Functional polarization of neuroglia: Implications in neuroinflammation and neurological disorders

Biochemical Pharmacology

Volumn 103, Issue , 2016, Pages 1-16

  Jha, Mithilesh Kumar ^a   Lee, Won Ha ^b   Suk, Kyoungho ^a  

^a Kyungpook National University School of Medicine   (South Korea)

^b Kyungpook National University   (South Korea)

Author keywords

Central nervous system; Functional polarization; Neuroglia; Neuroinflammation; Neurological disorders

Indexed keywords

AGING; ASTROCYTE; BRAIN ISCHEMIA; CENTRAL NERVOUS SYSTEM DISEASE; DEGENERATIVE DISEASE; DEMYELINATING DISEASE; GLIA; GLIA CELL; GLIOMA; HUMAN; INJURY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NEUROPATHIC PAIN; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; ANIMAL; CELL POLARITY; CENTRAL NERVOUS SYSTEM; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL POLARITY; CENTRAL NERVOUS SYSTEM; HUMANS; INFLAMMATION; NERVOUS SYSTEM DISEASES; NEUROGLIA;

EID: 84958970061     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.11.003     Document Type: Review

References (242)

1. D.N. Xanthos, and J. Sandkuhler Neurogenic neuroinflammation: inflammatory CNS reactions in response to neuronal activity Nat. Rev. Neurosci. 15 2014 43 53
2. B.S. Mietto, K. Mostacada, and A.M. Martinez Neurotrauma and inflammation: CNS and PNS responses Mediat. Inflamm. 2015 2015 251204
3. X. Hu, R.K. Leak, Y. Shi, J. Suenaga, Y. Gao, P. Zheng, and et al. Microglial and macrophage polarization - new prospects for brain repair Nat. Rev. Neurol. 11 2015 56 64
4. P.J. Murray, J.E. Allen, S.K. Biswas, E.A. Fisher, D.W. Gilroy, S. Goerdt, and et al. Macrophage activation and polarization: nomenclature and experimental guidelines Immunity 41 2014 14 20
5. C. Porta, M. Rimoldi, G. Raes, L. Brys, P. Ghezzi, D. Di Liberto, and et al. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB Proc. Natl. Acad. Sci. U. S. A. 106 2009 14978 14983
6. J.D. Cherry, J.A. Olschowka, and M.K. O'Banion Neuroinflammation and M2 microglia: the good, the bad, and the inflamed J. Neuroinflamm. 11 2014 98
7. A. Lampron, A. Elali, and S. Rivest Innate immunity in the CNS: redefining the relationship between the CNS and Its environment Neuron 78 2013 214 232
8. M.A. Ajmone-Cat, M. Mancini, R. De Simone, P. Cilli, and L. Minghetti Microglial polarization and plasticity: evidence from organotypic hippocampal slice cultures Glia 61 2013 1698 1711
9. S. David, and A. Kroner Repertoire of microglial and macrophage responses after spinal cord injury Nat. Rev. Neurosci. 12 2011 388 399
10. J. MacMicking, Q.W. Xie, and C. Nathan Nitric oxide and macrophage function Annu. Rev. Immunol. 15 1997 323 350
11. O. Bagasra, F.H. Michaels, Y.M. Zheng, L.E. Bobroski, S.V. Spitsin, Z.F. Fu, and et al. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis Proc. Natl. Acad. Sci. U. S. A. 92 1995 12041 12045
12. V. Chhor, T. Le Charpentier, S. Lebon, M.V. Ore, I.L. Celador, J. Josserand, and et al. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro Brain Behav. Immun. 32 2013 70 85
13. A. Sica, and V. Bronte Altered macrophage differentiation and immune dysfunction in tumor development J. Clin. Investig. 117 2007 1155 1166
14. A. Varin, and S. Gordon Alternative activation of macrophages: immune function and cellular biology Immunobiology 214 2009 630 641
15. D. Davalos, J. Grutzendler, G. Yang, J.V. Kim, Y. Zuo, S. Jung, and et al. ATP mediates rapid microglial response to local brain injury in vivo Nat. Neurosci. 8 2005 752 758
16. M.W. Salter, and S. Beggs Sublime microglia: expanding roles for the guardians of the CNS Cell 158 2014 15 24
17. R.M. Ransohoff, and A.E. Cardona The myeloid cells of the central nervous system parenchyma Nature 468 2010 253 262
18. R.M. Ransohoff, and M.A. Brown Innate immunity in the central nervous system J. Clin. Investig. 122 2012 1164 1171
