Сегодня: 18.07.2024
RU / EN
Последнее обновление: 01.07.2024
Роль ионных каналов церебральных эндотелиоцитов в интегральной связи элементов гематоэнцефалического барьера (обзор)

Роль ионных каналов церебральных эндотелиоцитов в интегральной связи элементов гематоэнцефалического барьера (обзор)

А.Н. Шуваев, Н.В. Кувачева, А.В. Моргун, Е.Д. Хилажева, А.Б. Салмина
Ключевые слова: нейроваскуляторная единица; церебральные эндотелиальные клетки; ионные каналы; гематоэнцефаличес­кий барьер.
2016, том 8, номер 4, стр. 241.

Полный текст статьи

pdf
1600
2104

Все анатомические элементы, которые входят в гематоэнцефалический барьер (ГЭБ), играют важную роль в регуляции проницаемости и гомеостаза ЦНС в норме и патологии. Этими элементами являются эндотелиальные клетки, перициты, астроглия и нейроны, и все они входят в понятие «нейроваскуляторная единица» (НВЕ). Будучи интеграционной системой, НВЕ тонко регулирует синаптическую пластичность нейронов, нейрогенез, межклеточные взаимодействия и проницаемость ГЭБ. Эндотелиальные клетки капилляров головного мозга являются важной составляющей НВЕ. В этом обзоре мы обсуждаем значительную роль эндотелиальных клеток капилляров мозга в поддержании структурной и функциональной целостности ГЭБ. В последние десятилетия большое внимание было уделено анализу экспрессии белков тесных контактов и белков адгезионных контактов в эндотелиальных клетках капилляров мозга и лишь относительно небольшое число исследований было сфокусировано на оценке экспрессии и функциональной активности ионных каналов в этих клетках, несмотря на то, что существует все большее число доказательств их важной роли в регуляции функций НВЕ/ГЭБ. В целом электрофизиологические свойства эндотелиальных клеток капилляров зависят от экспрессии различных ионных каналов, чья активность, по всей вероятности, координирует некоторые виды межклеточных взаимодействий в НВЕ и клетках артериол головного мозга. Мы остановили свое внимание на роли ионных каналов в регуляции активности клеток НВЕ, гладкомышечных клеток артериол и в модуляции локального кровотока головного мозга. Большое место в обзоре отведено лиганд-регулируемым ионным каналам, каналам, регулируемым внутриклеточными кальциевыми депо, TRP-каналам, кальций-активируемым и потенциалзависимым калиевым каналам в эндотелиальных клетках капилляров мозга и клетках артериол головного мозга. Понимание роли ионных каналов в контроле церебрального кровотока позволит определить новые терапевтические мишени для восстановления функциональной целостности НВЕ/ГЭБ при различных патологических состояниях (ишемия, нейровоспаление, нейродегенерация) in vivo и в моделях ГЭБ in vitro.

