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Chapter 121 - P2X7

3.3 P2X7 Receptors

P2X7 receptors were first expressed in a mouse microglial cell line, NTW8 (Chessell, Michel, & Humphrey, 1997), and later on rat brain microglia (Yu et al., 2008). Relief of inflammation-induced mechanical hyperalgesia in rats with the P2X7 receptor antagonist, oxidized ATP, was reported (Dell'Antonio et al., 2002). In P2X7 knockout mice, chronic inflammatory and neuropathic pain was abolished, as was release of IL-1β (Chessell et al., 2005). The authors suggested that the P2X7 receptor, via regulation of mature IL-1β production, plays an upstream transductional role in the development of neuropathic and inflammatory pain (see also Clark et al., 2010).

P2X7 receptor blockade reduced nociception in animal models of persistent neuropathic and inflammatory pain (Donnelly-Roberts et al., 2008; Hughes, Hatcher, & Chessell, 2007; Nelson et al., 2008). These findings together with growing evidence supporting the role of P2X7 receptor modulation in proinflammatory IL-1 processing (Ferrari et al., 2006) suggest a specific role for P2X7 receptors in neural–glial cell interactions associated with ongoing pain (Donnelly-Roberts & Jarvis, 2007).

P2X4 and P2X7 receptor knockout mice have a common pain phenotype, but this phenotype appears to be conferred via different mechanisms (Chessell et al., 2006). P2X7 receptor activation through the p38 MAPK system leads to TNF-α production in microglia and treatment with inhibitors of either TNF-α or p38 results in reduction of hyperalgesia (see Teixeira, Oliveira, Parada, & Tambeli, 2010). Immune cells expressing P2X7 receptors play a pivotal role in changes in pain thresholds (Chessell et al., 2005). After injury in a neuropathic pain model, there was increase in expression of P2X7 receptor mRNA and protein in spinal microglia (Kobayashi, Takahashi, Miyagawa, Yamanaka, & Noguchi, 2011). In an acute inflammatory pain model, P2X7 receptors on microglia in vivo were claimed to play a major role in the development of sensitization of nociceptive neurons in rat medullary dorsal horn (Itoh et al., 2011). Activation of P2X7 receptors releases glutamate in the spinal cord, which contributes to mechanical allodynia following partial nerve ligation of the sciatic nerve (Andó & Sperlágh, 2013). Oxaliplatin, an anticancer drug, which has been shown to induce painful neuropathy, causes P2X7 receptor activation (Massicot et al., 2013). The P2X7 receptor antagonist, A438079, prevented the effects on allodynia induced by paclitaxel, another anticancer drug (Ochi-ishi et al., 2014). Peripheral P2X7 receptor activation induced mechanical hyperalgesia via inflammatory mediators, especially bradykinin (Teixeira, de Oliveira-Fusaro, Parada, & Tambeli, 2014). Some of the P2X7 receptor single nucleotide polymorphisms correlate with pain sensitivity, including that in a diabetic pain patient population (Ursu et al., 2014).

Adenosine Metabolism

Jacqueline A. Hubbard, Devin K. Binder, in Astrocytes and Epilepsy, 2016

Human Tissue Studies

P2X7 receptors were found in neurons, astrocytes, and microglia in human patients [159]. Surgically resected tissue from patients with TLE [129] or FCD [159] had elevated P2X7 receptor expression. P2Y1, P2Y2, and P2Y4 receptor expression levels were also elevated in resected epileptic tissue from patients with FCD, tuberous sclerosis complex (TSC), or low-grade astrocytoma compared to autopsy control brains of either patients without epilepsy or patients with gliosis but no seizures [158]. A missense single nucleotide polymorphism (SNP) was commonly found in the P2X7 receptor gene in Caucasian children with febrile seizures compared to febrile cases without seizures [160]. In addition, SNPs were found in toll-like receptor 4 (TLR4), interleukin-6 (IL-6) receptor, and prostaglandin E receptor 3 subtype EP3 (PTGER3) genes, suggesting a link between P2X7 receptors and inflammation [160].

C Immune System and Inflammation

P2X7 receptors located on inflammatory and immune cells play a pivotal role in inflammation and immunomodulation (Di Virgilio, 2007). Purinergic compounds are being explored for the treatment of neurogenic inflammation, rheumatoid arthritis, and periodontitis. ATP-induced apoptosis in macrophages via P2X7 receptors results in killing of the mycobacteria contained within them, in contrast to the macrophage apoptosis produced by other agents (Lammas et al., 1997). The P2X7 receptor plays a fundamental role in lipopolysaccharide signal transduction and activation of macrophages and may therefore represent a therapeutic target for Gram-negative bacterial septicaemia (Sommer et al., 1999). Lesional accumulation of macrophages expressing P2X4 receptors in rat CNS during experimental autoimmune encephalomyelitis (EAE) has been described, and it was suggested that P2X4 receptors might be a valuable marker to dissect the local monocyte heterogeneity in autoimmune disease (Guo & Schluesener, 2005). ATP moderates anti-IgE-induced release of histamine from lung mast cells and may therefore be mechanistically involved in human allergic/asthmatic reactions (Schulman et al., 1999). Alveolar macrophages express P2X7 receptors, which upon stimulation trigger proinflammatory responses, including activation of interleukin (IL)1–6 cytokines and granulomatous reactions (Lemaire & Leduc, 2004).