19. H.K. Kimelberg, and M. Nedergaard Functions of astrocytes and their potential as therapeutic targets Neurotherapeutics 7 2010 338 353
20. M.K. Jha, S. Lee, D.H. Park, H. Kook, K.G. Park, I.K. Lee, and et al. Diverse functional roles of lipocalin-2 in the central nervous system Neurosci. Biobehav. Rev. 49 2015 135 156
21. E. Jang, J.H. Kim, S. Lee, J.W. Seo, M. Jin, M.G. Lee, and et al. Phenotypic polarization of activated astrocytes: the critical role of lipocalin-2 in the classical inflammatory activation of astrocytes J. Immunol. 191 2013 5204 5219
22. C. Brifault, M. Gras, D. Liot, V. May, D. Vaudry, and O. Wurtz Delayed pituitary adenylate cyclase-activating polypeptide delivery after brain stroke improves functional recovery by inducing m2 microglia/macrophage polarization Stroke 46 2015 520 528
23. M. Delgado, and D. Ganea Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit nuclear factor-kappa B-dependent gene activation at multiple levels in the human monocytic cell line THP-1 J. Biol. Chem. 276 2001 369 380
24. D. Ruffell, F. Mourkioti, A. Gambardella, P. Kirstetter, R.G. Lopez, N. Rosenthal, and et al. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair Proc. Natl. Acad. Sci. U. S. A. 106 2009 17475 17480
25. H. Xu, J. Zhu, S. Smith, J. Foldi, B. Zhao, A.Y. Chung, and et al. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization Nat. Immunol. 13 2012 642 650
26. T. Tanaka, K. Murakami, Y. Bando, and S. Yoshida Interferon regulatory factor 7 participates in the M1-like microglial polarization switch Glia 63 2015 595 610
27. M. Salem, J.T. Mony, M. Lobner, R. Khorooshi, and T. Owens Interferon regulatory factor-7 modulates experimental autoimmune encephalomyelitis in mice J. Neuroinflamm. 8 2011 181
28. T. Satoh, O. Takeuchi, A. Vandenbon, K. Yasuda, Y. Tanaka, Y. Kumagai, and et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection Nat. Immunol. 11 2010 936 944
29. T. Krausgruber, K. Blazek, T. Smallie, S. Alzabin, H. Lockstone, N. Sahgal, and et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses Nat. Immunol. 12 2011 231 238
30. M. Horiuchi, K. Wakayama, A. Itoh, K. Kawai, D. Pleasure, K. Ozato, and et al. Interferon regulatory factor 8/interferon consensus sequence binding protein is a critical transcription factor for the physiological phenotype of microglia J. Neuroinflamm. 9 2012 227
31. T. Masuda, M. Tsuda, R. Yoshinaga, H. Tozaki-Saitoh, K. Ozato, T. Tamura, and et al. IRF8 is a critical transcription factor for transforming microglia into a reactive phenotype Cell Rep. 1 2012 334 340
32. J.W. Graff, A.M. Dickson, G. Clay, A.P. McCaffrey, and M.E. Wilson Identifying functional microRNAs in macrophages with polarized phenotypes J. Biol. Chem. 287 2012 21816 21825
33. E.D. Ponomarev, T. Veremeyko, and H.L. Weiner MicroRNAs are universal regulators of differentiation, activation, and polarization of microglia and macrophages in normal and diseased CNS Glia 61 2013 91 103
34. X. Cai, Y. Yin, N. Li, D. Zhu, J. Zhang, C.Y. Zhang, and et al. Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155 J. Mol. Cell Biol. 4 2012 341 343
35. C.S. Moore, V.T. Rao, B.A. Durafourt, B.J. Bedell, S.K. Ludwin, A. Bar-Or, and et al. miR-155 as a multiple sclerosis-relevant regulator of myeloid cell polarization Ann. Neurol. 74 2013 709 720
36. E.D. Ponomarev, T. Veremeyko, N. Barteneva, A.M. Krichevsky, and H.L. Weiner MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway Nat. Med. 17 2011 64 70
37. X. Wang, Q. Liu, A. Ihsan, L. Huang, M. Dai, H. Hao, and et al. JAK/STAT pathway plays a critical role in the proinflammatory gene expression and apoptosis of RAW264.7 cells induced by trichothecenes as DON and T-2 toxin Toxicol. Sci. 127 2012 412 424
38. P. Przanowski, M. Dabrowski, A. Ellert-Miklaszewska, M. Kloss, J. Mieczkowski, B. Kaza, and et al. The signal transducers Stat1 and Stat3 and their novel target Jmjd3 drive the expression of inflammatory genes in microglia J. Mol. Med. (Berl.) 92 2014 239 254
