Astrocytes differentially respond to inflammatory autoimmune insults and imbalances of neural activity

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Jukkola, Peter ^a   Guerrero, Tomas ^b   Gray, Victoria ^a   Gu, Chen ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Ankyrin G; Astrocytic endfeet; Experimental autoimmune encephalomyelitis; Neurovascular coupling; Voltage gated potassium (Kv) channel; Water channel

Indexed keywords

ANK3 PROTEIN, MOUSE; ANKYRIN; AQP4 PROTEIN, MOUSE; AQUAPORIN 4; BACTERIAL PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; KCNC1 PROTEIN, MOUSE; PHOTOPROTEIN; SHAW POTASSIUM CHANNEL; VIMENTIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CHRONIC DISEASE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MYELIN SHEATH; NERVE CELL; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX; SPINAL CORD; TRANSGENIC MOUSE;

ANIMALS; ANKYRINS; AQUAPORIN 4; ASTROCYTES; BACTERIAL PROTEINS; BRAIN; CHRONIC DISEASE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; LUMINESCENT PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELIN SHEATH; NEURONS; SEVERITY OF ILLNESS INDEX; SHAW POTASSIUM CHANNELS; SPINAL CORD; VIMENTIN;

EID: 85005766538     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/20515960170     Document Type: Article

References (94)

