References
Anderson, W. W., & Collingridge, G. L. (2007). Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. Journal of Neuroscience Methods162 (1-2), 346–356. https://doi.org/10.1016/j.jneumeth.2006.12.018
Baltos, J. A., Casillas-Espinosa, P. M., Rollo, B., Gregory, K. J., White, P. J., Christopoulos, A., Kwan, P., O’Brien, T. J., & May, L. T. (2023). The role of the adenosine system in epilepsy and its comorbidities. British Journal of Pharmacology , 10.1111/bph.16094. Advance online publication. https://doi.org/10.1111/bph.16094
Bauer, J., & Cooper-Mahkorn, D. (2008). Tiagabine: efficacy and safety in partial seizures - current status. Neuropsychiatric disease and treatment, 4(4), 731–736. https://doi.org/10.2147/ndt.s833
Beamer, E., Kuchukulla, M., Boison, D., & Engel, T. (2021). ATP and adenosine-Two players in the control of seizures and epilepsy development. Progress in Neurobiology204 , 102105. https://doi.org/10.1016/j.pneurobio.2021.102105
Berdichevsky, Y., Dzhala, V., Mail, M., & Staley, K. J. (2012). Interictal spikes, seizures and ictal cell death are not necessary for post-traumatic epileptogenesis in vitro. Neurobiology of Disease45 (2), 774–785. https://doi.org/10.1016/j.nbd.2011.11.001
Blümcke, I., Thom, M., Aronica, E., Armstrong, D. D., Bartolomei, F., Bernasconi, A., Bernasconi, N., Bien, C. G., Cendes, F., Coras, R., Cross, J. H., Jacques, T. S., Kahane, P., Mathern, G. W., Miyata, H., Moshé, S. L., Oz, B., Özkara, Ç., Perucca, E., Sisodiya, S., & Spreafico, R. (2013). International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia54 (7), 1315–1329. https://doi.org/10.1111/epi.12220
Boison, D., & Jarvis, M. F. (2021). Adenosine kinase: A key regulator of purinergic physiology. Biochemical Pharmacology187 , 114321. https://doi.org/10.1016/j.bcp.2020.114321
Carlin, J. L., Jain, S., Gizewski, E., Wan, T. C., Tosh, D. K., Xiao, C., Auchampach, J. A., Jacobson, K. A., Gavrilova, O., & Reitman, M. L. (2017). Hypothermia in mouse is caused by adenosine A1 and A3 receptor agonists and AMP via three distinct mechanisms. Neuropharmacology114 , 101–113. https://doi.org/10.1016/j.neuropharm.2016.11.026
Chazalon, M., Paredes-Rodriguez, E., Morin, S., Martinez, A., Cristóvão-Ferreira, S., Vaz, S., Sebastiao, A., Panatier, A., Boué-Grabot, E., Miguelez, C., & Baufreton, J. (2018). GAT-3 Dysfunction Generates Tonic Inhibition in External Globus Pallidus Neurons in Parkinsonian Rodents. Cell Reports23 (6), 1678–1690. https://doi.org/10.1016/j.celrep.2018.04.014
Cheng, P., Zhang, J., Chu, Z., Liu, W., Lin, H., Wu, Y., & Zhu, J. (2022). A3 adenosine receptor agonist IB-MECA reverses chronic cerebral ischemia-induced inhibitory avoidance memory deficit. European Journal of Pharmacology921 , 174874. https://doi.org/10.1016/j.ejphar.2022.174874
Coppi, E., Cherchi, F., Venturini, M., Lucarini, E., Corradetti, R., Di Cesare Mannelli, L., Ghelardini, C., Pedata, F., & Pugliese, A. M. (2022). Therapeutic Potential of Highly Selective A3 Adenosine Receptor Ligands in the Central and Peripheral Nervous System. Molecules (Basel, Switzerland)27 (6), 1890. https://doi.org/10.3390/molecules27061890