39. Z. Yu, D. Sun, J. Feng, W. Tan, X. Fang, M. Zhao, and et al. MSX3 switches microglia polarization and protects from inflammation-induced demyelination J. Neurosci. 35 2015 6350 6365
40. E. Jang, S. Lee, J.H. Kim, J.W. Seo, W.H. Lee, K. Mori, and et al. Secreted protein lipocalin-2 promotes microglial M1 polarization FASEB J. 27 2013 1176 1190
41. L.L. Lanier DAP10- and DAP12-associated receptors in innate immunity Immunol. Rev. 227 2009 150 160
42. M. Kobayashi, H. Konishi, T. Takai, and H. Kiyama A DAP12-dependent signal promotes pro-inflammatory polarization in microglia following nerve injury and exacerbates degeneration of injured neurons Glia 63 2015 1073 1082
43. T.R. Jay, C.M. Miller, P.J. Cheng, L.C. Graham, S. Bemiller, M.L. Broihier, and et al. TREM2 deficiency eliminates TREM2+ inflammatory macrophages and ameliorates pathology in Alzheimer's disease mouse models J. Exp. Med. 212 2015 287 295
44. L. Zhong, X.F. Chen, Z.L. Zhang, Z. Wang, X.Z. Shi, K. Xu, and et al. DAP12 stabilizes the C-terminal fragment of the triggering receptor expressed on myeloid cells-2 (TREM2) and protects against LPS-induced pro-inflammatory response J. Biol. Chem. 290 2015 15866 15877
45. M. Kawabori, R. Kacimi, T. Kauppinen, C. Calosing, J.Y. Kim, C.L. Hsieh, and et al. Triggering receptor expressed on myeloid cells 2 (TREM2) deficiency attenuates phagocytic activities of microglia and exacerbates ischemic damage in experimental stroke J. Neurosci. 35 2015 3384 3396
46. Y. Wang, M. Cella, K. Mallinson, J.D. Ulrich, K.L. Young, M.L. Robinette, and et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model Cell 160 2015 1061 1071
47. C.H. Cohan, J.T. Neumann, K.R. Dave, A. Alekseyenko, M. Binkert, K. Stransky, and et al. Effect of cardiac arrest on cognitive impairment and hippocampal plasticity in middle-aged rats PLoS One 10 2015 e0124918
48. J. Wang, T. Fujiyoshi, Y. Kosaka, J.D. Raybuck, K.M. Lattal, M. Ikeda, and et al. Inhibition of soluble epoxide hydrolase after cardiac arrest/cardiopulmonary resuscitation induces a neuroprotective phenotype in activated microglia and improves neuronal survival J. Cereb. Blood Flow Metab. 33 2013 1574 1581
49. S. Galvan-Pena, and L.A. O'Neill Metabolic reprograming in macrophage polarization Front. Immunol. 5 2014 420
50. G.M. Tannahill, N. Iraci, E. Gaude, C. Frezza, and S. Pluchino Metabolic reprograming of mononuclear phagocytes in progressive multiple sclerosis Front. Immunol. 6 2015 106
51. M.K. Jha, G.J. Song, M.G. Lee, N.H. Jeoung, Y. Go, R.A. Harris, and et al. Metabolic connection of inflammatory pain: pivotal role of a pyruvate dehydrogenase kinase-pyruvate dehydrogenase-lactic acid axis J. Neurosci 35 2015 14353 14369
52. R. Orihuela, C.A. McPherson, and G.J. Harry Microglial M1 /M2 polarization and metabolic states Br. J. Pharmacol. 2015 10.1111/bph.13139 (in press) [Epub ahead of print]
53. Q. Zhang, G. Bian, P. Chen, L. Liu, C. Yu, F. Liu, and et al. Aldose reductase regulates microglia/macrophages polarization through the cAMP response element-binding protein after spinal cord injury in mice Mol. Neurobiol. 2014 10.1007/s12035-014-9035-8 (in press) [Epub ahead of print]
54. L. Rajendran, J. Bali, M.M. Barr, F.A. Court, E.M. Kramer-Albers, F. Picou, and et al. Emerging roles of extracellular vesicles in the nervous system J. Neurosci. 34 2014 15482 15489
55. C. Fruhbeis, D. Frohlich, W.P. Kuo, and E.M. Kramer-Albers Extracellular vesicles as mediators of neuron-glia communication Front. Cell. Neurosci. 7 2013 182
56. C. Fruhbeis, D. Frohlich, and E.M. Kramer-Albers Emerging roles of exosomes in neuron-glia communication Front. Physiol. 3 2012 119
57. M. Gabrielli, N. Battista, L. Riganti, I. Prada, F. Antonucci, L. Cantone, and et al. Active endocannabinoids are secreted on extracellular membrane vesicles EMBO Rep. 16 2015 213 220
