The multifaceted role of astrocytes in regulating myelination

Experimental Neurology

Volumn 283, Issue , 2016, Pages 541-549

  Kıray, Hülya ^a   Lindsay, Susan L ^a   Hosseinzadeh, Sara ^a   Barnett, Susan C ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Astrocytes; Microglia; Myelination; Neurons; Oligodendrocytes; Phenotypes

Indexed keywords

CHEMOKINE; CHOLESTEROL; CYTOKINE; GAMMA INTERFERON; TUMOR NECROSIS FACTOR;

ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL ENERGY; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; MOLECULAR INTERACTION; MYELINATION; NEUROMODULATION; NONHUMAN; OLIGODENDROCYTE PROGENITOR; OLIGODENDROGLIA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; ANIMAL; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CHEMISTRY; HUMAN; METABOLISM; MYELIN SHEATH; NERVE CELL; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CYTOKINES; HUMANS; MYELIN SHEATH; NEURONS;

EID: 84961282185     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.03.009     Document Type: Review

References (160)

1. Albrecht, P.J., Dahl, J.P., Stoltzfus, O.K., Levenson, R., Levison, S.W., Ciliary neurotrophic factor activates spinal cord astrocytes, stimulating their production and release of fibroblast growth factor-2, to increase motor neuron survival. Exp. Neurol. 173 (2002), 46–62.
2. Albrecht, P.J., Murtie, J.C., Ness, J.K., Redwine, J.M., Enterline, J.R., Armstrong, R.C., Levison, S.W., Astrocytes produce CNTF during the remyelination phase of viral-induced spinal cord demyelination to stimulate FGF-2 production. Neurobiol. Dis. 13 (2003), 89–101.
3. Albrecht, P.J., Enterline, J.C., Cromer, J., Levison, S.W., CNTF-activated astrocytes release a soluble trophic activity for oligodendrocyte progenitors. Neurochem. Res. 32 (2007), 263–271.
4. Aloisi, F., Rosa, S., Testa, U., Bonsi, P., Russo, G., Peschle, C., Levi, G., Regulation of leukemia inhibitory factor synthesis in cultured human astrocytes. J. Immunol. 152 (1994), 5022–5031.
5. Amiry-Moghaddam, M., Williamson, A., Palomba, M., Eid, T., de Lanerolle, N.C., Nagelhus, E.A., Adams, M.E., Froehner, S.C., Agre, P., Ottersen, O.P., Delayed K + clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc. Natl. Acad. Sci. 100 (2003), 13615–13620.
6. Arai, K., Lo, E.H., Astrocytes protect oligodendrocyte precursor cells via MEK/ERK and PI3K/Akt signaling. J. Neurosci. Res. 88 (2010), 758–763.
7. Araque, A., Parpura, V., Sanzgiri, R.P., Haydon, P.G., Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10 (1998), 2129–2142.
8. Araque, A., Parpura, V., Sanzgiri, R.P., Haydon, P.G., Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22 (1999), 208–215.
9. Aránguez, I., Torres, C., Rubio, N., The receptor for tumor necrosis factor on murine astrocytes: characterization, intracellular degradation, and regulation by cytokines and Theiler's murine encephalomyelitis virus. Glia. 13 (1995), 185–194.
10. Auron, P.E., The interleukin 1 receptor: ligand interactions and signal transduction. Cyto. Growth Factor Rev. 9 (1998), 221–237.
11. Barnett, S.C., Linington, C., Myelination: do astrocytes play a role?. Neuroscientist 19 (2013), 442–450.
12. Barres, B.A., The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60 (2008), 430–440.
13. Bekar, L.K., He, W., Nedergaard, M., Locus coeruleus alpha-adrenergic-mediated activation of cortical astrocytes in vivo. Cereb. Cortex. 18 (2008), 2789–2795.
14. Bergles, D.E., Jahr, C.E., Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19 (1997), 1297–1308.
15. Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B.L., Pozzan, T., Volterra, A., Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391 (1998), 281–285.
16. Bitsch, A., Kuhlmann, T., Da Costa, C., Bunkowski, S., Polak, T., Brück, W., Tumour necrosis factor alpha mRNA expression in early multiple sclerosis lesions: correlation with demyelinating activity and oligodendrocyte pathology. Glia 29 (2000), 366–375.
17. Bögler, O., Wren, D., Barnett, S.C., Land, H., Noble, M., Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2 A) progenitor cells. Proc. Natl. Acad. Sci. 87 (1990), 6368–6372.
