Preview

Фундаментальная и клиническая медицина

Расширенный поиск

Эпендимоциты головного мозга в нейрогенезе и регуляции структурно-функциональной целостности гемато-ликворного барьера

https://doi.org/10.23946/2500-0764-2019-4-3-83-94

Полный текст:

Аннотация

Выполнен обзор литературы, посвященный роли эпендимальных клеток головного мозга в центральной нервной системе, в том числе продукции ликвора, регуляции работы нейрогенных ниш и нейрогенеза в физиологических условиях и ряде заболеваний. В обзоре приведены современные данные о роли реснитчатого аппарата эпендимоцитов в обеспечении нормального функционирования этих клеток. Функциональная активность эпендимальных клеток может существенно отличаться в зависимости от их локализации в центральной нервной системе (ЦНС). Изучение роли эпендимоцитов в функционировании головного мозга необходимо для полноценного понимания механизмов неврологических заболеваний и может открыть новые фармакотерапевтические стратегии, ориентированные на коррекцию нейродегенерации и аберрантного развития головного мозга.

Об авторах

Ю. А. Успенская
НИИ молекулярной медицины и патобиохимии ФГБОУ ВО «Красноярский государственный медицинский университет имени профессора В.Ф. Войно-Ясенецкого» Министерства здравоохранения Российской Федерации; ФГБОУ ВО «Красноярский государственный аграрный университет»
Россия

доктор биологических наук, доцент, научный сотрудник;

профессор кафедры внутренних незаразных болезней, акушерства и физиологии сельскохозяйственных животных ,

г. Красноярск



А. В. Моргун
НИИ молекулярной медицины и патобиохимии ФГБОУ ВО «Красноярский государственный медицинский университет имени профессора В.Ф. Войно-Ясенецкого» Министерства здравоохранения Российской Федерации
Россия

доктор медицинских наук, научный сотрудник,

660022, г. Красноярск, ул. Партизана Железняка, д. 1



Е. Д. Осипова
НИИ молекулярной медицины и патобиохимии ФГБОУ ВО «Красноярский государственный медицинский университет имени профессора В.Ф. Войно-Ясенецкого» Министерства здравоохранения Российской Федерации
Россия

научный сотрудник,

г. Красноярск



С К. Антонова
НИИ молекулярной медицины и патобиохимии ФГБОУ ВО «Красноярский государственный медицинский университет имени профессора В.Ф. Войно-Ясенецкого» Министерства здравоохранения Российской Федерации
Россия

старший преподаватель кафедры биологической химии с курсом медицинской, фармацевтической и токсикологической химии,

г. Красноярск



А. Б. Салмина
НИИ молекулярной медицины и патобиохимии ФГБОУ ВО «Красноярский государственный медицинский университет имени профессора В.Ф. Войно-Ясенецкого» Министерства здравоохранения Российской Федерации
Россия

доктор медицинских наук, профессор, главный научный сотрудник и руководитель НИИ молекулярной медицины и патобиохимии, заведующая кафедрой биологической химии с курсами медицинской, фармацевтической и токсикологической химии,

г. Красноярск



Список литературы

1. Rose CR, Kirchhoff F. Glial heterogeneity: the increasing complexity of the brain. e-Neuroforum. 2015; 6 (3): 59-62. DOI: 10.1007/s13295-015-0012-0.

2. Jiménez AJ, Domínguez-Pinos MD, Guerra MM, Fernández-Llebrez P, Pérez-Fígares JM. Structure and function of the ependymal barrier and diseases associated with ependyma disruption. Tissue Barriers. 2014; 2: e28426. DOI: https://doi.org/10.4161/tisb.28426.

3. Рыжавский БЯ, Демидова ОВ, Литвинцева ЕМ, Ткач ОВ. Сравнительная оценка стероидогенной активности клеток мозга, продуцирующих стероиды, и клеток эндокринных желез // Дальневосточный медицинский журнал. 2015; (4): 72-75.