In addition to the apoptosis mediated by P2X7 receptors, a lower level of activation sometimes results in cell proliferation; it has been suggested that the expression and function of P2X7 receptors on B lymphocytes may correlate with the severity of B-cell chronic lymphocytic leukemia (Adinolfi et al., 2002).

During the acute phase of Trypanosoma cruzi infection, the etiologic agent of Chagas disease, thymic atrophy occurs; ATP also induces cell death in CD4+/CD8+ double-positive thymocytes and may play a central role in thymus atrophy during T. cruzi infection (Mantuano-Barradas et al., 2003). Infection by the parasitic blood fluke Schistosoma mansoni also leads to thymic atrophy. The cloning and characterization of a P2X receptor (schP2X) from S. mansoni provides the first example of a nonvertebrate ATP-gated ion channel and may provide an alternative drug target for the treatment of schistosomiasis (Agboh et al., 2004).

Allopurinal and captopril have a therapeutic effect on granulomatous disorders, such as sarcoidosis, by a direct action on monocyte/macrophage lineage cells partly by downregulation of intracellular adhesion molecular-1 and P2X7 receptors (Mizuno et al., 2004). P2X7 receptors control endocannabinoid production by microglia cells and might constitute promising therapeutics to temper exacerbated microinflammatory responses and allied cell damage (Witting et al., 2004).

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Adaptive Immunity and Genetics of the Host Immune Response

Craig W. Roberts, ... Rima McLeod, in Toxoplasma Gondii (Second Edition), 2014

25.4.2.7 P2X7R

The P2X7 receptor (P2X7R) is inserted into macrophage, neuronal, and other cell membranes and is increased by IFNγ (Fig. 25.24A). Ligation of P2X7R by ATP kills host cells, leading to killing of intracellular pathogens (Lees et al., 2010) (Fig. 25.24B). ATP levels are high in the cytoplasm of these cells, and ATP is released into the extracellular environment when cells are damaged. P2X7R stimulation with extracellular ATP opens a cation-specific ion channel that allows the influx of Ca++ and Na+ and efflux of K+ into the cell (Fig. 25.24D). Prolonged exposure to ATP creates a pore in the cell membrane that increases intracellular Ca++ concentration and allows passage of larger molecules (Fig. 25.24D). This pore formation causes cell lysis via activation of NLRP3 and NFκB, phospholipase D, release of reactive oxygen and nitrogen intermediates, and stimulation of caspases (Zakrzewski, 2011).

In order to determine whether P2X7R contributes to susceptibility to congenital toxoplasmosis, P2X7R SNPs were genotyped from a cohort of 149 children with congenital toxoplasmosis and their available parents from the NCCCTS and 68 individuals with ocular toxoplasmosis from Campos dos Goyatacazes in Brazil (Jamieson et al., 2010) (Fig 25.24E, F). Using transmission disequilibrium testing (TDT), susceptibility alleles of P2X7R were identified (Jamieson et al., 2010; Lees et al., 2010).

To further determine relevance of this susceptibility allele to illness due to the parasite and possible mechanisms involved in susceptibility and resistance mediated by this gene, assays were performed to characterize P2X7R in human monocytes. Macrophage P2X7R function was measured by treatment of human monocyte-derived macrophages with ATP, followed by quantitation of ethidium bromide flux through P2X7R generated pores using flow cytometry (Lees et al., 2010). First, it was found that three persons from the Nepean hospital in Australia with severe toxoplasmosis had reduced or absent P2X7R function (Fig. 25.24G) (Lees et al., 2010): One was heterozygous for 1513A>C, the most common loss-of-function polymorphism. The second was heterozygous for 946G>A and 1096C>G and the third was heterozygous for 946G>A and 1513A>C loss-of-function SNPs. Then, persons in the NCCCTS with a loss-of-function polymorphism in P2X7R (the 1514A>C polymorphism), in addition to those with wild-type P2RX7 who had been identified as above, were studied (Lees et al., 2010). ATP treatment of monocyte-derived macrophages cultured from persons homozygous for the 1513A>C loss-of-function polymorphism did not significantly reduce the number of intracellular T. gondii tachyzoites, whereas ATP treatment of monocyte-derived macrophages from persons with wild-type, with no loss-of-function polymorphisms, reduced the number of parasites (Lees et al., 2010) (Fig. 25.24K).