1. Zlokovic BV: The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008,57(2):178-201. 10.1016/j.neuron.2008.01.003
2. Quaegebeur A, Lange C, Carmeliet P: The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 2011,71(3):406-424. 10.1016/j.neuron.2011.07.013
3. Ransohoff RM, Brown MA: Innate immunity in the central nervous system. J Clin Invest 2012,122(4):1164-1171. 10.1172/JCI58644
4. Nedergaard M, Ransom B, Goldman SA: New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 2003,26(10):523-530. 10.1016/j.tins.2003.08.008
5. Eroglu C, Barres BA: Regulation of synaptic connectivity by glia. Nature 2010,468(7321):223-231. 10.1038/nature09612
6. Sorensen A, et al.: Astrocytes, but not olfactory ensheathing cells or Schwann cells, promote myelination of CNS axons in vitro. Glia 2008,56(7):750-763. 10.1002/glia.20650
7. Nash B, et al.: Functional duality of astrocytes in myelination. J Neurosci 2011,31(37):13028-13038. 10.1523/JNEUROSCI.1449-11.2011
8. Petzold GC, Murthy VN: Role of astrocytes in neurovascular coupling. Neuron 2011,71(5):782-797. 10.1016/j.neuron.2011.08.009
9. Barres BA: The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 2008,60(3):430-440. 10.1016/j.neuron.2008.10.013
10. Dunn KM, Nelson MT: Potassium channels and neurovascular coupling. Circ J 2010,74(4):608-616. 10.1253/circj.CJ-10-0174
11. Lucchinetti CF, et al.: Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 2011,365(23):2188-2197. 10.1056/NEJMoa1100648
12. Brosnan CR, Raine CS: The astrocyte in multiple sclerosis revisited. Glia 2013, 61: 453-465. 10.1002/glia.22443
13. King IL, Dickendesher TL, Segal BM: Circulating Ly-6C+myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009,113(14):3190-3197. 10.1182/blood-2008-07-168575
14. Young NP, et al.: Perivenous demyelination: association with clinically defined acute disseminated encephalomyelitis and comparison with pathologically confirmed multiple sclerosis. Brain 2010,133(Pt 2):333-348.
15. Eng LF, et al.: An acidic protein isolated from fibrous astrocytes. Brain Res 1971,28(2):351-354. 10.1016/0006-8993(71)90668-8
16. Lennon VA, et al.: A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004,364(9451):2106-2112. 10.1016/S0140-6736(04)17551-X
17. Hinson SR, et al.: Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci USA 2012,109(4):1245-1250. 10.1073/pnas.1109980108
18. Waters P, Vincent A: Detection of anti-aquaporin-4 antibodies in neuromyelitis optica: current status of the assays. Int Ms J 2008,15(3):99-105.
19. Barnett MH, Sutton I: Neuromyelitis optica: not a multiple sclerosis variant. Curr Opin Neurol 2012,25(3):215-220. 10.1097/WCO.0b013e3283533a3f
20. Jarius S, Wildemann B: AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat Rev Neurol 2010,6(7):383-392. 10.1038/nrneurol.2010.72
21. Higashimori H, Sontheimer H: Role of Kir4.1 channels in growth control of glia. GLIA 2007,55(16):1668-1679. 10.1002/glia.20574
22. Stephan J, et al.: Kir4.1 channels mediate a depolarization of hippocampal astrocytes under hyperammonemic conditions in situ. GLIA 2012,60(6):965-978. 10.1002/glia.22328
23. Bay V, Butt AM: Relationship between glial potassium regulation and axon excitability: a role for glial Kir4.1 channels. GLIA 2012,60(4):651-660. 10.1002/glia.22299
24. Srivastava R, et al.: Potassium channel KIR4.1 as an immune target in multiple sclerosis. N Engl J Med 2012,367(2):115-123. 10.1056/NEJMoa1110740
25. Jukkola PI, et al.: K+ channel alterations in the progression of experimental autoimmune encephalomyelitis. Neurobiol Dis 2012,47(2):280-293. 10.1016/j.nbd.2012.04.012
26. Ishibashi T, et al.: Astrocytes promote myelination in response to electrical impulses. Neuron 2006,49(6):823-832. 10.1016/j.neuron.2006.02.006
27. Watkins TA, et al.: Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 2008,60(4):555-569. 10.1016/j.neuron.2008.09.011
28. Schipke CG, Kettenmann H: Astrocyte responses to neuronal activity. Glia 2004,47(3):226-232. 10.1002/glia.20029
29. Binder DK, Steinhauser C: Functional changes in astroglial cells in epilepsy. Glia 2006,54(5):358-368. 10.1002/glia.20394
30. Eid T, et al.: Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats. Brain 2008,131(Pt 8):2061-2070.
31. Eid T, et al.: Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 2004,363(9402):28-37. 10.1016/S0140-6736(03)15166-5
32. Alvestad S, et al.: Mislocalization of AQP4 precedes chronic seizures in the kainate model of temporal lobe epilepsy. Epilepsy Res 2013,105(1-2):30-41.
33. Custer SK, et al.: Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nat Neurosci 2006,9(10):1302-1311. 10.1038/nn1750
34. Gu C, Gu Y: Clustering and activity tuning of kv1 channels in myelinated hippocampal axons. J Biol Chem 2011,286(29):25835-25847. 10.1074/jbc.M111.219113
