Astrocytes and their participation in the mechanisms of therapeutic action of MSC in ischemic brain injury



Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

This review summarizes data on the role of astrocytes in the normal brain function and disease. After ischemic injury astroglia participates in the processes of endogenous repair and helps the surviving nerve cells to regain their lost functions. The response of astrocytes to ischemia depends on the severity of the disease and can determine its further development. To date, cellular therapy is a promising strategy in the treatment of post-stroke states. Numerous studies have shown the positive effect of mesenchymal stem cells (MSC) on functional recovery after ischemic stroke. The main effect is probably associated to the ability of MSC to enhance the endogenous restoration potential of nerve tissue. Recent experimental data have demonstrated that a special role in the therapeutic effects of cell therapy belongs to astroglial cells. Further study of the interaction of MSC and astrocytes will help in the search for new approaches in the treatment of the ischemic injury consequences.

Full Text

Restricted Access

About the authors

Y. A Kalinina

“Trans-Technologies", Ltd

Email: Yuakalinina@alkorbio.ru

E. G Gilerovich

Institution of Experimental Medicine

D. E Korzhevskii

Institution of Experimental Medicine

References

  1. Гусев Е.И., Скворцова В.И. Ишемия головного мозга. Москва: Медицина; 2001. (Gusev Eu.I., Skvortsova V.I. Brain ischemia. Moscow: Meditsina Publishers 2001].
  2. Meschia J.F., Brott T. Ischemic stroke. Eur. J. Neurol. 2018; 25(1]: 35-40.
  3. Onwuekwe I., Ezeala-Adikaibe B. Ischemic stroke and neuroprotection. Ann. Med. Health Sci. Res. 2012; 2(2]: 186-90.
  4. Marrif H., Juurlink B.H. Astrocytes respond to hypoxia by increasing glycolytic capacity. J. Neurosci. Res. 1999; 57(2]: 255-60.
  5. Mishra A., Reynolds J.P., Chen Y. et al. Astrocytes mediate neurovascular signaling to capillary pericytes but not to arterioles. Nat. Neurosci. 2016; 19(12]: 1619-27.
  6. Викторов И.В. Стволовые клетки млекопитающих: биология стволовых клеток in vivo и in vitro. Известия АН Серия биологическая 2001; 6: 646-55. (Viktorov I.V. Stem cells of mammalian brain: biology of the stem cells in vivo and in vitro. Izvestiya Academy of Sciences. Biological series 2001; 6: 646-55.].
  7. Prockop D.J., Oh J.Y. Mesenchymal stem/stromal cells (MSCs]: role as guardians of inflammation. Mol. Ther. 2012; 20(1]: 14-20.
  8. Dezawa M., Kanno H., Hoshino M. et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J. Clin. Invest. 2004; 113(12]: 1701-10.
  9. Fu X.B., Fang L.J., Wang Y.X. et al. Enhancing the repair quality of skin injury on porcine after autografting with the bone marrow mesenchymal stem cells. Zhonghua Yi Xue Za Zhi 2004; 84(11]: 920-4.
  10. Kurozumi K., Nakamura K., Tamiya T. et al. Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol. Ther. 2005; 11(1]: 96-104.
  11. Кругляков П.В., Соколова И.Б., Полынцев Д.Г. Стволовые клетки дифференцированных тканей взрослого организма. Цитология 2008; 50(7]: 557-67. (Kruglyakov P.V., Sokolova I.B., Polyntsev D.G. Stem cells from adult differentiated tissues. Tsytologiya 2008; 50(7]: 557-67].
  12. Woodbury D., Schwarz E.J., Prockop D.J. et al. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 2000; 61(4]: 364-70.
  13. Fu L., Zhu L., Huang Y. et al. Derivation of neural stem cells from mesenchymal stem cells: evidence for a bipotential stem cell population. Stem Cells Dev. 2008; 17(6]: 1109-22.
  14. Fu Y., Karbaat L., Wu L. et al. Trophic effects of mesenchymal stem cells in tissue regeneration. Tissue Eng. Part B Rev. 2017; 23(6]: 515-28.
  15. Xin H., Li Y., Shen L.H. et al. Increasing tPA activity in astrocytes induced by multipotent mesenchymal stromal cells facilitate neurite outgrowth after stroke in the mouse. PLoS One 2010; 5(2]: e9027.
  16. Zhao Y., Rempe D.A. Targeting astrocytes for stroke therapy. Neurotherapeutics 2010; 7(4]: 439-51.