  1. Hawkins B.T., Davis I.P. The blound-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005; 57(2): 173–185, https://doi.org/10.1124/pr.57.2.4.
  2. Morgun A.V., Kuvacheva N.V., Khilazheva E.D., Pozhilenkova E.A., Salmina A.B. Research of the metabolic conjugation and intercellular interactions on the model of neurovascular unit in vitro. Sibirskoe meditsinskoe obozrenie 2015; 1(91): 28–31.
  3. Jennings J.R., Muldoon M.F., Ryan C., Price J.C., Greer P., Sutton-Tyrrell K., van der Veen F.M., Meltzer C.C. Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology 2005; 64(8): 1358–1365, https://doi.org/10.1212/01.wnl.0000158283.28251.3c.
  4. Prunell G.F., Mathiesen T., Svendgaard N.-A. Experimental subarachnoid hemorrhage: cerebral blood flow and brain metabolism during the acute phase in three different models in the rat. Neurosurgery 2004; 54(2): 426–437, https://doi.org/10.1227/01.neu.0000103670.09687.7a.
  5. O’Brien J.T., Eagger S., Syed G.M., Sahakian B.J., Levy R. A study of regional cerebral blood flow and cognitive performance in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 1992; 55(12): 1182–1187, https://doi.org/10.1136/jnnp.55.12.1182.
  6. Dandona P., James I.M., Newbury P.A., Woollard M.L., Beckett A.G. Cerebral blood flow in diabetes mellitus: evidence of abnormal cerebrovascular reactivity. Br Med J 1978; 2(6133): 325–326, https://doi.org/10.1136/bmj.2.6133.325.
  7. Chabriat H., Joutel A., Dichgans M., Tournier-Lasserve E., Bousser M.G. CADASIL. Lancet Neurol 2009; 8(7): 643–653, https://doi.org/10.1016/S1474-4422(09)70127-9.
  8. Calabria A.R., Shusta E.V. A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab 2008; 28(1): 135–148, https://doi.org/10.1038/sj.jcbfm.9600518.
  9. Hawkins B.T., Egleton R.D. Fluorescence imaging of blood–brain barrier disruption. J Neurosci Methods 2006; 151(2): 262–267, https://doi.org/10.1016/j.jneumeth.2005.08.006.
  10. Khan E. An examination of the blood-brain barrier in health and disease. Br J Nurs 2005; 14(9): 509–513, https://doi.org/10.12968/bjon.2005.14.9.18076.
  11. Brightman M.W., Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 1969; 40(3): 648–677, https://doi.org/10.1083/jcb.40.3.648.
  12. Coomber B.L., Stewart P.A. Morphometric analysis of CNS microvascular endothelium. Microvasc Res 1985; 30(1): 99–115, https://doi.org/10.1016/0026-2862(85)90042-1.
  13. Persidsky Y., Ramirez S.H., Haorah J., Kanmogne G.D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006; 1(3): 223–236, https://doi.org/10.1007/s11481-006-9025-3.
  14. Salmina A.B., Morgun A.V., Kuvacheva N.V., Lopatina O.L., Komleva Y.K., Malinovskaya N.A., Pozhilenkova E.A. Establishment of neurogenic microenvironment in the neurovascular unit: the connexin 43 story. Rev Neurosci 2014; 25(1): 97–111, https://doi.org/10.1515/revneuro-2013-0044.
  15. Salmina A.B., Kuvacheva N.V., Morgun A.V., Komleva Y.K., Pozhilenkova E.A., Lopatina O.L., Gorina Y.V., Taranushenko T.E., Petrova L.L. Glycolysis-mediated control of blood-brain barrier development and function. Int J Biochem Cell Biol 2015; 64: 174–184, https://doi.org/10.1016/j.bioce l.2015.04.005.
  16. Zheng W., Wang S., Chen X., Hu Z. Analysis of Sarcandra glabra and its medicinal preparations by capillary electrophoresis. Talanta 2003; 60(5): 955–960, https://doi.org/10.1016/S0039-9140(03)00178-4.