4. Nomura K, Hiyama TY, Sakuta H, Matsuda T, Lin CH, Kobayashi K, , Kobayashi K, Kuwaki T, Takahashi K, Matsui S, Noda M. [Na+] increases in body fluids sensed by central Nax induce sympathetically mediated blood pressure elevations via H+-dependent activation of ASIC1a. Neuron. 2019; 101 (1): 60- 75.e6. DOI: 10.1016/j.neuron.2018.11.017.

5. Delgehyr N, Meunier A, Faucourt M, Bosch Grau M, Strehl L, Janke C, Spassky N.Ependymal cell differentiation, from monociliated to multiciliated cells. Methods Cell Biol. 2015; 127: 19- 35. DOI: 10.1016/bs.mcb.2015.01.004.

6. Olstad EW, Ringers C, Hansen JN, Wens A, Brandt C, Wachten D, Yaksi E, Jurisch-Yaksi N. Ciliary beating compartmentalizes cerebrospinal fluid flow in the brain and regulates ventricular development. Curr Biol. 2019; 29 (2): 229-241.e6. DOI: 10.1016/j.cub.2018.11.059.

7. Omran AJA, Saternos HC, Althobaiti YS, Wisner A, Sari Y, Nauli SM, Abou Alaiwi WA. Alcohol consumption impairs the ependymal cilia motility in the brain ventricles. Sci Rep. 2017; 7 (1): 13652. DOI: 10.1038/s41598-017-13947-3.

8. Liu T, Jin X, Prasad RM, Sari Y, Nauli SM. Three types of ependymal cells with intracellular calcium oscillation are characterized by distinct cilia beating properties. J Neurosci Res. 2014; 92 (9): 1199-1204. DOI: 10.1002/jnr.23405.

9. Cifuentes M, Baeza V, Arrabal PM, Visser R, Grondona JM, Saldivia N, Martínez F, Nualart F, Salazar K. Expression of a novel ciliary protein, IIIG9, during the differentiation and maturation of ependymal cells. Mol Neurobiol. 2018; 55 (2): 1652- 1664. DOI: 10.1007/s12035-017-0434-5.

10. Chouaf-Lakhdar L, Fèvre-Montange M, Brisson C, Strazielle N, Gamrani H, Didier-Bazès M. Proliferative activity and nestin expression in periventricular cells of the adult rat brain. Neuroreport. 2003; 14 (4): 633-636. DOI: 10.1097/00001756-200303240-00022.

11. Gonzalez-Cano L, Fuertes-Alvarez S, Robledinos-Anton N, Bizy A, Villena-Cortes A, Fariñas I, Marques MM, Marin MC. p73 is required for ependymal cell maturation and neurogenic SVZ cytoarchitecture. Dev Neurobiol. 2016; 76 (7): 730-747. DOI: 10.1002/dneu.22356.

12. Fuertes-Alvarez S, Maeso-Alonso L, Villoch-Fernandez J, Wildung M, Martin-Lopez M, Marshall C, Villena-Cortes AJ, Diez-Prieto I, Pietenpol JA, Tissir F, Lizé M, Marques MM, Marin MC. p73 regulates ependymal planar cell polarity by modulating actin and microtubule cytoskeleton. Cell Death Dis. 2018;9(12):1183. DOI: http://dx.doi.org/10.1038/s41419-018-1205-6

13. Shimada IS, Acar M, Burgess RJ, Zhao Z, Morrison SJ. Prdm16 is required for the maintenance of neural stem cells in the postnatal forebrain and their differentiation into ependymal cells. Genes Dev. 2017; 31 (11): 1134-1146. DOI: 10.1101/gad.291773.116.

14. Abdelhamed Z, Vuong SM, Hill L, Shula C, Timms A, Beier D, Campbell K, Mangano FT, Stottmann RW, Goto J. A mutation in Ccdc39 causes neonatal hydrocephalus with abnormal motile cilia development in mice. Development. 2018; 145 (1): dev154500. DOI: 10.1242/dev.154500.

