Prospects of pharmacological regulation of aquaporin function in CNS diseases
Natalia S. Ponamareva , Vasiliy E. Novikov , Elena V. Pozhilova
Reviews on Clinical Pharmacology and Drug Therapy ›› 2023, Vol. 21 ›› Issue (1) : 35 -48.
Prospects of pharmacological regulation of aquaporin function in CNS diseases
The review analyzes the results of scientific research on the role of aquaporins in the pathogenesis of CNS diseases and the possibility of their pharmacological regulation.
Aquaporins (AQP) are proteins involved in the transmembrane transport of water and other substances. They form the water channels of cell membranes and are widely represented in various mammalian cells, including the membranes of human brain and spinal cord cells. To date, about 300 types of proteins of the aquaporin family have been discovered, of which 13 (AQP0–AQP12) have been identified in human cells. Localization of different types of AQP in CNS structures, their functional activity and involvement in the development of CNS diseases differ. There are mainly three types of AQPs in the central nervous system: AQP1, AQP4 and AQP9. The results of scientific research indicate the most important role of AQP in maintaining water-salt homeostasis and ensuring physiological processes in the central nervous system, and also confirm the role of AQP in the pathogenesis of a number of diseases of the central nervous system (cerebral edema of various genesis, invasion of tumor cells and the formation of peritumorous edema, in the development of autoimmune diseases — opticomyelitis, Alzheimer’s disease). Pharmacological regulation of the functional activity of aquaporins can influence the course of these diseases. Therefore, there is a natural interest in drugs that can change the expression of AQP.
Proteins of the aquaporin family provide transmembrane transport of water and play an essential role in the development of pathological conditions of the central nervous system. They can be potential targets for pharmacological effects in a number of diseases of the central nervous system. The search and study of drugs affecting the expression and functional activity of AQP is pathogenetically justified and is a promising direction in the development of pharmacotherapy strategies for cerebral edema, malignant brain tumors and other CNS diseases.
aquaporins / water transport / brain edema / brain tumors / pharmacological targets
| [1] |
Levchenkova OS, Novikov VE, Pozhilova EV. Mitochondrial pore as a pharmacological target. Vestnik of the Smolensk State Medical Academy. 2014;13(4):24–33. (In Russ.) |
| [2] |
Левченкова О.С., Новиков В.Е., Пожилова Е.В. Митохондриальная пора как мишень фармакологического воздействия // Вестник Смоленской государственной медицинской академии. 2014. Т. 13, № 4. С. 24–33. |
| [3] |
Novikov VE, Levchenkova OS. Perspectives of Use of Inducers of the Hypoxia Adaptation Factor in Therapy of Ischemic Diseases. Journal of the Ural Medical Academic Science. 2014;51(5):132–138. (In Russ.) |
| [4] |
Новиков В.Е., Левченкова О.С. Перспективы применения индукторов фактора адаптации к гипоксии в терапии ишемических заболеваний // Вестник Уральской медицинской академической науки. 2014. Т. 51, № 5. С. 132–138. |
| [5] |
Novikov VE, Levchenkova OS, Pozhilova EV. The role of the mitochondrial ATP-dependent potassium channel and its modulators in cell adaptation to hypoxia. Vestnik of the Smolensk State Medical Academy. 2014;13(2):48–54. (In Russ.) |
| [6] |
Новиков В.Е., Левченкова О.С., Пожилова Е.В. Роль митохондриального АТФ-зависимого калиевого канала и его модуляторов в адаптации клетки к гипоксии // Вестник Смоленской государственной медицинской академии. 2014. Т. 13, № 2. С. 48–54. |
| [7] |
Pozhilova EV, Novikov VE. Physiological and pathological value of cellular synthase of nitrogen oxide and endogenous nitrogen oxide. Vestnik of the Smolensk State Medical Academy. 2015;14(4):35–41. (In Russ.) |
| [8] |
Пожилова Е.В., Новиков В.Е. Синтаза оксида азота и эндогенный оксид азота в физиологии и патологии клетки // Вестник Смоленской государственной медицинской академии. 2015. Т. 14, № 4. С. 35–41 |
| [9] |
Finn RN, Cerdа J. Evolution and Functional Diversity of Aquaporins. Biology Bulletin. 2015;229(1):6–23. DOI: 10.1086/BBLv229n1p6 |
| [10] |
Finn R.N., Cerdа J. Evolution and Functional Diversity of Aquaporins // Biology Bulletin. 2015. Vol. 229, No. 1. P. 6–23. DOI: 10.1086/BBLv229n1p6 |
| [11] |
Xu M, Xiao M, Li S, et al. Aquaporins in Nervous System. Adv Exp Med Biol. 2017;969:81–103. DOI: 10.1007/978-94-024-1057-0_5 |
| [12] |
