Abstract
The review addresses current ideas about the morphological and histophysiological features of the brain capillary endothelium with a special focus on the ultrastructure of endotheliocytes, which are part of the neurovascular unit. The relationship between their main characteristics and the implementation of the barrier function is discussed. The specificity of intercellular contacts in capillary endotheliocytes within the blood–brain barrier (BBB) and the structure of their cytoskeleton and glycocalyx are analyzed. The structural peculiarities of capillaries in the neurogenic niches, as well as in the anatomical formations, where the BBB is absent or poorly expressed, are considered. A separate section of the review is devoted to transcellular transport of substances (transcytosis) in cerebral endotheliocytes. Despite a wealth of publications on the subject, many issues remain unresolved, and the study of the structure and functioning of the cerebral microvascular endothelium is still on the agenda.
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REFERENCES
Zhiven’ MK, Zaharova IS, Shevchenko AI, Pokushalov EA, Zakiyan SM (2015) Heterogeneity of endothelial cells. Pathol Blood Circul Card Surg 19(4–2):104–112. https://doi.org/10.21688/1681-3472-2015-4-2-104-112
Atkins G, Jain M, Hamik A (2011) Endothelial differentiation: molecular mechanisms of specification and heterogeneity. Arteriosclerosis, Thrombosis, and Vasc Biol 31(7):1476–1484. https://doi.org/10.1161/ATVBAHA.111.228999
Lippmann E, Azarin S, Kay J, Nessler R, Wilson H, Al-Ahmad A, Palecek S, Shusta E (2012) Derivation of blood–brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 30(8):783–791. https://doi.org/10.1038/nbt.2247
Timmermans F, Plum J, Yöder M, Ingram D, Vandekerckhove B, Case J (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13(1):87–102. https://doi.org/10.1111/j.1582-4934.2008.00598.x
Stankovich B, Aguayo E, Barragan F, Sharma A, Pallavicini M (2011) Differential adhesion molecule expression during murine embryonic stem cell commitment to the hematopoietic and endothelial lineages. PLoS One 6(9):e23810. https://doi.org/10.1371/journal.pone.0023810
Shapoval NS, Malinovskaya NA, Morgun AV, Salmina AB, Obolenskaya ON, Medvedeva NA, Medvedev OS (2021) The effect of ubiquinol on cerebral endothelial cells in different regions of rat brain. Cell and Tissue Biol 15:260–266. https://doi.org/10.1134/S1990519X21030111
Uryu K, Laurer H, McIntosh T, Praticò D, Martinez D, Leight S, Lee VM, Trojanowski JQ (2002) Repetitive mild brain trauma accelerates Aβ deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J Neurosci 22 (2):446–454. https://doi.org/10.1523/JNEUROSCI.22-02-00446.2002
Ling Guo, Hongyan Zhang, Yinglong Hou, Tianshu Wei, Ju Liu (2016) Plasmalemma vesicle-associated protein: A crucial component of vascular homeostasis. Exp Therap Med 12:1639–1644. https://doi.org/10.3892/etm.2016.3557
Strickland LA, Jubb AM, Hongo JA, Zhong F, Burwick J, Fu L, Frantz GD, Koeppen H (2005) Plasmalemmal vesicle-associated protein (PLVAP) is expressed by tumour endothelium and is upregulated by vascular endothelial growth factor-A (VEGF). J Pathol 206(4):466–475. https://doi.org/10.1002/path.1805