58. P. Joshi, L. Benussi, R. Furlan, R. Ghidoni, and C. Verderio Extracellular vesicles in Alzheimer's disease: friends or foes? Focus on abeta-vesicle interaction Int. J. Mol. Sci. 16 2015 4800 4813
59. E. Turola, R. Furlan, F. Bianco, M. Matteoli, and C. Verderio Microglial microvesicle secretion and intercellular signaling Front. Physiol. 3 2012 149
60. T. Goldmann, and M. Prinz Role of microglia in CNS autoimmunity Clin. Dev. Immunol. 2013 2013 208093
61. T. Goldmann, P. Wieghofer, P.F. Muller, Y. Wolf, D. Varol, S. Yona, and et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation Nat. Neurosci. 16 2013 1618 1626
62. C. Jack, F. Ruffini, A. Bar-Or, and J.P. Antel Microglia and multiple sclerosis J. Neurosci. Res. 81 2005 363 373
63. M. Politis, P. Giannetti, P. Su, F. Turkheimer, S. Keihaninejad, K. Wu, and et al. Increased PK11195 PET binding in the cortex of patients with MS correlates with disability Neurology 79 2012 523 530
64. P. van der Valk, and S. Amor Preactive lesions in multiple sclerosis Curr. Opin. Neurol. 22 2009 207 213
65. S. Singh, I. Metz, S. Amor, P. van der Valk, C. Stadelmann, and W. Bruck Microglial nodules in early multiple sclerosis white matter are associated with degenerating axons Acta Neuropathol. 125 2013 595 608
66. L. Peferoen, M. Kipp, P. van der Valk, J.M. van Noort, and S. Amor Oligodendrocyte-microglia cross-talk in the central nervous system Immunology 141 2014 302 313
67. K. Janssens, A. Maheshwari, C. Van den Haute, V. Baekelandt, P. Stinissen, J.J. Hendriks, and et al. Oncostatin M protects against demyelination by inducing a protective microglial phenotype Glia 63 10 2015 1729 1737
68. Y.H. Li, J.Z. Yu, C.Y. Liu, H. Zhang, H.F. Zhang, W.F. Yang, and et al. Intranasal delivery of FSD-C10, a novel Rho kinase inhibitor, exhibits therapeutic potential in experimental autoimmune encephalomyelitis Immunology 143 2014 219 229
69. C. Gao, L. Huang, Y. Long, J. Zheng, J. Yang, S. Pu, and et al. Y-39983, a selective Rho-kinase inhibitor, attenuates experimental autoimmune encephalomyelitis via inhibition of demyelination Neuroimmunomodulation 20 2013 334 340
70. C. Chen, Y.H. Li, Q. Zhang, J.Z. Yu, Y.F. Zhao, C.G. Ma, and et al. Fasudil regulates T cell responses through polarization of BV-2 cells in mice experimental autoimmune encephalomyelitis Acta Pharmacol. Sin. 35 2014 1428 1438
71. Y.F. Zhao, X. Zhang, Z.B. Ding, X.W. Yang, H. Zhang, J.Z. Yu, and et al. The therapeutic potential of Rho kinase inhibitor fasudil derivative FaD-1 in experimental autoimmune encephalomyelitis J. Mol. Neurosci. 55 2015 725 732
72. J. Ni, X. Wang, S. Chen, H. Liu, Y. Wang, X. Xu, and et al. MicroRNA let-7c-5p protects against cerebral ischemia injury via mechanisms involving the inhibition of microglia activation Brain Behav. Immun. 49 2015 75 85
73. B.P. Gaire, O.W. Kwon, S.H. Park, K.H. Chun, S.Y. Kim, D.Y. Shin, and et al. Neuroprotective effect of 6-paradol in focal cerebral ischemia involves the attenuation of neuroinflammatory responses in activated microglia PLoS One 10 2015 e0120203
74. R. Barakat, and Z. Redzic The role of activated microglia and resident macrophages in the neurovascular unit during cerebral ischemia: is the jury still out? Med. Princ. Pract. 2015 10.1159/000435858 (in press) [Epub ahead of print]
75. X. Zhao, H. Wang, G. Sun, J. Zhang, N.J. Edwards, and J. Aronowski Neuronal interleukin-4 as a modulator of microglial pathways and ischemic brain damage J. Neurosci. 35 2015 11281 11291
76. J.R. Weinstein, I.P. Koerner, and T. Moller Microglia in ischemic brain injury Future Neurol. 5 2010 227 246
77. J.V. Emmrich, T.C. Hornik, J.J. Neher, and G.C. Brown Rotenone induces neuronal death by microglial phagocytosis of neurons FEBS J. 280 2013 5030 5038
78. J.J. Neher, J.V. Emmrich, M. Fricker, P.K. Mander, C. Thery, and G.C. Brown Phagocytosis executes delayed neuronal death after focal brain ischemia Proc. Natl. Acad. Sci. U. S. A. 110 2013 E4098 E4107
79. X. Hu, A.K. Liou, R.K. Leak, M. Xu, C. An, J. Suenaga, and et al. Neurobiology of microglial action in CNS injuries: receptor-mediated signaling mechanisms and functional roles Prog. Neurobiol. 119-120 2014 60 84
80. H.A. Seifert, and K.R. Pennypacker Molecular and cellular immune responses to ischemic brain injury Transl. Stroke Res. 5 2014 543 553
81. R.N. Dilger, and R.W. Johnson Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system J. Leukoc. Biol. 84 2008 932 939
82. D.M. Norden, and J.P. Godbout Review: microglia of the aged brain: primed to be activated and resistant to regulation Neuropathol. Appl. Neurobiol. 39 2013 19 34
83. J. Suenaga, X. Hu, H. Pu, Y. Shi, S.H. Hassan, M. Xu, and et al. White matter injury and microglia/macrophage polarization are strongly linked with age-related long-term deficits in neurological function after stroke Exp. Neurol. 272 2015 109 119
84. X. Hu, P. Li, Y. Guo, H. Wang, R.K. Leak, S. Chen, and et al. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia Stroke 43 2012 3063 3070
85. M.J. Quattromani, P. Cordeau, K. Ruscher, J. Kriz, and T. Wieloch Enriched housing down-regulates the Toll-like receptor 2 response in the mouse brain after experimental stroke Neurobiol. Dis. 66 2014 66 73
86. I. Bohacek, P. Cordeau, M. Lalancette-Hebert, D. Gorup, Y.C. Weng, S. Gajovic, and et al. Toll-like receptor 2 deficiency leads to delayed exacerbation of ischemic injury J. Neuroinflamm. 9 2012 191
87. C. Mallard, and Z.S. Vexler Modeling ischemia in the immature brain: how translational are animal models? Stroke 46 10 2015 3006 3011
88. Z.S. Vexler, and M.A. Yenari Does inflammation after stroke affect the developing brain differently than adult brain? Dev. Neurosci. 31 2009 378 393
89. V. Donega, C.H. Nijboer, T. van, G. ilborg, R.M. Dijkhuizen, A. Kavelaars, and C.J. Heijnen Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury Exp. Neurol. 261 2014 53 64
90. E.R. Zanier, F. Pischiutta, L. Riganti, F. Marchesi, E. Turola, S. Fumagalli, and et al. Bone marrow mesenchymal stromal cells drive protective M2 microglia polarization after brain trauma Neurotherapeutics 11 2014 679 695
91. L.N. Pan, W. Zhu, Y. Li, X.L. Xu, L.J. Guo, Q. Lu, and et al. Astrocytic Toll-like receptor 3 is associated with ischemic preconditioning-induced protection against brain ischemia in rodents PLoS One 9 2014 e99526
92. Z.F. Ma, W. Chen, C.C. Cao, and X. Chen Ischemic preconditioning attenuates brain injury induced by ischemia/reperfusion during moderate hypothermia low-flow procedures Int. J. Neurosci. 124 2014 824 833
93. J. Parmar, and N.M. Jones Hypoxic preconditioning can reduce injury-induced inflammatory processes in the neonatal rat brain Int. J. Dev. Neurosci. 43 2015 35 42
94. G. Cantarella, G. Pignataro, G. Di Benedetto, S. Anzilotti, A. Vinciguerra, O. Cuomo, and et al. Ischemic tolerance modulates TRAIL expression and its receptors and generates a neuroprotected phenotype Cell Death Dis. 5 2014 e1331
95. G. Umschweif, A.G. Alexandrovich, V. Trembovler, M. Horowitz, and E. Shohami Hypoxia-inducible factor 1 is essential for spontaneous recovery from traumatic brain injury and is a key mediator of heat acclimation induced neuroprotection J. Cereb. Blood Flow Metab. 33 2013 524 531
96. K.M. Kinnunen, R. Greenwood, J.H. Powell, R. Leech, P.C. Hawkins, V. Bonnelle, and et al. White matter damage and cognitive impairment after traumatic brain injury Brain 134 2011 449 463
97. G. Harish, A. Mahadevan, N. Pruthi, S.K. Sreenivasamurthy, V.N. Puttamallesh, T.S. Keshava Prasad, and et al. Characterization of traumatic brain injury in human brains reveals distinct cellular and molecular changes in contusion and pericontusion J. Neurochem. 134 2015 156 172
98. D.C. Anthony, and Y. Couch The systemic response to CNS injury Exp. Neurol. 258 2014 105 111