Xu M., Xiao M., Li S., et al. Aquaporins in Nervous System // Adv Exp Med Biol. 2017. Vol. 969. P. 81–103. DOI: 10.1007 /978-94-024-1057-0_5 |
| [13] |
Bon EI, Maksimovich NE. Morphofunctional features of different types of channels of cytoplasmatic membrane. Vestnik of the Novgorod State University. 2020;(4(120)):5–12. (In Russ.) DOI: 10.34680/2076-8052.2020.4(120).5-12 |
| [14] |
Бонь Е.И., Максимович Н.Е. Морфофункциональные особенности различных типов каналов цитоплазматической мембраны // Вестник Новгородского государственного университета. 2020. № 4(120). С. 5–12. DOI: 10.34680/2076-8052.2020.4(120).5-12 |
| [15] |
Novikov VE, Ponamareva NS, Yasnetsov VV, Kulagin KN. Pharmacotherapy of brain edema: the current state of the problem. Vestnik of the Smolensk State Medical Academy. 2021;20(3):25–42. (In Russ.) DOI: 10.37903/vsgma.2021.3.4 |
| [16] |
Новиков В.Е., Понамарева Н.С., Яснецов В.В., Кулагин К.Н. Фармакотерапия отека головного мозга: современное состояние проблемы // Вестник Смоленской государственной медицинской академии. 2021. Т. 20, № 3. С. 25–42. DOI: 10.37903/vsgma.2021.3.4 |
| [17] |
Maugeri R, Schiera G, Di Liegro C, et al. Aquaporins and Brain Tumors. International J Molecular Sciences. 2016;17(7):1029. DOI: 10.3390 /ijms17071029 |
| [18] |
Maugeri R., Schiera G., Di Liegro C., et al. Aquaporins and Brain Tumors // International J Molecular Sciences. 2016. Vol. 17, No. 7. P. 1029. DOI: 10.3390 /ijms17071029 |
| [19] |
Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci. 2013;14(14):265–277. DOI: 10.1038/nrn3468 |
| [20] |
Papadopoulos M.C., Verkman A.S. Aquaporin water channels in the nervous system // Nat Rev Neurosci. 2013. Vol. 14, No. 14. P. 265–277. DOI: 10.1038/nrn3468 |
| [21] |
Oshio K, Watanabe H, Song Y, et al. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J. 2005;19(1):76–78. DOI: 10.1096/fj.04-1711fje |
| [22] |
Oshio K., Watanabe H., Song Y., et al. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1 // FASEB J. 2005. Vol. 19, No. 1. P. 76–78. DOI: 10.1096/fj.04-1711fje |
| [23] |
Rauen K, Pop V, Trabold R, et al. Vasopressin V1a Receptors Regulate Cerebral Aquaporin 1 after Traumatic Brain Injury. J Neurotrauma. 2020;37(4):665–674. DOI: 10.1089/neu.2019.6653 |
| [24] |
Rauen K., Pop V., Trabold R., et al. Vasopressin V1a Receptors Regulate Cerebral Aquaporin 1 after Traumatic Brain Injury // J Neurotrauma. 2020. Vol. 37, No. 4. P. 665–674. DOI: 10.1089/neu.2019.6653 |
| [25] |
Deckmann I, Santos-Terra J, Fontes-Dutra M, et al. Resveratrol prevents brain edema, blood-brain barrier permeability, and altered aquaporin profile in autism animal model. Int J Dev Neurosci. 2021;81(7):579–604. DOI: 10.1002/jdn.10137 |
| [26] |
Deckmann I., Santos-Terra J., Fontes-Dutra M., et al. Resveratrol prevents brain edema, blood-brain barrier permeability, and altered aquaporin profile in autism animal model // Int J Dev Neurosci. 2021. Vol. 81, No. 7. P. 579–604. DOI: 10.1002/jdn.10137 |
| [27] |
Novikov VE. Possibilities of pharmacological neuroprotection in traumatic brain injury. Psychopharmacology and Biological Narcology. 2007;7(2):1500–1509. (In Russ.) |
| [28] |
Новиков В.Е. Возможности фармакологической нейропротекции при черепно-мозговой травме // Психофармакология и биологическая наркология. 2007. Т. 7, № 2. С. 1500–1509. |
| [29] |
Novikov VE, Kovaleva LA. The effect of substances with nootropic activity on oxidative phosphorylation in the mitochondria of the brain in acute traumatic brain injury. Russian Journal of Experimental and Clinical Pharmacology. 1997;60(1):59–61. (In Russ.) |
| [30] |
Новиков В.Е., Ковалева Л.А. Влияние веществ с ноотропной активностью на окислительное фосфорилирование в митохондриях мозга при острой черепно-мозговой травме // Экспериментальная и клиническая фармакология. 1997. Т. 60, № 1. С. 59–61. |
| [31] |
Novikov VE, Kovaleva LA. The effect of nootropics on the function of brain mitochondria in the dynamics of traumatic brain injury in the age aspect. Russian Journal of Experimental and Clinical Pharmacology. 1998;61(2):65–68. (In Russ.) |
| [32] |
Новиков В.Е., Ковалева Л.А. Влияние ноотропов на функцию митохондрий мозга в динамике черепно-мозговой травмы в возрастном аспекте // Экспериментальная и клиническая фармакология. 1998. Т. 61, № 2. С. 65–68. |
| [33] |
Novikov VE, Maslova NN. The effect of mexidol on the course of posttraumatic epilepsy treatment. Russian Journal of Experimental and Clinical Pharmacology. 2003;66(4):9–11. (In Russ.) |
| [34] |
Новиков В.Е., Маслова Н.Н. Влияние мексидола на течение посттравматической эпилепсии // Экспериментальная и клиническая фармакология. 2003. Т. 66, № 4. С. 9–11. |
| [35] |