Cristóvão-Ferreira, S., Navarro, G., Brugarolas, M., Pérez-Capote, K., Vaz, S. H., Fattorini, G., Conti, F., Lluis, C., Ribeiro, J. A., McCormick, P. J., Casadó, V., Franco, R., & Sebastião, A. M. (2013). A1R-A2AR heteromers coupled to Gs and G i/0 proteins modulate GABA transport into astrocytes. Purinergic Signalling9 (3), 433–449. https://doi.org/10.1007/s11302-013-9364-5
Cristóvão-Ferreira, S., Vaz, S. H., Ribeiro, J. A., & Sebastião, A. M. (2009). Adenosine A2A receptors enhance GABA transport into nerve terminals by restraining PKC inhibition of GAT-1. Journal of Neurochemistry109 (2), 336–347. https://doi.org/10.1111/j.1471-4159.2009.05963.x
Dale, N., & Frenguelli, B. G. (2009). Release of adenosine and ATP during ischemia and epilepsy. Current Neuropharmacology7 (3), 160–179. https://doi.org/10.2174/157015909789152146
Diógenes, M. J., Neves-Tomé, R., Fucile, S., Martinello, K., Scianni, M., Theofilas, P., Lopatár, J., Ribeiro, J. A., Maggi, L., Frenguelli, B. G., Limatola, C., Boison, D., & Sebastião, A. M. (2014). Homeostatic control of synaptic activity by endogenous adenosine is mediated by adenosine kinase. Cerebral Cortex (New York, N.Y.), 24(1), 67–80. https://doi.org/10.1093/cercor/bhs284
Dunwiddie T. V. (1980). Endogenously released adenosine regulates excitability in the in vitro hippocampus. Epilepsia, 21(5), 541–548. https://doi.org/10.1111/j.1528-1157.1980.tb04305.x
Dunwiddie, T. V., Diao, L., Kim, H. O., Jiang, J. L., & Jacobson, K. A. (1997). Activation of hippocampal adenosine A3 receptors produces a desensitization of A1 receptor-mediated responses in rat hippocampus.The Journal of Neuroscience: , 17(2), 607–614. https://doi.org/10.1523/JNEUROSCI.17-02-00607.1997
Dunwiddie, T. V., & Masino, S. A. (2001). The role and regulation of adenosine in the central nervous system. Annual Review of Neuroscience , 24, 31–55. https://doi.org/10.1146/annurev.neuro.24.1.31
Dyhrfjeld-Johnsen, J., Berdichevsky, Y., Swiercz, W., Sabolek, H., & Staley, K. J. (2010). Interictal spikes precede ictal discharges in an organotypic hippocampal slice culture model of epileptogenesis. Journal of Clinical Neurophysiology27 (6), 418–424. https://doi.org/10.1097/WNP.0b013e3181fe0709
Gao, Z. G., Auchampach, J. A., & Jacobson, K. A. (2023). Species dependence of A3 adenosine receptor pharmacology and function. Purinergic Signalling19 (3), 523–550. https://doi.org/10.1007/s11302-022-09910-1
Jacobson, K. A., & Gao, Z. G. (2006). Adenosine receptors as therapeutic targets. Nature Reviews. Drug discovery5 (3), 247–264. https://doi.org/10.1038/nrd1983
Jacobson, K. A., Tosh, D. K., Jain, S., & Gao, Z. G. (2019). Historical and Current Adenosine Receptor Agonists in Preclinical and Clinical Development. Frontiers in Cellular Neuroscience13 , 124. https://doi.org/10.3389/fncel.2019.00124
Javaid, S., Alqahtani, F., Ashraf, W., Anjum, S. M. M., Rasool, M. F., Ahmad, T., Alasmari, F., Alasmari, A. F., Alqarni, S. A., & Imran, I. (2023). Tiagabine suppresses pentylenetetrazole-induced seizures in mice and improves behavioral and cognitive parameters by modulating BDNF/TrkB expression and neuroinflammatory markers. Biomedicine & Pharmacotherapy , 160 , 114406. https://doi.org/10.1016/j.biopha.2023.114406