  17. Kito H., Yamamura H., Suzuki Y., Ohya S., Asai K., Imaizumi Y. Membrane hyperpolarization induced by endoplasmic reticulum stress facilitates Ca2+ influx to regulate cell cycle progression in brain capillary endothelial cells. J Pharmacol Sci 2014; 125(2): 227–232, https://doi.org/10.1254/jphs.14002sc.
  18. Yang L., Shah K.K., Abbruscato T.J. An in vitro model of ischemic stroke. Methods Mol Biol 2012; 814: 451–466, https://doi.org/10.1007/978-1-61779-452-0_30.
  19. Brillault J., Berezowski V., Cecchelli R., Dehouck M.P. Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J Neurochem 2002; 83(4): 807–817, https://doi.org/10.1046/j.1471-4159.2002.01186.x.
  20. Goldberg M.P., Ransom B.R. New light on white matter. Stroke 2003; 34(2): 330–332, https://doi.org/10.1161/01.STR.0000054048.22626.B9.
  21. Arakawa S., Wright P.M., Koga M., Phan T.G., Reutens D.C., Lim I., Gunawan M.R., Ma H., Perera N., Ly J., Zavala J., Fitt G., Donnan G.A. Ischemic thresholds for gray and white matter: a diffusion and perfusion magnetic resonance study. Stroke 2006; 37(5): 1211–1216, https://doi.org/10.1161/01.STR.0000217258.63925.6b.
  22. Song M., Yu S.P. Ionic regulation of cell volume changes and cell death after ischemic stroke. Transl Stroke Res 2014; 5(1): 17–27, https://doi.org/10.1007/s12975-013-0314-x.
  23. Morita K., Sasaki H., Furuse M., Tsukita S. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 1999; 147(1): 185–194, https://doi.org/10.1083/jcb.147.1.185.
  24. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 1993; 123(6 Pt 2): 1777–1788, https://doi.org/10.1083/jcb.123.6.1777.
  25. Bazzoni G., Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 2004; 84(3): 869–901, https://doi.org/10.1152/physrev.00035.2003.
  26. Wolburg H., Lippoldt A., Ebnet K. Tight junctions and the blood-brain barrier. In: Tight junctions. Gonzales-Mariscal L. (editor). New York: Landes Bioscience and Springer Science + Business Media; 2006; p. 175–195, https://doi.org/10.1007/0-387-36673-3_13.
  27. Takeichi M. The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 2007; 8(1): 11–20, https://doi.org/10.1038/nrn2043.
  28. Liebner S., Engelhardt B. Development of the blood–brain barrier. In: The blood-brain barrier and its microenvironment. Informa UK Limited; 2005; p. 1–26, https://doi.org/10.1201/b14290-2.
  29. Iwao B., Yara M., Hara N., Kawai Y., Yamanaka T., Nishihara H., Inoue T., Inazu M. Functional expression of choline transporter like-protein 1 (CTL1) and CTL2 in human brain microvascular endothelial cells. Neurochem Int 2015; pii: S0197-0186(15)30080-2, https://doi.org/10.1016/j.neuint.2015.12.011.
  30. Burkhart A., Skjørringe T., Johnsen K.B., Siupka P., Thomsen L.B., Nielsen M.S., Thomsen L.L., Moos T. Expression of iron-related proteins at the neurovascular unit supports reduction and reoxidation of iron for transport through the blood-brain barrier. Mol Neurobiol 2015, https://doi.org/10.1007/s12035-015-9582-7. [Epub ahead of print].
  31. Matsumoto K., Chiba Y., Fujihara R., Kubo H., Sakamoto H., Ueno M. Immunohistochemical analysis of transporters related to clearance of amyloid-β peptides through blood-cerebrospinal fluid barrier in human brain. Histochem Cell Biol 2015; 144(6): 597–611, https://doi.org/10.1007/s00418-015-1366-7.