Novikov VE, Sharov AN. The effect of GABA-ergic agents on oxidative phosphorylation in the brain mitochondria in traumatic edema. Pharmacology and Toxicology. 1991;54(6):44–46. (In Russ.) |
| [36] |
Новиков В.Е., Шаров А.Н. Влияние ГАМК-ергических средств на окислительное фосфорилирование в митохондриях мозга при его травматическом отеке // Фармакология и токсикология. 1991. Т. 54, № 6. С. 44–46. |
| [37] |
Noell S, Fallier-Becker P, Mack AF, et al. Water channels aquaporin 4 and -1 expression in subependymoma depends on the localization of the tumors. PLOS One. 2015;10(6):e0131367. DOI: 10.1371/journal.pone.0131367 |
| [38] |
Noell S., Fallier-Becker P., Mack A.F., et al. Water channels aquaporin 4 and -1 expression in subependymoma depends on the localization of the tumors // PLOS One. 2015. Vol. 10, No. 6. P. e0131367. DOI: 10.1371/journal.pone.0131367 |
| [39] |
Hayashi Y, Edwards NA, Proescholdt MA, et al. Regulation and function of aquaporin-1 in glioma cells. Neoplasia. 2007;9(9): 777–787. DOI: 10.1593/neo.07454 |
| [40] |
Hayashi Y., Edwards N.A., Proescholdt M.A., et al. Regulation and function of aquaporin-1 in glioma cells // Neoplasia. 2007. Vol. 9, No. 9. P. 777–787. DOI: 10.1593/neo.07454 |
| [41] |
El Hindy, Bankfalvi A, Herring A, et al. Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma. Anticancer Res. 2013;33(2):609–613. |
| [42] |
El Hindy., Bankfalvi A., Herring A., et al. Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma // Anticancer Res. 2013. Vol. 33. No. 2. P. 609–613. |
| [43] |
Papadopoulos MC, Saadoun S. Key roles of aquaporins in tumor biology. Biochim Biophys Acta. 2015;1848(10 (Pt B)):2576–2583. DOI: 10.1016/j.bbamem.2014.09.001 |
| [44] |
Papadopoulos M.C., Saadoun S. Key roles of aquaporins in tumor biology // Biochim Biophys Acta. 2015. Vol. 1848, No. 10 (Pt B). P. 2576–2583. DOI: 10.1016 / j.bbamem.2014.09.001 |
| [45] |
Pozhilova EV, Novikov VE. Adaptation to hypoxia in tumour growth. Vestnik of the Smolensk state medical Academy. 2015;14(3):16–20. (In Russ.) |
| [46] |
Пожилова Е.В., Новиков В.Е. Роль фактора адаптации к гипоксии в развитии опухолей // Вестник Смоленской государственной медицинской академии. 2015. Т. 14, № 3. С. 16–20. |
| [47] |
Kim JH, Lee YW, Park KA, et al. Agmatine Attenuates Brain Edema through Reducing the Expression of Aquaporin-1 after Cerebral Ischemia. J Cereb Blood Flow Metab. 2010;30(5):943–949. DOI: 10.1038/jcbfm.2009.260 |
| [48] |
Kim J.H., Lee Y.W., Park K.A., et al. Agmatine Attenuates Brain Edema through Reducing the Expression of Aquaporin-1 after Cerebral Ischemia // J Cereb Blood Flow Metab. 2010. Vol. 30, No. 5. P. 943–949. DOI: 10.1038 / jcbfm.2009.260 |
| [49] |
Hoshi A, Tsunoda A, Tada M, et al. Expression of Aquaporin 1 and Aquaporin 4 in the Temporal Neocortex of Patients with Parkinson’s Disease. Brain Pathol. 2017;27(2):160–168. DOI: 10.1111/bpa.12369 |
| [50] |
Hoshi A., Tsunoda A., Tada M., et al. Expression of Aquaporin 1 and Aquaporin 4 in the Temporal Neocortex of Patients with Parkinson’s Disease // Brain Pathol. 2017. Vol. 27, No. 2. P. 160–168. DOI: 10.1111/bpa.12369 |
| [51] |
Lu DC, Zador Z, Yao J, et al. Aquaporin-4 Reduces Post-Traumatic Seizure Susceptibility by Promoting Astrocytic Glial Scar Formation in Mice. J Neurotrauma. 2021;38(8):1193–1201. DOI: 10.1089/neu.2011.2114 |
| [52] |
Lu D.C., Zador Z., Yao J., et al. Aquaporin-4 Reduces Post-Traumatic Seizure Susceptibility by Promoting Astrocytic Glial Scar Formation in Mice // J Neurotrauma. 2021. Vol. 38, No. 8. P. 1193–1201. DOI: 10.1089/neu.2011.2114 |
| [53] |
Smith AJ, Jin BJ, Ratelade J, et al. Aggregation state determines the localization and function of M1- and M23-aquaporin-4 in astrocytes. J Cell Biol. 2014;204(4):559–573. DOI: 10.1083/jcb.201308118 |
| [54] |
Smith A.J., Jin B.J., Ratelade J., et al. Aggregation state determines the localization and function of M1- and M23-aquaporin-4 in astrocytes // J Cell Biol. 2014. Vol. 204, No. 4. P. 559–573. DOI: 10.1083/jcb.201308118 |
| [55] |
Stokum JA, Gerzanich V, Simard JM. Molecular pathophysiology of cerebral edema. J Cereb Blood Flow Metab. 2016;36(3):513–538. DOI: 10.1177/0271678X15617172 |
| [56] |
Stokum J.A., Gerzanich V., Simard J.M. Molecular pathophysiology of cerebral edema // J Cereb Blood Flow Metab. 2016. Vol. 36, No. 3. P. 513–538. DOI: 10.1177/0271678X15617172 |
| [57] |
Warth A, Simon P, Capper D, et al. Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood-brain barrier disturbance but not with patient survival. J Neurosci Res. 2007;85(6):1336–1346. DOI: 10.1002/jnr.21224 |
| [58] |
