CrossRef] [PubMed]
- Lange, I.; Penner, R.; Fleig, A.; Beck, A. Synergistic regulation of endogenous TRPM2 channels by adenine dinucleotides in primary human neutrophils. Cell Calcium 2008, 44, 604–615. [Google Scholar] [CrossRef] [PubMed]
- Du, J.; Xie, J.; Yue, L. Intracellular calcium activates TRPM2 and tis alternative spliced isoforms. Proc. Natl. Acad. Sci. USA 2009, 106, 7239–7244. [Google Scholar] [CrossRef] [PubMed]
- Heiner, I.; Eisfeld, J.; Warnstedt, M.; Radukina, N.; Jüngling, E.; Lückhoff, A. Endogenous ADP-ribose enables calcium-regulated cation currents through TRPM2 channels in neutrophil granulocytes. Biochem. J. 2006, 398, 225–232. [Google Scholar] [CrossRef] [PubMed]
- Tóth, B.; Csanády, L. Identification of direct and indirect effectors of the transient receptor potential melastatin 2 (TRPM2) cation channel. J. Biol. Chem. 2010, 285, 30091–30102. [Google Scholar] [CrossRef] [PubMed]
- Tóth, B.; Iordanov, I.; Csanády, L. Ruling out pyridine dinucleotides as true TRPM2 channel activators reveals novel direct agonist ADP-ribose-2’-phosphate. J. Gen. Physiol. 2015, 145, 419–430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grubisha, O.; Rafty, L.A.; Takanishi, C.L.; Xu, X.; Tong, L.; Perraud, A.L.; Scharenberg, A.M.; Denu, J.M. Metabolite of SIR2 reaction modulates TRPM2 ion channel. J. Biol. Chem. 2006, 281, 14057–14065. [Google Scholar] [CrossRef] [PubMed]
- Hara, Y.; Wakamori, M.; Ishii, M.; Maeno, E.; Nishida, M.; Yoshida, T.; Yamada, H.; Shimizu, S.; Mori, E.; Kudoh, J.; et al. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol. Cell 2002, 9, 163–173. [Google Scholar] [CrossRef]
- Perraud, A.L.; Takanishi, C.L.; Shen, B.; Kang, S.; Smith, M.K.; Schmitz, C.; Knowles, H.M.; Ferraris, D.; Li, W.; Zhang, J.; et al. Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels. J. Biol. Chem. 2005, 280, 6138–6148. [Google Scholar] [CrossRef] [PubMed]
- Malavasi, F.; Deaglio, S.; Funaro, A.; Ferrero, E.; Horenstein, A.L.; Ortolan, E.; Vaisitti, T.; Aydin, S. Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol. Rev. 2008, 88, 841–886. [Google Scholar] [CrossRef] [PubMed]
- Magnone, M.; Bauer, I.; Poggi, A.; Mannino, E.; Sturla, L.; Brini, M.; Zocchi, E.; De Flora, A.; Nencioni, A.; Bruzzone, S. NAD+ levels control Ca2+ sore replenishment and mitogen-induced increase of cytosolic Ca2+ by cyclic ADP-ribose-dependent TRPM2 channel gating in human T lymphocytes. J. Biol. Chem. 2012, 287, 21067–21081. [Google Scholar] [CrossRef] [PubMed]
- Tanuma, S.; Yagi, T.; Johnson, G.S. Endogenous ADP ribosylation of high mobility group proteins 1 and 2 and histone H1 following DNA damage in intact cells. Arch. Biochem. Biophys. 1985, 237, 38–42. [Google Scholar] [CrossRef]
- De Murcia, G.; de Murcia, J.M. Poly(ADP-ribose) polymerase: A molecular nick-sensor. Trends Biochem. Sci. 1994, 19, 172–176. [Google Scholar] [CrossRef]
- Oliver, F.J.; Menissier-de Murcia, J.; Nacci, C.; Decker, P.; Andriantsitohaina, R.; Muller, S.; de la Rubia, G.; Stoclet, J.C.; de Murcia, G. Resistance to endotoxic shock as a consequence of defective NF-κB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J. 1999, 18, 4446–4454. [Google Scholar] [CrossRef] [PubMed]
- Virág, L.; Szabo, C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 2002, 54, 375–429. [Google Scholar] [CrossRef] [PubMed]