  32. Akkaya B.G., Zolnerciks J.K., Ritchie T.K., Bauer B., Hartz A.M., Sullivan J.A., Linton K.J. The multidrug resistance pump ABCB1 is a substrate for the ubiquitin ligase NEDD4-1. Mol Membr Biol 2015; 32(2): 39–45, https://doi.org/10.3109/09687688.2015.1023378.
  33. Simard J.M., Kahle K.T., Gerzanich V. Molecular mechanisms of microvascular failure in central nervous system injury — synergistic roles of NKCC1 and SUR1/TRPM4. J Neurosurg 2010; 113(3): 622–629, https://doi.org/10.3171/2009.11.JNS081052.
  34. Longden T.A., Hill-Eubanks D.C., Nelson M.T. Ion channel networks in the control of cerebral blood flow. J Cereb Blood Flow Metab 2015; pii: 0271678X15616138, https://doi.org/10.1177/0271678X15616138. [Epub ahead of print].
  35. Stokum J.A., Gerzanich V., Simard J.M. Molecular pathophysiology of cerebral edema. J Cereb Blood Flow Metab 2015; pii: 0271678X15617172, https://doi.org/10.1177/0271678x15617172. [Epub ahead of print].
  36. Millar I.D., Wang S., Brown P.D., Barrand M.A., Hladky S.B. Kv1 and Kir2 potassium channels are expressed in rat brain endothelial cells. Pflügers Arch — Eur J Physiol 2008; 456(2): 379–391, https://doi.org/10.1007/s00424-007-0377-1.
  37. Vargas F.F., Caviedes P.F., Grant D.S. Electrophysiological characteristics of cultured human umbilical vein endothelial cells. Microvasc Res 1994; 47(2): 153–165, https://doi.org/10.1006/mvre.1994.1012.
  38. Foroutan S., Brillault J., Forbush B., O’Donnell M.E. Moderate-to-severe ischemic conditions increase activity and phosphorylation of the cerebral microvascular endothelial cell Na+-K+-Cl– cotransporter. Am J Physiol 2005; 289(6): 1492–1501, https://doi.org/10.1152/ajpcell.00257.2005.
  39. Betz A.L., Firth J.A., Goldstein G.W. Polarity of the blood-brain barrier: distribution of enzymes between the luminal and antiluminal membranes of brain capillary endothelial cells. Brain Res 1980; 192(1): 17–28, https://doi.org/10.1016/0006-8993(80)91004-5.
  40. Nag S. Ultracytochemical studies of the compromised blood–brain barrier. Methods Mol Med 2003; 89: 145–160, https://doi.org/10.1385/1592594190.
  41. Funck V.R., Ribeiro L.R., Pereira L.M., de Oliveira C.V., Grigoletto J., Della-Pace I.D., Fighera M.R., Royes L.F., Furian A.F., Larrick J.W., Oliveira M.S. Contrasting effects of Na+, K+-ATPase activation on seizure activity in acute versus chronic models. Neuroscience 2015; 298: 171–179, https://doi.org/10.1016/j.neuroscience.2015.04.031.
  42. Sánchez del Pino M.M., Hawkins R.A., Peterson D.R. Biochemical discrimination between luminal and abluminal enzyme and transport activities of the blood–brain-barrier. J Biol Chem 1995; 270(25): 14907–14912, https://doi.org/10.1074/jbc.270.25.14907.
  43. DiPolo R., Beaugé L. Sodium/calcium exchanger: influence of metabolic regulation on ion carrier interactions. Physiol Rev 2006; 86(1): 155–203, https://doi.org/10.1152/physrev.00018.2005.
  44. Strehler E.E., Zacharias D.A. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 2001; 81(1): 21–50.
  45. Emerson G.G., Segal S.S. Electrical activation of endothelium evokes vasodilation and hyperpolarization along hamster feed arteries. Am J Physiol Heart Circ Physiol 2001; 280(1): H160–H167.
  46. Dora K.A., Xia J., Duling B.R. Endothelial cell signaling during conducted vasomotor responses. Am J Physiol Heart Circ Physiol 2003; 285(1): H119–H126, https://doi.org/10.1152/ajpheart.00643.2002.