35. Gu Y, Gu C: Dynamics of Kv1 channel transport in axons. PLoS One 2010,5(8):e11931. 10.1371/journal.pone.0011931
36. Jenkins SM, Bennett V: Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 2001,155(5):739-746. 10.1083/jcb.200109026
37. Ho CS, Grange RW, Joho RH: Pleiotropic effects of a disrupted K+channel gene: reduced body weight, impaired motor skill and muscle contraction, but no seizures. Proc Natl Acad Sci USA 1997,94(4):1533-1538. 10.1073/pnas.94.4.1533
38. Hurlock EC, et al.: Rescue of motor coordination by Purkinje cell-targeted restoration of Kv3.3 channels in Kcnc3-null mice requires Kcnc1. J Neurosci 2009,29(50):15735-15744. 10.1523/JNEUROSCI.4048-09.2009
39. Sanchez JA, et al.: Muscle and motor-skill dysfunction in a K+channel-deficient mouse are not due to altered muscle excitability or fiber type but depend on the genetic background. Pflugers Arch 2000,440(1):34-41.
40. Bignami A, Raju T, Dahl D: Localization of vimentin, the nonspecific intermediate filament protein, in embryonal glia and in early differentiating neurons. In vivo and in vitro immunofluorescence study of the rat embryo with vimentin and neurofilament antisera. Dev Biol 1982,91(2):286-295. 10.1016/0012-1606(82)90035-5
41. Lazarides E: Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins. Annu Rev Biochem 1982, 51: 219-250. 10.1146/annurev.bi.51.070182.001251
42. Eriksson JE, et al.: Introducing intermediate filaments: from discovery to disease. J Clin Invest 2009,119(7):1763-1771. 10.1172/JCI38339
43. Stuart G, Schiller J, Sakmann B: Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol 1997,505(Pt 3):617-632.
44. Clark BD, Goldberg EM, Rudy B: Electrogenic tuning of the axon initial segment. Neuroscientist 2009,15(6):651-668. 10.1177/1073858409341973
45. Zhou L, et al.: Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: role of potassium channels under the myelin sheath in young nerves. J Neurosci 1998,18(18):7200-7215.
46. Salzer JL: Polarized domains of myelinated axons. Neuron 2003,40(2):297-318. 10.1016/S0896-6273(03)00628-7
47. Bennett V, Baines AJ: Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 2001,81(3):1353-1392.
48. Pan Z, et al.: A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 2006,26(10):2599-2613. 10.1523/JNEUROSCI.4314-05.2006
49. Song AH, et al.: A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009,136(6):1148-1160. 10.1016/j.cell.2009.01.016
50. Sobotzik JM, et al.: AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc Natl Acad Sci USA 2009,106(41):17564-17569. 10.1073/pnas.0909267106
51. Rudy B, McBain CJ: Kv3 channels: voltage-gated K + channels designed for high-frequency repetitive firing. Trends Neurosci 2001,24(9):517-526. 10.1016/S0166-2236(00)01892-0
52. Jonas P, et al.: Interneuron Diversity series: Fast in, fast out-temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci 2004,27(1):30-40. 10.1016/j.tins.2003.10.010
53. Gu C, Barry J: Function and mechanism of axonal targeting of voltage-sensitive potassium channels. Prog Neurobiol 2011,94(2):115-132. 10.1016/j.pneurobio.2011.04.009
54. Coetzee WA, et al.: Molecular diversity of K + channels. Ann N Y Acad Sci 1999, 868: 233-285. 10.1111/j.1749-6632.1999.tb11293.x
55. Gu Y, et al.: Alternative splicing regulates Kv3.1 polarized targeting to adjust the maximal spiking frequency. J Biol Chem 2012, 287: 1755-1769. 10.1074/jbc.M111.299305
56. Gu Y, Barry J, Gu C: Kv3 channel assembly, trafficking and activity are regulated by zinc through different binding sites. J Physiol 2013, 591: 2475-2490.
57. Xu M, et al.: The axon-dendrite targeting of Kv3 (Shaw) channels is determined by a targeting motif that associates with the T1 domain and ankyrin G. J Neurosci 2007,27(51):14158-14170. 10.1523/JNEUROSCI.3675-07.2007
58. Xu M, et al.: Kinesin I transports tetramerized Kv3 channels through the axon initial segment via direct binding. J Neurosci 2010,30(47):15987-16001. 10.1523/JNEUROSCI.3565-10.2010
59. Barry J, Xu M, Gu Y, Dangel A, Jukkola P, Shrestha C, Gu C: Activation of conventional kinesin motors in clusters by Shaw voltage-gated K + channels. J Cell Sci 2013, 126: 2027-2041. 10.1242/jcs.122234
60. Zagha E, Lang EJ, Rudy B: Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform. J Neurosci 2008,28(6):1291-1300. 10.1523/JNEUROSCI.4358-07.2008
61. Hurlock EC, McMahon A, Joho RH: Purkinje-cell-restricted restoration of Kv3.3 function restores complex spikes and rescues motor coordination in Kcnc3 mutants. J Neurosci 2008,28(18):4640-4648. 10.1523/JNEUROSCI.5486-07.2008
62. Devaux J, et al.: Kv3.1b is a novel component of CNS nodes. J Neurosci 2003,23(11):4509-4518.
63. Wu X, et al.: Upregulation of astrocytic leptin receptor in mice with experimental autoimmune encephalomyelitis. J Mol Neurosci 2012,49(3):446-456.