Kalilani, L., Sun, X., Pelgrims, B., Noack-Rink, M., & Villanueva, V. (2018). The epidemiology of drug-resistant epilepsy: A systematic review and meta-analysis. Epilepsia59 (12), 2179–2193. https://doi.org/10.1111/epi.14596
Kälviäinen R. (2001). Long-term safety of tiagabine. Epilepsia42 Suppl 3 , 46–48. https://doi.org/10.1046/j.1528-1157.2001.042suppl.3046.x
Kwan, P., Schachter, S. C., & Brodie, M. J. (2011). Drug-resistant epilepsy. The New England Journal of Medicine365 (10), 919–926. https://doi.org/10.1056/NEJMra1004418
Laudadio, M. A., & Psarropoulou, C. (2004). The A3 adenosine receptor agonist 2-Cl-IB-MECA facilitates epileptiform discharges in the CA3 area of immature rat hippocampal slices. Epilepsy Research59 (2-3), 83–94. https://doi.org/10.1016/j.eplepsyres.2004.03.005
Li, A. H., Moro, S., Melman, N., Ji, X. D., & Jacobson, K. A. (1998). Structure-activity relationships and molecular modeling of 3, 5-diacyl-2,4-dialkylpyridine derivatives as selective A3 adenosine receptor antagonists. Journal of Medicinal Chemistry41 (17), 3186–3201. https://doi.org/10.1021/jm980093j
Liston, T. E., Hinz, S., Müller, C. E., Holstein, D. M., Wendling, J., Melton, R. J., Campbell, M., Korinek, W. S., Suresh, R. R., Sethre-Hofstad, D. A., Gao, Z. G., Tosh, D. K., Jacobson, K. A., & Lechleiter, J. D. (2020). Nucleotide P2Y1 receptor agonists are in vitro and in vivo prodrugs of A1/A3 adenosine receptor agonists: implications for roles of P2Y1 and A1/A3 receptors in physiology and pathology. Purinergic Signalling16 (4), 543–559. https://doi.org/10.1007/s11302-020-09732-z
Liston, T. E., Hama, A., Boltze, J., Poe, R. B., Natsume, T., Hayashi, I., Takamatsu, H., Korinek, W. S., & Lechleiter, J. D. (2022). Adenosine A1R/A3R (Adenosine A1 and A3 Receptor) Agonist AST-004 Reduces Brain Infarction in a Nonhuman Primate Model of Stroke. Stroke53 (1), 238–248. https://doi.org/10.1161/STROKEAHA.121.036396
Lohse, M. J., Maurer, K., Gensheimer, H. P., & Schwabe, U. (1987). Dual actions of adenosine on rat peritoneal mast cells. Naunyn-Schmiedeberg’s Archives of Pharmacology335 (5), 555–560. https://doi.org/10.1007/BF00169124
Löscher, W., & Klein, P. (2021). The Pharmacology and Clinical Efficacy of Antiseizure Medications: From Bromide Salts to Cenobamate and Beyond. CNS Drugs35 (9), 935–963. https://doi.org/10.1007/s40263-021-00827-8
Magalhães, D. M., Pereira, N., Rombo, D. M., Beltrão-Cavacas, C., Sebastião, A. M., & Valente, C. A. (2018). Ex vivo model of epilepsy in organotypic slices-a new tool for drug screening. Journal of Neuroinflammation15 (1), 203. https://doi.org/10.1186/s12974-018-1225-2
Masocha, W., & Parvathy, S. S. (2016). Preventative and therapeutic effects of a GABA transporter 1 inhibitor administered systemically in a mouse model of paclitaxel-induced neuropathic pain. PeerJ4 , e2798. https://doi.org/10.7717/peerj.2798
McNeill, S. M., Baltos, J. A., White, P. J., & May, L. T. (2021). Biased agonism at adenosine receptors. Cellular Signalling82 , 109954. https://doi.org/10.1016/j.cellsig.2021.109954
Medina-Ceja, L., Sandoval-García, F., Morales-Villagrán, A., & López-Pérez, S. J. (2012). Rapid compensatory changes in the expression of EAAT-3 and GAT-1 transporters during seizures in cells of the CA1 and dentate gyrus. Journal of biomedical science19 (1), 78. https://doi.org/10.1186/1423-0127-19-78
Meldrum, B. S., & Chapman, A. G. (1999). Basic mechanisms of gabitril (tiagabine) and future potential developments. Epilepsia40 Suppl 9 , S2–S6. https://doi.org/10.1111/j.1528-1157.1999.tb02087.x
Miledi, R., Eusebi, F., Martínez-Torres, A., Palma, E., & Trettel, F. (2002). Expression of functional neurotransmitter receptors inXenopus oocytes after injection of human brain membranes. Proceedings of the National Academy of Sciences of the United States of America99 (20), 13238–13242. https://doi.org/10.1073/pnas.192445299
Miledi, R., Palma, E., & Eusebi, F. (2006). Microtransplantation of neurotransmitter receptors from cells to Xenopus oocyte membranes: new procedure for ion channel studies. Methods in Molecular Biology (Clifton, N.J.)322 , 347–355. https://doi.org/10.1007/978-1-59745-000-3_24
Naylor D. E. (2023). In the fast lane: Receptor trafficking during status epilepticus. Epilepsia Open8 Suppl 1 (Suppl 1), S35–S65. https://doi.org/10.1002/epi4.12718
Noe, F. M., Polascheck, N., Frigerio, F., Bankstahl, M., Ravizza, T., Marchini, S., Beltrame, L., Banderó, C. R., Löscher, W., & Vezzani, A. (2013). Pharmacological blockade of IL-1β/IL-1 receptor type 1 axis during epileptogenesis provides neuroprotection in two rat models of temporal lobe epilepsy. Neurobiology of Disease59 , 183–193. https://doi.org/10.1016/j.nbd.2013.07.015
Nguyen, A. T. N., Tran, Q. L., Baltos, J. A., McNeill, S. M., Nguyen, D. T. N., & May, L. T. (2023). Small molecule allosteric modulation of the adenosine A1 receptor. Frontiers in Endocrinology14 , 1184360. https://doi.org/10.3389/fendo.2023.1184360
Palma, E., Trettel, F., Fucile, S., Renzi, M., Miledi, R., & Eusebi, F. (2003). Microtransplantation of membranes from cultured cells toXenopus oocytes: a method to study neurotransmitter receptors embedded in native lipids. Proceedings of the National Academy of Sciences of the United States of America100 (5), 2896–2900. https://doi.org/10.1073/pnas.0438006100
Palumbo, L., Carinci, M., Guarino, A., Asth, L., Zucchini, S., Missiroli, S., Rimessi, A., Pinton, P., & Giorgi, C. (2023). The NLRP3 Inflammasome in Neurodegenerative Disorders: Insights from Epileptic Models. Biomedicines11 (10), 2825. https://doi.org/10.3390/biomedicines11102825
Racine R. J. (1972). Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalography and Clinical Neurophysiology32 (3), 281–294. https://doi.org/10.1016/0013-4694(72)90177-0
Reddy, D. S., & Kuruba, R. (2013). Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions. International Journal of Molecular Sciences14 (9), 18284–18318. https://doi.org/10.3390/ijms140918284
Richerson G. B. (2004). Looking for GABA in all the wrong places: the relevance of extrasynaptic GABA(A) receptors to epilepsy. Epilepsy Currents , 4 (6), 239–242. https://doi.org/10.1111/j.1535-7597.2004.46008.x
Rombo, D.M., Ribeiro, J.A., Sebastião, A.M. (2018). Role of Adenosine Receptors in Epileptic Seizures. In: Borea, P., Varani, K., Gessi, S., Merighi, S., Vincenzi, F. (eds) The Adenosine Receptors. The Receptors, vol 34. Humana Press, Cham. https://doi.org/10.1007/978-3-319-90808-3_13