Warth A., Simon P., Capper D., et al. Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood-brain barrier disturbance but not with patient survival // J Neurosci Res. 2007. Vol. 85, No. 6. P. 1336–1346. DOI: 10.1002 / jnr.21224 |
| [59] |
Wolburg H, Noell S, Fallier-Becker P, et al. The disturbed blood-brain barrier in human glioblastoma. Molecular Aspects of Medicine. 2012;32(5–6):579–589. DOI: 10.1016/j.mam.2012.02.003 |
| [60] |
Wolburg H., Noell S., Fallier-Becker P., et al. The disturbed blood-brain barrier in human glioblastoma // Molecular Aspects of Medicine. 2012. Vol. 32, No. 5–6. P. 579–589. DOI: 10.1016/j.mam.2012.02.003 |
| [61] |
Previch LE, Ma L, Wright JC. Progress in AQP Research and New Developments in Therapeutic Approaches to Ischemic and Hemorrhagic Stroke. Int J Mol Sci. 2016;17(7):1146. DOI: 10.3390/ijms17071146 |
| [62] |
Previch L.E., Ma L., Wright J.C. Progress in AQP Research and New Developments in Therapeutic Approaches to Ischemic and Hemorrhagic Stroke // Int J Mol Sci. 2016. Vol. 17, No. 7. P. 1146. DOI: 10.3390/ijms17071146 |
| [63] |
Chen JQ, Zhang CC, Jiang SN, et al. Effects of Aquaporin 4 Knockdown on Brain Edema of the Uninjured Side аfter Traumatic Brain Injury in Rats. Med Sci Monit. 2016;22:4809–4819. DOI: 10.12659/msm.898190 |
| [64] |
Chen J.Q., Zhang C.C., Jiang S.N., et al. Effects of Aquaporin 4 Knockdown on Brain Edema of the Uninjured Side after Traumatic Brain Injury in Rats // Med Sci Monit. 2016. Vol. 22. P. 4809–4819. DOI: 10.12659 / msm.898190 |
| [65] |
Farr GW, Hall CH, Farr SM, et al. Functionalized Phenylbenzamides Inhibit Aquaporin-4 Reducing Cerebral Edema and Improving Outcome in Two Models of CNS Injury. Neuroscience. 2019;404: 484–498. DOI: 10.1016/j.neuroscience.2019.01.034 |
| [66] |
Farr G.W., Hall C.H., Farr S.M., et al. Functionalized Phenylbenzamides Inhibit Aquaporin-4 Reducing Cerebral Edema and Improving Outcome in Two Models of CNS Injury // Neuroscience. 2019. Vol. 404. P. 484–498. DOI: 10.1016 / j.neuroscience.2019.01.034 |
| [67] |
Xiong A, Xiong R, Yu J, Liu Y, et al. Aquaporin-4 is a potential drug target for traumatic brain injury via aggravating the severity of brain edema. Burns Trauma. 2021;9: tkaa050. DOI: 10.1093/burnst /tkaa050 |
| [68] |
Xiong A., Xiong R., Yu J., Liu Y., et al. Aquaporin-4 is a potential drug target for traumatic brain injury via aggravating the severity of brain edema // Burns Trauma. 2021. Vol. 9. P. tkaa050. DOI: 10.1093/burnst /tkaa050 |
| [69] |
Rao KV, Reddy PV, Curtis KM, et al. Aquaporin-4 expression in cultured astrocytes after fluid percussion injury. J Neurotrauma. 2011;28(3):371–381. DOI: 10.1089/neu.2010.1705 |
| [70] |
Rao K.V., Reddy P.V., Curtis K.M., et al. Aquaporin-4 expression in cultured astrocytes after fluid percussion injury // J Neurotrauma. 2011. Vol. 28, No. 3. P. 371–381. DOI: 10.1089/neu.2010.1705 |
| [71] |
Tang G, Liu Y, Zhang Z, et al. Mesenchymal stem cells maintain blood-brain barrier integrity by inhibiting aquaporin-4 upregulation after cerebral ischemia. Stem Cells. 2014;32(12): 3150–3162. DOI: 10.1002/stem.1808 |
| [72] |
Tang G., Liu Y., Zhang Z., et al. Mesenchymal stem cells maintain blood-brain barrier integrity by inhibiting aquaporin-4 upregulation after cerebral ischemia // Stem Cells. 2014. Vol. 32, No. 12. P. 3150–3162. DOI: 10.1002/stem.1808 |
| [73] |
Zeng XN, Xie LL, Liang R, et al. AQP4 knockout aggravates ischemia/reperfusion injury in mice. CNS Neurosci Ther. 2012;18(5): 388–394. DOI: 10.1111/j.1755–5949.2012.00308.x |
| [74] |
Zeng X.N., Xie L.L., Liang R., et al. AQP4 knockout aggravates ischemia/reperfusion injury in mice // CNS Neurosci Ther. 2012. Vol. 18, No. 5. P. 388–394. DOI: 10.1111/j.1755-5949.2012.00308.x |
| [75] |
Tang Y, Wu P, Su J, Xiang J, et al. Effects of aquaporin-4 on edema formation following intracerebral hemorrhage. Exp Neurol. 2010;223(2):485–495. DOI: 10.1016/j.expneurol.2010.01.015 |
| [76] |
Tang Y., Wu P., Su J., Xiang J., et al. Effects of aquaporin-4 on edema formation following intracerebral hemorrhage // Exp Neurol. 2010. Vol. 223, No. 2. P. 485–495. DOI: 10.1016 /j.expneurol.2010.01.015 |
| [77] |
Sadana P, Coughlin L, Burke J, et al. Anti-edema action of thyroid hormone in MCAO model of ischemic brain stroke: Possible association with AQP4 modulation. J Neurol Sci. 2015;354:37–45. DOI: 10.1016/j.jns.2015.04.042 |
| [78] |
Sadana P., Coughlin L., Burke J., et al. Anti-edema action of thyroid hormone in MCAO model of ischemic brain stroke: Possible association with AQP4 modulation // J Neurol Sci. 2015. Vol. 354. P. 37–45. DOI: 10.1016/j.jns.2015.04.042 |
| [79] |