Shue EH, Carson-Walter EB, Liu Y, Winans BN, Ali ZS, Chen J, Walter KA (2008) Plasmalemmal vesicle associated protein-1 (PV-1) is a marker of blood–brain barrier disruption in rodent models. BMC Neurosci 9:29. https://doi.org/10.1186/1471-2202-9-29
Salmina AB, Kuvacheva NV, Morgun AV, Komleva YK, Pozhilenkova EA, Lopatina OL, Gorina YV, Taranushenko TE, Petrova LL (2015) Glycolysis-mediated control of blood–brain barrier development and function. Int J Biochem Cell Biol 64:17–184. https://doi.org/10.1016/j.biocel.2015.04.005
Rutkai I, Evans WR, Bess N, Salter-Cid T, Cikic S, Chandra PK, Katakam PVG, Mostany R, Busija DW (2020) Chronic imaging of mitochondria in the murine cerebral vasculature using in vivo two-photon microscopy. Am J Physiol Heart Circul Physiol 318(6):1379–1386. https://doi.org/10.1152/ajpheart.00751.2019
Figley CR (2011) Lactate transport and metabolism in the human brain: implications for the astrocyte-neuron lactate shuttle hypothesis. J Neurosci 31(13):4768–4770. https://doi.org/10.1523/JNEUROSCI.6612-10.2011
Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F (2009) The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 8(23):3984–4001. https://doi.org/10.4161/cc.8.23.10238
Shakhov AS, Dugina VB, Alieva IB (2019) Actin cytoskeleton of endotheliocytes—structural features of the organization guarding the barrier function (review). Biochemistry 84(4):494–508. https://doi.org/10.1134/S0320972519040031
Zielinski A, Linnartz C, Pleschka C, Dreissen G, Springer R, Merkel R, Hoffmann B (2018) Reorientation dynamics and structural interdependencies of actin, microtubules and intermediate filaments upon cyclic stretch application. Cytoskeleton. 75(9):385–394. https://doi.org/10.1002/cm.21470
Zhang C, Chen H, He Q, Luo Y, He A, Tao A, Yan J (2021) Fibrinogen/akt/microfilament axis promotes colitis by enhancing vascular permeability. CMGH Cell Mol Gastroenterol Hepatol 11(3):683–696. https://doi.org/10.1016/j.jcmgh.2020.10.007
Amann KJ, Pollard TD (2000) Cellular regulation of actin network assembly. Curr Biol 10(20):728–730. https://doi.org/10.1016/S0960-9822(00)00751-X
Cerutti C, Ridley AJ (2017) Endothelial cell adhesion and signaling. Exper Cell Res 358(1):31–38. https://doi.org/10.1016/j.yexcr.2017.06.003
Alieva IB (2014) The role of cytoskeletal microtubules in the regulation of endothelial barrier function. Biochemistry 79(9):964–975. https://doi.org/10.1134/S0006297914090119
Vlasov TD, Lazovskaya OA, Shiman’ski DA, Nesterovich II, Shaporova NL (2020) Endothelial glycocalyx: research methods and prospects for their application in assessing endothelial dysfunction. Region Вlood Сircul and Microcircul 19 (1):5–16. https://doi.org/10.24884/1682-6655-2020-19-1
Chertok VM, Chertok AG (2016) Regulatory potential of brain capillaries. Pacific Med J 2:72–80. (In Russ).
Song HW, Foreman KL, Gastfriend BD, Kuo JS, Palecek SP, Shusta EV (2020) Transcriptomic comparison of human and mouse brain microvessels. Sci Rep 10:12358. https://doi.org/10.1038/s41598-020-69096-7
Zeng Y (2016) Endothelial glycocalyx as a critical signalling platform integrating the extracellular hemodynamic forces and chemical signalling. J Cell Mol Med 221(8):1457–1462. https://doi.org/10.1111/jcmm.13081
Maksimenko AV, Turashev AD (2014) Endothelial glycocalyx of blood circulation. I. Finding, components, structure organization (Review). Bioorgan Chem 40(2):119–128. https://doi.org/10.1134/s1068162014020113.