99. I.P. Karve, J.M. Taylor, and P.J. Crack The contribution of astrocytes and microglia to traumatic brain injury Br. J. Pharmacol. 2015 10.1111/bph.13125 (in press) [Epub ahead of print]
100. J.E. Burda, A.M. Bernstein, and M.V. Sofroniew Astrocyte roles in traumatic brain injury Exp. Neurol. 2015 10.1016/j.expneurol.2015.03.020 (in press) [Epub ahead of print]
101. G. Wang, J. Zhang, X. Hu, L. Zhang, L. Mao, X. Jiang, and et al. Microglia/macrophage polarization dynamics in white matter after traumatic brain injury J. Cereb. Blood Flow Metab. 33 2013 1864 1874
102. D.J. Loane, B.A. Stoica, F. Tchantchou, A. Kumar, J.P. Barrett, T. Akintola, and et al. Novel mGluR5 positive allosteric modulator improves functional recovery, attenuates neurodegeneration, and alters microglial polarization after experimental traumatic brain injury Neurotherapeutics 11 2014 857 869
103. P.G. Popovich, Z. Guan, V. McGaughy, L. Fisher, W.F. Hickey, and D.M. Basso The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation J. Neuropathol. Exp. Neurol. 61 2002 623 633
104. J.C. Fleming, M.D. Norenberg, D.A. Ramsay, G.A. Dekaban, A.E. Marcillo, A.D. Saenz, and et al. The cellular inflammatory response in human spinal cords after injury Brain 129 2006 3249 3269
105. K.A. Kigerl, J.C. Gensel, D.P. Ankeny, J.K. Alexander, D.J. Donnelly, and P.G. Popovich Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord J. Neurosci. 29 2009 13435 13444
106. L. Longhi, R. Gesuete, C. Perego, F. Ortolano, N. Sacchi, P. Villa, and et al. Long-lasting protection in brain trauma by endotoxin preconditioning J. Cereb. Blood Flow Metab. 31 2011 1919 1929
107. W.C. Li, D.M. Jiang, N. Hu, X.T. Qi, B. Qiao, and X.J. Luo Lipopolysaccharide preconditioning attenuates neuroapoptosis and improves functional recovery through activation of Nrf2 in traumatic spinal cord injury rats Int. J. Neurosci. 123 2013 240 247
108. S.L. Stevens, P.Y. Leung, K.B. Vartanian, B. Gopalan, T. Yang, R.P. Simon, and et al. Multiple preconditioning paradigms converge on interferon regulatory factor-dependent signaling to promote tolerance to ischemic brain injury J. Neurosci. 31 2011 8456 8463
109. K. Hayakawa, R. Okazaki, K. Morioka, K. Nakamura, S. Tanaka, and T. Ogata Lipopolysaccharide preconditioning facilitates M2 activation of resident microglia after spinal cord injury J. Neurosci. Res. 92 2014 1647 1658
110. R. Martini, and H. Willison Neuroinflammation in the peripheral nerve: cause, modulator, or bystander in peripheral neuropathies? Glia 2015 10.1002/glia.22899 (in press) [Epub ahead of print]
111. C.J. Perera, S.S. Duffy, J.G. Lees, C.F. Kim, B. Cameron, V. Apostolopoulos, and et al. Active immunization with myelin-derived altered peptide ligand reduces mechanical pain hypersensitivity following peripheral nerve injury J. Neuroinflamm. 12 2015 28
112. J.G. Lees, S.S. Duffy, C.J. Perera, and G. Moalem-Taylor Depletion of Foxp3+ regulatory T cells increases severity of mechanical allodynia and significantly alters systemic cytokine levels following peripheral nerve injury Cytokine 71 2015 207 214
113. P.J. Austin, C.F. Kim, C.J. Perera, and G. Moalem-Taylor Regulatory T cells attenuate neuropathic pain following peripheral nerve injury and experimental autoimmune neuritis Pain 153 2012 1916 1931
114. K. Popiolek-Barczyk, N. Kolosowska, A. Piotrowska, W. Makuch, E. Rojewska, A.M. Jurga, and et al. Parthenolide relieves pain and promotes M2 microglia/macrophage polarization in rat model of neuropathy Neural Plast. 2015 2015 676473
115. M.T. Heneka, M.J. Carson, J. El Khoury, G.E. Landreth, F. Brosseron, D.L. Feinstein, and et al. Neuroinflammation in Alzheimer's disease Lancet Neurol. 14 2015 388 405
116. Y. Tang, and W. Le Differential roles of M1 and M2 microglia in neurodegenerative diseases Mol. Neurobiol. 2015 10.1007/s12035-014-9070-5 (in press) [Epub ahead of print]