Kaur C, Sivakumar V, Zhang Y, et al. Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia. 2006;54(8):826–839. DOI: 10.1002/glia.20420 |
| [80] |
Kaur C., Sivakumar V., Zhang Y., et al. Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum // Glia. 2006. Vol. 54, No. 8. P. 826–839. DOI: 10.1002/glia.20420 |
| [81] |
Bhattacharya P, Pandey AK, Paul S, et al. Melatonin renders neuroprotection by protein kinase C mediated aquaporin-4 inhibition in animal model of focal cerebral ischemia. Life Sci. 2014;100(2): 97–109. DOI: 10.1016/j.lfs.2014.01.085 |
| [82] |
Bhattacharya P., Pandey A.K., Paul S., et al. Melatonin renders neuroprotection by protein kinase C mediated aquaporin-4 inhibition in animal model of focal cerebral ischemia // Life Sci. 2014. Vol. 100, No. 2. P. 97–109. DOI: 10.1016/j.lfs.2014.01.085 |
| [83] |
Blixt J, Gunnarson E, Wanecek M. Erythropoietin Attenuates the Brain Edema Response after Experimental Traumatic Brain Injury. J Neurotrauma. 2018;35(4):671–680. DOI: 10.1089/neu.2017.5015 |
| [84] |
Blixt J, Gunnarson E, Wanecek M. Erythropoietin Attenuates the Brain Edema Response after Experimental Traumatic Brain Injury // J Neurotrauma. 2018. Vol. 35, No. 4. P. 671–680. DOI: 10.1089 / neu.2017.5015 |
| [85] |
Gunnarson E, Song Y, Kowalewski JM, et al. Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection. Proc Natl Acad Sci USA. 2009;106(5):1602–1607. DOI: 10.1073/pnas.0812708106 |
| [86] |
Gunnarson E., Song Y., Kowalewski J.M., et al. Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection // Proc Natl Acad Sci USA. 2009. Vol. 106, No. 5. P. 1602–1607. DOI: 10.1073/pnas.0812708106 |
| [87] |
Töllner K, Brandt C, Römermann K, et al. Тhe organic anion transport inhibitor probenecid increases brain concentrations of the NKCC1 inhibitor bumetanide. Europ J Pharmacol. 2015;746:167–173. DOI: 10.1016/j.ejphar.2014.11.019 |
| [88] |
Töllner K., Brandt C., Römermann K., et al. Тhe organic anion transport inhibitor probenecid increases brain concentrations of the NKCC1 inhibitor bumetanide // Europ J Pharmacol. 2015. Vol. 746. P. 167–173. DOI: 10.1016/j.ejphar.2014.11.019 |
| [89] |
Huber VJ, Tsujita M, Yamazaki M, et al. Identification of arylsulfonamides as Aquaporin 4 inhibitors. Bioorg Med Chem Lett. 2007;17(5):1270–1273. DOI: 10.1016/j.bmcl.2006.12.010 |
| [90] |
Huber V.J., Tsujita M., Yamazaki M., et al. Identification of arylsulfonamides as Aquaporin 4 inhibitors // Bioorg Med Chem Lett. 2007. Vol. 17, No. 5. P. 1270–1273. DOI: 10.1016/j.bmcl.2006.12.010 |
| [91] |
Huber VJ, Tsujita M, Kwee IL, et al. Inhibition of aquaporin 4 by antiepileptic drugs. Bioorg Med Chem Lett. 2009;17(1):418–424. DOI: 10.1016/j.bmc.2007.12.038 |
| [92] |
Huber V.J., Tsujita M., Kwee I.L., et al. Inhibition of aquaporin 4 by antiepileptic drugs // Bioorg Med Chem Lett. 2009. Vol. 17, No. 1. P. 418–424. DOI: 10.1016/j.bmc.2007.12.038 |
| [93] |
Ding Z, Zhang J, Xu J, et al. Propofol administration modulates AQP-4 expression and brain edema after traumatic brain injury. Cell Biochem Biophys. 2013;67(2):615–622. DOI: 10.1007/s12013-013-9549-0 |
| [94] |
Ding Z., Zhang J., Xu J., et al. Propofol administration modulates AQP-4 expression and brain edema after traumatic brain injury // Cell Biochem Biophys. 2013. Vol. 67, No. 2. P. 615–622. DOI: 10.1007/s12013-013-9549-0 |
| [95] |
Mazumder MK, Borah A. Piroxicam confer neuroprotection in Cerebral Ischemia by inhibiting cyclooxygenases, acid- sensing ion channel-1a and aquaporin-4: An in silico comparison with Aspirin and Nimesulide. Bioinformation. 2015;11(4):217–222. DOI: 10.6026/97320630011217 |
| [96] |
Mazumder M.K., Borah A. Piroxicam confer neuroprotection in Cerebral Ischemia by inhibiting cyclooxygenases, acid- sensing ion channel-1a and aquaporin-4: An in silico comparison with Aspirin and Nimesulide // Bioinformation. 2015. Vol. 11, No. 4. P. 217–222. DOI: 10.6026 / 97320630011217 |
| [97] |
Kikuchi K, Tancharoen S, Matsuda F, et al. Edaravone attenuates cerebral ischemic injury by suppressing aquaporin-4. Biochemical and Biophysical Research. 2009;390(4):1121–1125. DOI: 10.1016/j.bbrc.2009.09.015 |
| [98] |
Kikuchi K, Tancharoen S, Matsuda F., et al. Edaravone attenuates cerebral ischemic injury by suppressing aquaporin-4 // Biochemical and Biophysical Research. 2009. Vol. 390, No. 4. P. 1121–1125. DOI: 10.1016 / j.bbrc.2009.09.015 |
| [99] |
Popescu ES, Pirici I, Ciurea RN, et al. Three-dimensional organ scanning reveals brain edema reduction in a rat model of stroke treated with an aquaporin 4 inhibitor. Rom J Morphol Embryol. 2017;58:59–66. |
| [100] |