To prove that P2X7R played a role in toxoplasmosis a murine model of toxoplasmosis was studied. P2X7R function of macrophages from BALB/c mice (i.e. with fully functional P2X7R), C57BL/6J mice (i.e. with a polymorphism with variable effects on P2X7R function), and P2X7R−/− mice on a C57BL/6J background then were studied. ATP treatment of macrophages from BALB/c and C57BL/6J reduced viability of T. gondii, while ATP treatment of P2X7R−/− murine macrophages did not produce a loss of T. gondii viability (Lees et al., 2010) (Fig. 25.24L). There was a similar effect on parasite burden following challenge with type 1 and type 2 parasites in vivo (Lees et al., 2010). Death of the parasite was a function of host cell death and was not due to NO.

Thus, P2X7R plays an important role in immune response to T. gondii in humans. Loss of function of the P2X7R gene inhibits ATP-dependent killing of T. gondii tachyzoites, while ATP-dependent killing contributes to protection when there are wild-type P2X7R or polymorphisms that do not cause loss of function in the receptors. P2X7R is proven to be causal in protection against T. gondii in mouse models (Lees et al., 2010). Lees et al. also recently summarized and discussed P2X7R and some remaining questions about its role in toxoplasmosis in humans.

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Ion channels as therapeutic targets, part B

Elena De Marchi, ... Elena Adinolfi, in Advances in Protein Chemistry and Structural Biology, 2016

Abstract

P2X7 receptor is an ATP-gated cation channel that upon agonist interaction leads to cellular influx of Na+ and Ca2 + and efflux of K+. P2X7 is expressed by a wide variety of cells and its activation mediates a large number of biological processes like inflammation, neuromodulation, cell death or cell proliferation and it has been associated to related pathological conditions including infectious, inflammatory, autoimmune, neurological, and musculoskeletal disorders and, in the last years, to cancer. This chapter describes structural features of P2X7, chemical properties of its agonist, antagonist, and allosteric modulators and summarizes recent advances on P2X7 receptor as therapeutic target in the aforementioned diseases. We also give an overview on recent literature suggesting that P2X7 single-nucleotide polymorphisms could be exploited as diagnostic biomarkers for the development of tailored therapies.

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Role of Autophagy in P2X7 Receptor-Mediated Maturation and Unconventional Secretion of IL-1β in Microglia

Takato Takenouchi, ... Makoto Hashimoto, in Autophagy: Cancer, Other Pathologies, Inflammation, Immunity, Infection, and Aging, 2015

P2X7R-Mediated Regulation of Autophagy

The P2X7R signaling pathway has been reported to be involved in the regulation of autophagy. The membrane-associated form of LC3 (LC3-II) is often used as a marker of autophagosome formation, while LC3 is a cytoplasmic microtubule-associated protein (LC3-I) (Mizushima and Yoshimori, 2007). Using human THP-1 cells and human monocyte-derived macrophages, Biswas et al. (2008) reported that P2X7R activation by ATP increases the expression of LC3-II in an extracellular Ca2+-dependent manner and induces the formation of autophagosome-like structures. They suggested that P2X7R activation induces conventional autophagy and that induced autophagy positively contributes to the ATP-induced rapid killing of intracellular mycobacteria in Mycobacterium bovis BCG-infected macrophages.

Similarly, we reported that the expression of LC3-II and the formation of autophagosome-like structures are upregulated by the activation of P2X7R in mouse microglial cells (Takenouchi et al., 2009b). However, we also showed that P2X7R activation induces the dysregulation of lysosomal functions by increasing lysosomal pH in a Ca2+ influx-dependent manner and triggers the secretion of components derived from lysosome-related organelles, such as phagolysosomes and autolysosomes, via exocytosis (Figure 14.2B). Based on these findings, we proposed that P2X7R activation results in the impairment of basal autophagy flux via lysosome dysfunction and promotes the secretion of phagolysosomal/autolysosomal components to further eliminate undigested components or bacteria by exposing them to digestion or rapid killing by adjacent neutrophils or macrophages.

The precise reason for the discrepancies between our results and those of Biswas et al. is unclear. However, they could be due to the differences between the two experimental systems; i.e., while monocytes/THP-1 cells and live mycobacteria were used by Biswas et al., microglial cells and inactivated E. coli were employed in our study. Future studies are required to demonstrate whether the P2X7R activation-based mechanisms regulating lysosomal fusion and exocytotic processes differ between immune cell types and different pathogens.