  17. Shen L.H., Li Y., Gao Q. et al. Down-regulation of neurocan expression in reactive astrocytes promotes axonal regeneration and facilitates the neurorestorative effects of bone marrow stromal cells in the ischemic rat brain. Glia 2008; 56(16]: 1747-54.
  18. Li Y., Liu Z., Xin H. et al. The role of astrocytes in mediating exogenous cell-based restorative therapy for stroke. Glia 2014; 62(1]: 1-16.
  19. Magistretti P.J., Ransom B.R. Astrocytes. Neuropsychopharmacol. Fifth Gener. Prog. 2002: 133-45.
  20. Alvarez J.I., Katayama T., Prat A. Glial influence on the blood brain barrier. Glia 2013; 61(12]: 1939-58.
  21. Gordon G.R., Mulligan S.J., MacVicar B.A. Astrocyte control of the cerebrovasculature. Glia 2007; 55(12]: 1214-21.
  22. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 2007; 10(11]: 1369-76.
  23. MacVicar B.A., Newman E.A. Astrocyte regulation of blood flow in the brain. Cold Spring Harb. Perspect. Biol. 2015; 7(5]: 1-14.
  24. Koehler R.C., Roman R.J., Harder D.R. Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 2009; 32(3]: 160-9.
  25. Higashi K., Fujita A., Inanobe A. et al. An inwardly rectifying K(+] channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am. J. Physiol. Cell Physiol. 2001; 281(3]: 922-31.
  26. Lien C.F., Mohanta S.K., Frontczak-Baniewicz M. et al. Absence of glial a-dystrobrevin causes abnormalities of the blood-brain barrier and progressive brain edema. J. Biol. Chem. 2012; 287(49]: 41374-85.
  27. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M. et al. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 1997; 17(1]: 171-80.
  28. Stokum J.A., Gerzanich V., Simard J.M. Molecular pathophysiology of cerebral edema. J. Cereb. Blood Flow Metab. 2016; 36(3]: 513-38.
  29. Thrane A.S., Rappold P.M., Fujita T. et al. Critical role of aquaporin-4 (AQP4] in astrocytic Ca2+ signaling events elicited by cerebral edema. PNAS USA 2011; 108(2]: 846-51.
  30. Skucas V.A., Mathews I.B., Yang J. et al. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J. Neurosci. 2011; 31(17]: 6392-7.
  31. Saadoun S., Papadopoulos M.C., Watanabe H. et al. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell Sci. 2005; 118(Pt 24]: 5691-8.
  32. Kong H., Sha L., Fan Y. et al. Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis. Neuropsychopharmacology 2009; 34(5]: 1263-76.
  33. Li L., Zhang H., Varrin-Doyer M. et al. Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. FASEB J. 2011; 25(5]: 1556-66.
  34. Amiry-Moghaddam M., Ottersen O.P. The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 2003; 4(12]: 991-1001.
  35. Chew S.S., Johnson C.S., Green C.R. et al. Role of connexin43 in central nervous system injury. Exp. Neurol. 2010; 225(2]: 250-61.
  36. Nakase T., Fushiki S., Naus C.C. Astrocytic gap junctions composed of connexin 43 reduce apoptotic neuronal damage in cerebral ischemia. Stroke 2003; 34(8): 1987-93.
  37. Сухорукова Е.Г., Гусельникова В.В., Коржевский Д.Э. Глутамин-синтетаза в клетках головного мозга крысы. Морфология 2017; 152(6): 7-10. (Sukhorukova Ye.G., Gusel'nikova V.V., Korzhevskiy D.E. Glutamine synthetase in rat brain cells. Morphology 2017; 152(6): 7-10).
  38. Rose C.F., Verkhratsky A., Parpura V. Astrocyte glutamine synthetase: pivotal in health and disease. Biochem. Soc. Trans. 2013; 41(6): 1518-24.
  39. Коржевский Д.Э., Ленцман М.В., Гиляров А.В. и др. Морфологические проявления локальной функциональной активации астроцитов, вызванной кратковременной общей ишемией головного мозга. Журнал эволюционной биохимии и физиологии 2007; 43(5): 505-8. (Korzhevskii D.E., Gilyarov A.V., Otellin V.A. et al. Morphological manifestations of local functional activation of astrocytes induced by transient global cerebral ischemia. Journal of Evolutionary Biochemistry and Physiology 2007; 43(5): 505-8).
  40. Сухорукова Е.Г., Коржевский Д.Э., Алексеева О.С. Глиальный фибриллярный кислый белок - компонент промежуточных филаментов астроцитов мозга позвоночных. Журнал эволюционной биохимии и физиологии 2015; 51(1): 3-10. (Sukhorukova E.G., Korzhevskii D.E., Alekseeva O.S. Glial fibrillary acidic protein: The component of intermediate filaments in the vertebrate brain astrocytes. Journal of Evolutionary Biochemistry and Physiology 2015; 51(1): 3-10).