18. Boyles, J.K., Pitas, R.E., Wilson, E., Mahley, R.W., Taylor, J.M., Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76 (1985), 1501–1513.
19. Brenner, M., Johnson, A.B., Boespflug-Tanguy, O., Rodriguez, D., Goldman, J.E., Messing, A., Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat. Genet. 27 (2001), 117–120.
20. Bugga, L., Gadient, R.A., Kwan, K., Stewart, C.L., Patterson, P.H., Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. J. Neurobiol. 36 (1998), 509–524.
21. Butzkueven, H., Zhang, J.G., Soilu-Hanninen, M., Hochrein, H., Chionh, F., Shipham, K.A., Emery, B., Turnley, A.M., Petratos, S., Ernst, M., Bartlett, P.F., Kilpatrick, T.J., LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat. Med. 8 (2002), 613–619.
22. Cammer, W., Zhang, H., Maturation of oligodendrocytes is more sensitive to TNF alpha than is survival of precursors and immature oligodendrocytes. J. Neuroimmunol. 97 (1999), 37–42.
23. Cao, Q., He, Q., Wang, Y., Cheng, X., Howard, R.M., Zhang, Y., DeVries, W.H., Shields, C.B., Magnuson, D.S., Xu, X.M., Kim, D.H., Whittemore, S.R., Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J. Neurosci. 30 (2010), 2989–3001.
24. Carter, S.L., Müller, M., Manders, P.M., Campbell, I.L., Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia 55 (2007), 1728–1739.
25. Christopherson, K.S., Ullian, E.M., Stokes, C.C., Mullowney, C.E., Hell, J.W., Agah, A., Lawler, J., Mosher, D.F., Bornstein, P., Barres, B.A., Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120 (2005), 421–433.
26. Coco, S., Calegari, F., Pravettoni, E., Pozzi, D., Taverna, E., Rosa, P., Matteoli, M., Verderio, C., Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 278 (2003), 1354–1362.
27. Dallner, C., Woods, A.G., Deller, T., Kirsch, M., Hofmann, H.D., CNTF and CNTF receptor alpha are constitutively expressed by astrocytes in the mouse brain. Glia 37 (2002), 374–378.
28. Ding, X., Yan, Y., Li, X., Li, K., Ciric, B., Yang, J., Zhang, Y., Wu, S., Xu, H., Chen, W., Lovett-Racke, A.E., Zhang, G.X., Rostami, A., Silencing IFN-γ binding/signaling in astrocytes versus microglia leads to opposite effects on central nervous system autoimmunity. J. Immunol. 194 (2015), 4251–4264.
29. Dreyfus, C.F., Dai, X., Lercher, L.D., Racey, B.R., Friedman, W.J., Black, I.B., Expression of neurotrophins in the adult spinal cord in vivo. J. Neurosci. Res. 56 (1999), 1–7.
30. Eng, L.F., Vanderhaeghen, J.J., Bignami, A., Gerstl, B., An acidic protein isolated from fibrous astrocytes. Brain Res. 28 (1971), 351–354.
31. Eng, D.L., Lee, Y.L., Lal, P.G., Expression of glutamate uptake transporters after dibutyryl cyclic AMP differentiation and traumatic injury in cultured astrocytes. Brain Res. 778 (1997), 215–221.
32. Faden, A.I., Demediuk, P., Panter, S.S., Vink, R., The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244 (1989), 798–800.
33. Farina, C., Aloisi, F., Meinl, E., Astrocytes are active players in cerebral innate immunity. Trends Immunol. 28 (2007), 138–145.
34. Faulkner, J.R., Herrmann, J.E., Woo, M.J., Tansey, K.E., Doan, N.B., Sofroniew, M.V., Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24 (2004), 2143–2155.
35. Ferrara, N., Ousley, F., Gospodarowicz, D., Bovine brain astrocytes express basic fibroblast growth factor, a neurotropic and angiogenic mitogen. Brain Res. 462 (1988), 223–232.
36. Fife, B.T., Kennedy, K.J., Paniagua, M.C., Lukacs, N.W., Kunkel, S.L., Luster, A.D., Karpus, W.J., CXCL10 (IFN-gamma-inducible protein-10) control of encephalitogenic CD4 + T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. J. Immunol. 166 (2001), 7617–7624.
37. Froger, N., Orellana, J.A., Calvo, C.F., Amigou, E., Kozoriz, M.G., Naus, C.C., Sáez, J.C., Giaume, C., Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Mol. Cell. Neurosci. 45 (2010), 37–46.