Popescu E.S., Pirici I., Ciurea R.N., et al. Three-dimensional organ scanning reveals brain edema reduction in a rat model of stroke treated with an aquaporin 4 inhibitor // Rom J Morphol Embryol. 2017. Vol. 58. P. 59–66. |
| [101] |
Novikov VE, Levchenkova OS, Pozhilova EV. Preconditioning as a method of metabolic adaptation to hypoxia and ischemia. Vestnik of the Smolensk State Medical Academy. 2018;17(1):69–79. (In Russ.) |
| [102] |
Новиков В.Е., Левченкова О.С., Пожилова Е.В. Прекондиционирование как способ метаболической адаптации организма к состояниям гипоксии и ишемии // Вестник Смоленской государственной медицинской академии. 2018. Т. 17, № 1. С. 69–79. |
| [103] |
Novikov VE, Levchenkova OS, Pozhilova EV. Pharmacological preconditioning: opportunities and prospects. Vestnik of the Smolensk state medical Academy. 2020;19(2):36–49. (In Russ.) DOI: 10.37903/vsgma.2020:2.6 |
| [104] |
Новиков В.Е., Левченкова О.С., Пожилова Е.В. Фармакологическое прекондиционирование: возможности и перспективы // Вестник Смоленской государственной медицинской академии. 2020. Т. 19, № 2. С. 36–49. DOI: 10.37903/vsgma.2020:2.6 |
| [105] |
Hoshi A, Yamamoto T, Shimizu K, et al. Chemical preconditioning-induced reactive astrocytosis contributes to the reduction of post-ischemic edema through aquaporin-4 downregulation. Exp Neurol. 2011;227:89–95. DOI: 10.1016/j.expneurol.2010.09.016 |
| [106] |
Hoshi A., Yamamoto T., Shimizu K., et al. Chemical preconditioning-induced reactive astrocytosis contributes to the reduction of post-ischemic edema through aquaporin-4 downregulation // Exp Neurol. 2011. Vol. 227. P. 89–95. DOI: 10.1016/j.expneurol.2010.09.016 |
| [107] |
Levchenkova OS, Novikov VE. Possibilities of pharmacological preconditioning. Vestnik of the Russian Academy of medical Sciences. 2016;71(1):16–24. (In Russ.). DOI: 10.15690/vramn626 |
| [108] |
Левченкова О.С., Новиков В.Е. Возможности фармакологического прекондиционирования // Вестник РАМН. 2016. Т. 71, № 1. С. 16–24. DOI: 10.15690/vramn626 |
| [109] |
Novikov VE, Levchenkova OS, Pozhilova EV. Mitochondrial nitric oxide synthase in mechanisms of cell adaptation and its pharmacological regulation. Vestnik of the Smolensk State Medical Academy. 2016;15(1):14–22. (In Russ.) |
| [110] |
Новиков В.Е., Левченкова О.С., Пожилова Е.В. Митохондриальная синтаза оксида азота в механизмах клеточной адаптации и ее фармакологическая регуляция // Вестник Смоленской государственной медицинской академии. 2016. Т. 15, № 1. С. 14–22. |
| [111] |
Novikov VE, Levchenkova OS, Pozhilova EV. Mitochondrial nitric oxide synthase and its role in the mechanisms of cell adaptation to hypoxia. Reviews on Clinical Pharmacology and Drug Therapy. 2016;14(2):38–46. (In Russ.) DOI: 10.17816/RCF14238-46 |
| [112] |
Новиков В.Е., Левченкова О.С., Пожилова Е.В. Митохондриальная синтаза оксида азота и ее роль в механизмах адаптации клетки к гипоксии // Обзоры по клинической фармакологии и лекарственной терапии. 2016. Т. 14, № 2. С. 38–46. DOI: 10.17816/RCF14238-46 |
| [113] |
Novikov VE, Ponamareva NS, Shabanov PD. Aminotiolovye antigipoksanty pri travmaticheskom oteke mozga. Saint Petersburg: Elbi-SPb; 2008. 176 p. |
| [114] |
Новиков В.Е., Понамарева Н.С., Шабанов П.Д. Аминотиоловые антигипоксанты при травматическом отеке мозга. Санкт-Петербург: Элби-СПб, 2008. 176 с. |
| [115] |
Pozhilova EV, Novikov VE, Levchenkova OS. The regulatory role of the mitochondrial pore and the possibility of its pharmacological modulation. Reviews on Clinical Pharmacology and Drug Therapy. 2014;12(3):13–19. (In Russ.) |
| [116] |
Пожилова Е.В., Новиков В.Е., Левченкова О.С. Регуляторная роль митохондриальной поры и возможности ее фармакологической модуляции // Обзоры по клинической фармакологии и лекарственной терапии. 2014. Т. 12, № 3. С. 13–19. |
| [117] |
Pozhilova EV, Novikov VE, Levchenkova OS. Reactive oxygen species in cell physiology and pathology. Vestnik of the Smolensk State Medical Academy. 2015;14(2):13–22. (In Russ.) |
| [118] |
Пожилова Е.В., Новиков В.Е., Левченкова О.С. Активные формы кислорода в физиологии и патологии клетки // Вестник Смоленской государственной медицинской академии. 2015. Т. 14, № 2. С. 13–22. |
| [119] |
Pogilova EV, Novikov VE, Levchenkova OS. The mitochondrial ATP-dependent potassium channel and its pharmacological modulators. Reviews on Clinical Pharmacology and Drug Therapy. 2016;14(1):29–36. (In Russ.) DOI: 10.17816/RCF14129-36 |
| [120] |
Пожилова Е.В., Новиков В.Е., Левченкова О.С. Митохондриальный АТФ-зависимый калиевый канал и его фармакологические модуляторы // Обзоры по клинической фармакологии и лекарственной терапии. 2016. Т. 14, № 1. С. 29–36. DOI: 10.17816/RCF14129-36 |
| [121] |
Ding T, Zhou Y, Sun K, et al. Knockdown a water channel protein, aquaporin-4, induced glioblastoma cell apoptosis. PLOS One. 2013;8(8): e66751. DOI: 10.1371/journal.pone.0066751 |
| [122] |
Ding T., Zhou Y., Sun K., et al. Knockdown a water channel protein, aquaporin-4, induced glioblastoma cell apoptosis // PLOS One. 2013. No. 8, No. 8. P. e66751. DOI: 10.1371/journal.pone.0066751 |
| [123] |
Saadoun S, Papadopoulos MC, Watanabe H, et al. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci. 2005;118(24):5691–5698. DOI: 10.1242/jcs.02680 |
| [124] |
Saadoun S., Papadopoulos M.C., Watanabe H., et al. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation // J Cell Sci. 2005. Vol. 118, No. 24. P. 5691–5698. DOI: 10.1242 /jcs.02680 |
| [125] |
McCoy ES, Haas BR, Sontheimer H. Water permeability through aquaporin-4 is regulated by protein kinase C and becomes rate-limiting for glioma invasion. Neuroscience. 2010;168(4): 971–981. DOI: 10.1016/j.neuroscience.2009.09.020 |
| [126] |
McCoy E.S., Haas B.R., Sontheimer H. Water permeability through aquaporin-4 is regulated by protein kinase C and becomes rate-limiting for glioma invasion // Neuroscience. 2010. Vol. 168, No. 4. P. 971–981. DOI: 10.1016/j.neuroscience.2009.09.020 |
| [127] |
Ponomarev VV, Mazgo NV. Devic’s disease: literature analysis and clinical discussion. International Neurological Journal. 2019;110(8): 51–58. (In Russ.) DOI: 10.22141/2224-0713.8.110.2019.187893 |
| [128] |
Пономарев В.В., Мазго Н.В. Болезнь Девика: анализ литературы и клинический разбор // Международный неврологический журнал. 2019. № 8(110). С. 51–58. DOI: 10.22141/2224-0713.8.110.2019.187893 |
| [129] |
Tradtrantip L, Asavapanumas N, Verkman AS. Emerging therapeutic targets for neuromyelitisoptica spectrum disorder. Expert Opin Ther Targets. 2020;24(3):219–229. DOI: 10.1080/14728222.2020.1732927 |
| [130] |
Tradtrantip L., Asavapanumas N., Verkman A.S. Emerging therapeutic targets for neuromyelitisoptica spectrum disorder // Expert Opin Ther Targets. 2020. Vol. 24, No. 3. P. 219–229. DOI: 10.1080 /14728222.2020.1732927 |
| [131] |
Abe Y, Yasui M. Aquaporin-4 in Neuromyelitis Optica Spectrum Disorders: A Target of Autoimmunity in the Central Nervous System. Biomolecules. 2022;12(4):591. DOI: 10.3390/biom12040591 |
| [132] |
Abe Y., Yasui M. Aquaporin-4 in Neuromyelitis Optica Spectrum Disorders: A Target of Autoimmunity in the Central Nervous System // Biomolecules. 2022. Vol. 12. No. 4. P. 591. DOI: 10.3390 /biom12040591 |
| [133] |
Tradtrantip L, Zhang H, Saadoun S, et al. Anti-Aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. Ann Neurol. 2012;71(3):314–322. DOI:10.1002/ana.22657 |
| [134] |
Tradtrantip L., Zhang H., Saadoun S., et al. Anti-Aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica // Ann Neurol. 2012. Vol. 71, No. 3. P. 314–322. DOI:10.1002/ana.22657 |
| [135] |
Verkman AS, Smith AJ, Phuan PW. The aquaporin-4 water channel as a potential drug target in neurological disorders. Expert Opinion on Therapeutic Targets. 2017;21(12):1161–1170. DOI: 10.1080/14728222.2017.1398236 |
| [136] |
Verkman A.S., Smith A.J., Phuan P.W. The aquaporin-4 water channel as a potential drug target in neurological disorders // Expert Opinion on Therapeutic Targets. 2017. Vol. 21, No. 12. P. 1161–1170. DOI: 10.1080 /14728222.2017.1398236 |
| [137] |
Nikolenko VN, Oganesyan MV, Yakhno NN, et al. The brain’s glymphatic system: physiological anatomy and clinical perspectives. Neurology, Neuropsychiatry, Psychosomatics. 2018;10(4):94–100. (In Russ.). DOI: 10.14412/2074-2711-2018-4-94-100 |
| [138] |
Николенко В.Н. Оганесян М.В., Яхно Н.Н., и др. Глимфатическая система головного мозга: функциональная анатомия и клинические перспективы // Неврология, нейропсихиатрия, психосоматика. 2018. Т. 10, № 4. С. 94–100. DOI: 10.14412/2074-2711-2018-4-94-100 |
| [139] |
Mestre H, Mori Y, Nedergaard M. The Brain’s Glymphatic System: Current Controversies. Trends Neurosci. 2020;43(7):458–466. DOI: 10.1016/j.tins.2020.04.003 |
| [140] |
Mestre H., Mori Y., Nedergaard M. The Brain’s Glymphatic System: Current Controversies // Trends Neurosci. 2020. Vol. 43, No. 7. P. 458–466. DOI:10. 1016/j.tins.2020.04.003 |
| [141] |
Wei F, Song J, Zhang C, et al. Chronic stress impairs the aquaporin-4-mediated glymphatic transport through glucocorticoid signaling. Psychopharmacology (Berl). 2019;236(4):1367–1384. DOI: 10.1007/s00213-018-5147-6 |
| [142] |
Wei F., Song J., Zhang C., et al. Chronic stress impairs the aquaporin-4-mediated glymphatic transport through glucocorticoid signaling // Psychopharmacology (Berl). 2019. Vol. 236, No. 4. P. 1367–1384. DOI: 10.1007/s00213-018-5147-6 |