  41. Wallraff A., Kohling R., Heinemann U. et al. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 2006; 26(20): 5438-47.
  42. Parpura V., Verkhratsky A. Neuroglia at the crossroads of homoeo-stasis, metabolism and signalling: evolution of the concept. ASN Neuro 2012; 4(4): e00087.
  43. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001; 65(1): 1-105.
  44. Boison D., Chen J.F., Fredholm B.B. Adenosine signaling and function in glial cells. Cell Death Differ. 2010; 17(7): 1071-82.
  45. van der Hel W.S., Notenboom R.G.E., Bos I.W.M. et al. Reduced glutamine synthetase in hippocampal areas with neuron loss in temporal lobe epilepsy. Neurology 2005; 64(2): 326-33.
  46. Eid T., Thomas M.J., Spencer D.D. et al. Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet (London, England) 2004; 363(9402): 28-37.
  47. Lensman M., Korzhevskii D.E., Mourovets V.O. et al. Intracerebro-ventricular administration of creatine protects against damage by global cerebral ischemia in rat. Brain Res. 2006; 1114(1): 187-94.
  48. Tanaka H., Katoh A., Oguro K. et al. Disturbance of hippocampal long-term potentiation after transient ischemia in GFAP deficient mice. J. Neurosci. Res. 2002; 67(1): 11-20.
  49. Verkhratsky A., Zorec R., Rodriguez J.J. et al. Pathobiology of neurodegeneration: the role for astroglia. Opera medica Physiol. 2016; 1: 13-22.
  50. Kettenmann H., Ransom B.R., editors. Neuroglia. USA: Oxford University Press; 2004.
  51. Kintner D.B., Su G., Lenart B. et al. Increased tolerance to oxygen and glucose deprivation in astrocytes from Na(+)/H(+) exchanger isoform 1 null mice. Am. J. Physiol. Cell Physiol. 2004; 287(1): C12-21.
  52. Stokum J.A., Kurland D.B., Gerzanich V. et al. Mechanisms of astrocyte-mediated cerebral edema. Neurochem. Res. 2015; 40(2): 317-28.
  53. Manley G.T., Fujimura M., Ma T. et al. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 2000; 6(2): 159-63.
  54. Papadopoulos M.C., Krishna S., Verkman A.S. Aquaporin water channels and brain edema. Mt. Sinai J. Med. 2002; 69(4): 242-8.
  55. Panickar K.S., Norenberg M.D. Astrocytes in cerebral ischemic injury: morphological and general considerations. Glia 2005; 50(4): 287-98.
  56. Dombro R.S., Bender A.S., Norenberg M.D. Association between cell swelling and glycogen content in cultured astrocytes. Int. J. Dev. Neurosci. 2000; 18(2-3): 161-9.
  57. Hansson E., Muyderman H., Leonova J. et al. Astroglia and glutamate in physiology and pathology: aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication. Neurochem. Int. 2000; 37(2-3): 317-29.
  58. Ding S. Ca(2+) signaling in astrocytes and its role in ischemic stroke. Adv. Neurobiol. 2014; 11: 189-211.
  59. Panickar K.S., Noremberg M.D. Astrocytes in cerebral ischemic injury: Morphological and general considerations. Glia 2005; 50(4): 287-98.
  60. Kamphuis W., Mamber C., Moeton M. et al. GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One 2012; 7(8): e42823.
  61. Schmidt-Kastner R., Szymas J., Hossmann K.A. Immunohisto-chemical study of glial reaction and serum-protein extravasation in relation to neuronal damage in rat hippocampus after ischemia. Neuroscience 1990; 38(2): 527-40.
  62. Faulkner J.R., Herrmann J.E., Woo M.J. et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. Neuroscience 2004; 24(9): 2143-55.
  63. Rolls A., Shechter R., Schwartz M. The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 2009; 10(3): 235-41.
  64. Stichel C.C., Muller H.W. The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res. 1998; 294(1): 1-9.
  65. Almeida A., Delgado-Esteban M., Bolanos J.P. et al. Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture. J. Neurochem. 2002; 81(2): 207-17.
  66. Sochocka E., Juurlink B.H., Code W.E. et al. Cell death in primary cultures of mouse neurons and astrocytes during exposure to and “recovery” from hypoxia, substrate deprivation and simulated ischemia. Brain Res. 1994; 638(1-2): 21-8.