38. Frost, E.E., Nielsen, J.A., Le, T.Q., Armstrong, R.C., PDGF and FGF2 regulate oligodendrocyte progenitor responses to demyelination. J. Neurobiol. 54 (2003), 457–472.
39. Fujita, H., Sato, K., Wen, T.C., Peng, Y., Sakanaka, M., Differential expressions of glycine transporter 1 and three glutamate transporter mRNA in the hippocampus of gerbils with transient forebrain ischemia. J. Cereb. Blood Flow Metab. 19 (1999), 604–615.
40. Fünfschilling, U., Supplie, L.M., Mahad, D., Boretius, S., Saab, A.S., Edgar, J., Brinkmann, B.G., Kassmann, C.M., Tzvetanova, I.D., Möbius, W., Diaz, F., Meijer, D., Suter, U., Hamprecht, B., Sereda, M.W., Moraes, C.T., Frahm, J., Goebbels, S., Nave, K.A., Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485 (2012), 517–521.
41. Glabinski, A.R., Tani, M., Strieter, R.M., Tuohy, V.K., Ransohoff, R.M., Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis. Am. J. Pathol. 150 (1997), 617–630.
42. Godiska, R., Chantry, D., Dietsch, G.N., Gray, P.W., Chemokine expression in murine experimental allergic encephalomyelitis. J. Neuroimmunol. 58 (1995), 167–176.
43. Gundersen, V., Ottersen, O.P., Storm-Mathisen, J., Selective excitatory amino acid uptake in glutamatergic nerve terminals and in glia in the rat striatum: quantitative electron microscopic immunocytochemistry of exogenous (D)-aspartate and endogenous glutamate and GABA. Eur. J. Neurosci. 8 (1996), 758–765.
44. Guthrie, K.M., Woods, A.G., Nguyen, T., Gall, C.M., Astroglial ciliary neurotrophic factor mRNA expression is increased in fields of axonal sprouting in deafferented hippocampus. J. Comp. Neurol. 386 (1997), 137–148.
45. Halassa, M.M., Fellin, T., Haydon, P.G., The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13 (2007), 54–63.
46. Haroon, F., Drögemüller, K., Händel, U., Brunn, A., Reinhold, D., Nishanth, G., Mueller, W., Trautwein, C., Ernst, M., Deckert, M., Schlűter, D., Gp130-dependent astrocytic survival is critical for the control of autoimmune central nervous system inflammation. J. Immunol. 186 (2011), 6521–6531.
47. Hashioka, S., Klegeris, A., Schwab, C., Mcgeer, P.L., Interferon-gamma-dependent cytotoxic activation of human astrocytes and astrocytoma cells. Neurobiol. Aging 30 (2009), 1924–1935.
48. Herrmann, J.E., Imura, T., Song, B., Qi, J., Ao, Y., Nguyen, T.K., Korsak, R.A., Takeda, K., Akira, S., Sofroniew, M.V., STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J. Neurosci. 28 (2008), 7231–7243.
49. Herx, L.M., Rivest, S., Yong, V.W., Central nervous system-initiated inflammation and neurotrophism in trauma: IL-1 beta is required for the production of ciliary neurotrophic factor. J. Immunol. 165 (2000), 2232–2239.
50. Hindinger, C., Bergmann, C.C., Hinton, D.R., Phares, T.W., Parra, G.I., Hussain, S., Savarin, C., Atkinson, R.D., Stohlman, S.A., IFN-γ signaling to astrocytes protects from autoimmune mediated neurological disability. PLoS ONE, 7, 2012, e42088.
51. Hirrlinger, J., Nave, K.A., Adapting brain metabolism to myelination and long-range signal transduction. Glia 62 (2014), 1749–1761.
52. Hofman, F.M., Hinton, D.R., Johnson, K., Merrill, J.E., Tumor necrosis factor identified in multiple sclerosis brain. J Exp. Med. 170 (1989), 607–612.
53. Hudgins, S.N., Levison, S.W., Ciliary neurotrophic factor stimulates astroglial hypertrophy in vivo and in vitro. Exp. Neurol. 150 (1998), 171–182.
54. Ionescu, V.A., Villanueva, E.B., Hashioka, S., Bahniwal, M., Klegeris, A., Cultured adult porcine astrocytes and microglia express functional interferon-γ receptors and exhibit toxicity towards SH-SY5Y cells. Brain Res. Bull. 84 (2011), 244–251.
55. Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L., Fields, R.D., Astrocytes promote myelination in response to electrical impulses. Neuron 49 (2006), 823–832.