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Annual Reports in Medicinal Chemistry

Allen T. Hopper, ... Roland G.W. Staal, in Annual Reports in Medicinal Chemistry, 2012

2.1.2 P2X7 receptor (P2X7R)

The P2X7R is activated by high extracellular concentrations of ATP (> 100 μM) that leads to Ca2 + influx/K+ efflux and initiation of a cascade leading to maturation and release of the proinflammatory cytokine IL-1β. In the CNS, P2X7R is primarily expressed on microglia, oligodendrocytes, and activated astrocytes, though the data supporting neuronal expression are controversial. Elevated receptor expression and function have been associated with various CNS diseases, including depression, AD, MS, epilepsy, ALS, and neuropathic pain.18 Several compounds have entered clinical trials for peripheral indications, but to date, this target has not been probed clinically for a CNS indication. 1-Hydroxycycloheptyl analog 4 (CE-224,535) is a potent human P2X7R antagonist that inhibits IL-1β release from lipopolysaccharide (LPS)- and ATP-stimulated human whole blood with IC50 and IC90 values of 1.0 and 4.7 nM, respectively.27 This candidate was evaluated in a clinical trial for rheumatoid arthritis, but failed to show significant efficacy, even with trough free plasma concentrations significantly above the IC90 in human whole blood. The CNS penetrability of this compound is not reported, and it lacks sufficient rodent P2X7R potency for testing in preclinical models, a common issue with P2X7R antagonists due to wide differences in receptor homology across species.

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Many of the early P2X7R antagonists either lack sufficient CNS penetration or rodent P2X7R antagonist activity to support testing in preclinical in vivo NI models. However, there have been recent advances in overcoming these challenges. For instance, 2-cyano-guanidine analog 5 (A-804598) is one of the few selective P2X7R antagonists with good CNS penetration and similar activity in human, rat, and mouse (P2X7R IC50: 11, 10, and 9 nM, respectively), thus making it a potential tool compound to probe preclinical rodent models where NI is a component. In addition, tritiation of 5 at the 4-position of the phenyl ring (6) provides a radioligand with high specific activity.28

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A series of pyroglutamic acid amides, represented by 7, with a human pIC50 of 8.5 and a rat pIC50 of 6.5 were reported recently. While 7 is 100-fold less active in rat, efficacy was still observed in a rat model of Freund's complete adjuvant (FCA)-induced centralized inflammatory knee joint pain and in a chronic constriction injury model of neuropathic pain. Exposure at the minimal effective doses provided free drug fractions in excess of the rat pIC50 in both the periphery and the CNS.29 The importance of CNS activity in the FCA knee joint pain model was supported by a comparative study of 2-oxo-4-imidazolidinecarboxamide analogs 8 and 9 differing in their brain penetration capabilities. Compound 9 which was inactive in the FCA model had superior free plasma exposure and P2X7R potency, but poor brain penetration. On the other hand, the less potent, brain penetrant P2X7R antagonist 8 showed efficacy in this knee joint pain model.30

In summary, significant progress has been made in identifying tools that offer both sufficient CNS penetration and rodent potency to probe the utility of P2X7R antagonism for the treatment of disease where NI is present.

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Spider Peptides

Graham M. Nicholson, in Handbook of Biologically Active Peptides (Second Edition), 2013

Purinergic (P2X) Receptors

P2X1–P2X7 purinergic receptors are ATP-gated cation-selective ion channels, of which some subtypes are associated with the transmission of nociception. In particular, P2X3 receptors are involved in a wide range of pain states. Purotoxin-1 from Geolycosa sp. is the first potent and selective modulator of P2X3 receptors from spider venom (Fig. 5). This 35-residue ICK peptide produces potent analgesic effects in the low nanomolar range in a variety of inflammatory pain models. This involves a complex mechanism of action to prolong the rate of recovery from P2X3 channel desensitization.10 Thus, purotoxin-1 represents a promising lead compound for the development of analgesics targeting P2X3 receptors.

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Receptors on Autonomic Neurons and Neuroeffector Cells: Purinergic Receptors☆

Gillian E. Knight, in Reference Module in Neuroscience and Biobehavioral Psychology, 2017

Connective Tissue

Fibroblasts express predominately P2X7 receptors, involved in cell death, in addition to P2Y1 and P2Y2 receptors, shown to be involved in the control of proliferation. Fibroblasts express all of the adenosine receptor subtypes; in particular the A2A receptor has been shown to be involved in stimulating wound healing.

Brown adipocytes express multiple P2X and P2Y receptor, although the dominant functional receptors belong to the P2Y1 and P2Y2 or P2Y4 subtypes. While a functional P2Y receptor has been described in white adipocytes, it has yet to be characterized. A1 receptors have been shown to be expressed by both brown and white adipocytes.

Cod A1 ,A2,A3 ,A4