  67. Kelleher J.A., Chan P.H., Chan T.Y. et al. Modification of hypoxia-induced injury in cultured rat astrocytes by high levels of glucose. Stroke 1993; 24(6): 855-63.
  68. White S.V., Czisch C.E., Han M.H. et al. intravenous transplantation of mesenchymal progenitors distribute solely to the lungs and improve outcomes in cervical spinal cord injury. Stem Cells 2016; 34(7): 1812-25.
  69. Kurtz A. Mesenchymal stem cell delivery routes and fate. Int. J. Stem Cells 2008; 1(1): 1-7.
  70. English K. Mechanisms of mesenchymal stromal cell immunomodu-lation. Immunol. Cell Biol. 2013; 91(1): 19-26.
  71. Klinker M.W., Wei C.H. Mesenchymal stem cells in the treatment of inflammatory and autoimmune diseases in experimental animal models. World J. Stem Cells 2015; 7(3): 556-67.
  72. Sun L., Cui M., Wang Z. et al. Mesenchymal stem cells modified with angiopoietin-1 improve remodeling in a rat model of acute myocardial infarction. Biochem. Biophys. Res. Commun. 2007; 357(3): 779-84.
  73. Spanholtz T.A., Theodorou P., Holzbach T. et al. Vascular endothelial growth factor (VEGF165) plus basic fibroblast growth factor (bFGF) producing cells induce a mature and stable vascular network--a future therapy for ischemically challenged tissue. J. Surg. Res. 2011; 171(1): 329-38.
  74. Block G.J., Ohkouchi S., Fung F. et al. Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stan-niocalcin-1. Stem Cells 2009; 27(3): 670-81.
  75. Kuchroo P., Dave V., Vijayan A. et al. Paracrine factors secreted by umbilical cord-derived mesenchymal stem cells induce angiogenesis in vitro by a VEGF-independent pathway. Stem Cells Dev. 2015; 24(4): 437-50.
  76. Kim Y., Kim H., Cho H. et al. Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell. Physiol. Biochem. 2007; 20(6): 867-76.
  77. Pavlichenko N., Sokolova I., Vijde S. et al. Mesenchymal stem cells transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res. 2008; 1233: 203-13.
  78. Chu Q., Yu Z., Zhang S. et al. Astrocytes facilitate the growth and differentiation of co-cultured mesenchymal stem cells. J. Huazhong Univ. Sci. Technol. Med. Sci. 2008; 28(3): 333-6.
  79. Jiang Y., Jahagirdar B.N., Reinhardt R.L. et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418(6893): 41-9.
  80. Sun H., Benardais K., Stanslowsky N. et al. Therapeutic potential of mesenchymal stromal cells and msc conditioned medium in amyotrophic lateral sclerosis (ALS) - in vitro evidence from primary motor neuron cultures, NSC-34 cells, astrocytes and microglia. PLoS One 2013; 8(9): e72926.
  81. Fang H., Song P., Shen Y. et al. Bone mesenchymal stem cell-conditioned medium decreases the generation of astrocytes during the process of neural stem cells differentiation. J. Spinal Cord Med. 2018; 41(1): 10-6.
  82. D’alessandro J.S., Wang E.A. Bone morphogenetic proteins inhibit proliferation, induce reversible differentiation and prevent cell death in astrocyte lineage cells. Growth Factors 1994; 11(1): 45-52.
  83. Gross R.E., Mehler M.F., Mabie P.C. et al. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996; 17(4): 595-606.
  84. Mabie P.C., Mehler M.F., Marmur R. et al. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 1997; 17(11): 4112-20.
  85. Karsenty G., Luo G., Hofmann C. et al. BMP 7 is required for nephrogenesis, eye development, and skeletal patterning. Ann. N.Y. Acad. Sci. 1996; 785: 98-107.
  86. Jordan J., Bottner M., Schluesener H.J. et al. Bone morphogenetic proteins: neurotrophic roles for midbrain dopaminergic neurons and implications of astroglial cells. Eur. J. Neurosci. 1997; 9(8): 1699-709.
  87. Withers G.S., Higgins D., Charette M. et al. Bone morphogenetic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. Eur. J. Neurosci. 2000; 12(1): 106-16.
  88. Chalazonitis A., D’Autreaux F., Guha U. et al. Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset. J. Neurosci. 2004; 24(17): 4266-82.
  89. Xin H., Li Y., Chen X. et al. Bone marrow stromal cells induce BMP2/4 production in oxygen-glucose-deprived astrocytes, which promotes an astrocytic phenotype in adult subventricular progenitor cells. J. Neurosci. Res. 2006; 83(8): 1485-93.