  47. Emerson G.G., Segal S.S. Electrical coupling between endothelial cells and smooth muscle cells in hamster feed arteries: role in vasomotor control. Circ Res 2000; 87(6): 474–479, https://doi.org/10.1161/01.res.87.6.474.
  48. Yamamoto Y., Imaeda K., Suzuki H. Endothelium-dependent hyperpolarization and intercellular electrical coupling in guinea-pig mesenteric arterioles. J Physiol 1999; 514(2): 505–513, https://doi.org/10.1111/j.1469-7793.1999.505ae.x.
  49. Wallraff A., Odermatt B., Willecke K., Steinhäuser C. Distinct types of astroglial cells in the hippocampus differ in gap junction coupling. Glia 2004; 48(1): 36–43, https://doi.org/10.1002/glia.20040.
  50. Tang X., Taniguchi K., Kofuji P. Heterogeneity of Kir4.1 channel expression in glia revealed by mouse transgenesis. Glia 2009; 57(16): 1706–1715, https://doi.org/10.1002/glia.20882.
  51. Zhou M., Schools G.P., Kimelberg H.K. Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 2005; 95(1): 134–143, https://doi.org/10.1152/jn.00570.2005.
  52. Callies C., Fels J., Liashkovich I., Kliche K., Jeggle P., Kusche-Vihrog K., Oberleithner H. Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J Cell Sci 2011; 124(11): 1936–1942, https://doi.org/10.1242/jcs.084657.
  53. Sarada S.K., Titto M., Himadri P., Saumya S., Vijayalakshmi V. Curcumin prophylaxis mitigates the incidence of hypobaric hypoxia-induced altered ion channels expression and impaired tight junction proteins integrity in rat brain. J Neuroinflammation 2015; 12: 113, https://doi.org/10.1186/s12974-015-0326-4.
  54. Kito H., Yamamura H., Suzuki Y., Yamamura H., Ohya S., Asai K., Imaizumi Y. Regulation of store-operated Ca2+ entry activity by cell cycle dependent up-regulation of Orai2 in brain capillary endothelial cells. Biochem Biophys Res Commun 2015; 459(3): 457–462, https://doi.org/10.1016/j.bbrc.2015.02.127.
  55. Zimmermann J., Latta L., Beck A., Leidinger P., Fecher-Trost C., Schlenstedt G., Meese E., Wissenbach U., Flockerzi V. Trans-activation response (TAR) RNA-binding protein 2 is a novel modulator of transient receptor potential canonical 4 (TRPC4) protein. J Biol Chem 2014; 289(14): 9766–9780, https://doi.org/10.1074/jbc.M114.557066.
  56. Park L., Wang G., Moore J., Girouard H., Zhou P., Anrather J., Iadecola C. The key role of transient receptor potential melastatin-2 channels in amyloid-β-induced neurovascular dysfunction. Nat Commun 2014; 5: 5318, https://doi.org/10.1038/ncomms6318.
  57. Caffes N., Kurland D.B., Gerzanich V., Simard J.M. Glibenclamide for the treatment of ischemic and hemorrhagic stroke. Int J Mol Sci 2015; 16(3): 4973–4984, https://doi.org/10.3390/ijms16034973.
  58. Neuroscience, 2nd edition. Purves D., Augustine G.J., Fitzpatrick D., Katz L.C., LaMantia A.S., McNamara J.O., Williams S.M. (editors). Sunderland (MA): Sinauer Associates; 2001.
  59. Mignery G.A., Südhof T.C. The ligand binding site and transduction mechanism in the inositol-1,4,5-triphosphate receptor. EMBO J 1990; 9(12): 3893–3898.
  60. Ledoux J., Taylor M.S., Bonev A.D., Hannah R.M., Solodushko V., Shui B., Tallini Y., Kotlikoff M.I., Nelson M.T. Functional architecture of inositol 1,4,5-trisphosphate signaling in restricted spaces of myoendothelial projections. Proc Natl Acad Sci USA 2008; 105(28): 9627–9632, https://doi.org/10.1073/pnas.0801963105.