Roseti, C., Martinello, K., Fucile, S., Piccari, V., Mascia, A., Di Gennaro, G., Quarato, P. P., Manfredi, M., Esposito, V., Cantore, G., Arcella, A., Simonato, M., Fredholm, B. B., Limatola, C., Miledi, R., & Eusebi, F. (2008). Adenosine receptor antagonists alter the stability of human epileptic GABAA receptors. Proceedings of the National Academy of Sciences of the United States of America105 (39), 15118–15123. https://doi.org/10.1073/pnas.0807277105
Roseti, C., Palma, E., Martinello, K., Fucile, S., Morace, R., Esposito, V., Cantore, G., Arcella, A., Giangaspero, F., Aronica, E., Mascia, A., Di Gennaro, G., Quarato, P. P., Manfredi, M., Cristalli, G., Lambertucci, C., Marucci, G., Volpini, R., Limatola, C., & Eusebi, F. (2009). Blockage of A2A and A3 adenosine receptors decreases the desensitization of human GABA(A) receptors microtransplanted toXenopus oocytes. Proceedings of the National Academy of Sciences of the United States of America106 (37), 15927–15931. https://doi.org/10.1073/pnas.0907324106
Ruffolo, G., Cifelli, P., Miranda-Lourenço, C., De Felice, E., Limatola, C., Sebastião, A. M., Diógenes, M. J., Aronica, E., & Palma, E. (2020). Rare Diseases of Neurodevelopment: Maintain the Mystery or Use a Dazzling Tool for Investigation? The Case of Rett Syndrome. Neuroscience439 , 146–152. https://doi.org/10.1016/j.neuroscience.2019.06.015
Sakurai, M., Suzuki, H., Tomita, N., Sunden, Y., Shimada, A., Miyata, H., & Morita, T. (2018). Enhanced neurogenesis and possible synaptic reorganization in the piriform cortex of adult rat following kainic acid-induced status epilepticus. Neuropathology38 (2), 135–143. https://doi.org/10.1111/neup.12445
Sandau, U. S., Colino-Oliveira, M., Jones, A., Saleumvong, B., Coffman, S. Q., Liu, L., Miranda-Lourenço, C., Palminha, C., Batalha, V. L., Xu, Y., Huo, Y., Diógenes, M. J., Sebastião, A. M., & Boison, D. (2016). Adenosine Kinase Deficiency in the Brain Results in Maladaptive Synaptic Plasticity. The Journal of Neuroscience36 (48), 12117–12128. https://doi.org/10.1523/JNEUROSCI.2146-16.2016
Sebastião, A. M., Stone, T. W., & Ribeiro, J. A. (1990). The inhibitory adenosine receptor at the neuromuscular junction and hippocampus of the rat: antagonism by 1,3,8-substituted xanthines. British Journal of Pharmacology101 (2), 453–459. https://doi.org/10.1111/j.1476-5381.1990.tb12729.x
Sebastião, A. M., & Ribeiro, J. A. (2009). Adenosine receptors and the central nervous system. Handbook of Experimental Pharmacology , (193), 471–534. https://doi.org/10.1007/978-3-540-89615-9_16
Sebastião, A. M., & Ribeiro, J. A. (2023). Adjusting the brakes to adjust neuronal activity: Adenosinergic modulation of GABAergic transmission. Neuropharmacology , 236 , 109600. https://doi.org/10.1016/j.neuropharm.2023.109600
Segall M. D. (2012). Multi-parameter optimization: identifying high quality compounds with a balance of properties. Current Pharmaceutical Design , 18 (9), 1292–1310. https://doi.org/10.2174/138161212799436430
Sills, G. J., & Rogawski, M. A. (2020). Mechanisms of action of currently used antiseizure drugs. Neuropharmacology168 , 107966. https://doi.org/10.1016/j.neuropharm.2020.107966
