Перспективы фармакологической регуляции функции аквапоринов при заболеваниях центральной нервной системы
- Авторы: Понамарева Н.С.1, Новиков В.Е.1, Пожилова Е.В.1
-
Учреждения:
- Смоленский государственный медицинский университет
- Выпуск: Том 21, № 1 (2023)
- Страницы: 35-48
- Раздел: Научные обзоры
- URL: https://journal-vniispk.ru/RCF/article/view/131539
- DOI: https://doi.org/10.17816/RCF21135-48
- ID: 131539
Цитировать
Аннотация
В обзоре проанализированы результаты научных исследований о роли аквапоринов в патогенезе заболеваний центральной нервной системы и возможности их фармакологической регуляции.
Аквапорины (AQP) — белки, участвующие в трансмембранном транспорте воды и других веществ. Они формируют водные каналы клеточных мембран и широко представлены в различных клетках млекопитающих, в том числе мембранах клеток головного и спинного мозга человека. К настоящему времени открыто около 300 типов белков семейства аквапоринов, из них 13 (AQP0–AQP12) выявлены в клетках человека. Локализация разных типов AQP в структурах центральной нервной системы, их функциональная активность и вовлеченность в развитие заболеваний данной системы различаются и представлены в основном тремя типами: AQP1, AQP4 и AQP9. Результаты научных исследований свидетельствуют о важнейшей роли AQP в поддержании водно-солевого гомеостаза и обеспечении физиологических процессов в центральной нервной системе, а также подтверждают роль AQP в патогенезе ряда заболеваний: отеке головного мозга различного генеза, инвазии опухолевых клеток и формировании перитуморозного отека, развитии аутоиммунного заболевания — оптикомиелита, болезни Альцгеймера. Фармакологическая регуляция функциональной активности аквапоринов может оказывать влияние на течение этих заболеваний. Поэтому закономерен интерес к лекарственным средствам, способным изменять экспрессию AQP.
Белки семейства аквапоринов обеспечивают трансмембранный транспорт воды и играют существенную роль в развитии патологических состояний центральной нервной системы, а также могут быть потенциальными мишенями для фармакологического воздействия при ряде заболеваний. Поиск и изучение лекарственных средств, влияющих на экспрессию и функциональную активность AQP, патогенетически обоснован и является перспективным направлением в разработке стратегий фармакотерапии отека головного мозга, злокачественных опухолей мозга и других заболеваний центральной нервной системы.
Ключевые слова
Полный текст
Открыть статью на сайте журналаОб авторах
Наталья Сергеевна Понамарева
Смоленский государственный медицинский университет
Автор, ответственный за переписку.
Email: Ponamareva-n@yandex.ru
ORCID iD: 0000-0001-8996-1753
SPIN-код: 4403-1981
канд. мед. наук, доцент, доцент кафедры фармакологии
Россия, СмоленскВасилий Егорович Новиков
Смоленский государственный медицинский университет
Email: nau@sgmu.info
ORCID iD: 0000-0002-0953-7993
SPIN-код: 1685-1028
д-р мед. наук, профессор, заведующий кафедрой фармакологии
Россия, СмоленскЕлена Васильевна Пожилова
Смоленский государственный медицинский университет
Email: elena-pozh2008@yandex.ru
ORCID iD: 0000-0002-7372-7329
SPIN-код: 6371-6930
ассистент кафедры ортопедической стоматологии с курсом ортодонтии
Россия, СмоленскСписок литературы
- 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.)
- 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.)
- 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.)
- 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.)
- Finn RN, Cerdа J. Evolution and Functional Diversity of Aquaporins. Biology Bulletin. 2015;229(1):6–23. doi: 10.1086/BBLv229n1p6
- 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
- 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
- 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
- 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
- Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci. 2013;14(14):265–277. doi: 10.1038/nrn3468
- 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
- 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
- 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
- Novikov VE. Possibilities of pharmacological neuroprotection in traumatic brain injury. Psychopharmacology and Biological Narcology. 2007;7(2):1500–1509. (In Russ.)
- 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.)
- 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.)
- 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.)
- 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.)
- 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
- 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
- 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.
- 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
- Pozhilova EV, Novikov VE. Adaptation to hypoxia in tumour growth. Vestnik of the Smolensk state medical Academy. 2015;14(3):16–20. (In Russ.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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.)
- 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
- 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
- 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
- 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.)
- 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
- Novikov VE, Ponamareva NS, Shabanov PD. Aminotiolovye antigipoksanty pri travmaticheskom oteke mozga. Saint Petersburg: Elbi-SPb; 2008. 176 p.
- 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.)
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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.)
- 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
- 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
- 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
- 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
- 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.
- 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