| [143] |
Badaut J, Brunet J-F, Guérin C. Alteration of glucose metabolism in cultured astrocytes after AQP9-small interference RNA application. Brain Res. 2012;1473:19–24. DOI: 10.1016/j.brainres.2012.07.041 |
| [144] |
Badaut J., Brunet J-F., Guérin C. Alteration of glucose metabolism in cultured astrocytes after AQP9-small interference RNA application // Brain Res. 2012. Vol. 1473. P. 19–24. DOI: 10.1016/j.brainres.2012.07.041 |
| [145] |
Fossdal G, Vik-Mo EO, Sandberg C, et al. Aqp 9 and brain tumour stem cells. Scientific World Journal. 2012;2012:915176. DOI: 10.1100/2012/915176 |
| [146] |
Fossdal G., Vik-Mo E.O., Sandberg C., et al. Aqp 9 and brain tumour stem cells // Scientific World Journal. 2012. Vol. 2012. P. 915176. DOI: 10.1100/2012/915176 |
| [147] |
Yang M, Gao F, Liu H, et al. Temporal changes in expression of aquaporin 3, -4, -5 and -8 in rat brains after permanent focal cerebral ischemia. Brain Res. 2009;1290:121–132. DOI: 10.1016/j.brainres.2009.07.018 |
| [148] |
Yang M., Gao F., Liu H., et al. Temporal changes in expression of aquaporin 3, -4, -5 and -8 in rat brains after permanent focal cerebral ischemia // Brain Res. 2009. Vol. 1290. P. 121–132. DOI: 10.1016 /j.brainres.2009.07.018 |
| [149] |
Levchenkova OS, Novikov VE. Antihypoxants: possible mechanisms of action and their clinical uses. Vestnik of the Smolensk State Medical Academy. 2011;10(4):43–57. (In Russ.) |
| [150] |
Левченкова О.С., Новиков В.Е. Антигипоксанты: возможные механизмы действия и клиническое применение // Вестник Смоленской государственной медицинской академии. 2011. Т. 10, № 4. С. 43–57. |
| [151] |
Novikov VE, Ilyuhin SA. Influence of hypoxen on acetylsalicylic acid efficiency in acute inflammation. Russian Journal of Experimental and Clinical Pharmacology. 2013;76(4):32–35. (In Russ.) |
| [152] |
Новиков В.Е., Илюхин С.А. Влияние гипоксена на эффективность кислоты ацетилсалициловой при остром воспалении // Экспериментальная и клиническая фармакология. 2013. Т. 76, № 4. С. 32–35. |
| [153] |
Novikov VE, Ilyuhin SA, Pozhilova EV. Influence of metaprot and hypoxen on the inflammatory reaction development in the experiment. Reviews on Clinical Pharmacology and Drug Therapy. 2012;10(4):63–66. (In Russ.) DOI: 10.17816/RCF10463-66 |
| [154] |
Новиков В.Е., Илюхин С.А., Пожилова Е.В. Влияние метапрота и гипоксена на развитие воспалительной реакции в эксперименте // Обзоры по клинической фармакологии и лекарственной терапии. 2012. Т. 10, № 4. С. 63–66. DOI: 10.17816/RCF10463-66 |
| [155] |
González-Dávalos L, Álvarez-Pérez M, Quesada-López T, et al. Glucocorticoid gene regulation of aquaporin-7. Vitam Horm. 2020;112:179–207. DOI: 10.1016/bs.vh.2019.08.005 |
| [156] |
González-Dávalos L., Álvarez-Pérez M., Quesada-López T., et al. Glucocorticoid gene regulation of aquaporin-7 // Vitam Horm. 2020. Vol. 112. P. 179–207. DOI: 10.1016 / bs.vh.2019.08.005 |
| [157] |
de Maré SW, Venskutonytė R, Eltschkner S, et al. Structural Basis for Glycerol Efflux and Selectivity of Human Aquaporin 7. Structure. 2020;28(2):215–222.e3. DOI: 10.1016/j.str.2019.11.011 |
| [158] |
de Maré S.W., Venskutonytė R., Eltschkner S., et al. Structural Basis for Glycerol Efflux and Selectivity of Human Aquaporin 7 // Structure. 2020. Vol. 28, No. 2. P. 215–222.e3. DOI: 10.1016/j.str.2019.11.011 |
| [159] |
Zhu SJ, Wang KJ, Gan S, et al. Expression of aquaporin8 in human astrocytomas: correlation with pathologic grade. Biochem Biophys Res Commun. 2013;440(1):168–172. DOI: 10.1016/j.bbrc.2013.09.057 |
| [160] |
Zhu S.J., Wang K.J., Gan S., et al. Expression of aquaporin8 in human astrocytomas: correlation with pathologic grade // Biochem Biophys Res Commun. 2013. Vol. 440, No. 1. P. 168–172. DOI: 10.1016/j.bbrc.2013.09.057 |
| [161] |
Schnabel B, Kuhrt H, Wiedemann P, et al. Osmotic regulation of aquaporin-8 expression in retinal pigment epithelial cells in vitro: Dependence on KATP channel activation. Mol Vis. 2020;26:797–817. |
| [162] |
Schnabel B., Kuhrt H., Wiedemann P., et al. Osmotic regulation of aquaporin-8 expression in retinal pigment epithelial cells in vitro: Dependence on KATP channel activation // Mol Vis. 2020. Vol. 26. P. 797–817. |
| [163] |
Bestetti S, Medraño-Fernandez I, Galli M, et al. A persulfidation-based mechanism controls aquaporin-8 conductance. Sci Adv. 2018;4(5): eaar5770. DOI: 10.1126/sciadv.aar5770 |
| [164] |
Bestetti S., Medraño-Fernandez I., Galli M., et al. A persulfidation-based mechanism controls aquaporin-8 conductance // Sci Adv. 2018. Vol. 4, No. 5. P. eaar5770. DOI: 10.1126/sciadv.aar5770 |
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