117. A.J. Herrera, A.M. Espinosa-Oliva, A. Carrillo-Jimenez, M.J. Oliva-Martin, J. Garcia-Revilla, A. Garcia-Quintanilla, and et al. Relevance of chronic stress and the two faces of microglia in Parkinson's disease Front. Cell. Neurosci. 9 2015 312
118. J. Koenigsknecht-Talboo, and G.E. Landreth Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines J. Neurosci. 25 2005 8240 8249
119. V. Porrini, A. Lanzillotta, C. Branca, M. Benarese, E. Parrella, L. Lorenzini, and et al. CHF5074 (CSP-1103) induces microglia alternative activation in plaque-free Tg2576 mice and primary glial cultures exposed to beta-amyloid Neuroscience 302 2014 112 120
120. P. Mesci, S. Zaidi, C.S. Lobsiger, S. Millecamps, C. Escartin, D. Seilhean, and et al. System xC- is a mediator of microglial function and its deletion slows symptoms in amyotrophic lateral sclerosis mice Brain 138 2015 53 68
121. W.J. Streit, and Q.S. Xue Life and death of microglia J. Neuroimmune Pharmacol. 4 2009 371 379
122. W.J. Streit, and Q.S. Xue Microglial senescence CNS Neurol. Disord. Drug Targets 12 2013 763 767
123. W.J. Streit, Q.S. Xue, J. Tischer, and I. Bechmann Microglial pathology Acta Neuropathol. Commun. 2 2014 142
124. W.J. Streit, and Q.S. Xue Human CNS immune senescence and neurodegeneration Curr. Opin. Immunol. 29 2014 93 96
125. A.M. Smith, and M. Dragunow The human side of microglia Trends Neurosci. 37 2014 125 135
126. W.J. Streit, N.W. Sammons, A.J. Kuhns, and D.L. Sparks Dystrophic microglia in the aging human brain Glia 45 2004 208 212
127. A.M. Smith, E.S. Graham, S.X. Feng, R.L. Oldfield, P.M. Bergin, E.W. Mee, and et al. Adult human glia, pericytes and meningeal fibroblasts respond similarly to IFNy but not to TGFbeta1 or M-CSF PLoS One 8 2013 e80463
128. A.M. Smith, H.M. Gibbons, R.L. Oldfield, P.M. Bergin, E.W. Mee, M.A. Curtis, and et al. M-CSF increases proliferation and phagocytosis while modulating receptor and transcription factor expression in adult human microglia J. Neuroinflamm. 10 2013 85
129. H.M. Gibbons, A.M. Smith, H.H. Teoh, P.M. Bergin, E.W. Mee, R.L. Faull, and et al. Valproic acid induces microglial dysfunction, not apoptosis, in human glial cultures Neurobiol. Dis. 41 2011 96 103
130. H. Zong, R.G. Verhaak, and P. Canoll The cellular origin for malignant glioma and prospects for clinical advancements Expert Rev. Mol. Diagn. 12 2012 383 394
131. F. Szulzewsky, A. Pelz, X. Feng, M. Synowitz, D. Markovic, T. Langmann, and et al. Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1 PLoS One 10 2015 e0116644
132. L. Lisi, E. Laudati, P. Navarra, and C. Dello Russo The mTOR kinase inhibitors polarize glioma-activated microglia to express a M1 phenotype J. Neuroinflamm. 11 2014 125
133. J. Kopatz, C. Beutner, K. Welle, L.G. Bodea, J. Reinhardt, J. Claude, and et al. Siglec-h on activated microglia for recognition and engulfment of glioma cells Glia 61 2013 1122 1133
134. F. Hu, O.D. Dzaye, A. Hahn, Y. Yu, R.J. Scavetta, G. Dittmar, and et al. Glioma-derived versican promotes tumor expansion via glioma-associated microglial/macrophages Toll-like receptor 2 signaling Neuro Oncol. 17 2015 200 210
135. A. Ellert-Miklaszewska, M. Dabrowski, M. Lipko, M. Sliwa, M. Maleszewska, and B. Kaminska Molecular definition of the pro-tumorigenic phenotype of glioma-activated microglia Glia 61 2013 1178 1190
136. M. Sielska, P. Przanowski, B. Wylot, K. Gabrusiewicz, M. Maleszewska, M. Kijewska, and et al. Distinct roles of CSF family cytokines in macrophage infiltration and activation in glioma progression and injury response J. Pathol. 230 2013 310 321
137. M.B. Nijaguna, V. Patil, S. Urbach, S.D. Shwetha, K. Sravani, A.S. Hegde, and et al. Glioblastoma-derived macrophage colony stimulating factor (MCSF) induces microglial release of insulin-like growth factor-binding protein 1 (IGFBP1) to promote angiogenesis J. Biol. Chem. 290 38 2015 23401 23415