56. Izadpanah, K., Freyer, D., Weber, J.R., Braun, J.S., Brain parenchymal TNF-α and IL-1β induction in experimental pneumococcal meningitis. J. Neuroimmunol. 276 (2014), 104–111.
57. Ji, K., Miyauchi, J., Tsirka, S.E., Microglia: an active player in the regulation of synaptic activity. Neural. Plast., 2013, 2013, 627325.
58. John, G.R., Lee, S.C., Brosnan, C.F., Cytokines: powerful regulators of glial cell activation. Neuroscientist 9 (2003), 10–22.
59. Jordan, C.A., Friedrich, V.L., Godfraind, C., Cardellechio, C.B., Holmes, K.V., Dubois-Dalcq, M., Expression of viral and myelin gene transcripts in a murine CNS demyelinating disease caused by a coronavirus. Glia 2 (1989), 318–329.
60. Kamphuis, W., Mamber, C., Moeton, M., Kooijman, L., Sluijs, J.A., Jansen, AH., Verveer, M., de Groot, L.R., Smith, V.D., Rangarajan, S., Rodríguez, J.J, Orre, M., Hol, E.M. 2012. GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One 7, e42823.
61. Karpuk, N., Burkovetskaya, M., Fritz, T., Angle, A., Kielian, T., Neuroinflammation leads to region-dependent alterations in astrocyte gap junction communication and hemichannel activity. J. Neurosci. 31 (2011), 414–425.
62. Khan, M.A., De Vellis, J., Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia 12 (1994), 87–98.
63. Kim, S., Steelman, A.J., Koito, H., Li, J., Astrocytes promote TNF-mediated toxicity to oligodendrocyte precursors. J. Neurochem. 116 (2011), 53–66.
64. Koulakoff, A., Ezan, P., Giaume, C., Neurons control the expression of connexin 30 and connexin 43 in mouse cortical astrocytes. Glia 56 (2008), 1299–1311.
65. Krum, J.M., Phillips, T.M., Rosenstein, J.M., Changes in astroglial GLT-1 expression after neural transplantation or stab wounds. Exp. Neurol. 174 (2002), 137–149.
66. Kuchibhotla, K.V., Lattarulo, C.R., Hyman, B.T., Bacskai, B.J., Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323 (2009), 1211–1215.
67. Kuhlmann, T., Remington, L., Cognet, I., Bourbonniere, L., Zehntner, S., Guilhot, F., Herman, A., Guay-Giroux, A., Antel, J.P., Owens, T., Gauchat, J.F., Continued administration of ciliary neurotrophic factor protects mice from inflammatory pathology in experimental autoimmune encephalomyelitis. Am. J. Pathol. 169 (2006), 584–598.
68. Kurumada, S., Onishi, A., Imai, H., Ishii, K., Kobayashi, T., Sato, S.B., Stage-specific association of apolipoprotein A-I and E in developing mouse retina. Invest. Ophthalmol. Vis. Sci. 48 (2007), 1815–1823.
69. Laferla, F.M., Sugarman, M.C., Lane, T.E., Leissring, M.A., Regional hypomyelination and dysplasia in transgenic mice with astrocyte-directed expression of interferon-gamma. J. Mol. Neurosci. 15:1 (2000), 45–59.
70. Levison, S.W., Ducceschi, M.H., Young, G.M., Wood, T.L., Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp. Neurol. 141 (1996), 256–268.
71. Levison, S.W., Hudgins, S.N., Crawford, J.L., Ciliary neurotrophic factor stimulates nuclear hypertrophy and increases the GFAP content of cultured astrocytes. Brain Res. 803 (1998), 189–193.
72. Li, R., Messing, A., Goldman, J.E., Brenner, M., GFAP mutations in Alexander disease. Int. J. Dev. Neurosci. 20 (2002), 259–268.
73. Liberto, C.M., Albrecht, P.J., Herx, L.M., Yong, V.W., Levison, S.W., Pro-regenerative properties of cytokine-activated astrocytes. J. Neurochem. 89 (2004), 1092–1100.
74. Liedtke, W., Edelmann, W., Bieri, P.L., Chiu, F.C., Cowan, N.J., Kucherlapati, R., Raine, C.S., GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17 (1996), 607–615.
75. Lin, C.T., Xu, Y.F., Wu, J.Y., Chan, L., Immunoreactive apolipoprotein E is a widely distributed cellular protein. Immunohistochemical localization of apolipoprotein E in baboon tissues. J. Clin. Invest. 78 (1986), 947–958.