15. Abdi K, Lai CH, Paez-Gonzalez P, Lay M, Pyun J, Kuo CT. Uncovering inherent cellular plasticity of multiciliated ependyma leading to ventricular wall transformation and hydrocephalus. Nat Commun. 2018; 9 (1): 1655. DOI: 10.1038/s41467-018- 03812-w.

16. Kyrousi C, Arbi M, Pilz GA, Pefani DE, Lalioti ME, Ninkovic J, Götz M, Lygerou Z, Taraviras S. Mcidas and GemC1 are key regulators for the generation of multiciliated ependymal cells in the adult neurogenic niche. Development. 2015; 142 (21): 3661- 3674. DOI: 10.1242/dev.126342.

17. Del Bigio MR. Ependymal cells: biology and pathology. Acta Neuropathol. 2010; 119 (1): 55-73. DOI: 10.1007/s00401-009-0624-y.

18. Chau KF, Shannon ML, Fame RM, Fonseca E, Mullan H, Johnson MB, Sendamarai AK, Springel MW, Laurent B, Lehtinen MK. Downregulation of ribosome biogenesis during early forebrain development. eLife. 2018; 7: e36998.

19. Nałęcz KA. Solute carriers in the blood-brain barier: safety in abundance. Neurochem Res. 2017; 42 (3): 795-809. DOI: 10.1007/s11064-016-2030-x.

20. Todd KL, Brighton T, Norton ES, Schick S, Elkins W, Pletnikova O, Fortinsky RH, Troncoso JC, Molfese PJ, Resnick SM, Conover JC; Alzheimer’s Disease Neuroimaging Initiative. Ventricular and periventricular anomalies in the aging and cognitively impaired brain. Front Aging Neurosci. 2018; 9: 445. DOI: 10.3389/fnagi.2017.00445.

21. Chojnacki AK, Mak GK, Weiss S. Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci. 2009; 10 (2): 153- 163. DOI: 10.1038/nrn2571.

22. Faissner A, Reinhard J. The extracellular matrix compartment of neural stem and glial progenitor cells. Glia. 2015; 63 (8): 1330- 1349. DOI: 10.1002/glia.22839.

23. Lim DA, Alvarez-Buylla A. Adult neural stem cells stake their ground. Trends Neurosci. 2014; 37 (10): 563-571. DOI: 10.1016/j.tins.2014.08.006.

24. Menon V, Thomas R, Ghale AR, Reinhard C, Pruszak J. Flow cytometry protocols for surface and intracellular antigen analyses of neural cell types. J Vis Exp. 2014; 94: 52241.

25. Carlén M, Meletis K, Göritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabé-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z,Shupliakov O, Cassidy RM, Lindvall O, Frisén J. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci. 2009; 12 (3): 259-267. DOI: 10.1038/nn.2268.

26. Shah PT, Stratton JA, Stykel MG, Abbasi S, Sharma S, Mayr KA, Koblinger K, Whelan PJ, Biernaskie J. Single-cell transcriptomics and fate mapping of ependymal cells reveals an absence of neural stem cell function. Cell. 2018; 173 (4): 1045- 1057. DOI: 10.1016/j.cell.2018.03.063.

27. Xing L, Anbarchian T, Tsai JM, Plant GW, Nusse R. Wnt/β-catenin signaling regulates ependymal cell development and adult homeostasis. Proc Natl Acad Sci USA. 2018; 115 (26): 5954- 5962. DOI: 10.1073/pnas.1803297115.

28. Sun W, Cornwell A, Li J, Peng S, Osorio MJ, Aalling N, Wang S, Benraiss A,Lou N, Goldman SA, Nedergaard M. SOX9 is an astrocyte-specific nuclear marker in the adult brain outside the neurogenic regions. J Neurosci. 2017; 37 (17): 4493-4507. DOI: 10.1523/JNEUROSCI.3199-16.2017.

