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Morphological and Histophysiological Features of the Brain Capillary Endothelium

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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

  1. 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

    Article  Google Scholar 

  2. 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

    Article  CAS  Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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

    Article  CAS  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  CAS  Google Scholar 

  13. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. Chertok VM, Chertok AG (2016) Regulatory potential of brain capillaries. Pacific Med J 2:72–80. (In Russ).

    Article  Google Scholar 

  23. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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.

  34. Lennon FE, Singleton PA (2011) Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 1(3):200–213. ISSN: 2160-200X/AJCD1107003

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  PubMed  PubMed Central  Google Scholar 

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. 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

    CAS  PubMed  Google Scholar 

  49. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

  51. 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

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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

    Article  Google Scholar 

  55. 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).

    CAS  Google Scholar 

  56. 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

    Article  CAS  Google Scholar 

  57. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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

    Article  Google Scholar 

  59. 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

    Article  Google Scholar 

  60. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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

    Article  Google Scholar 

  63. 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).

    Google Scholar 

  64. 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

    Article  Google Scholar 

  65. 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

    Article  CAS  Google Scholar 

  66. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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

    Article  PubMed  Google Scholar 

  68. 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

    Article  Google Scholar 

  69. 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).

    Google Scholar 

  70. 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

    Article  PubMed  Google Scholar 

  71. 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

    Article  PubMed  PubMed Central  Google Scholar 

  72. Morgun AV (2012) The main functions of the blood-brain barrier. Siber Med J 109(2):5–7. (In Russ).

    Google Scholar 

  73. Freeman MR (2010) Specification and Morphogenesis of Astrocytes. Science 330(6005):774–778. https://doi.org/10.1126/science.1190928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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

  75. Alyautdin RN (2012) Drugs targeting through the blood-brain barrier: Maginot line or magic sesame? Mol Med 3:3–12. (In Russ).

    Google Scholar 

  76. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. https://doi.org/10.1146/annurev.biochem.78.081307.110540

    Article  CAS  PubMed  Google Scholar 

  80. 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

    Article  CAS  Google Scholar 

  81. 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

    Article  CAS  PubMed  Google Scholar 

  82. 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

    Article  CAS  PubMed  Google Scholar 

  83. 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

    Article  CAS  PubMed  Google Scholar 

  84. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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

    Article  CAS  PubMed  Google Scholar 

  86. 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

    Article  CAS  PubMed  Google Scholar 

  87. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Verkman AS (2011) Aquaporins at a glance. J Cell Sci 124(13):2107–2112. https://doi.org/10.1242/jcs.079467

    Article  CAS  PubMed  Google Scholar 

  90. 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).

    Google Scholar 

  91. 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

    Article  CAS  Google Scholar 

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Funding

The writing of this review was supported by the state budget of the Russian Federation.

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Writing a manuscript (A.V.E.); surveying the pertinent publications (E.A.V., T.I.B., A.V.B., V.S.S., V.V.G.); editing a manuscript (V.S.S., V.V.G.).

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Correspondence to A. V. Egorova.

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Translated by A. Polyanovsky

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

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