Su, J., Yin, J., Qin, W., Sha, S., Xu, J., & Jiang, C. (2015). Role for pro-inflammatory cytokines in regulating expression of GABA transporter type 1 and 3 in specific brain regions of kainic acid-induced status epilepticus. Neurochemical research40 (3), 621–627. https://doi.org/10.1007/s11064-014-1504-y
Świąder, M. J., Kotowski, J., & Łuszczki, J. J. (2014). Modulation of adenosinergic system and its application for the treatment of epilepsy. Pharmacological Reports: PR66 (3), 335–342. https://doi.org/10.1016/j.pharep.2013.10.005
Tosh, D. K., Paoletta, S., Deflorian, F., Phan, K., Moss, S. M., Gao, Z. G., Jiang, X., & Jacobson, K. A. (2012a). Structural sweet spot for A1 adenosine receptor activation by truncated (N)-methanocarba nucleosides: receptor docking and potent anticonvulsant activity. Journal of Medicinal Chemistry55 (18), 8075–8090. https://doi.org/10.1021/jm300965a
Tosh, D. K., Deflorian, F., Phan, K., Gao, Z. G., Wan, T. C., Gizewski, E., Auchampach, J. A., & Jacobson, K. A. (2012b). Structure-guided design of A (3) adenosine receptor-selective nucleosides: combination of 2-arylethynyl and bicyclo[3.1.0]hexane substitutions. Journal of Medicinal Chemistry55 (10), 4847–4860. https://doi.org/10.1021/jm300396n
Tosh, D. K., Rao, H., Bitant, A., Salmaso, V., Mannes, P., Lieberman, D. I., Vaughan, K. L., Mattison, J. A., Rothwell, A. C., Auchampach, J. A., Ciancetta, A., Liu, N., Cui, Z., Gao, Z. G., Reitman, M. L., Gavrilova, O., & Jacobson, K. A. (2019). Design and in vivo Characterization of A1 Adenosine Receptor Agonists in the Native Ribose and Conformationally Constrained (N)-Methanocarba Series. Journal of Medicinal Chemistry62 (3), 1502–1522. https://doi.org/10.1021/acs.jmedchem.8b01662
Tescarollo, F. C., Rombo, D. M., DeLiberto, L. K., Fedele, D. E., Alharfoush, E., Tomé, Â. R., Cunha, R. A., Sebastião, A. M., & Boison, D. (2020). Role of Adenosine in Epilepsy and Seizures. Journal of Caffeine and Adenosine Research10 (2), 45–60. https://doi.org/10.1089/caff.2019.0022
Valente, C. A., Meda, F. J., Carvalho, M., & Sebastião, A. M. (2021). A Model of Epileptogenesis in Rhinal Cortex-Hippocampus Organotypic Slice Cultures. Journal of visualized experiments: JoVE , (169), 10.3791/61330. https://doi.org/10.3791/61330
Vezzani, A., Di Sapia, R., Kebede, V., Balosso, S., & Ravizza, T. (2023). Neuroimmunology of status epilepticus. Epilepsy & Behavior: E&B140 , 109095. https://doi.org/10.1016/j.yebeh.2023.109095
Von Lubitz, D. K., Lin, R. C., Boyd, M., Bischofberger, N., & Jacobson, K. A. (1999). Chronic administration of adenosine A3 receptor agonist and cerebral ischemia: neuronal and glial effects. European Journal of Pharmacology367 (2-3), 157–163. https://doi.org/10.1016/s0014-2999(98)00977-7
Wan, T. C., Tampo, A., Kwok, W. M., & Auchampach, J. A. (2019). Ability of CP-532,903 to protect mouse hearts from ischemia/reperfusion injury is dependent on expression of A3 adenosine receptors in cardiomyoyctes. Biochemical Pharmacology163 , 21–31. https://doi.org/10.1016/j.bcp.2019.01.022
Table 1. Evaluation of the intrinsic parameters of the epileptiform activity depicted by organotypic rhinal-hippocampal slices perfused under depolarizing conditions (8.5mM of KCl in aCSF) or non-depolarizing conditions (Neurobasal A medium), in the absence or presence of MRS5474 (250nM).