29. Ortiz-Álvarez G, Daclin M, Shihavuddin A, Lansade P, Fortoul A, Faucourt M, Clavreul S, Lalioti ME, Taraviras S, Hippenmeyer S, Livet J, Meunier A, Genovesio A, Spassky N. Adult neural stem cells and multiciliated ependymal cells share a common lineage regulated by the Geminin family members. Neuron. 2019; 102 (1): 159-172. DOI:10.1016/j.neuron.2019.01.051.

30. Park S, Lee H, Lee J, Park E, Park S. Ependymal cells require Anks1a for their proper development. Mol Cells. 2019; 42 (3): 245-251. DOI: 10.14348/molcells.2018.0432.

31. Saunders NR, Liddelow SA, Dziegielewska KM. Barrier mechanisms in the developing brain. Front Pharmacol. 2012; 3: 46. DOI: 10.3389/fphar.2012.00046.

32. Задворнов А.А., Голомидов А.В., Григорьев Е.В. Клиническая патофизиология отека головного мозга (часть 1) // Вестник анестезиологии и реаниматологии. 2017. № 14 (3). С. 44-50. DOI: 10.21292/2078-5658-2017-14-3-44-50.

33. Casaca-Carreira J, Temel Y, Hescham SA, Jahanshahi A. Transependymal cerebrospinal fluid flow: opportunity for drug delivery? Mol Neurobiol. 2018; 55 (4): 2780-2788. DOI: 10.1007/s12035-017-0501-y.

34. Saunders NR, Dziegielewska KM, Møllgård K, Habgood MD, Wakefield MJ, Lindsay H, Stratzielle N, Ghersi-Egea JF, Liddelow SA. Influx mechanisms in the embryonic and adult rat choroid plexus: a transcriptome study. Front Neurosci. 2015; 9: 123. DOI: 10.3389/fnins.2015.00123.

35. Grondona JM, Granados-Durán P, Fernández-Llebrez P, LópezÁvalos MD. A simple method to obtain pure cultures of multiciliated ependymal cells from adult rodents. Histochem Cell Biol. 2013; 139 (1): 205-220. DOI: 10.1007/s00418-012-1008-2.

36. Alonso MI, Gato A. Cerebrospinal fluid and neural stem cell niche control. Neural Regen Res. 2018; 13 (9): 1546-1547. DOI: 10.4103/1673-5374.237114.

37. Bátiz LF, Castro MA, Burgos PV, Velásquez ZD, Muñoz RI, Lafourcade CA, Troncoso-Escudero P, Wyneken U. Exosomes as novel regulators of adult neurogenic niches. Front Cell Neurosci. 2016; 9: 501. DOI: 10.3389/fncel.2015.00501.

38. Komleva YK, Kuvacheva NV, Malinocskaya NA, Gorina YV, Lopatina OL, Teplyashina E A., Pozhilenkova EA, Zamay AS, Morgun AV, Salmina AB. Regenerative potential of the brain: composition and forming of regulatory microenvironment in neurogenic niches. Hum Physiol. 2016; 42 (8): 865-873.

39. Kyrousi C, Lygerou Z, Taraviras S. How a radial glial cell decides to become a multiciliated ependymal cell. Glia. 2017; 65 (7): 1032-1042. DOI: 10.1002/glia.23118.

40. Ogino T, Sawada M, Takase H, Nakai C, Herranz-Pérez V, Cebrián-Silla A, Kaneko N, García-Verdugo JM, Sawamoto K. Characterization of multiciliated ependymal cells that emerge in the neurogenic niche of the aged zebrafish brain. J Comp Neurol. 2016; 524 (15): 2982-2992. DOI: 10.1002/cne.24001.