- Fonfria, E.; Marshall, I.C.; Benham, C.D.; Boyfield, I.; Brown, J.D.; Hill, K.; Hughes, J.P.; Skaper, S.D.; McNulty, S. TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br. J. Pharmacol. 2004, 143, 186–192. [Google Scholar] [CrossRef] [PubMed]
- Buelow, B.; Song, Y.; Andrew, M.; Scharenberg, A.M. The poly(ADP-ribose) polymerase PARP-1 is required for oxidative stress-induced TRPM2 activation in lymphocytes. J. Biol. Chem. 2008, 283, 24571–24583. [Google Scholar] [CrossRef] [PubMed]
- Ishii, M.; Shimizu, S.; Hara, Y.; Hagiwara, T.; Miyazaki, A.; Mori, Y.; Kiuchi, Y. Intracellular-produced hydroxyl radical mediates H2O2-induced Ca2+ influx and cell death in rat beta-cell line RIN-5F. Cell Calcium 2006, 39, 487–494. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, S.; Yonezawa, R.; Negoro, T.; Yamamoto, S.; Numata, T.; Ishii, M.; Mori, Y.; Toda, T. Sensitization of H2O2-induced TRPM2 activation and subsequent interleukin-8 (CXCL8) production by intracellular Fe2+ in human monocytic U937 cells. Int. J. Biochem. Cell Biol. 2015, 68, 119–127. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Tong, Q.; Conrad, K.; Wozney, J.; Cheung, J.Y.; Miller, B.A. Regulation of TRP channel TRPM2 by the tyrosine phosphatase PTPL1. Am. J. Physiol. Cell Physiol. 2007, 292, C1746–C1758. [Google Scholar] [CrossRef] [PubMed]
- Hill, K.; McNulty, S.; Randall, A.D. Inhibition of TRPM2 channels by the antifungal agents clotrimazole and econazole. Naunyn-Schmiedeberg's Arch. Pharmacol. 2004, 370, 227–237. [Google Scholar] [CrossRef] [PubMed]
- Hill, K.; Benham, C. D.; McNulty, S.; Randall, A.D. Flufenamic acid is a pH-dependent antagonist of TRPM2 channels. Neuropharmacology 2004, 47, 450–460. [Google Scholar] [CrossRef] [PubMed]
- Togashi, K.; Inada1, H.; Tominaga, M. Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB). Br. J. Pharmacol. 2008, 153, 1324–1330. [Google Scholar] [CrossRef] [PubMed]
- Bari, M.R.; Akbar, S.; Eweida, M.; Kühn, F.J.; Gustafsson, A.J.; Lückhoff, A.; Islam, M.S. H2O2-induced Ca2+ influx and its inhibition by N-(p-amylcinnamoyl) anthranilic acid in the beta-cells: Involvement of TRPM2 channels. J. Cell. Mol. Med. 2009, 13, 3260–3267. [Google Scholar] [CrossRef] [PubMed]
- Kheradpezhouh, E.; Barritt, G.J.; Rychkov, G.Y. Curcumin inhibits activation of TRPM2 channels in rat hepatocytes. Redox Biol. 2016, 7, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, S.; Yonezawa, R.; Hagiwara, T.; Yoshida, T.; Takahashi, N.; Hamano, S.; Negoro, T.; Toda, T.; Wakamori, M.; Mori, Y.; et al. Inhibitory effects of AG490 on H2O2-induced TRPM2-mediated Ca2+ entry. Eur. J. Pharmacol. 2014, 742, 22–30. [Google Scholar] [CrossRef] [PubMed]
- Toda, T.; Yamamoto, S.; Yonezawa, R.; Mori, Y.; Shimizu, S. Inhibitory effects of Tyrphostin AG-related compounds on oxidative stress-sensitive transient receptor potential channel activation. Eur. J. Pharmacol. 2016, 786, 19–28. [Google Scholar] [CrossRef] [PubMed]
- Berton, G.; Castaldi, M.A.; Cassatella, M.A.; Nauseef, W.M. Celebrating the 50th anniversary of the seminal discovery that the phagocyte respiratory burst enzyme is an NADPH oxidase. J. Leukoc. Biol. 2015, 97, 1–2. [Google Scholar] [CrossRef] [PubMed]
- Lambeth, J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4, 181–189. [Google Scholar] [CrossRef] [PubMed]
- Akira, S.; Takeda, K. Toll-like receproe signaling. Nat. Rev. Immunol. 2004, 4, 499–511. [Google Scholar] [CrossRef] [PubMed]
- Kohchi, C.; Inagawa, H.; Nishizawa, T.; Soma, G. ROS and innate immunity. Anticancer Res. 2009, 29, 817–822. [Google Scholar] [PubMed]
- Schwabe, R.F.; Brenner, D.A. Mechanisms of liver injury. I. TNF-α-induced liver injury: Role of IKK, JNK, and ROS pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, 583–589. [Google Scholar] [CrossRef] [PubMed]
- Simon, H.U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415–418. [Google Scholar] [CrossRef] [PubMed]
- Kalogeris, T.; Bao, Y.; Korthuis, R.J. Mitochondrial reactive oxygen species: A double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol. 2014, 2, 702–714. [Google Scholar] [CrossRef] [PubMed]
- Kleikers, P.W.; Wingler, K.; Hermans, J.J.; Diebold, I.; Altenhöfer, S.; Radermacher, K.A.; Janssen, B.; Görlach, A.; Schmidt, H.H. NADPH oxidases as a source of oxidative stress and molecular target in ischemia/reperfusion injury. J. Mol. Med. 2012, 90, 1391–1406. [Google Scholar] [CrossRef] [PubMed]
- Pacher, P.; Nivorozhkin, A.; Szabó, C. Therapeutic effects of xanthine oxidase inhibitors: Renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 2006, 58, 87–114. [Google Scholar] [CrossRef] [PubMed]
- Luster, A.D. Chemokines—Chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 1998, 338, 436–445. [Google Scholar] [PubMed]
- Haraguchi, K.; Kawamoto, A.; Isami, K.; Maeda, S.; Kusano, A.; Asakura, K.; Shirakawa, H.; Mori, Y.; Nakagawa, T.; Kaneko, S. TRPM2 contributes to inflammatory and neuropathic pain through the aggravation of pronociceptive inflammatory responses in mice. J. Neurosci. 2012, 32, 3931–3941. [Google Scholar] [CrossRef] [PubMed]
- Yonezawa, R.; Yamamoto, S.; Takenaka, M.; Kage, Y.; Negoro, T.; Toda, T.; Ohbayashi, M.; Numata, T.; Nakano, Y.; Yamamoto, T.; et al. TRPM2 channels in alveolar epithelial cells mediate bleomycin-induced lung inflammation. Free Radic. Biol. 2016, 90, 101–113. [Google Scholar] [CrossRef] [PubMed]
- Wehrhahn, J.; Kraft, R.; Harteneck, C.; Hauschildt, S. Transient receptor potential melastatin 2 is required for lipopolysaccharide-induced cytokine production in human monocytes. J. Immunol. 2010, 184, 2386–2393. [Google Scholar] [CrossRef] [PubMed]
- Hardaker, L.; Bahra, P.; de Billy, B.C.; Freeman, M.; Kupfer, N.; Wyss, D.; Trifilieff, A. The ion channel transient receptor potential melastatin-2 does not play a role in inflammatory mouse models of chronic obstructive pulmonary diseases. Respir. Res. 2012, 13, 30. [Google Scholar] [CrossRef] [PubMed]
- Di, A.; Gao, X.; Qian, F.; Kawamura, T.; Han, J.; Hecquet, C.; Ye, R.D.; Vogel, S.M.; Malik, A.B. The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat. Immunol. 2012, 13, 29–34. [Google Scholar] [CrossRef] [PubMed]
- Mohapatra, N.P.; Soni, S.; Rajaram, M.V.; Dang, P.M.; Reilly, T.J.; El-Benna, J.; Clay, C.D.; Schlesinger, L.S.; Gunn, J.S. Francisella acid phosphatases inactivate the NADPH oxidase in human phagocytes. J. Imunnol. 2010, 184, 5141–5150. [Google Scholar] [CrossRef] [PubMed]
- Shakerley, N.L.; Chandrasekaran, A.; Trebak, M.; Miller, B.A.; Melendez, J.A. Francisella tularensis catalase restricts immune function by impairing TRPM2 channel activity. J. Imunnol. 2016, 291, 3871–3881. [Google Scholar]
- Knowles, H.; Heizer, J.W.; Li, Y.; Chapman, K.; Ogden, C.A.; Andreasen, K.; Shapland, E.; Kucera, G.; Mogan, J.; Humann, J.; et al. Transient receptor potential melastatin 2 (TRPM2) ion channel is required for innate immunity against Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 2011, 108, 11578–11583. [Google Scholar] [CrossRef] [PubMed]
- Partida-Sánchez, S.; Cockayne, D.A.; Monard, S.; Jacobson, E.L.; Oppenheimer, N.; Garvy, B.; Kusser, K.; Goodrich, S.; Howard, M.; Harmsen, A.; et al. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat. Med. 2001, 7, 1209–1216. [Google Scholar] [CrossRef] [PubMed]
- Tschopp, J.; Schroder, K. NLRP3 inflammasome activation: The convergence of multiple signaling pathways on ROS production? Nat. Rev. Immunol. 2010, 10, 210–215. [Google Scholar] [CrossRef] [PubMed]
- Zhong, Z.; Zhai, Y.; Liang, S.; Mori, Y.; Han, R.; Sutterwala, F.S.; Qiao, L. TRPM2 links oxidative stress to NLRP3 inflammasome activation. Nat. Commun. 2013, 4, 1611. [Google Scholar] [CrossRef] [PubMed]
- West, A.P.; Shadel, G.S.; Ghosh, S. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11, 389–402. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Surmeier, D.J.; Reiner, A. NMDA and non-NMDA receptor-mediated excitotoxicity are potentiated in cultured striatal neurons by prior chronic depolarization. Exp. Neurol. 1999, 159, 283–296. [Google Scholar] [CrossRef] [PubMed]
- Burgoyne, R.D. Neuronal calcium sensor proteins: Generating diversity in neuronal Ca2+ signaling. Nat. Rev. Neurosci. 2007, 8, 182–193. [Google Scholar] [CrossRef] [PubMed]
- Jia, J.; Verma, S.; Nakayama, S.; Quillinan, N.; Grafe, M.R.; Hurn, P.D.; Herson, P.S. Sex differences in neuroprotection provided by inhibition of TRPM2 channels following experimental stroke. J. Cereb. Blood Flow Metab. 2011, 31, 2160–2168. [Google Scholar] [CrossRef] [PubMed]
- Verma, S.; Quillinan, N.; Yang, Y.; Nakayama, S.; Cheng, J.; Kelley, M.H.; Herson, P.S. TRPM2 channel activation following in vitro ischemia contributes to male hippocampal cell death. Neurosci. Lett. 2012, 530, 41–46. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, T.; Macey, T.A.; Quillinan, N.; Klawitter, J.; Perraud, A.L.; Traystman, R.J.; Herson, P.S. Androgen and PARP-1 regulation of TRPM2 channels after ischemic injury. J. Cereb. Blood Flow Metab. 2013, 33, 1549–1555. [Google Scholar] [CrossRef] [PubMed]
- Alim, I.; Teves, L.; Li, R.; Mori, Y.; Tymianski, M. Modulation of NMDAR subunit expression by TRPM2 channels regulates neuronal vulnerability of ischemic cell death. J. Neurosci. 2013, 33, 17264–17277. [Google Scholar] [CrossRef] [PubMed]
- Gelderblom, M.; Melzer, N.; Schattling, B.; Gob, E.; Hicking, G.; Arunachalam, P.; Bittner, S.; Ufer, F.; Herrmann, A.M.; Bernreuther, C.; et al. Transient receptor potential melastatin subfamily member 2 cation channel regulates detrimental immune cell invasion in ischemic stroke. Stroke 2014, 45, 3395–3402. [Google Scholar] [CrossRef] [PubMed]
- Miller, B.A.; Hoffman, N.E.; Merali, S.; Zhang, X.Q.; Wang, J.; Rajan, S.; Shanmughapriya, S.; Gao, E.; Barrero, C.A.; Mallilankaraman, K.; et al. TRPM2 cahnnels protect against cardiac ischemia-reperfusion injury. J. Biol. Chem. 2014, 289, 7615–7629. [Google Scholar] [CrossRef] [PubMed]
- Hoffman, N.E.; Miller, B.A.; Wang, J.; Elrod, J.W.; Rajan, S.; Gao, E.; Song, J.; Zhang, X.; Hirschler-Laszkiewicz, I.; Shanmughapriya, S.; et al. Ca2+ entry via Trpm2 is essential for cardiac myocyte bioenergetics maintenance. Am. J. Physiol. Heart Circ. Physiol. 2015, 308, H637–H650. [Google Scholar] [CrossRef] [PubMed]
- Hiroi, T.; Wajima, T.; Nrgoro, T.; Ishii, M.; Nakano, Y.; Kiuchi, Y.; Mori, Y.; Shimizu, S. Neutrophil TRPM2 channels are implicated in the exacerbation of myocardial ishchemia/reperfusion injury. Cardiovasc. Res. 2013, 97, 271–281. [Google Scholar] [CrossRef] [PubMed]
- Gao, G.; Wang, W.; Tadagavadi, R.K.; Briley, N.E.; Love, M.I.; Miller, B.A.; Reeves, W.B. TRPM2 mediates ischemic kidney injury and oxidant stress through RAC1. J. Clin. Investig. 2014, 124, 4989–5001. [Google Scholar] [CrossRef] [PubMed]
- Davidson, D.G.; Eastham, W.N. Acute liver necrosis following overdose of paracetamol. BMJ 1966, 2, 497–499. [Google Scholar] [CrossRef] [PubMed]
- Mitchell, J.R.; Jollow, D.J.; Potter, W.Z.; Davis, D.C.; Gillette, J.R.; Brodie, B.B. Acetaminophen-induced hepatic necrosis. I. role of drug metabolism. J. Pharmacol. Exp. Ther. 1971, 187, 185–194. [Google Scholar]
- Kheradpezhouh, E.; Ma, L.; Morphett, A.; Barritt, G.J.; Rychkov, G.Y. TRPM2 channels mediate acetaminophen-induced liver damage. Proc. Natl. Acad. Sci. USA 2014, 111, 3176–3181. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Cotrim, A.; Teos, L.; Zheng, C.; Swaim, W.; Mitchell, J.; Mori, Y.; Ambudkar, I. Loss of TRPM2 function protects against irradiation-induced salivary gland dysfunction. Nat. Commun. 2013, 4, 1515. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, S.; Wajima, T.; Hara, Y.; Nishida, M.; Mori, Y. Transient receptor potential channels in Alzheimer’s disease. Biochim. Biophys. Acta 2007, 1772, 958–967. [Google Scholar] [CrossRef] [PubMed]
- Ostapchenko, V.G.; Chen, M.; Guzman, M.S.; Xie, Y.F.; Lavine, N.; Fan, J.; Beraldo, F.H.; Martyn, A.C.; Belrose, J.C.; Mori, Y.; et al. The transient receptor potential melastatin 2 (TRPM2) channel contributes to β-amyloid oligomer-related neurotoxicity and memory impairment. J. Neurosci. 2015, 35, 15157–15169. [Google Scholar] [CrossRef] [PubMed]
- Zuo, L.; Hemmelgarn, B.T.; Chuang, C.; Besr, T.M. The role of oxidative stress-induced epigenetic alterations in amyloid-β production in Alzheimer’s disease. Oxid. Med. Cell. Longev. 2015, 2015. Article ID 604658. [Google Scholar] [CrossRef] [PubMed]
- Lustbader, J.W.; Cirilli, M.; Lin, C.; Xu, H.W.; Takuma, K.; Wang, N.; Caspersen, C.; Chen, X.; Pollak, S.; Chaney, M.; et al. ABAD directly links Aβ to mitochondrial toxicity in Alzheimer’s disease. Science 2004, 304, 448–452. [Google Scholar] [CrossRef] [PubMed]
- Park, L.; Wang, G.; Moore, J.; Girouard, H.; Zhou, P.; Anrather, J.; Iadecola, C. The key role of transient receptor potential melastatin-2 channels in amyloid-β-induced neurovascular dysfunction. Nat. Commun. 2014, 5, 5318. [Google Scholar] [CrossRef] [PubMed]
© 2016 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license ( http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yamamoto, S.; Shimizu, S. Targeting TRPM2 in ROS-Coupled Diseases. Pharmaceuticals 2016, 9, 57. https://doi.org/10.3390/ph9030057
Yamamoto S, Shimizu S. Targeting TRPM2 in ROS-Coupled Diseases. Pharmaceuticals. 2016; 9(3):57. https://doi.org/10.3390/ph9030057
Chicago/Turabian StyleYamamoto, Shinichiro, and Shunichi Shimizu. 2016. "Targeting TRPM2 in ROS-Coupled Diseases" Pharmaceuticals 9, no. 3: 57. https://doi.org/10.3390/ph9030057