64. Kurkowska-Jastrzebska I, et al.: Neurodegeneration and inflammation in hippocampus in experimental autoimmune encephalomyelitis induced in rats by one - Time administration of encephalitogenic T cells. Neuroscience 2013, 248: 690-698.
65. Ziehn MO, et al.: Hippocampal CA1 atrophy and synaptic loss during experimental autoimmune encephalomyelitis. EAE. Lab Invest 2010,90(5):774-786. 10.1038/labinvest.2010.6
66. Ziehn MO, et al.: Therapeutic testosterone administration preserves excitatory synaptic transmission in the hippocampus during autoimmune demyelinating disease. J Neurosci 2012,32(36):12312-12324. 10.1523/JNEUROSCI.2796-12.2012
67. Ziehn MO, et al.: Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease. Lab Invest 2012,92(8):1234-1245. 10.1038/labinvest.2012.76
68. Bardehle S, et al.: Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci 2013,16(5):580-586. 10.1038/nn.3371
69. Popko B, et al.: The effects of interferon-gamma on the central nervous system. Mol Neurobiol 1997,14(1-2):19-35.
70. Yong VW, et al.: Gamma-interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo. Proc Natl Acad Sci USA 1991,88(16):7016-7020. 10.1073/pnas.88.16.7016
71. Iliff JJ, et al.: A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 2012,4(147):147ra111. 10.1126/scitranslmed.3003748
72. Chan KH, et al.: Aquaporin-4 autoantibodies cause asymptomatic aquaporin-4 loss and activate astrocytes in mouse. J Neuroimmunol 2012,245(1-2):32-38.
73. Kim JE, et al.: Astroglial loss and edema formation in the rat piriform cortex and hippocampus following pilocarpine-induced status epilepticus. J Comp Neurol 2010,518(22):4612-4628. 10.1002/cne.22482
74. Miyamoto K, et al.: Upregulation of water channel aquaporin-4 in experimental autoimmune encephalomyeritis. J Neurol Sci 2009,276(1-2):103-107.
75. Sinclair C, et al.: Absence of aquaporin-4 expression in lesions of neuromyelitis optica but increased expression in multiple sclerosis lesions and normal-appearing white matter. Acta Neuropathol 2007,113(2):187-194. 10.1007/s00401-006-0169-2
76. Bennett JL, et al.: Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol 2009,66(5):617-629. 10.1002/ana.21802
77. Kinoshita M, Nakatsuji Y: Where do AQP4 antibodies fit in the pathogenesis of NMO?. Multiple Sclerosis International; 2012:862169. doi:10.1155/2012/862169
78. Misu T, et al.: Loss of aquaporin 4 in lesions of neuromyelitis optica: distinction from multiple sclerosis. Brain 2007,130(Pt 5):1224-1234.
79. Matthews L, et al.: Distinction of seropositive NMO spectrum disorder and MS brain lesion distribution. Neurology 2013,80(14):1330-1337. 10.1212/WNL.0b013e3182887957
80. Bukhari W, et al.: Molecular pathogenesis of neuromyelitis optica. Int J Mol Sci 2012,13(10):12970-12993.
81. Marignier R, et al.:Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury. Brain 2010,133(9):2578-2591. 10.1093/brain/awq177
82. Tomizawa Y, et al.: Blood-brain barrier disruption is more severe in neuromyelitis optica than in multiple sclerosis and correlates with clinical disability. J Int Med Res 2012,40(4):1483-1491. 10.1177/147323001204000427
83. Saadoun S, et al.: T cell deficiency does not reduce lesions in mice produced by intracerebral injection of NMO-IgG and complement. J Neuroimmunol 2011,235(1-2):27-32.
84. Li L, et al.: Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. Faseb J 2011,25(5):1556-1566. 10.1096/fj.10-177279
85. Li L, Zhang H, Verkman AS: Greatly attenuated experimental autoimmune encephalomyelitis in aquaporin-4 knockout mice. BMC Neurosci 2009, 10: 94. 10.1186/1471-2202-10-94
86. Kimura A, et al.: Protective role of aquaporin-4 water channels after contusion spinal cord injury. Ann Neurol 2010,67(6):794-801.
87. Sofroniew MV, Vinters HV: Astrocytes: biology and pathology. Acta Neuropathol 2010,119(1):7-35. 10.1007/s00401-009-0619-8
88. Charles AC, et al.: Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 1991,6(6):983-992. 10.1016/0896-6273(91)90238-U
89. Cornell-Bell AH, et al.: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 1990,247(4941):470-473. 10.1126/science.1967852
90. Shigetomi E, et al.: Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J Neurosci 2008,28(26):6659-6663. 10.1523/JNEUROSCI.1717-08.2008
91. Halassa MM, Fellin T, Haydon PG: The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 2007,13(2):54-63. 10.1016/j.molmed.2006.12.005
92. Perea G, Navarrete M, Araque A: Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 2009,32(8):421-431. 10.1016/j.tins.2009.05.001
93. Volterra A, Meldolesi J: Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 2005,6(8):626-640. 10.1038/nrn1722
94. Moore CS, et al.: How factors secreted from astrocytes impact myelin repair. J Neurosci Res 2011,89(1):13-21. 10.1002/jnr.22482