41. Malchenko S, Sredni ST, Boyineni J, Bi Y, Margaryan NV, Guda MR, Kostenko Y, Tomita T, Davuluri RV, Mary VK, Hendrix JC, Soares MB. Characterization of brain tumor initiating cells isolated from an animal model of CNS primitive neuroectodermal tumors. Oncotarget. 2018; 9 (17): 3733-13747.

42. Michell-Robinson MA, Touil H, Healy LM, Owen DR, Durafourt BA, Bar-Or A, Antel JP, Moore CS. Roles of microglia in brain development, tissue maintenance and repair. Brain. 2015; 138 (5): 1138-1159. DOI: 10.1093/brain/awv066.

43. Akhtar AA, Breunig JJ. Lost highway(s): barriers to postnatal cortical neurogenesis and implications for brain repair. Front Cell Neurosci. 2015; 9: 216. DOI: 10.3389/fncel.2015.00216.

44. Zaky AZ, Moftah MZ. Neurogenesis and growth factors expression after complete spinal cord transection in Pleurodeles waltlii. Front Cell Neurosci. 2014; 8: 458. DOI: 10.3389/fncel.2014.00458.

45. Meletis K, Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, et al. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 2008; 6 (7): e182. DOI: 10.1371/journal.pbio.0060182.

46. Henzi R, Guerra M, Vío K, González C, Herrera C, McAllister P, Johanson C, Rodríguez EM. Neurospheres from neural stem/ neural progenitor cells (NSPCs) of non-hydrocephalic HTx rats produce neurons, astrocytes and multiciliated ependyma: the cerebrospinal fluid of normal and hydrocephalic rats supports sucha differentiation. Cell Tissue Res. 2018; 373 (2): 421-438. DOI: 10.1007/s00441-018-2828-8.

47. Del Carmen Gómez-Roldán M, Pérez-Martín M, CapillaGonzález V, Cifuentes M, Pérez J, García-Verdugo JM, GarcíaVerdugo JM, Fernández-Llebrez P. Neuroblast proliferation on the surface of the adult rat striatal wall after focal ependymal loss by intracerebroventricular injection of neuraminidase. J Comp Neurol. 2008; 507 (4): 1571-1587. DOI: 10.1002/cne.21618.

48. Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M, Rawlins E, Bennett V, Garcia-Verdugo JM, Kuo CT. Ank3- dependent SVZ niche assembly is required for the continued production of new neurons. Neuron. 2011; 71 (1): 61-75. DOI: 10.1016/j.neuron.2011.05.029.

49. Lehtinen MK, Zappaterra MW, Chen X, Yang YJ, Hill AD, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, D'Ercole AJ, Wong ET, LaMantia AS, Walsh CA. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron. 2011; 69 (5): 893-905. DOI: 10.1016/j.neuron.2011.01.023.

50. Brinker T, Stopa E, Morrison J, Klinge P. A new look at cerebrospinal fluid circulation. Fluids Barriers CNS. 2014; 11: 10. DOI: 10.1186/2045-8118-11-10.

51. Alonso MI, Lamus F, Carnicero E, Moro JA, de la Mano A, Fernández JMF, Desmond ME, Gato A. Embryonic cerebrospinal fluid increases neurogenic activity in the brain ventricularsubventricular zone of adult mice. Front Neuroanat. 2017; 11: 124. DOI: 10.3389/fnana.2017.00124.

52. Zappaterra MW, Lehtinen MK. The cerebrospinal fluid: regulator of neurogenesis, behavior, and beyond. Cell Mol Life Sci. 2012; 69 (17): 2863-2878. DOI: 10.1007/s00018-012-0957-x.

53. Toyoda R, Assimacopoulos S, Wilcoxon J, Taylor A, Feldman P, Suzuki-Hirano A, Shimogori T, Grove EA. FGF8 acts as a classic diffusible morphogen to pattern the neocortex. Development. 2010; 137 (20): 3439-3448. DOI: 10.1242/dev.055392.

54. Martin C, Bueno D, Alonso MI, Moro JA, Callejo S, Parada C, Martín P, Carnicero E, Gato A. FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev Biol. 2006; 297 (2): 402-416. DOI: 10.1016/j.ydbio.2006.05.010.