  90. Xu W., Zheng J., Gao L. et al. Neuroprotective effects of stem cells in ischemic stroke. Stem Cells Int. 2017; 2017: 1-7.
  91. Mead B., Hill L.J., Blanch R.J. et al. Mesenchymal stromal cell-mediated neuroprotection and functional preservation of retinal ganglion cells in a rodent model of glaucoma. Cytotherapy 2016; 18(4): 487-96.
  92. Galindo L.T., Filippo T.R.M., Semedo P. et al. Mesenchymal stem cell therapy modulates the inflammatory response in experimental traumatic brain injury. Neurol. Res. Int. 2011; 2011: 564089.
  93. Gu Y., He M., Zhou X. et al. Endogenous IL-6 of mesenchymal stem cell improves behavioral outcome of hypoxic-ischemic brain damage neonatal rats by supressing apoptosis in astrocyte. Sci. Rep. 2016; 6(1]: 18587.
  94. Acalovschi D., Wiest T., Hartmann M. et al. Multiple levels of regulation of the interleukin-6 system in stroke. Stroke 2003; 34(8]: 1864-9.
  95. Cho S.R., Suh H., Yu J. et al. Astroglial activation by an enriched environment after transplantation of mesenchymal stem cells enhances angiogenesis after hypoxic-ischemic brain injury. Int. J. Mol. Sci. 2016; 17(9]: 1550.
  96. Chen J., Li Y., Katakowski M. et al. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J. Neurosci. Res. 2003; 73(6]: 778-86.
  97. Wei L., Fraser J.L., Lu Z.Y. et al. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol. Dis. 2012; 46(3]: 635-45.
  98. Tang G., Liu Y., Zhang Z. et al. Mesenchymal stem cells maintain blood-brain barrier integrity by inhibiting aquaporin-4 upregulation after cerebral ischemia. Stem Cells 2014; 32(12]: 3150-62.
  99. Li L., Lundkvist A., Andersson D. et al. Protective role of reactive astrocytes in brain ischemia. J. Cereb. Blood Flow Metab. 2008; 28(3]: 468-81.
  100. Wind T., Hansen M., Jensen J.K. et al. The molecular basis for anti-proteolytic and non-proteolytic functions of plasminogen activator inhibitor type-1: roles of the reactive centre loop, the shutter region, the flexible joint region and the small serpin fragment. Biol. Chem. 2002; 383(1]: 21-36.
  101. Bernd P. The role of neurotrophins during early development. Gene Expr. 2008; 14(4]: 241-50.
  102. Crutcher K.A. The role of growth factors in neuronal development and plasticity. CRC Crit. Rev. Clin. Neurobiol. 1986; 2(3]: 297-333.
  103. Edgar D. Nerve growth factors and molecules of the extracellular matrix in neuronal development. J. Cell Sci. Suppl. 1985; 3: 107-13.
  104. Fahnestock M., Yu G., Coughlin M.D. ProNGF: a neurotrophic or an apoptotic molecule? Prog. Brain Res. 2004; 146: 101-10.
  105. Wozniak W. Brain-derived neurotrophic factor (BDNF]: role in neuronal development and survival. Folia Morphol. (Warsz.] 1993; 52(4]: 173-81.
  106. Aoki C., Bredt D.S., Fenstemaker S. et al. The subcellular distribution of nitric oxide synthase relative to the NR1 subunit of NMDA receptors in the cerebral cortex. Prog. Brain Res. 1998; 118: 83-97.
  107. Park H.J., Shin J.Y., Kim H.N. et al. Mesenchymal stem cells stabilize the blood-brain barrier through regulation of astrocytes. Stem Cell Res. Ther. 2015; 6(1]: 1-12.
  108. Argaw A.T., Gurfein B.T., Zhang Y. et al. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. PNAS USA 2009; 106(6]: 1977-82.
  109. Bush T.G., Puvanachandra N., Horner C.H. et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999; 23(2]: 297-308.
  110. Herx L.M., Yong V.W. Interleukin-1 beta is required for the early evolution of reactive astrogliosis following CNS lesion. J. Neuropathol. Exp. Neurol. 2001; 60(10]: 961-71.
  111. Argaw A.T., Asp L., Zhang J. et al. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Invest. 2012; 122(7]: 2454-68.
  112. Tomas-Camardiel M., Rite I., Herrera A.J. et al. Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol. Dis. 2004; 16(1]: 190-201.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2019 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: 

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies