Adenosine Inhibits Cell Proliferation Differently in Human Astrocytes and in Glioblastoma Cell Lines

Alarcón, 2020, Decreased equilibrative nucleoside transporter 1 (ENT1) activity contributes to the high extracellular adenosine levels in mesenchymal glioblastoma stem-like cells, Cells, 9, 1914, 10.3390/cells9081914 Azambuja, 2020, CD73 as a target to improve temozolomide chemotherapy effect in glioblastoma preclinical model, Cancer Chemother Pharmacol, 85, 1177, 10.1007/s00280-020-04077-1 Azambuja, 2020, Blockade of CD73 delays glioblastoma growth by modulating the immune environment, Cancer Immunol Immunother, 69, 1801, 10.1007/s00262-020-02569-w Bar, 2011, Glioblastoma, cancer stem cells and hypoxia, Brain Pathol, 21, 11929, 10.1111/j.1750-3639.2010.00460.x Bicíková, 2006, Aminothiols in human brain tumors, Clin Chem Lab Med, 44, 978, 10.1515/CCLM.2006.170 Boison, 2008, The adenosine kinase hypothesis of epileptogenesis, Prog Neurobiol, 84, 249, 10.1016/j.pneurobio.2007.12.002 Boison, 2013, Adenosine kinase: exploitation for therapeutic gain, Pharmacol Rev, 65, 906, 10.1124/pr.112.006361 Boison, 2013, Homeostatic control of brain function new approaches to understand epileptogenesis, Front Cell Neurosci, 7, 109, 10.3389/fncel.2013.00109 Cascalheira, 2015, Association of the transcobalamin II gene 776C→G polymorphism with Alzheimer’s type dementia: dependence on the 5,10-methylenetetrahydrofolate reductase 1298A→G polymorphism genotype, Ann Clin Biochem, 52, 448, 10.1177/0004563214561770 Cascalheira, 2009, Serum homocysteine: Interplay with other circulating and genetic factors in association to Alzheimer's type dementia, Clin Biochem, 42, 783, 10.1016/j.clinbiochem.2009.02.006 Ceruti, 2013, Adenosine signaling in glioma cells, Adv Exp Med Biol, 986, 13, 10.1007/978-94-007-4719-7_2 Chen, 2019, 5'-Iodotubercidin represses insulinoma-associated-1 expression, decreases cAMP levels, and suppresses human neuroblastoma cell growth, J Biol Chem, 294, 5456, 10.1074/jbc.RA118.006761 Ciccarelli, 1994, Effects of exogenous ATP and related analogues on the proliferation rate of dissociated primary cultures of rat astrocytes, J Neurosci Res, 39, 556, 10.1002/jnr.490390507 Daniele, 2014, Modulation of A1 and A2B adenosine receptor activity: a new strategy to sensitise glioblastoma stem cells to chemotherapy, Cell Death Dis, 5, 10.1038/cddis.2014.487 Daré, 2007, Modulation of glial cell functions by adenosine receptors, Physiol Behav, 92, 15, 10.1016/j.physbeh.2007.05.031 de Groot, 2012, Overexpression of ADK in human astrocytic tumors and peritumoral tissue is related to tumor-associated epilepsy, Epilepsia, 53, 58, 10.1111/j.1528-1167.2011.03306.x Di Iorio, 2002, Mechanisms of apoptosis induced by purine nucleosides in astrocytes, Glia, 38, 179, 10.1002/glia.10055 Dias, 2013, Adenosine: setting the stage for plasticity, Trends Neurosci, 36, 248, 10.1016/j.tins.2012.12.003 Fredholm, 2001, International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors, Pharmacol Rev, 53, 527 Gessi, 2010, Modulation of metalloproteinase-9 in U87MG glioblastoma cells by A3 adenosine receptors, Biochem Pharmacol, 79, 1483, 10.1016/j.bcp.2010.01.009 Golembiowska, 1996, Adenosine kinase inhibitors augment release of adenosine from spinal cord slices, Eur J Pharmacol, 307, 157, 10.1016/0014-2999(96)00248-8 Han, 2014, Aberrant DNA methylation of the PDGF gene in homocysteine-mediated VSMC proliferation and its underlying mechanism, Mol Med Rep, 10, 947, 10.3892/mmr.2014.2249 Huang, 2015, Adenosine deaminase and adenosine kinase expression in human glioma and their correlation with glioma-associated epilepsy, Mol Med Rep, 12, 6509, 10.3892/mmr.2015.4285 Jarvis, 2000, J Pharmacol Exp Ther, 295, 1156 Klohs, 1992, Pentostatin: future directions, Pharmacol Rev, 44, 459 Kulik, 2010, The relationship between oxygen and adenosine in astrocytic cultures, Glia, 58, 1335, 10.1002/glia.21011 Latini, 1999, Extracellular adenosine concentrations during in vitro ischemia in rat hippocampal slices, Br J Pharmacol, 127, 729, 10.1038/sj.bjp.0702591 Liu, 2014, The HIF-2alpha dependent induction of PAP and adenosine synthesis regulates glioblastoma stem cell function through the A2B adenosine receptor, Int J Biochem Cell Biol, 49, 8, 10.1016/j.biocel.2014.01.007 Lopes, 2011, Adenosine and related drugs in brain diseases: present and future in clinical trials, Curr Top Med Chem, 11, 1087, 10.2174/156802611795347591 Marcelino, 2020, Adenosine inhibits human astrocyte proliferation independently of adenosine receptor activation, J Neurochem, 153, 455, 10.1111/jnc.14937 Massillon, 1994, Identification of the glycogenic compound 5-iodotubercidin as a general protein