76. Lin, W., Kemper, A., Dupree, J.L., Harding, H.P., Ron, D., Popko, B., Interferon-gamma inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 129 (2006), 1306–1318.
77. Linker, R.A., Maurer, M., Gaupp, S., Martini, R., Holtmann, B., Giess, R., Rieckmann, P., Lassmann, H., Toyka, K.V., Sendtner, M., Gold, R., CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat. Med. 8 (2002), 620–624.
78. Liu, J.P., Tang, Y., Zhou, S., Toh, B.H., Mclean, C., Li, H., Cholesterol involvement in the pathogenesis of neurodegenerative diseases. Mol. Cell. Neurosci. 43 (2010), 33–42.
79. Lu, Z., Hu, X., Zhu, C., Wang, D., Zheng, X., Liu, Q., Overexpression of CNTF in mesenchymal stem cells reduces demyelination and induces clinical recovery in experimental autoimmune encephalomyelitis mice. J. Neuroimmunol. 206 (2009), 58–69.
80. Lutz, S.E., Zhao, Y., Gulinello, M., Lee, S.C., Raine, C.S., Brosnan, C.F., Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation. J. Neurosci. 29 (2009), 7743–7752.
81. Markoullis, K., Sargiannidou, I., Gardner, C., Hadjisavvas, A., Reynolds, R., Kleopa, K.A., Disruption of oligodendrocyte gap junctions in experimental autoimmune encephalomyelitis. Glia 60 (2012), 1053–1066.
82. May, P., Rohlmann, A., Bock, H.H., Zurhove, K., Marth, J.D., Schomburg, E.D., Noebels, J.L., Beffert, U., Sweatt, J.D., Weeber, E.J., Herz, J., Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice. Mol. Cell. Biol. 24 (2004), 8872–8883.
83. Mayer, M., Bhakoo, K., Noble, M., Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Dev. 120 (1994), 143–153.
84. Meeuwsen, S., Persoon-Deen, C., Bsibsi, M., Ravid, R., Van Noort, J.M., Cytokine, chemokine and growth factor gene profiling of cultured human astrocytes after exposure to proinflammatory stimuli. Glia 43 (2003), 243–253.
85. Mei, X., Ezan, P., Giaume, C., Koulakoff, A., Astroglial connexin immunoreactivity is specifically altered at β-amyloid plaques in β-amyloid precursor protein/presenilin1 mice. Neuroscience 171 (2010), 92–105.
86. Menichella, D.M., Goodenough, D.A., Sirkowski, E., Scherer, S.S., Paul, D.L., Connexins are critical for normal myelination in the CNS. J. Neurosci. 23 (2003), 5963–5973.
87. Mennerick, S., Benz, A., Zorumski, C.F., Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures. J. Neurosci. 16 (1996), 55–64.
88. Messersmith, D.J., Murtie, J.C., Le, T.Q., Frost, E.E., Armstrong, R.C., Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J. Neurosci. Res. 62 (2000), 241–256.
89. Miljkovic, D., Momcilovic, M., Stojanovic, I., Stosic-grujicic, S., Ramic, Z., Mostarica-stojkovic, M., Astrocytes stimulate interleukin-17 and interferon-gamma production in vitro. J. Neurosci. Res. 85 (2007), 3598–3606.
90. Moore, C.S., Abdullah, S.L., Brown, A., Areulpragasam, A., Crocker, S.J., How factors secreted from astrocytes impact myelin repair. J. Neurosci. Res. 89 (2011), 13–21.
91. Mothet, J.P., Parent, A.T., Wolosker, H., Brady, R.O. Jr., Linden, D.J., Ferris, C.D., Rogawski, M.A., Snyder, S.H., D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl. Acad. Sci. 97 (2000), 4926–4931.
92. Müller, E., Pathologische anatomie und pathogenese. Fisher G, (eds.) Die multiple Skleroze des Gehirns und Rückenmarks: Jena, 1904, 300–344.
93. Nagy, J.I., Li, W., Hertzberg, E.L., Marotta, C.A., Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer's disease. Brain Res. 717 (1996), 173–178.
94. Nash, B., Ioannidou, K., Barnett, S.C., Astrocyte phenotypes and their relationship to myelination. J. Anat. 219 (2011), 44–52.
95. Nash, B., Thomson, C.E., Linington, C., Arthur, A.T., McClure, J.D., McBride, M.W., Barnett, S.C., Functional duality of astrocytes in myelination. J. Neurosci. 31 (2011), 13028–13038.
96. Nielsen, S., Nagelhus, E.A., Amiry-Moghaddam, M., Bourque, C., Agre, P., Ottersen, O.P., Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17 (1997), 171–180.