  61. Parekh A.B., Putney J.W. Store-operated calcium channels. Physiol Rev 2005; 85(2): 757–810, https://doi.org/10.1152/physrev.00057.2003.
  62. Li J., Cubbon R.M., Wilson L.A., Amer M.S., McKeown L., Hou B., Majeed Y., Tumova S., Seymour V.A., Taylor H., Stacey M., O’Regan D., Foster R., Porter K.E., Kearney M.T., Beech D.J. Orai1 and CRAC channel dependence of VEGF-activated Ca2+ entry and endothelial tube formation. Circ Res 2011; 108(10): 1190–1198. https://doi.org/10.1161/CIRCRESAHA.111.243352.
  63. Lewis R.S. Calcium signaling mechanisms in T lymphocytes. Annual Rev Immunol 2001; 19: 497–521, https://doi.org/10.1146/annurev.immunol.19.1.497.
  64. Yamazaki D., Kito H., Yamamoto S., Ohya S., Yamamura H., Asai K., Imaizumi Y. Contribution of Kir2 potassium channels to ATP-induced cell death in brain capillary endothelial cells and reconstructed HEK293 cell model. Am J Physiol Cell Physiol 2011; 300(1): C75–C86, https://doi.org/10.1152/ajpcell.00135.2010.
  65. Kito H., Yamazaki D., Ohya S., Yamamura H., Asai K., Imaizumi Y. Up-regulation of K(ir)2.1 by ER stress facilitates cell death of brain capillary endothelial cells. Biochem Biophys Res Commun 2011; 411(2): 293–298, https://doi.org/10.1016/j.bbrc.2011.06.128.
  66. Yamazaki D., Aoyama M., Ohya S., Muraki K., Asai K., Imaizumi Y. Novel functions of small conductance Ca2+-activated K+ channel in enhanced cell proliferation by ATP in brain endothelial cells. J Biol Chem 2006; 281(50): 38430–38439, https://doi.org/10.1074/jbc.M603917200.
  67. Sonkusare S.K., Bonev A.D., Ledoux J., Liedtke W., Kotlikoff M.I., Heppner T.J., Hill-Eubanks D.C., Nelson M.T. Elementary Ca2+ signals through endothelial TRPV4 channels regulate vascular function. Science 2012; 336(6081): 597–601, https://doi.org/10.1126/science.1216283.
  68. Owsianik G., D’Hoedt D., Voets T., Nilius B. Structure-function relationship of the TRP channel superfamily. Rev Physiol Biochem Pharmacol 2006; 156: 61–90, https://doi.org/10.1007/s10254-005-0006-0.
  69. Latorre R. Perspectives on TRP channel structure and the TRPA1 puzzle. J Gen Physiol 2009; 133(3): 227–229, https://doi.org/10.1085/jgp.200910199.
  70. Minke B. Drosophila mutant with a transducer defect. Biophys Struct Mech 1977; 3(1): 59–64, https://doi.org/10.1007/bf00536455.
  71. Abramowitz J., Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 2008; 23(2): 297–328, https://doi.org/10.1096/fj.08-119495.
  72. Marrelli S.P., O’neil R.G., Brown R.C., Bryan R.M. Jr. PLA2 and TRPV4 channels regulate endothelial calcium in cerebral arteries. Am J Physiol Heart Circ Physiol 2007; 292(3): 1390–1397, https://doi.org/10.1152/ajpheart.01006.2006.
  73. Zhang L., Papadopoulos P., Hamel E. Endothelial TRPV4 channels mediate dilation of cerebral arteries: impairment and recovery in cerebrovascular pathologies related to Alzheimer’s disease. Br J Pharmacol 2013; 170(3): 661–670, https://doi.org/10.1111/bph.12315.
  74. Pu J., Wang Z., Zhou H., Zhong A., Ruan L., Jin K., Yang G. Role of TRPV4 channels in regulation of eNOS expression in brain microvascular endothelial cells under the condition of mechanical stretch. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2015; 40(9): 960–966, https://doi.org/10.11817/j.issn.1672-7347.2015.09.003.