kinase inhibitor, Biochem J, 299, 123, 10.1042/bj2990123 Mattson, 2003, Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders, Trends Neurosci, 26, 137, 10.1016/S0166-2236(03)00032-8 Merighi, 2007, Hypoxia inhibits paclitaxel-induced apoptosis through adenosine-mediated phosphorylation of bad in glioblastoma cells, Mol Pharmacol, 72, 162, 10.1124/mol.106.031849 Michel, 1999, Adenosine prevents the death of mesencephalic dopaminergic neurons by a mechanism that involves astrocytes, J Neurochem, 72, 2074, 10.1046/j.1471-4159.1999.0722074.x Minniti, 2009, Chemotherapy for glioblastoma: current treatment and future perspectives for cytotoxic and targeted agents, Anticancer Res, 29, 5171 Niechi, 2019, Adenosine depletion as a new strategy to decrease glioblastoma stem-like cells aggressiveness, Cells, 8, 1353, 10.3390/cells8111353 Parhamifar, 2013, Lactate dehydrogenase assay for assessment of polycation cytotoxicity, Methods Mol Biol, 948, 13, 10.1007/978-1-62703-140-0_2 Parkinson, 1996, Effects of iodotubercidin on adenosine kinase activity and nucleoside transport in DDT1 MF-2 smooth muscle cells, J Pharmacol Exp Ther, 277, 1397 Pietrobono, 2020, High adenosine extracellular levels induce glioblastoma aggressive traits modulating the mesenchymal stromal cell secretome, Int J Mol Sci, 21, E7706, 10.3390/ijms21207706 Pignataro, 2008, Downregulation of hippocampal adenosine kinase after focal ischemia as potential endogenous neuroprotective mechanism, J Cereb Blood Flow Metab, 28, 17, 10.1038/sj.jcbfm.9600499 Pinto, 2016, The role of cGMP on adenosine A 1 receptor-mediated inhibition of synaptic transmission at the hippocampus, Front Pharmacol, 7, 103, 10.3389/fphar.2016.00103 Quezada, 2013, 5'-ectonucleotidase mediates multiple-drug resistance in glioblastoma multiforme cells, J Cell Physiol, 228, 602, 10.1002/jcp.24168 Sai, 2006, A(1) adenosine receptor signal and AMPK involving caspase-9/-3 activation are responsible for adenosine-induced RCR-1 astrocytoma cell death, Neurotoxicology, 27, 458, 10.1016/j.neuro.2005.12.008 Santschi, 2006, Activation of receptors negatively coupled to adenylate cyclase is required for induction of long-term synaptic depression at Schaffer collateral-CA1 synapses, J Neurobiol, 66, 205, 10.1002/neu.20213 Scholl, 2020, Characterization and antiproliferative activity of glioma-derived extracellular vesicles, Nanomedicine, 15, 1001, 10.2217/nnm-2019-0431 Semmler, 2006, The methionine synthase polymorphism c.2756A>G alters susceptibility to glioblastomamultiforme, Cancer Epidemiol Biomarkers Prev, 15, 2314, 10.1158/1055-9965.EPI-05-0979 Serpa, 2015, Combined neuroprotective action of adenosine A1 and cannabinoid CB1 receptors against NMDA-induced excitotoxicity in the hippocampus, Neurochem Int, 87, 106, 10.1016/j.neuint.2015.06.005 Serpa, 2009, Cannabinoid CB(1) and adenosine A(1) receptors independently inhibit hippocampal synaptic transmission, Eur J Pharmacol, 623, 41, 10.1016/j.ejphar.2009.09.020 Serpa, 2014, Modulation of cGMP accumulation by adenosine A1 receptors at the hippocampus: influence of cGMP levels and gender, Eur J Pharmacol, 744, 83, 10.1016/j.ejphar.2014.09.045 Stipanuk, 2004, Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine, Annu Rev Nutr, 24, 539, 10.1146/annurev.nutr.24.012003.132418 Torres, 2019, Extracellular adenosine promotes cell migration/invasion of Glioblastoma Stem-like Cells through A3 Adenosine Receptor activation under hypoxia, Cancer Lett, 446, 112, 10.1016/j.canlet.2019.01.004 Torres, 2016, Adenosine A3 receptor elicits chemoresistance mediated by multiple resistance-associated protein-1 in human glioblastoma stem-like cells, Oncotarget, 7, 67373, 10.18632/oncotarget.12033 White, 1996, Potentiation of excitatory amino acid-evoked adenosine release from rat cortex by inhibitors of adenosine kinase and adenosine deaminase and by acadesine, Eur J Pharmacol, 303, 27, 10.1016/0014-2999(96)00084-2 Williams-Karnesky, 2013, Epigenetic changes induced by adenosine augmentation therapy prevent epileptogenesis, J Clin Invest, 123, 3552, 10.1172/JCI65636 Wink, 2003, Altered extracellular ATP, ADP and AMP catabolism in glioma cell lines., Cancer Lett., 198, 211, 10.1016/S0304-3835(03)00308-2 Yan, 2019, CD73 promotes glioblastoma pathogenesis and enhances its chemoresistance via A2B adenosine receptor signaling, J Neurosci, 39, 4387, 10.1523/JNEUROSCI.1118-18.2019 Yang, 2012, Hypoxia and hypoxia inducible factors in glioblastoma multiforme progression and therapeutic implications, Exp Cell Res, 318, 2417, 10.1016/j.yexcr.2012.07.017 Yao, 2018, Cellular origin of glioblastoma and its implication in precision therapy, Cell Mol Immunol, 15, 737, 10.1038/cmi.2017.159