The role of microglia and P2X7 receptors in gliomas

Adinolfi, 2005, Basal activation of the P2X(7) ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth, Mol. Biol. Cell, 16, 3260, 10.1091/mbc.e04-11-1025 Adinolfi, 2012, Expression of P2X7 receptor increases in vivo tumor growth, Cancer Res., 72, 2957, 10.1158/0008-5472.CAN-11-1947 Adinolfi, 2015, Accelerated tumor progression in mice lacking the ATP receptor P2X7, Cancer Res., 75, 635, 10.1158/0008-5472.CAN-14-1259 Alves, 2014, The P2X7 receptor: shifting from a low- to a high-conductance channel — An enigmatic phenomenon?, Biochim. Biophys. Acta, 1838, 2578, 10.1016/j.bbamem.2014.05.015 Amoroso, 2015, The P2X7 receptor is a key modulator of the PI3K/GSK3beta/VEGF signaling network: evidence in experimental neuroblastoma, Oncogene, 34, 5240, 10.1038/onc.2014.444 Arcuri, 2017, Microglia-glioma cross-talk: a two way approach to new strategies against glioma, Front. Biosci., 22, 268, 10.2741/4486 Badie, 2001, Expression of Fas ligand by microglia: possible role in glioma immune evasion, J. Neuroimmunol., 120, 19, 10.1016/S0165-5728(01)00361-7 Barbera-Cremades, 2012, P2X7 receptor-stimulation causes fever via PGE2 and IL-1beta release, FASEB J., 26, 2951, 10.1096/fj.12-205765 Barden, 2014, Non-functional P2X7: a novel and ubiquitous target in human cancer, J. Clin. Cell. Immunol., 5 Bennett, 2016, New tools for studying microglia in the mouse and human CNS, Proc. Natl. Acad. Sci. U. S. A., 113, E1738, 10.1073/pnas.1525528113 Bergamin, 2012, Ectonucleotidases in tumor cells and tumor-associated immune cells: an overview, J. Biomed. Biotechnol., 2012, 959848 Bergamin, 2015, Involvement of purinergic system in the release of cytokines by macrophages exposed to glioma-conditioned medium, J. Cell. Biochem., 116, 721, 10.1002/jcb.25018 Bloch, 2012, Impact of extent of resection for recurrent glioblastoma on overall survival, J. Neurosurg., 117, 1032, 10.3171/2012.9.JNS12504 Boldrini, 2014, P2X7 protein expression and polymorphism in non-small cell lung cancer (NSCLC), J. Negat. Results Biomed., 13 Bondy, 2008, Brain tumor epidemiology: consensus from the brain tumor epidemiology consortium, Cancer., 113, 1953, 10.1002/cncr.23741 Buckner, 2016, Radiation plus Procarbazine, CCNU, and vincristine in low-grade glioma, N. Engl. J. Med., 374, 1344, 10.1056/NEJMoa1500925 Burnstock, 2006, Purinergic signalling, Br. J. Pharmacol., 147, S172, 10.1038/sj.bjp.0706429 Burnstock, 2013, Purinergic signalling and cancer, Purinerg. Signal., 9, 491, 10.1007/s11302-013-9372-5 Burnstock, 2018, The potential of P2X7 receptors as a therapeutic target, including inflammation and tumour progression, Purinerg. Signal., 14, 1, 10.1007/s11302-017-9593-0 Butovsky, 2014, Identification of a unique TGF-β-dependent molecular and functional signature in microglia, Nat. Neurosci., 17, 131, 10.1038/nn.3599 Cardis, 2010, Brain tumour risk in relation to mobile telephone use: results of the INTERPHONE international case-control study, Int. J. Epidemiol., 39, 675, 10.1093/ije/dyq079 Chaichana, 2012, Malignant brain astrocytomas: extent of resection affects survival Chamberlain, 2010, Temozolomide: therapeutic limitations in the treatment of adult high-grade gliomas, Expert. Rev. Neurother., 10, 1537, 10.1586/ern.10.32 Cohen, 2013, IDH1 and IDH2 mutations in gliomas, Curr. Neurol. Neurosci. Rep., 13, 345, 10.1007/s11910-013-0345-4 Coniglio, 2013, Review: molecular mechanism of microglia stimulated glioblastoma invasion, Matrix Biol., 32, 372, 10.1016/j.matbio.2013.07.008 Cuny, 2002, Association of elevated glial expression of interleukin-1beta with improved survival in patients with glioblastomas multiforme, J. Neurosurg., 96, 294, 10.3171/jns.2002.96.2.0294 D'Alimonte, 2015, Potentiation of temozolomide antitumor effect by purine receptor ligands able to restrain the in vitro growth of human glioblastoma stem cells, Purinerg. Signal, 11, 331, 10.1007/s11302-015-9454-7 Dello Russo, 2017, Exploiting microglial functions for the treatment of glioblastoma, Curr. Cancer Drug Targets, 17, 267, 10.2174/1568009616666160813191240 Deshmane, 2009, Monocyte chemoattractant protein-1 (MCP-1): an overview, J. Interf. Cytokine Res., 29, 313, 10.1089/jir.2008.0027 Di Virgilio, 2017, The P2X7 receptor in infection and inflammation, Immunity., 47, 15, 10.1016/j.immuni.2017.06.020 Ellert-Miklaszewska, 2013, Molecular definition of the pro-tumorigenic phenotype of glioma-activated microglia, Glia., 61, 1178, 10.1002/glia.22510 Fahey, 2018, Nitric oxide antagonism to glioblastoma photodynamic therapy and mitigation thereof by BET bromodomain inhibitor JQ1, J. Biol. Chem., 293, 5345, 10.1074/jbc.RA117.000443 Fang, 2011, Expression of macrophage inflammatory protein-1alpha and monocyte chemoattractant protein-1 in glioma-infiltrating microglia: involvement of ATP and P2X7 receptor, J. Neurosci. Res., 89, 199, 10.1002/jnr.22538 Fang, 2013, P2X7R suppression promotes glioma growth through epidermal growth factor receptor signal pathway, Int. J. Biochem. Cell Biol., 45, 1109, 10.1016/j.biocel.2013.03.005 Feng, 2011, Vascular CD39/ENTPD1 directly promotes tumor cell growth by scavenging extracellular adenosine triphosphate, Neoplasia, 13, 206, 10.1593/neo.101332 Ferrari, 1997, Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin, J. Exp. Med., 185, 579, 10.1084/jem.185.3.579 Franceschini, 2015, The P2X7 receptor directly interacts with the NLRP3 inflammasome scaffold protein, FASEB J., 29, 2450, 10.1096/fj.14-268714 Gabrusiewicz, 2016, Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype, JCI Insight., 1, e85841, 10.1172/jci.insight.85841 Galarneau, 2007, Increased glioma growth in mice depleted of macrophages, Cancer Res., 67, 8874, 10.1158/0008-5472.CAN-07-0177 Gehring, 2012, P2X7 receptor activation leads to increased cell death in a radiosensitive human glioma cell line, Purinerg. Signal, 8, 729, 10.1007/s11302-012-9319-2 Gehring, 2015, P2X7 receptor as predictor gene for glioma radiosensitivity and median survival, Int. J. Biochem. Cell Biol., 68, 92, 10.1016/j.biocel.2015.09.001 Giannuzzo, 2015, The P2X7 receptor regulates cell survival, migration and invasion of pancreatic ductal adenocarcinoma cells, Mol. Cancer, 14, 203, 10.1186/s12943-015-0472-4 Giannuzzo, 2016, Targeting of the P2X7 receptor in pancreatic cancer and stellate cells, Int. J. Cancer, 139, 2540, 10.1002/ijc.30380 Gieryng, 2017, Immune microenvironment of gliomas, Lab. Investig., 97, 498, 10.1038/labinvest.2017.19 Gilbert, 2017, A phase I clinical trial demonstrates that nfP2X7-targeted antibodies provide a novel, safe and tolerable topical therapy for basal cell carcinoma, Br. J. Dermatol., 177, 117, 10.1111/bjd.15364 Ginhoux, 2010, Fate mapping analysis reveals that adult microglia derive from primitive macrophages, Science, 330, 841, 10.1126/science.1194637 Glass, 2014, CNS macrophages and peripheral myeloid cells in brain tumours, Acta Neuropathol., 128, 347, 10.1007/s00401-014-1274-2 Goodenberger, 2012, Genetics of adult glioma, Cancer Genet., 205, 613, 10.1016/j.cancergen.2012.10.009 Gosselin, 2017, An environment-dependent transcriptional network specifies human microglia identity, Science, 356, eaal3222, 10.1126/science.aal3222 Graeber, 1994, CR3/43, a marker for activated human microglia: application to diagnostic neuropathology, Neuropathol. Appl. Neurobiol., 20, 406, 10.1111/j.1365-2990.1994.tb00987.x Graeber, 2002, Microglia in brain tumors, Glia, 40, 252, 10.1002/glia.10147 Greig, 2003, Expression of purinergic receptors in non-melanoma skin cancers and their functional roles in A431 cells, J. Invest. Dermatol., 121, 315, 10.1046/j.1523-1747.2003.12379.x Han, 2017, A molecular view of the radioresistance of gliomas, Oncotarget, 8, 100931, 10.18632/oncotarget.21753 Hide, 2000, Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia, J. Neurochem., 75, 965, 10.1046/j.1471-4159.2000.0750965.x Hoelzinger, 2007, Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment, JNCI, 99, 1583, 10.1093/jnci/djm187 Houillier, 2010, IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas, Neurology, 75, 1560, 10.1212/WNL.0b013e3181f96282 Huettner, 1997, Interleukin 10 is expressed in human gliomas in vivo and increases glioma cell proliferation and motility in vitro, Anticancer Res., 17, 3217 Hussain, 2006, The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses, Neuro-Oncology, 8, 261, 10.1215/15228517-2006-008 Jahani-Asl, 2013, iNOS: a potential therapeutic target for malignant glioma, Curr. Mol. Med., 13, 1241, 10.2174/1566524011313080002 Ji, 2018, Involvement of P2X7 receptor in proliferation and migration of human glioma cells, BioMed Res. Int., 2018, 8591397 Johnson, 2012, Recent medical management of glioblastoma Khakh, 2009, The double life of ATP, Sci. Am., 301, 84, 10.1038/scientificamerican1209-84 Klein, 2002, Effect of radiotherapy and other treatment-related factors on mid-term to long-term cognitive sequelae in low-grade gliomas: a comparative study, Lancet, 360, 1361, 10.1016/S0140-6736(02)11398-5 Kleinert, 2003, Regulation of the expression of inducible nitric oxide synthase, Biol. Chem., 384, 1343 Kojima, 2017, Role of ATP as a key signaling molecule mediating radiation-induced biological effects, Dose-Response, 15, 10.1177/1559325817690638 Komohara, 2008, Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas, J. Pathol., 216, 15, 10.1002/path.2370 Lara-Velazquez, 2017, Advances in brain tumor surgery for glioblastoma in adults, Brain Sci., 7, pii, 10.3390/brainsci7120166 Li, 2012, The molecular profile of microglia under the influence of glioma, Neuro-Oncology, 14, 958, 10.1093/neuonc/nos116 Li, 2006, The P2X7 receptor: a novel biomarker of uterine epithelial cancers, Cancer Epidemiol. Biomarker. Prev., 15, 1906, 10.1158/1055-9965.EPI-06-0407 Lisi, 2017, Expression of iNOS, CD163 and ARG-1 taken as M1 and M2 markers of microglial polarization in human glioblastoma and the surrounding normal parenchyma, Neurosci. Lett., 645, 106, 10.1016/j.neulet.2017.02.076 Liu, 2015, Prognostic value of purinergic P2X7 receptor expression in patients with hepatocellular carcinoma after curative resection, Tumour Biol., 36, 5039, 10.1007/s13277-015-3155-2 Liu, 2015, P2X7 receptor predicts postoperative cancer-specific survival of patients with clear-cell renal cell carcinoma, Cancer Sci., 106, 1224, 10.1111/cas.12736 Lorger, 2012, Tumor microenvironment in the brain, Cancers, 4, 218, 10.3390/cancers4010218 Louis, 2007, The 2007 WHO classification of tumours of the central nervous system, Acta Neuropathol., 114, 97, 10.1007/s00401-007-0243-4 Louis, 2016, The 2016 World Health Organization classification of tumors of the central nervous system: a summary, Acta Neuropathol., 131, 803, 10.1007/s00401-016-1545-1 Mackenzie, 2005, Pseudoapoptosis induced by brief activation of ATP-gated P2X7 receptors, J. Biol. Chem., 280, 33968, 10.1074/jbc.M502705200 Markovic, 2005, Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloprotease-2, J. Neuropathol. Exp. Neurol., 64, 754, 10.1097/01.jnen.0000178445.33972.a9 Marumoto, 2012, Molecular biology of glioma, Adv. Exp. Med. Biol., 746, 2, 10.1007/978-1-4614-3146-6_1 McGirt, 2009, Independent association of extent of resection with survival in patients with malignant brain astrocytoma, J. Neurosurg., 110, 156, 10.3171/2008.4.17536 McLarnon, 2017, Roles of purinergic P2X7 receptor in glioma and microglia in brain tumors, Cancer Lett., 402, 93, 10.1016/j.canlet.2017.05.004 Molenaar, 2018, Wild-type and mutated IDH1/2 enzymes and therapy responses, Oncogene, 37, 1949, 10.1038/s41388-017-0077-z Monif, 2009, The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore, J. Neurosci., 29, 3781, 10.1523/JNEUROSCI.5512-08.2009 Monif, 2014, P2X7 receptors are a potential novel target for anti-glioma therapies, J. Inflam., 11, 25, 10.1186/s12950-014-0025-4 Monif, 2016, Interleukin-1beta has trophic effects in microglia and its release is mediated by P2X7R pore, J. Neuroinflammation, 13, 173, 10.1186/s12974-016-0621-8 Morris, 1991, Immunocytochemical study of macrophages and microglial cells and extracellular matrix components in human CNS disease, J. Neurol. Sci., 101, 47, 10.1016/0022-510X(91)90017-2 Nagane, 2009, Prolonged and severe thrombocytopenia with pancytopenia induced by radiation-combined temozolomide therapy in a patient with newly diagnosed glioblastoma--analysis of O6-methylguanine-DNA methyltransferase status, J. Neuro-Oncol., 92, 227, 10.1007/s11060-008-9754-7 Nduom, 2015, Immunosuppressive mechanisms in glioblastoma, Neuro Oncol., 17, vii9, 10.1093/neuonc/nov151 Nimmerjahn, 2005, Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo, Science, 308, 1314, 10.1126/science.1110647 Nishie, 1999, Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas, Clin. Cancer Res., 5, 1107 Pelegrin, 2006, Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor, EMBO J., 25, 5071, 10.1038/sj.emboj.7601378 Pellegatti, 2008, Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase, PLoS One, 3, 10.1371/journal.pone.0002599 Pendergrass, 2018, Cognitive impairment associated with cancer: a brief review, Innov. Clin. Neurosci., 15, 36 Perry, 2016, Chapter 5 - histologic classification of gliomas, 10.1016/B978-0-12-802997-8.00005-0 Perry, 2010, Microglia in neurodegenerative disease, Nat. Rev. Neurol., 6, 193, 10.1038/nrneurol.2010.17 Qian, 2017, High expression of P2X7R is an independent postoperative indicator of poor prognosis in colorectal cancer, Hum. Pathol., 64, 61, 10.1016/j.humpath.2017.03.019 Quail, 2017, The microenvironmental landscape of brain tumors, Cancer Cell, 31, 326, 10.1016/j.ccell.2017.02.009 Rapaport, 1983, Treatment of human tumor cells with ADP or ATP yields arrest of growth in the S phase of the cell cycle, J. Cell. Physiol., 114, 279, 10.1002/jcp.1041140305 Reifenberger, 2016, Advances in the molecular genetics of gliomas — implications for classification and therapy, Nat. Rev. Clin. Oncol., 14, 434, 10.1038/nrclinonc.2016.204 Roessler, 1995, Detection of tumor necrosis factor-alpha protein and messenger RNA in human glial brain tumors: comparison of immunohistochemistry with in situ hybridization using molecular probes, J. Neurosurg., 83, 291, 10.3171/jns.1995.83.2.0291 Roger, 2015, Understanding the roles of the P2X7 receptor in solid tumour progression and therapeutic perspectives, Biochim. Biophys. Acta, 1848, 2584, 10.1016/j.bbamem.2014.10.029 Ryu, 2011, Block of purinergic P2X7R inhibits tumor growth in a C6 glioma brain tumor animal model, J. Neuropathol. Exp. Neurol., 70, 13, 10.1097/NEN.0b013e318201d4d4 Salter, 2017, Microglia emerge as central players in brain disease, Nat. Med., 23, 1018, 10.1038/nm.4397 Sanai, 2008, Glioma extent of resection and its impact on patient outcome, Neurosurgery, 62, 753, 10.1227/01.neu.0000318159.21731.cf Savio, 2018, The P2X7 receptor in inflammatory diseases: angel or demon?, Front. Pharmacol., 