Ostrowski SR, Gaïni S, Pedersen C, Johansson PI (2015) Sympathoadrenal activation and endothelial damage in patients with varying degrees of acute infectious disease: An observational study. J Crit Care Elsevier Inc 30(1):90–96. https://doi.org/10.1016/j.jcrc.2014.10.006
Zeng Y, Liu J (2016) Role of glypican-1 in endothelial NOS activation under various steady shear stress magnitudes. Exp Cell Res Elsevier 348(2):184–189. https://doi.org/10.1016/j.yexcr.2016.09.017
Mahmoud M, Mayer M, Cancel LM, Bartosch AM, Mathews R, Tarbell JM (2021) The Glycocalyx core protein Glypican 1 protects vessel wall endothelial cells from stiffness-mediated dysfunction and disease. Cardiovasc Res 117(6): 1592–1605. https://doi.org/10.1093/cvr/cvaa201
Yen W, Cai B, Yang J, Zhang L, Zeng M, Tarbell JM, Fu BM (2015) Endothelial surface glycocalyx can regulate flow-induced nitric oxide production in microvessels in vivo. PLoS One 10(1):1–20. https://doi.org/10.1371/journal.pone.0117133
Zeng Y (2017) Endothelial glycocalyx as a critical signalling platform integrating the extracellular hemodynamic forces and chemical signalling. J Cell Mol Med 21(8):1457–1462. https://doi.org/10.1111/jcmm.13081
Gao L, Lipowsky HH (2010) Composition of the endothelial glycocalyx and its relation to its Thickness and diffusion of small solutes. Microvasc Res 80(3):394–401. https://doi.org/10.1016/j.mvr.2010.06.005
Feng S, Cen J, Huang Y, Shen H, Yao L, Wang Y, Chen Z (2011) Matrix metalloproteinase-2 and -9 secreted by leukemic cells increase the permeability of blood–brain barrier by disrupting tight junction proteins. PLoS One 6 (8):e20599. https://doi.org/10.1371/journal.pone.0020599
Cao R-N, Li T, Zhong-Yuan X, Rui X (2019) Endothelial glycocalyx as a potential therapeutic target in organ injuries. Chin Med J (Engl) Ovid Technologies (Wolters Kluwer Health) 132(8):963–975. https://doi.org/10.1097/CM9.0000000000000177.
Lennon FE, Singleton PA (2011) Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 1(3):200–213. ISSN: 2160-200X/AJCD1107003
Lipowsky HH (2012) The Endothelial Glycocalyx as a Barrier to Leukocyte Adhesion and its Mediation by Extracellular Proteases. Annu Rev Biomed Eng 40(4):840–848. https://doi.org/10.1007/s10439-011-0427-x
Wolburg H, Lippoldt A (2002) Tight junctions of the blood- brain barrier: development, composition and regulation. Vasc Pharmacol 38:323–337. https://doi.org/10.1016/s1537-1891(02)00200-8
Nagafuchi A (2001) Molecular architecture of adherens junctions. Curr Opin Cell Biol 13(5):600–603. https://doi.org/10.1016/S0955-0674(00)00257-X
Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, Bartfai T, Dejana E, Brockhaus M (2000) Homophilic interaction of junctional adhesion molecule. J Biol Chem 275(40):30970–30976. https://doi.org/10.1074/jbc.M003946200
Hatzfeld M (2005) The p120 family of cell adhesion molecules. Eur J Cell Biol 84(2,3):205–214. https://doi.org/10.1016/J.EJCB.2004.12.016
Wimmer I, Tietz S, Nishihara H, Deutsch U, Sallusto F, Gosselet F, Lyck R, Muller WA, Lassman H, Engelhardt B (2019) PECAM-1 stabilizes blood-brain barrier integrity and favors paracellular t-cell diapedesis across the blood-brain barrier during neuroinflammation. Front Immunol 10:711. https://doi.org/10.3389/fimmu.2019.00711
Andjelkovic AV, Stamatovic SM, Martinez-Revollar G, Keep RF, Phillips CM (2020) Modeling blood-brain barrier pathology in cerebrovascular disease in vitro: current and future paradigms. Fluids and Barriers of the CNS 17(1):44. https://doi.org/10.1186/s12987-020-00202-7
Nusrat A, Brown GT, Tom J, Drake A, Bui TT, Quan C, Mrsny RJ (2005) Multiple protein interactions involving proposed extracellular loop domains of the tight junction protein occludin. Mol Biol Cell 16(4):1725–1734. https://doi.org/10.1091/MBC.E04-06-0465