  75. Liu L.B., Liu X.B., Ma J., Liu Y.H., Li Z.Q., Ma T., Zhao X.H., Xi Z., Xue Y.X. Bradykinin increased the permeability of BTB via NOS/NO/ZONAB-mediating down-regulation of claudin-5 and occludin. Biochem Biophys Res Commun 2015; 464(1): 118–125, https://doi.org/10.1016/j.bbrc.2015.06.082.
  76. Munsch T., Freichel M., Flockerzi V., Pape H.C. Contribution of transient receptor potential channels to the control of GABA release from dendrites. Proc Natl Acad Sci USA 2003; 100(26): 16065–16070, https://doi.org/10.1073/pnas.2535311100.
  77. Gees M., Colsoul B., Nilius B. The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harb Perspect Biol 2010; 2(10): a003962, https://doi.org/10.1101/cshperspect.a003962.
  78. Flockerzi V. An introduction on TRP channels. Handb Exp Pharmacol 2007; 179: 1–19, https://doi.org/10.1007/978-3-540-34891-7_1.
  79. Phelan K.D., Mock M.M., Kretz O., Shwe U.T., Kozhemyakin M., Greenfield L.J., Dietrich A., Birnbaumer L., Freichel M., Flockerzi V., Zheng F. Heteromeric canonical transient receptor potential 1 and 4 channels play a critical role in epileptiform burst firing and seizure-induced neurodegeneration. Mol Pharmacol 2012; 81(3): 384–392, https://doi.org/10.1124/mol.111.075341.
  80. Freichel M., Suh S.H., Pfeifer A., Schweig U., Trost C., Weissgerber P., Biel M., Philipp S., Freise D., Droogmans G., Hofmann F., Flockerzi V., Nilius B. Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4–/– mice. Nat Cell Biol 2001; 3(2): 121–127, https://doi.org/10.1038/35055019.
  81. Tiruppathi C., Freichel M., Vogel S.M., Paria B.C., Mehta D., Flockerzi V., Malik A.B. Impairment of store-operated Ca2+ entry in TRPC4–/– mice interferes with increase in lung microvascular permeability. Circ Res 2002; 91(1): 70–76, https://doi.org/10.1161/01.RES.0000023391.40106.A8.
  82. Tsvilovskyy V.V., Zholos A.V., Aberle T., Philipp S.E., Dietrich A., Zhu M.X., Birnbaumer L., Freichel M., Flockerzi V. Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology 2009; 137(4): 1415–1424, https://doi.org/10.1053/j.gastro.2009.06.046.
  83. Loh K.P., Ng G., Yu C.Y., Fhu C.K., Yu D., Vennekens R., Nilius B., Soong T.W., Liao P. TRPM4 inhibition promotes angiogenesis after ischemic stroke. Pflügers Arch — Europ J Physiol 2014; 466(3): 563–576, https://doi.org/10.1007/s00424-013-1347-4.
  84. Ghatta S., Nimmagadda D., Xu X., O’Rourke S.T. Large-conductance, calcium-activated potassium channels: structural and functional implications. Pharmacol Ther 2006; 110(1): 103–116, https://doi.org/10.1016/j.pharmthera.2005.10.007.
  85. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008; 7(12): 1013–1030, https://doi.org/10.1038/nrd2755.
  86. Wang X.C., Sun W.T., Yu C.M., Pun S.H., Underwood M.J., He G.W., Yang Q. ER stress mediates homocysteine-induced endothelial dysfunction: modulation of IKCa and SKCa channels. Atherosclerosis 2015; 242(1):
  87. 191–198, https://doi.org/10.1016/j.atherosclerosis.2015.07.021.
  88. Edwards G., Félétou M., Weston A.H. Endothelium-derived hyperpolarising factors and associated pathways: a synopsis. Pflügers Arch — Eur J Physiol 2010; 459(6): 863–879, https://doi.org/10.1007/s00424-010-0817-1.