97. Noble, M., Murray, K., Purified astrocytes promote the in vitro division of a bipotential glial progenitor cell. EMBO. J. 3 (1984), 2243–2247.
98. Noble, M., Murray, K., Stroobant, P., Waterfield, M.D., Riddle, P., Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333 (1988), 560–562.
99. Noble, M., Wolswijk, G., Wren, D., The complex relationship between cell division and the control of differentiation in oligodendrocyte-type-2 astrocyte progenitor cells isolated from perinatal and adult rat optic nerves. Prog. Growth Factor Res. 1 (1989), 179–194.
100. Odermatt, B., Wellershaus, K., Wallraff, A., Seifert, G., Degen, J., Euwens, C., Fuss, B., Büssow, H., Schilling, K., Steinhäuser, C., Willecke, K., Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J. Neurosci. 23 (2003), 4549–4559.
101. Okada, S., Nakamura, M., Katoh, H., Miyao, T., Shimazaki, T., Ishii, K., Yamane, J., Yoshimura, A., Iwamoto, Y., Toyama, Y., Okano, H., Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med. 12 (2006), 829–834.
102. Omari, K.M., John, G.R., Sealfon, S.C., Raine, C.S., CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis. Brain 128 (2005), 1003–1015.
103. Orth, M., Bellosta, S., Cholesterol: Its regulation and role in central nervous system disorders. Cholesterol, 2012, 292598.
104. Pannasch, U., Vargová, L., Reingruber, J., Ezan, P., Holcman, D., Giaume, C., Syková, E., Rouach, N., Astroglial networks scale synaptic activity and plasticity. Proc. Natl. Acad. Sci. 108 (2011), 8467–8472.
105. Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., Haydon, P.G., Glutamate-mediated astrocyte-neuron signalling. Nature 369 (1994), 744–747.
106. Pellegri, G., Rossier, C., Magistretti, P.J., Martin, J.L., Cloning, localization and induction of mouse brain glycogen synthase. Brain Res. Mol. Brain Res. 38 (1996), 191–199.
107. Pfeiffer-Guglielmi, B., Fleckenstein, B., Jung, G., Hamprecht, B., Immunocytochemical localization of glycogen phosphorylase isozymes in rat nervous tissues by using isozyme-specific antibodies. J. Neurochem. 85 (2003), 73–81.
108. Pfrieger, F.W., Ungerer, N., Cholesterol metabolism in neurons and astrocytes. Prog. Lipid Res. 50 (2011), 357–371.
109. Porter, J.T., Mccarthy, K.D., Astrocytic neurotransmitter receptors in situ and in vivo. Prog. Neurobiol. 51 (1997), 439–455.
110. Pringle, N., Collarini, E.J., Mosley, M.J., Heldin, C.H., Westermark, B., Richardson, W.D., PDGF A chain homodimers drive proliferation of bipotential (O-2A) glial progenitor cells in the developing rat optic nerve. EMBO. J. 8 (1989), 1049–1056.
111. Pulver, M., Carrel, S., Mach, J.P., De Tribolet, N., Cultured human fetal astrocytes can be induced by interferon-gamma to express HLA-DR. J. Neuroimmunol. 14 (1987), 123–133.
112. Raff, M.C., Miller, R.H., Noble, M., A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303 (1983), 390–396.
113. Raff, M.C., Lillien, L.E., Richardson, W.D., Burne, J.F., Noble, M.D., Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature 333 (1988), 562–565.
114. Ransohoff, R.M., Hamilton, T.A., Tani, M., Stoler, M.H., Shick, H.E., Major, J.A., Estes, M.L., Thomas, D.M., Tuohy, V.K., Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J. 7 (1993), 592–600.
115. Rash, J.E., Yasumura, T., Hudson, C.S., Agre, P., Nielsen, S., Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc. Natl. Acad. Sci. 95 (1998), 11981–11986.
116. Redwine, J.M., Armstrong, R.C., In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J. Neurobiol. 37 (1998), 413–428.
117. Redwine, J.M., Blinder, K.L., Armstrong, R.C., In situ expression of fibroblast growth factor receptors by oligodendrocyte progenitors and oligodendrocytes in adult mouse central nervous system. J. Neurosci. Res. 50 (1997), 229–237.
118. Rinholm, J.E., Bergersen, L.H., Neuroscience: the wrap that feeds neurons. Nature 487 (2012), 435–436.
119. Rinholm, J.E., Hamilton, N.B., Kessaris, N., Richardson, W.D., Bergersen, L.H., Attwell, D., Regulation of oligodendrocyte development and myelination by glucose and lactate. J. Neurosci. 31 (2011), 538–548.
120. Rouach, N., Koulakoff, A., Abudara, V., Willecke, K., Giaume, C., Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322 (2008), 1551–1555.
121. Rudge, J.S., Pasnikowski, E.M., Holst, P., Lindsay, R.M., Changes in neurotrophic factor expression and receptor activation following exposure of hippocampal neuron/astrocyte cocultures to kainic acid. J. Neurosci. 15 (1995), 6856–6867.
122. Salehi, Z., Hadiyan, S.P., Navidi, R., Ciliary neurotrophic factor role in myelin oligodendrocyte glycoprotein expression in cuprizone-induced multiple sclerosis mice. Cell. Mol. Neurobiol. 33 (2013), 531–535.
123. Sánchez-Abarca, L.I., Tabernero, A., Medina, J.M., Oligodendrocytes use lactate as a source of energy and as a precursor of lipids. Glia 36 (2001), 321–329.
124. Schafer, D.P., Lehrman, E.K., Stevens, B., The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61 (2013), 24–36.
125. Schulz, K., Kroner, A., David, S., Iron efflux from astrocytes plays a role in remyelination., 32, 2012, 4841–4847.
126. Schwartz, J.P., Nishiyama, N., Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res. Bull. 35 (1994), 403–407.
127. Selmaj, K., Raine, C.S., Tumor necrosis factor mediates myelin damage in organotypic cultures of nervous tissue. Ann. N. Y. Acad. Sci. 540 (1988), 568–570.
128. Selmaj, K., Raine, C.S., Cannella, B., Brosnan, C.F., Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest. 87 (1991), 949–954.
129. Siegel, G.J., Agranoff, B.W., Albers, R.W., Fisher, S.K., Uhler, M.D., Basic Neurochemistry: Molecular, Cellular and Medical Aspects. sixth ed, 1999, Lippincott-Raven, Philadelphia, 1999.
130. Silberstein, F.C., De Simone, R., Levi, G., Aloisi, F., Cytokine-regulated expression of platelet-derived growth factor gene and protein in cultured human astrocytes. J. Neurochem. 66 (1996), 1409–1417.
131. Sofroniew, M.V., Vinters, H.V., Astrocytes: biology and pathology. Acta Neuropathol. 11 (2010), 7–35.
132. Solenov, E., Watanabe, H., Manley, G.T., Verkman, A.S., Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am. J. Physiol, Cell Physiol. 286 (2004), C426–C432.
133. Stankoff, B., Aigrot, M.S., Noël, F., Wattilliaux, A., Zalc, B., Lubetzki, C., Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules. J. Neurosci. 22 (2002), 9221–9227.
134. Steinhäuser, C., Jabs, R., Kettenmann, H., Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice. Hippocampus 4 (1994), 19–35.
135. Stöckli, K.A., Lillien, L.E., Näher-Noé, M., Breitfeld, G., Hughes, R.A., Raff, M.C., Thoenen, H., Sendtner, M., Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J. Cell Biol. 115 (1991), 447–459.
136. Swanson, R.A., Ying, W., Kauppinen, T.M., Astrocyte influences on ischemic neuronal death. Curr. Mol. Med. 4 (2004), 193–205.
137. Tekkök, S.B., Brown, A.M., Westenbroek, R., Pellerin, L., Ransom, B.R., Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J. Neurosci. Res. 81 (2005), 644–652.
138. Traugott, U., Lebon, P., Interferon-gamma and Ia antigen are present on astrocytes in active chronic multiple sclerosis lesions. J. Neurol. Sci. 84 (1988), 257–264.
139. Tremblay, M.È., Lowery, R.L., Majewska, A.K., Microglial interactions with synapses are modulated by visual experience. PLoS Biol., 8(11), 2010, e1000527.
140. Tress, O., Maglione, M., May, D., Pivneva, T., Richter, N., Seyfarth, J., Binder, S., Zlomuzica, A., Seifert, G., Theis, M., Dere, E., Kettenmann, H., Willecke, K., Panglial gap junctional communication is essential for maintenance of myelin in the CNS. J. Neurosci. 32 (2012), 7499–74518.
141. Tsukada, N., Miyagi, K., Matsuda, M., Yanagisawa, N., Yone, K., Tumor necrosis factor and interleukin-1 in the CSF and sera of patients with multiple sclerosis. J. Neurol. Sci. 104 (1991), 230–234.