Van Itallie CM, Anderson JM (2004) The role of claudins in determining paracellular charge selectivity. Proc Am Thorac Soc 1(1):38–41. https://doi.org/10.1513/pats.2306013
Soma T, Chiba H, Kato-Mori Y, Wada T, Yamashita T, Kojima T, Sawada N (2004) Thr(207) of claudin-5 is involved in size-selective loosening of the endothelial barrier by cyclic AMP. Exp Cell Res 300(1):202–212. https://doi.org/10.1016/J.YEXCR.2004.07.012
Matter K, Balda MS (2003) Holey barrier: claudins and the regulation of brain endothelial permeability. J Cell Biol 161(3):459–460. https://doi.org/10.1083/jcb.200304039
Belanger M, Asashima T, Ohtsuki S, Yamaguchi H, Ito S, Terasaki T (2007) Hyperammonemia induces transport of taurine and creatine and suppresses claudin-12 gene expression in brain capillary endothelial cells in vitro. Neurochem Int 50(1):95–101. https://doi.org/10.1016/j.neuint.2006.07.005
Ohtsuki S, Sato S, Yamaguchi H, Kamoi M, Asashima T, Terasaki T (2007) Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J Cell Physiol. 210(1):81–86. https://doi.org/10.1007/s00441-005-1101-0
Bernacki J, Dobrowolska A, Nierwińska K, Małecki A (2008) Physiology and pharmacological role of the blood-brain barrier. Pharmacol Rep 60(5):600–622. PMID: 19066407
Cordenonsi M, D’Atri F, Hammar E, Parry DA, Kendrick-Jones J, Shore D, Citi S (1999) Cingulin contains globular and coiled-coil domains and interacts with ZO-1, ZO-2, ZO-3, and myosin. J Cell Biol 147(7):1569–1582. https://doi.org/10.1083/jcb.147.7.1569
Tiwari SB, Amiji MM (2006) A review of nanocarrier-based CNS delivery systems. Curr Drug Deliv 3(2):219–232. https://doi.org/10.2174/156720106776359230
Meyer TN, Hunt J, Schwesinger C, Denker BM (2003) Galpha12 regulates epithelial cell junctions through Src tyrosine kinases. Am J Physiol Cell Physiol 285(5):C1281–C1293. https://doi.org/10.1152/ajpcell.00548.2002
Van Hinsbergh VW, van Nieuw Amerongen GP (2002) Intracellular signalling involved in modulating human endothelial barrier function. J Anat 200(6):549–560. https://doi.org/10.1046/j.1469-7580.2002.00047_7.x
Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW (2005) ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 106(2):584–592. https://doi.org/10.1182/blood-2004-12-4942
Goncharov NV, Popova PI, Golovkin AS, Zaluckaya NM, Pal'chikova EI, Zanin KV, Avdonin PV (2020) Vascular endothelial dysfunction is a pathogenetic factor in the development of neurodegenerative diseases and cognitive disorders. Rev Psych Med Psychol named after VM Bekhterev 3:11–26. https://doi.org/10.31363/2313-7053-2020-3-11-26
Nadeev AD, Kudryavtsev IV, Serebriakova MK, Avdonin PV, Zinchenko VP, Goncharov NV (2015) Dual Proapoptotic and pronecrotic effect of hydrogen peroxide on human umbilical vein endothelial cells. Citologia 57(12):909–916. (In Russ).
Li Q, Syrovets T, Simmet T, Ding J, Xu J, Chen W, Zhu D, Gao P (2013) Plasmin induces intercellular adhesion molecule 1 expression in human endothelial cells via nuclear factor-κB/mitogen-activated protein kinases-dependent pathways. Exp Biol Med 238(2):176–186. https://doi.org/10.1177/1535370212473700
Hodo TW, de Aquino MTP, Shimamoto A, Shanker A (2020) Critical neurotransmitters in the neuroimmune network. Front Immunol 11: 1869. https://doi.org/10.3389/fimmu.2020.01869
Kuvacheva NV, Morgun AV, Malinovskaya NA, Gorina YV, Khilazheva ED, Pozhilenkova EA, Panina YA, Boytsova EB, Ruzaeva VA, Trufanova LV, Salmina AB (2016) Tight Junction Proteins of Cerebral Endothelial Cells in Early Postnatal Development. Cell Tissue Biol 10:372–377. https://doi.org/10.1134/S1990519X16050084