  89. Kubo Y., Adelman J.P., Clapham D.E., Jan L.Y., Karschin A., Kurachi Y., Lazdunski M., Nichols C.G., Seino S., Vandenberg C.A. International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels. Pharmacol Rev 2005; 57(4): 509–526, https://doi.org/10.1124/pr.57.4.11.
  90. Welschoff J., Matthey M., Wenzel D. RGD peptides induce relaxation of pulmonary arteries and airways via β3-integrins. FASEB J 2014; 28(5): 2281–2292, https://doi.org/10.1096/fj.13-246348.
  91. Cahalan M.D., Chandy K.G. The functional network of ion channels in T lymphocytes. Immunol Rev 2009; 231(1): 59–87, https://doi.org/10.1111/j.1600-065X.2009.00816.x.
  92. Van Renterghem C., Vigne P., Frelin C. A charybdotoxin-sensitive, Ca2+-activated K+ channel with inward rectifying properties in brain microvascular endothelial cells: properties and activation by endothelins. J Neurochem 1995; 65(3): 1274–1281, https://doi.org/10.1046/j.1471-4159.1995.65031274.x.
  93. von Weikersthal S.F., Barrand M.A., Hladky S.B. Functional and molecular characterization of a volume-sensitive chloride current in rat brain endothelial cells. J Physiol 1999; 516(1): 75–84, https://doi.org/10.1111/j.1469-7793.1999.075aa.x.
  94. Hoyer J., Popp R., Meyer J., Galla H.J., Gögelein H. Angiotensin II, vasopressin and GTP[γ-S] inhibit inward-rectifying K+ channels in porcine cerebral capillary endothelial cells. J Membr Biol 1991; 123(1): 55–62, https://doi.org/10.1007/bf01993963.
  95. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch — Europ J Physiol 1981; 391(2): 85–100, https://doi.org/10.1007/bf00656997.
  96. Single-channel recording. Sakmann B., Neher E. (editors). Springer Science + Business Media; 1995, https://doi.org/10.1007/978-1-4419-1229-9.
  97. Lécuyer M.A., Kebir H., Prat A. Glial influences on BBB functions and molecular players in immune cell trafficking. Biochim Biophys Acta 2015; pii: S0925-4439(15)00298-7, https://doi.org/10.1016/j.bbadis.2015.10.004.
  98. da Fonseca A.C., Matias D., Garcia C., Amaral R., Geraldo L.H., Freitas C., Lima F.R. The impact of microglial activation on blood-brain barrier in brain diseases. Front Cell Neurosci 2014; 8: 362, https://doi.org/10.3389/fncel.2014.00362.
  99. Muldoon L.L., Alvarez J.I., Begley D.J., Boado R.J., Del Zoppo G.J., Doolittle N.D., Engelhardt B., Hallenbeck J.M., Lonser R.R., Ohlfest J.R., Prat A., Scarpa M., Smeyne R.J., Drewes L.R., Neuwelt E.A. Immunologic privilege in the central nervous system and the blood-brain barrier. J Cereb Blood Flow Metab 2013; 33(1):13–21, https://doi.org/10.1038/jcbfm.2012.153.
  100. Chou C.H., Fan H.C., Hueng D.Y. Potential of neural stem cell-based therapy for Parkinson’s disease. Parkinsons Dis 2015; 2015: 571475, https://doi.org/10.1155/2015/571475.
  101. Nobutoki T., Ihara T. Early disruption of neurovascular units and microcirculatory dysfunction in the spinal cord in spinal muscular atrophy type I. Med Hypotheses 2015; 85(6): 842–845, https://doi.org/10.1016/j.mehy.2015.09.028.

Shuvaev A.N., Kuvacheva N.V., Morgun A.V., Khilazheva E.D., Salmina A.B. The Role of Ion Channels Expressed in Cerebral Endothelial Cells in the Functional Integrity of the Blood-Brain Barrier (Review). Sovremennye tehnologii v medicine 2016; 8(4): 241, https://doi.org/10.17691/stm2016.8.4.29


Журнал базах данных

pubmed_logo.jpg

web_of_science.jpg

scopus.jpg

crossref.jpg

ebsco.jpg

embase.jpg

ulrich.jpg

cyberleninka.jpg

e-library.jpg

lan.jpg

ajd.jpg