142. Uchida, K., Baba, H., Maezawa, Y., Furukawa, S., Furusawa, N., Imura, S., Histological investigation of spinal cord lesions in the spinal hyperostotic mouse (twy/twy): morphological changes in anterior horn cells and immunoreactivity to neurotropic factors. J. Neurol. 245 (1998), 781–793.
143. Ullian, E.M., Sapperstein, S.K., Christopherson, K.S., Barres, B.A., Control of synapse number by glia. Science 291 (2001), 657–661.
144. Vana, A.C., Flint, N.C., Harwood, N.E., Le, T.Q., Fruttiger, M., Armstrong, R.C., Platelet-derived growth factor promotes repair of chronically demyelinated white matter. J. Neuropathol. Exp. Neurol. 66 (2007), 975–988.
145. Vernerey, J., Macchi, M., Magalon, K., Cayre, M., Durbec, P., Ciliary neurotrophic factor controls progenitor migration during remyelination in the adult rodent brain. J. Neurosci. 33 (2013), 3240–3250.
146. Villarroya, H., Violleau, K., Ben Younes-Chennoufi, A., Baumann N. Myelin-induced experimental allergic encephalomyelitis in Lewis rats: tumor necrosis factor alpha levels in serum and cerebrospinal fluid immunohistochemical expression in glial cells and macrophages of optic nerve and spinal cord. J. Neuroimmunol. 64 (1996), 55–61.
147. Voskuhl, R.R., Peterson, S., Song, B., Ao, Y., Morales, L.B.R., Tiwari-Eoodruff, S., Sofroniew, M.V., Reactive astrocytes form scar-like perivascular barriers to leukocytes during adoptive immune inflammation of the CNS. J. Neurosci. 29 (2009), 11511–11522.
148. Wallraff, A., Köhling, R., Heinemann, U., Theis, M., Willecke, K., Steinhäuser, C., The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 26 (2006), 5438–5447.
149. Watkins, T.A., Emery, B., Mulinyawe, S., Barres, B.A., Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 60 (2008), 555–569.
150. Webster, H.D., Shii, H., Lassmann, H., Immunocytochemical study of myelin-associated glycoprotein (MAG), basic protein (BP), and glial fibrillary acidic protein (GFAP) in chronic relapsing experimental allergic encephalomyelitis (EAE). Acta Neuropathol. 65 (1985), 177–189.
151. Williams, A., Piaton, G., Lubetzki, C., Astrocytes—friends or foes in multiple sclerosis?. Glia 55 (2007), 1300–1312.
152. Winter, C.G., Saotome, Y., Levison, S.W., Hirsh, D., A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc. Natl. Acad. Sci. 92 (1995), 5865–5869.
153. Woodruff, R.H., Fruttiger, M., Richardson, W.D., Franklin, R.J., Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol. Cell. Neurosci. 25 (2004), 252–262.
154. Wu, Y., Dissing-Olesen, L., MacVicar, B.A., Stevens, B., Microglia: dynamic mediators of synapse development and plasticity. Trends Immunol. 36 (2015), 605–613.
155. Xu, Q., Bernardo, A., Walker, D., Kanegawa, T., Mahley, R.W., Huang, Y., Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. J. Neurosci. 26 (2006), 4985–4994.
156. Yamamuro, A., Ago, Y., Takuma, K., Maeda, S., Sakai, Y., Baba, A., Matsuda, T., Possible involvement of astrocytes in neuroprotection by the cognitive enhancer T-588. Neurochem. Res. 28 (2003), 1779–1783.
157. Yong, V.W., Moumdjian, R., Yong, F.P., Ruijs, T.C., Freedman, M.S., Cashman, N., Antel, J.P., Gamma-interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo. Proc. Natl. Acad. Sci. U.S.A. 88 (1991), 7016–:7020.
158. Yoshida, M., Saito, H., Katsuki, H., Neurotrophic effects of conditioned media of astrocytes isolated from different brain regions on hippocampal and cortical neurons. Experientia 51 (1995), 133–136.
159. Zamanian, J.L., Xu, L., Foo, L.C., Nouri, N., Zhou, L., Giffard, R.G., Barres, B.A., Genomic analysis of reactive astrogliosis. J. Neurosci. 32 (2012), 6391–6410.
160. Zhu, Z.H., Yang, R., Fu, X., Wang, Y.Q., Wu, G.C. 2006. Astrocyte-conditioned medium protecting hippocampal neurons in primary cultures against corticosterone-induced damages via PI3-K/Akt signal pathway. Brain Res. 1114, 1–10.