55. Parada C, Gato A, Bueno D. All-trans retinol and retinol-binding protein from embryonic cerebrospinal fluid exhibit dynamic behaviour during early central nervous system development. Neuroreport. 2008; 19 (9): 945-950. DOI: 10.1097/WNR.0b013e3283021c94.

56. Salehi Z, Mashayekhi F, Naji M, Pandamooz S. Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos. J Clin Neurosci. 2009; 16 (7): 950-953. DOI: 10.1016/j.jocn.2008.09.018.

57. Huang X, Liu J, Ketova T, Fleming JT, Grover VK, Cooper MK, Litingtung Y, Chiang C. Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc Natl Acad Sci USA. 2010; 107 (18): 8422-8427. DOI: 10.1073/pnas.0911838107.

58. Parada C, Gato A, Bueno D. Mammalian embryonic cerebrospinal fluid proteome has greater apolipoprotein and enzyme pattern complexity than the avian proteome. J Proteome Res. 2005; 4 (6): 2420-2428. DOI: http://dx.doi.org/10.1021/pr050213t.

59. Mashayekhi F, Azari M, Moghadam LM, Yazdankhah M, Naji M, Salehi Z. Changes in cerebrospinal fluid nerve growth factor levels during chick embryonic development. J Clin Neurosci. 2009; 16 (10): 1334-1337. DOI: 10.1016/j.jocn.2009.03.023.

60. Hediger MA, Clémençon B, Burrier RE, Bruford EA. The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol Aspects Med. 2013; 34 (2-3): 95-107. DOI: 10.1016/j.mam.2012.12.009.

61. Freire-Regatillo A, Argente-Arizón P, Argente J, García-Segura LM, Chowen JA. Non-neuronal cells in the hypothalamic adaptation to metabolic signals. Front Endocrinol. 2017; 8: 51. DOI: 10.3389/fendo.2017.00051.

62. Mao Y, Nguyen T, Sutherland T, Gorrie CA. Endogenous neural progenitor cells in the repair of the injured spinal cord. Neural Regen Res. 2016; 11 (7): 1075-1076. DOI: 10.4103/1673-5374.187035.

63. Lazarevic I, Engelhardt B. Modeling immune functions of the mouse blood-cerebrospinal fluid barrier in vitro: primary rather than immortalized mouse choroid plexus epithelial cells are suited to study immune cell migration across this brain barrier. Fluids Barriers CNS. 2016; 13: 2. DOI: 10.1186/s12987-016-0027-0.

64. Vandenbroucke RE. A hidden epithelial barrier in the brain with a central role in regulating brain homeostasis. Implications for aging. Ann Am Thorac Soc. 2016; 13 (5): 407-410. DOI: 10.1513/AnnalsATS.201609-676AW.

65. Brkic M, Balusu S, Van Wonterghem E, Gorlé N, Benilova I, Kremer A, Van Hove I, Moons L, De Strooper B, Kanazir S, Libert C, Vandenbroucke RE. Amyloid β oligomers disrupt bloodCSF barrier integrity by activating matrix metalloproteinases. J Neurosci. 2015; 35 (37): 12766-12778. DOI: 10.1523/JNEUROSCI.0006-15.2015.

66. Méndez-Gómez HR, Galera-Prat A, Meyers C, Chen W, Singh J, Carrión-Vázquez M, Muzyczka N Transcytosis in the blood-cerebrospinal fluid barrier of the mouse brain with an engineered receptor/ligand system. Mol Ther Methods Clin Dev. 2015; 2: 15037. DOI: 10.1038/mtm.2015.37.

67. Rodríguez EM, Blázquez JL, Pastor FE, Peláez B, Peña P, Peruzzo B, Amat P. Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int Rev Cytol. 2005; 247: 89-164. DOI: 10.1016/S0074-7696(05)47003-5.

68. Langlet F, Mullier A, Bouret SG, Prevot V, Dehouck B. Tanycyte-like cells form a blood-cerebrospinal fluid barrier in the circumventricular organs of the mouse brain. J Comp Neurol. 2013; 521 (15): 3389-3405. DOI: 10.1002/cne.23355.

69. Garcia MA, Carrasco M, Godoy A, Reinicke K, Montecinos VP, Aguayo LG, Tapia JC, Vera JC, Nualart F. Elevated expression of glucose transporter-1 in hypothalamic ependymal cells not involved in the formation of the brain-cerebrospinal fluid barrier. J Cell Biochem. 2001; 80 (4): 491-503.

70. Raikwar SP, Bhagavan SM, Ramaswamy SB, Thangavel R, Dubova I, Selvakumar GP, Ahmed ME, Kempuraj D, Zaheer S, Iyer S, Zaheer A. Are tanycytes the missing link between type 2 diabetes and Alzheimer's disease? Mol Neurobiol. 2019; 56 (2): 833-843. DOI: 10.1007/s12035-018-1123-8.

71. Chalbot S, Zetterberg H, Blennow K, Fladby T, Andreasen N, Grundke-Iqbal I, Iqbal K. Blood-cerebrospinal fluid barrier permeability in Alzheimer's disease. J Alzheimers Dis. 2011; 25 (3): 505-515. DOI: 10.3233/JAD-2011-101959.

72. Kant S, Stopa EG, Johanson CE, Baird A, Silverberg GD. Choroid plexus genes for CSF production and brain homeostasis are altered in Alzheimer's disease. Fluids Barriers CNS. 2018; 5 (1): 34. DOI: 10.1186/s12987-018-0095-4.

73. Goodman T, Hajihosseini MK. Hypothalamic tanycytes-masters and servants of metabolic, neuroendocrine, and neurogenic functions. Front Neurosci. 2015; 9: 387. DOI: 10.3389/fnins.2015.00387.

74. Kimura K, Matsumoto N, Kitada M, Mizoguchi A, Ide C. Neurite outgrowth from hippocampal neurons is promoted by choroid plexus ependymal cells in vitro. J Neurocytol. 2004; 33 (4): 465- 476. DOI: 10.1023/B:NEUR.0000046576.70319.3a.

75. Genzen JR, Platel JC, Rubio ME, Bordey A. Ependymal cells along the lateral ventricle express functional P2X(7) receptors. Purinergic Signal. 2009; 5 (3): 299-307. DOI: 10.1007/s11302-009-9143-5.

76. Nguyen DTT, Richter D, Michel G, Mitschka S, Kolanus W, Cuevas E, Wulczyn FG. The ubiquitin ligase LIN41/TRIM71 targets p53 to antagonize cell death and differentiation pathways during stem cell differentiation. Cell Death Differ. 2017; 24 (6): 1063-1078. DOI: 10.1038/cdd.2017.54.


Для цитирования:


Успенская Ю.А., Моргун А.В., Осипова Е.Д., Антонова С.К., Салмина А.Б. Эпендимоциты головного мозга в нейрогенезе и регуляции структурно-функциональной целостности гемато-ликворного барьера. Фундаментальная и клиническая медицина. 2019;4(3):83-94. https://doi.org/10.23946/2500-0764-2019-4-3-83-94

For citation:


Uspenskaya Yu.A., Morgun A.V., Osipova E.D., Antonova S.K., Salmina A.B. Brain ependymocytes in neurogenesis and maintaining integrity of blood-cerebrospinal fluid barrier. Fundamental and Clinical Medicine. 2019;4(3):83-94. (In Russ.) https://doi.org/10.23946/2500-0764-2019-4-3-83-94

Просмотров: 417


Creative Commons License
Контент доступен под лицензией Creative Commons Attribution 4.0 License.


ISSN 2500-0764 (Print)
ISSN 2542-0941 (Online)