Erickson MA, Wilson ML, Banks WA (2020) In vitro modeling of blood-brain barrier and interface functions in neuroimmune communication. Fluids Barr CNS 17:26. https://doi.org/10.1186/s12987-020-00187-3
Yang AC, Stevens MY, Chen MB, Lee DP, Stähli D, Gate D, Contrepois K, Chen W, Iram T, Zhang L, Vest RT, Chaney A, Lehallier B, Olsson N, Bois H, Hsieh R, Cropper HC, Berdnik D, Li L, Wang EY, Traber GM, Bertozzi CR, Luo J, Snyder MP, Elias JE, Quake SR, James ML, Wyss-Coray T (2020) Physiological blood–brain transport is impaired with age by a shift in transcytosis. Nature 583(7816):425–430. https://doi.org/10.1038/s41586-020-2453-z
Kaplan L, Chow BW, Gu C (2020) Neuronal regulation of the blood-brain barrier and neurovascular coupling. Nat Rev Neurosci 21:416–432. https://doi.org/10.1038/s41583-020-0322-2
Luis A-M, Muge Y, Turgay D (2021) Pericyte morphology and function. Hystol Histopathol 36(6):18314. https://doi.org/10.14670/HH-18-314
Blinov DV (2014) Modern ideas about the role of violation of the resistance of the blood-brain barrier in the pathogenesis of CNS diseases. Part 2: Functions and mechanisms of the blood-brain barrier. Epilepsy and Paroxysmal States 6(1):70–84. (In Russ).
Komleva Y, Kuvacheva NV, Malinovskaya NA, Gorina YV, Lopatina OL, Teplyashina EA, Pozhilenkova EA, Zamay AS, Morgun AJ, Salmina AB (2016) Regenerative potential of the brain: Composition and forming of regulatory microenvironment in neurogenic niches. Human Physiol 42:865–873. https://doi.org/10.1134/s0362119716080077
Mesnil M, Defamie N, Naus C, Sarrouilhe D (2021) Brain disorders and chemical pollutants: a gap junction link? Biomolecules 11(1):51. https://doi.org/10.3390/biom11010051
Salmina AB, Kapkaeva MR, Vetchinova AS, Illarioshkin SN (2021) Novel approaches used to examine and control neurogenesis in Parkinson’s decease. Int J Mol Sci 22(17):9608. https://doi.org/10.3390/ijms22179608
Pozhilenkova EA, Lopatina OL, Komleva YK, Salmin VV, Salmina AB (2017) Blood-brain barrier-supported neurogenesis in healthy and diseased brain. Rev Neurosci 28(4):397–415. https://doi.org/10.1515/revneuro-2016-0071
Erdö F, Denes L, de Lange E (2017) Age-associated physiological and pathological changes at the blood-brain barrier: A review. J Cerebral Blood Flow & Metabolism 37(1):4–24. https://doi.org/10.1177/0271678X16679420
Gorbachev VI, Man’kov AV, Hristenko IV, Kapustina AV (2006) About some mechanisms of homeostasis of the central nervous system. Acta Biomed Scient 5(51):52–54. (In Russ).
Morris ME, Rodriguez-Cruz V, Felmlee MA (2017) SLC and ABC Transporters: Expression, Localization, and Species Differences at the Blood-Brain and the Blood-Cerebrospinal Fluid Barriers. The AAPS J 19(5):1317–1331. https://doi.org/10.1208/s12248-017-0110-8
Girardin F (2006) Membrane transporter proteins: a challenge for CNS drug development. Dialogues Clin Neurosci 8(3):311–321. https://doi.org/10.31887/dcns.2006.8.3/fgirardin
Morgun AV (2012) The main functions of the blood-brain barrier. Siber Med J 109(2):5–7. (In Russ).
Freeman MR (2010) Specification and Morphogenesis of Astrocytes. Science 330(6005):774–778. https://doi.org/10.1126/science.1190928
Miziryak EV, Krivoshapkin AL, Pedder VV, Bgatova NP, Kotlyarova AA (2019) Morphofunctional features of the hemato-encephalic barrier and possible ways to bypass it with the help of physical and physico-chemical factors (review). South Siber Scient Bull 4(28) 2:45–51. https://doi.org/10.25699/SSSB.2019.28.48974
Alyautdin RN (2012) Drugs targeting through the blood-brain barrier: Maginot line or magic sesame? Mol Med 3:3–12. (In Russ).
Ben-Zvi A, Lacoste B, Kur E, Andreone BJ, Mayshar Y, Yan H, Gu C (2014) Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 509(7501):507–511. https://doi.org/10.1038/nature13324
Andreone BJ, Chow BW, Tata A, Lacoste B, Ben-Zvi A, Bullock K, Deik AA, Ginty DD, Clish CB, Gu C (2017) Blood-brain barrier permeability is regulated by lipid transport-dependent suppression of caveolae-mediated transcytosis. Neuron 94(3):581–594. https://doi.org/10.1016/j.neuron.2017.03.043
Zhao Z, Nelson AR, Betsholtz C, Zlokovic BV (2015) Establishment and dysfunction of the blood-brain barrier. Cell 163(5):1064–1078. https://doi.org/10.1016/j.cell.2015.10.067
Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. https://doi.org/10.1146/annurev.biochem.78.081307.110540
Leite DM, Matias D, Battaglia G (2020) The Role of BAR Proteins and the Glycocalyx in Brain Endothelium Transcytosis. Cells 9 (12):E2685. https://doi.org/10.3390/cells9122685
Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33–39. https://doi.org/10.1038/9004
Slepnev VI, Ochoa G, Butler MH, De Camilli P (2000) Tandem Arrangement of the Clathrin and AP-2 Binding Domains in Amphiphysin 1 and Disruption of Clathrin Coat Function by Amphiphysin Fragments Comprising These Sites. J Biol Chem 275(23):17583–17589. https://doi.org/10.1074/jbc.M910430199
Villasenor R, Schilling M, Sundaresan J, Lutz Y, Collin L (2017) Sorting Tubules Regulate Blood-Brain Barrier Transcytosis. Cell Rep 21(11):3256–3270. https://doi.org/10.1016/j.celrep.2017.11.055
Tian X, Leite DM, Scarpa E, Nyberg S, Fullstone G, Forth J, Matias D, Apriceno A, Poma A, Duro-Castano A, Vuyyuru M, Harker-Kirschneck L, Šarić A, Zhang Z, Xiang P, Fang B, Tian Y, Luo L, Rizzello L, Battaglia G (2020) On the shuttling across the blood-brain barrier via tubule formation: Mechanism and cargo avidity bias. Sci Adv 6:eabc4397. https://doi.org/10.1101/2020.04.04.025866
Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S (2011) Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 124(12):2032–2040. https://doi.org/10.1242/jcs.086264
Hansen CG, Howard G, Nichols BJ (2011) Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 124 (16):2777–2785. https://doi.org/10.1242/jcs.084319
Chandrasekaran R, Kenworthy AK, Lacy DB (2016) Clostridium difficile Toxin A Undergoes Clathrin-Independent, PACSIN2-Dependent Endocytosis. PLoS Pathog 12(12): e1006070. https://doi.org/10.1371/journal.ppat.1006070
De Kreuk B, Anthony EC, Geerts D, Hordijk PL (2012) The F-BAR Protein PACSIN2 Regulates Epidermal Growth Factor Receptor Internalization. J Biol Chem 287(52):43438–43453. https://doi.org/10.1074/jbc.M112.391078
Verkman AS (2011) Aquaporins at a glance. J Cell Sci 124(13):2107–2112. https://doi.org/10.1242/jcs.079467
Shchepareva ME, Zaharova MN (2020) The role of aquaporins in the functioning of the nervous system in normal and pathological conditions. Neurochemistry 37(1):5–14. (In Russ).
Saadoun S, Papadopoulos MC, Davies DC, Bell BA, Krishna S (2002) Increased aquaporin I water channel expression in human brain tumors. Brain J Cancer 87(6):621–623. https://doi.org/10.1038/sj.bjc.6600512
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The writing of this review was supported by the state budget of the Russian Federation.
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Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 5, pp. 562–578https://doi.org/10.31857/S086981392205003X.
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Egorova, A.V., Baranich, T.I., Brydun, A.V. et al. Morphological and Histophysiological Features of the Brain Capillary Endothelium. J Evol Biochem Phys 58, 755–768 (2022). https://doi.org/10.1134/S0022093022030115
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DOI: https://doi.org/10.1134/S0022093022030115