9, 52, 10.3389/fphar.2018.00052 Solini, 2008, Increased P2X7 receptor expression and function in thyroid papillary cancer: a new potential marker of the disease?, Endocrinology, 149, 389, 10.1210/en.2007-1223 Sperlágh, 2014, P2X7 receptor: an emerging target in central nervous system diseases, Trends Pharmacol. Sci., 35, 537, 10.1016/j.tips.2014.08.002 Streit, 2005, Role of microglia in the central nervous system's immune response, Neurol. Res., 27, 685, 10.1179/016164105X49463a Stupp, 2005, Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma, N. Engl. J. Med., 352, 987, 10.1056/NEJMoa043330 Sutter, 1991, Antibody-mediated tumor cytotoxicity of microglia, Pathobiology, 59, 254, 10.1159/000163657 Tamajusuku, 2010, Characterization of ATP-induced cell death in the GL261 mouse glioma, J. Cell. Biochem., 109, 983, 10.1002/jcb.22478 Taniguchi, 2000, Antigen-presenting capability of glial cells under glioma-harboring conditions and the effect of glioma-derived factors on antigen presentation, J. Neuroimmunol., 111, 177, 10.1016/S0165-5728(00)00361-1 Tarique, 2015, Phenotypic, functional, and plasticity features of classical and alternatively activated human macrophages, Am. J. Respir. Cell Mol. Biol., 53, 676, 10.1165/rcmb.2015-0012OC Tran, 2017, NOS expression and NO function in glioma and implications for patient therapies, Antioxid. Redox Signal., 26, 986, 10.1089/ars.2016.6820 Villeneuve, 2005, Tumor necrosis factor reduces brain tumor growth by enhancing macrophage recruitment and microcyst formation, Cancer Res., 65, 3928, 10.1158/0008-5472.CAN-04-3612 Volonte, 2003, Extracellular ATP and neurodegeneration, Curr. Drug Targets CNS Neurol. Disord., 2, 403, 10.2174/1568007033482643 Volonte, 2012, P2X7 receptors: channels, pores and more, CNS Neurol. Disord. Drug Targets, 11, 705, 10.2174/187152712803581137 Wagner, 1999, Microglial/macrophage expression of interleukin 10 in human glioblastomas, Int. J. Cancer, 82, 12, 10.1002/(SICI)1097-0215(19990702)82:1<12::AID-IJC3>3.0.CO;2-O Wang, 2008, Hypoxia enhances CXCR4 expression favoring microglia migration via HIF-1α activation, Biochem. Biophys. Res. Commun., 371, 283, 10.1016/j.bbrc.2008.04.055 Wei, 2008, Expression and function of the P2X(7) receptor in rat C6 glioma cells, Cancer Lett., 260, 79, 10.1016/j.canlet.2007.10.025 Wei, 2013, The controversial role of microglia in malignant gliomas, Clin. Dev. Immunol., 2013, 285246, 10.1155/2013/285246 Wen, 2008, Malignant gliomas in adults, N. Engl. J. Med., 359, 492, 10.1056/NEJMra0708126 White, 2005, Human melanomas express functional P2X(7) receptors, Cell Tissue Res., 321, 411, 10.1007/s00441-005-1149-x Williams, 1995, Traffic of hematogenous cells through the central nervous system Wink, 2003, Altered extracellular ATP, ADP and AMP catabolism in glioma cell lines, Cancer Lett., 198, 211, 10.1016/S0304-3835(03)00308-2 Xia, 2015, P2X7 receptor stimulates breast cancer cell invasion and migration via the AKT pathway, Oncol. Rep., 34, 103, 10.3892/or.2015.3979 Yan, 2009, IDH1 and IDH2 mutations in gliomas, N. Engl. J. Med., 360, 765, 10.1056/NEJMoa0808710 Yi, 2011, Glioma-initiating cells: a predominant role in microglia/macrophages tropism to glioma, J. Neuroimmunol., 232, 75, 10.1016/j.jneuroim.2010.10.011 Zhang, 2004, Expression of P2X7 in human hematopoietic cell lines and leukemia patients, Leuk. Res., 28, 1313, 10.1016/j.leukres.2004.04.001 Zhang, 2009, The role of P2X7 receptor in ATP-mediated human leukemia cell death: calcium influx-independent, Acta Biochim. Biophys. Sin., 41, 362, 10.1093/abbs/gmp016 Zheng, 2014, Regulation of the P2X7R by microRNA-216b in human breast cancer, Biochem. Biophys. Res. Commun., 452, 197, 10.1016/j.bbrc.2014.07.101