Alternative splicing of P2RX7 pre-messenger RNA in health and diseases: Myth or reality?

Chow, 1977, An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA, Cell, 12, 1, 10.1016/0092-8674(77)90180-5 Tazi, 2009, Alternative splicing and disease, Biochim Biophys Acta – Mol Basis Dis, 1792, 14, 10.1016/j.bbadis.2008.09.017 Bessonov, 2010, Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis, RNA, 16, 2384, 10.1261/rna.2456210 Chabot, 2016, Defective control of pre-messenger RNA splicing in human disease, J Cell Biol, 212, 13, 10.1083/jcb.201510032 Keren, 2010, Alternative splicing and evolution: diversification, exon definition and function, Nat Rev Genet, 11, 345, 10.1038/nrg2776 Buratti, 2006, Defective splicing, disease and therapy: searching for master checkpoints in exon definition, Nucleic Acids Res, 34, 3494, 10.1093/nar/gkl498 Stamm, 2008, Regulation of alternative splicing by reversible protein phosphorylation, J Biol Chem, 283, 1223, 10.1074/jbc.R700034200 Pan, 2008, Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing, Nat Genet, 40, 1413, 10.1038/ng.259 Wang, 2008, Alternative isoform regulation in human tissue transcriptomes, Nature, 456, 470, 10.1038/nature07509 Kim, 2018, Alternative splicing isoforms in health and disease, Pflugers Arch Eur J Physiol, 470, 995, 10.1007/s00424-018-2136-x Merkin, 2012, Evolutionary dynamics of gene and isoform regulation in mammalian tissues, Science (80), 338, 1593, 10.1126/science.1228186 Cesaro, 2010, Amplification loop of the inflammatory process is induced by P2X 7 R activation in intestinal epithelial cells in response to neutrophil transepithelial migration, Am J Physiol Cell Physiol, 299, 32 Mishra, 2011, Purinergic P2X 7 receptor regulates lung surfactant secretion in a paracrine manner, J Cell Sci, 124, 657, 10.1242/jcs.066977 Ruzsnavszky, 2011, Journal of Photochemistry and Photobiology B : biology UV-B induced alteration in purinergic receptors and signaling on HaCaT keratinocytes, J Photochem Photobiol B Biol, 105, 113, 10.1016/j.jphotobiol.2011.07.009 Jørgensen, 2002, Intercellular calcium signaling occurs between human osteoblasts and osteoclasts and requires activation of osteoclast P2X7 receptors *, J Biol Chem, 277, 7574, 10.1074/jbc.M104608200 Solini, 1999, Human primary fibroblasts in vitro express a purinergic P2X 7 receptor coupled to ion fluxes, microvesicle formation and IL-6 release, J Cell Sci, 305, 297, 10.1242/jcs.112.3.297 Sluyter, 2004, Extracellular ATP increases cation fluxes in human erythrocytes by activation of the P2X 7 receptor *, J Biol Chem, 279, 44749, 10.1074/jbc.M405631200 Georgiou, 2005, Human epidermal and monocyte-derived langerhans cells express functional P2X 7 receptors, J Investig Dermatol, 125, 482, 10.1111/j.0022-202X.2005.23835.x Baroni, 2007, Stimulation of P2 ( P2X 7 ) receptors in human dendritic cells induces the release of tissue factor-bearing microparticles, FASEB J, 21, 1926, 10.1096/fj.06-7238com Idzko, 2002, Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors, Blood, 100, 925, 10.1182/blood.V100.3.925 Christenson, 2008, Serum amyloid A inhibits apoptosis of human neutrophils via a P2X7-sensitive pathway independent of formyl peptide receptor like 1, J Leukoc Biol, 83, 139, 10.1189/jlb.0507276 Wareham, 2009, Functional evidence for the expression of P2X1, P2X4 and P2X7 receptors in human lung mast cells abbreviations, Br J Pharmacol, 157, 1215, 10.1111/j.1476-5381.2009.00287.x Gu, 2000, Expression of P2X7 purinoceptors on human lymphocytes and monocytes: evidence for nonfunctional P2X7 receptors, Am J Physiol Cell Physiol, 279, 1189, 10.1152/ajpcell.2000.279.4.C1189 Chiozzi, 1997, Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X 7 receptor, J Cell Biol, 138, 697, 10.1083/jcb.138.3.697 Borges, 2018, Fitness of long-lived memory CD8 + T cells, Nature, 559, 264, 10.1038/s41586-018-0282-0 Idzko, 2001, Functional characterization of P2Y and P2X receptors in human eosinophils, J Cell Physiol, 188, 329, 10.1002/jcp.1129 Bianchi, 2014, ATP/P2X7 axis modulates myeloid-derived suppressor cell functions in neuroblastoma microenvironment, Cell Death Dis, 5, 10.1038/cddis.2014.109 Deli, 2007, Functional genomics of calcium channels in human melanoma cells, Int J Cancer, 121, 55, 10.1002/ijc.22621 Solini, 2008, Increased P2X 7 receptor expression and function in thyroid papillary cancer : a new potential marker of the disease?, Endocrinology, 149, 389, 10.1210/en.2007-1223 Vázquez-cuevas, 2014, Paracrine stimulation of P2X7 receptor by ATP activates a proliferative pathway in ovarian carcinoma cells, J Cell Biochem, 1966, 1955 Santos, 2017, Potential role of P2X7R in esophageal squamous cell carcinoma proliferation, Purine Pyrimidine Recept Pharmacol (Jacobson KA, Linden J, Eds), 13, 279 Li, 2009, P2X 7 receptor expression is decreased in epithelial cancer cells of ectodermal, uro-genital sinus, and distal paramesonephric duct origin, Purinergic Signal, 5, 351, 10.1007/s11302-009-9161-3 Adinolfi, 2002, Brief report P2X 7 receptor expression in evolutive and indolent forms of chronic B lymphocytic leukemia, Blood, 99, 706, 10.1182/blood.V99.2.706 Zhang, 2004, Expression of P2X7 in human hematopoietic cell lines and leukemia patients, Leuk Res, 28, 1313, 10.1016/j.leukres.2004.04.001 Chong, 2010, Abnormal expression of P2X family receptors in Chinese pediatric acute leukemias, Biochem Biophys Res Commun, 391, 498, 10.1016/j.bbrc.2009.11.087 Pineda, 2018, Most human introns are recognized via multiple and tissue-specific branchpoints, Genes Dev, 32, 577, 10.1101/gad.312058.118 Kaczmarek-Hajek, 2018, Re-evaluation of neuronal P2X7 expression using novel mouse models and a P2X7-specific nanobody, Elife, 7, 1, 10.7554/eLife.36217 Barbosa-Morais, 2012, The evolutionary landscape of alternative splicing in vertebrate species, Science (80), 338, 1587, 10.1126/science.1230612 Graveley, 2001, Alternative splicing: increasing diversity in the proteomic world, Trends Genet, 17, 100, 10.1016/S0168-9525(00)02176-4 Czubaty, 2017, Protein kinases that phosphorylate splicing factors: roles in cancer development, progression and possible therapeutic options, Int J Biochem Cell Biol, 91, 102, 10.1016/j.biocel.2017.05.024 Lim, 2011, Using positional distribution to identify splicing elements and predict pre-mRNA processing defects in human genes, Proc Natl Acad Sci Unit States Am, 108, 11093, 10.1073/pnas.1101135108 Carazo, 2018, Upstream analysis of alternative splicing: a review of computational approaches to predict context-dependent splicing factors, Briefings Bioinf, 1 Montes, 2019, RNA splicing and disease: animal models to therapies, Trends Genet, 35, 68, 10.1016/j.tig.2018.10.002 Drury, 1929, The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart, J Physiol, 68, 213, 10.1113/jphysiol.1929.sp002608 Burnstock, 1985, Is there a basis for distinguishing two types of purinergic receptor, Gen Pharmacol, 16, 141, 10.1016/0306-3623(85)90001-1 Jacobson, 2009, Introduction to adenosine receptors as therapeutic targets, Handb Exp Pharmacol, 193, 1, 10.1007/978-3-540-89615-9_1 Burnstock, 2000, P2 purinergic receptors: modulation of cell function and therapeutic potential, J Pharmacol Exp Ther, 23, 862 North, 2002, Molecular physiology of P2X receptors, Physiol Rev, 82, 1013, 10.1152/physrev.00015.2002 Surprenant, 1996, The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7), Science (80-), 272, 735, 10.1126/science.272.5262.735 Denlinger, 2001, Cutting edge: the nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide, J Immunol, 167, 1871, 10.4049/jimmunol.167.4.1871 Burnstock, 2011, P2X receptors in health and disease, vol. 61, 333 Darmellah, 2012, Ezrin/radixin/moesin are required for the purinergic P2X7 receptor (P2X7R)-dependent processing of the amyloid precursor protein, J Biol Chem, 287, 34583, 10.1074/jbc.M112.400010 Sluyter, 2017, The P2X7 receptor, Adv Exp Med Biol, 1051, 17, 10.1007/5584_2017_59 Mellouk, 2019, CD8 + , but not CD4 + effector/memory T cells, express the CD44 high CD45RB high phenotype with aging, which displays reduced expression levels of P2X 7 receptor and ATP-induced cellular responses, FASEB J, 33, 3225, 10.1096/fj.201800867R Karasawa, 2016, Structural basis for subtype-specific inhibition of the P2X7 receptor, Elife, 5, 10.7554/eLife.22153 Kasuya, 2017, Structural insights into the nucleotide base specificity of P2X receptors, Sci Rep, 7, 45208, 10.1038/srep45208 Kawate, 2009, Crystal structure of the ATP-gated P2X4ion channel in the closed state, Nature, 460, 592, 10.1038/nature08198 Hattori, 2012, A fluorescence-detection size-exclusion chromatography-based thermostability assay to identify membrane protein expression and crystallization conditions, Structure, 20, 1293, 10.1016/j.str.2012.06.009 Mansoor, 2016, X-ray structures define human P2X 3 receptor gating cycle and antagonist action, Nature, 538, 66, 10.1038/nature19367 Karasawa, 2017, The P2X7 receptor forms a dye-permeable pore independent of its intracellular domain but dependent on membrane lipid composition, Elife, 6, 10.7554/eLife.31186 Gonnord, 2009, Palmitoylation of the P2X7 receptor, an ATP-gated channel, controls its expression and association with lipid rafts, FASEB J, 23, 795, 10.1096/fj.08-114637 Robinson, 2014, Plasma membrane cholesterol as a regulator of human and rodent P2X7 receptor activation and sensitization, J Biol Chem, 289, 31983, 10.1074/jbc.M114.574699 Allsopp, 2015, Contribution of the juxtatransmembrane intracellular regions to the time course and permeation of ATP-gated P2X7 receptor ion channels, J Biol Chem, 290, 14556, 10.1074/jbc.M115.642033 Pippel, 2017, Localization of the gate and selectivity filter of the full-length P2X7 receptor, Proc Natl Acad Sci USA, 114, 2156, 10.1073/pnas.1610414114 Harkat, 2017, On the permeation of large organic cations through the pore of ATP-gated P2X receptors, Proc Natl Acad Sci USA, 114, 3786, 10.1073/pnas.1701379114 Di Virgilio, 2018, The elusive P2X7 macropore, Trends Cell Biol, 28, 392, 10.1016/j.tcb.2018.01.005 Cheewatrakoolpong, 2005, Identification and characterization of splice variants of the human P2X7ATP channel, Biochem Biophys Res Commun, 332, 17, 10.1016/j.bbrc.2005.04.087 Adinolfi, 2010, Trophic activity of a naturally occurring truncated isoform of the P2X7 receptor, FASEB J, 24, 3393, 10.1096/fj.09-153601 Smart, 2003, P2X7 receptor cell surface expression and cytolytic pore formation are regulated by a distal C-terminal region, J Biol Chem, 278, 8853, 10.1074/jbc.M211094200 Denlinger, 2003, Mutation of a dibasic amino acid motif within the C terminus of the P2X7 nucleotide receptor results in trafficking defects and impaired function, J Immunol, 171, 1304, 10.4049/jimmunol.171.3.1304 Murrell-Lagnado, 2008, Assembly and trafficking of P2X purinergic receptors (Review), Mol Membr Biol, 25, 321, 10.1080/09687680802050385 Feng, 2006, A truncated P2X7 receptor variant (P2X7-j) endogenously expressed in cervical cancer cells antagonizes the full-length P2X7 receptor through hetero-oligomerization, J Biol Chem, 281, 17228, 10.1074/jbc.M602999200 Guzman-Aranguez, 2017, Hyperosmotic stress induces ATP release and changes in P2X7 receptor levels in human corneal and conjunctival epithelial cells, Purinergic Signal, 13, 249, 10.1007/s11302-017-9556-5 Kido, 2014, Regulation of activity of P2X7 receptor by its splice variants in cultured mouse astrocytes, Glia, 62, 440, 10.1002/glia.22615 Nicke, 2009, A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice, J Biol Chem, 284, 25813, 10.1074/jbc.M109.033134 Schwarz, 2012, Alternative splicing of the N-terminal cytosolic and transmembrane domains of P2X7 controls gating of the ion channel by ADP-ribosylation, PLoS One, 7, 10.1371/journal.pone.0041269 Haanes, 2012, The P2X7 receptor supports both life and death in fibrogenic pancreatic stellate cells, PLoS One, 7, 10.1371/journal.pone.0051164 Masin, 2012, Expression, assembly and function of novel C-terminal truncated variants of the mouse P2X7 receptor: Re-evaluation of P2X7 knockouts, Br J Pharmacol, 165, 978, 10.1111/j.1476-5381.2011.01624.x Csóka, 2015, Extracellular ATP protects against sepsis through macrophage P2X7 purinergic receptors by enhancing intracellular bacterial killing, FASEB J, 29, 3626, 10.1096/fj.15-272450 Metzger, 2016, Genetically dissecting P2rx7 expression within the central nervous system using conditional humanized mice, 13, 153 Gudipaty, 2001, Regulation of P2X7 nucleotide receptor function in human monocytes by extracellular ions and receptor density, Am J Physiol Cell Physiol, 280, C943, 10.1152/ajpcell.2001.280.4.C943 Gudipaty, 2003, Essential role for Ca 2 + in regulation of IL-1β secretion by P2X 7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells, Am J Physiol Physiol, 285, C286, 10.1152/ajpcell.00070.2003 Rissiek, 2015, P2X7 on mouse T cells: one channel, many functions, Front Immunol, 6, 1, 10.3389/fimmu.2015.00204 Liang, 2015, Quantifying Ca 2+ current and permeability in ATP-gated P2X7 receptors, J Biol Chem, 290, 7930, 10.1074/jbc.M114.627810 Barden, 2014, Non-functional P2X7: a novel and ubiquitous target in human cancer, J Clin Cell Immunol, 05, 237, 10.4172/2155-9899.1000237 Buell, 1998, Blockade of human P2X7 receptor function with a monoclonal antibody, Blood, 92, 3521, 10.1182/blood.V92.10.3521 Kim, 2001, Proteomic and functional evidence for a P2X7 receptor signalling complex, EMBO J, 20, 6347, 10.1093/emboj/20.22.6347 Sluyter, 2011, Significance of P2X7 receptor variants to human health and disease, Recent Pat DNA Gene Sequences, 5, 41, 10.2174/187221511794839219 Zhang, 2013, Misregulation of pre-mRNA alternative splicing in cancer, Cancer Discov, 3, 1228, 10.1158/2159-8290.CD-13-0253 Wu, 2015, AT-AC pre-mRNA splicing mechanisms and conservation of minor introns in voltage-gated ion channel genes, Mol Cell Biol, 19, 3225, 10.1128/MCB.19.5.3225 Adinolfi, 2012, Expression of P2X7 receptor increases in vivo tumor growth, Cancer Res, 72, 2957, 10.1158/0008-5472.CAN-11-1947 Pellegatti, 2008, Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase, PLoS One, 3, 1, 10.1371/journal.pone.0002599 Barden, 2003, Specific detection of non-functional human P2X7 receptors in HEK293 cells and B-lymphocytes, FEBS Lett, 538, 159, 10.1016/S0014-5793(03)00172-8 Slater, 2004, Differentiation between cancerous and normal hyperplastic lobules in breast lesions, Breast Cancer Res Treat, 83, 1, 10.1023/B:BREA.0000010670.85915.0f Gilbert, 2018, ATP in the tumour microenvironment drives expression of nfP2X7, a key mediator of cancer cell survival, Oncogene, 38, 194, 10.1038/s41388-018-0426-6 Zaidi, 2013, Lipogenesis and lipolysis: the pathways exploited by the cancer cells to acquire fatty acids, Prog Lipid Res, 52, 585, 10.1016/j.plipres.2013.08.005 Rysman, 2010, De novo lipogenesis protects cancer cells from free radicals and chemotherapeutics by promoting membrane lipid saturation, Cancer Res, 70, 8117, 10.1158/0008-5472.CAN-09-3871 Garcia-Marcos, 2006, P2X7 and phospholipid signalling: the search of the “missing link” in epithelial cells, Cell Signal, 18, 2098, 10.1016/j.cellsig.2006.05.008 Le Stunff, 2007, P2X7 receptor-mediated phosphatidic acid production delays ATP-induced pore opening and cytolysis of RAW 264.7 macrophages, Cell Signal, 19, 1909, 10.1016/j.cellsig.2007.04.015 Costa-Junior, 2011, Lipid metabolism modulation by the P2X7 receptor in the immune system and during the course of infection: new insights into the old view, Purinergic Signal, 7, 381, 10.1007/s11302-011-9255-6 Pan, 2016, P2RX7-V3 is a novel oncogene that promotes tumorigenesis in uveal melanoma, Tumor Biol, 37, 13533, 10.1007/s13277-016-5141-8 Fernandes, 2019, Long non-coding RNAs in the regulation of gene expression: physiology and disease, Non-Coding RNA, 5, E17, 10.3390/ncrna5010017 Kahles, 2019, Comprehensive analysis of alternative splicing across tumor form 8705 patients, Cancer Cell, 34, 211, 10.1016/j.ccell.2018.07.001