138. L. Lisi, E. Stigliano, L. Lauriola, P. Navarra, and C. Dello Russo Proinflammatory-activated glioma cells induce a switch in microglial polarization and activation status, from a predominant M2b phenotype to a mixture of M1 and M2a/B polarized cells ASN Neuro 6 2014 171 183
139. P.S. Zeiner, C. Preusse, A.E. Blank, C. Zachskorn, P. Baumgarten, L. Caspary, and et al. MIF receptor CD74 is restricted to microglia/macrophages, associated with a M1-polarized immune milieu and prolonged patient survival in gliomas Brain Pathol. 25 2015 491 504
140. D.T. Theodosis, D.A. Poulain, and S.H. Oliet Activity-dependent structural and functional plasticity of astrocyte-neuron interactions Physiol. Rev. 88 2008 983 1008
141. N.R. Blumenthal, O. Hermanson, B. Heimrich, and V.P. Shastri Stochastic nanoroughness modulates neuron-astrocyte interactions and function via mechanosensing cation channels Proc. Natl. Acad. Sci. U. S. A. 111 2014 16124 16129
142. C.M. Galtrey, and J.W. Fawcett The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system Brain Res. Rev. 54 2007 1 18
143. W.L. Gu, S.L. Fu, Y.X. Wang, Y. Li, H.Z. Lu, X.M. Xu, and et al. Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway BMC Neurosci. 10 2009 128
144. T.M. Mathiisen, K.P. Lehre, N.C. Danbolt, and O.P. Ottersen The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction Glia 58 2010 1094 1103
145. L.K. Lunde, L.M. Camassa, E.H. Hoddevik, F.H. Khan, O.P. Ottersen, H.B. Boldt, and et al. Postnatal development of the molecular complex underlying astrocyte polarization Brain Struct. Funct. 220 4 2014 2087 2101
146. G.A. Gundersen, G.F. Vindedal, O. Skare, and E.A. Nagelhus Evidence that pericytes regulate aquaporin-4 polarization in mouse cortical astrocytes Brain Struct. Funct. 219 2014 2181 2186
147. O. Pascual, K.B. Casper, C. Kubera, J. Zhang, R. Revilla-Sanchez, J.Y. Sul, and et al. Astrocytic purinergic signaling coordinates synaptic networks Science 310 2005 113 116
148. J.D. Cahoy, B. Emery, A. Kaushal, L.C. Foo, J.L. Zamanian, K.S. Christopherson, and et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function J. Neurosci. 28 2008 264 278
149. J.R. Faulkner, J.E. Herrmann, M.J. Woo, K.E. Tansey, N.B. Doan, and M.V. Sofroniew Reactive astrocytes protect tissue and preserve function after spinal cord injury J. Neurosci. 24 2004 2143 2155
150. L. Tarassishin, O. Loudig, A. Bauman, B. Shafit-Zagardo, H.S. Suh, and S.C. Lee Interferon regulatory factor 3 inhibits astrocyte inflammatory gene expression through suppression of the proinflammatory miR-155 and miR-155∗ Glia 59 2011 1911 1922
151. C. Farina, F. Aloisi, and E. Meinl Astrocytes are active players in cerebral innate immunity Trends Immunol. 28 2007 138 145
152. M.V. Sofroniew, and H.V. Vinters Astrocytes: biology and pathology Acta Neuropathol. 119 2010 7 35
153. U. Wilhelmsson, E.A. Bushong, D.L. Price, B.L. Smarr, V. Phung, M. Terada, and et al. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury Proc. Natl. Acad. Sci. U. S. A. 103 2006 17513 17518
154. P.A. Carpentier, D.S. Duncan, and S.D. Miller Glial toll-like receptor signaling in central nervous system infection and autoimmunity Brain Behav. Immun. 22 2008 140 147
155. G.R. John, S.C. Lee, and C.F. Brosnan Cytokines: powerful regulators of glial cell activation Neuroscientist 9 2003 10 22
156. S. Gordon Alternative activation of macrophages Nat. Rev. Immunol. 3 2003 23 35
157. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat. Neurosci. 10 2007 1387 1394
158. F.O. Martinez, L. Helming, and S. Gordon Alternative activation of macrophages: an immunologic functional perspective Annu. Rev. Immunol. 27 2009 451 483
159. J. Fraussen, N. Claes, L. de Bock, and V. Somers Targets of the humoral autoimmune response in multiple sclerosis Autoimmun. Rev. 13 2014 1126 1137
160. P. Jukkola, T. Guerrero, V. Gray, and C. Gu Astrocytes differentially respond to inflammatory autoimmune insults and imbalances of neural activity Acta Neuropathol. Commun. 1 2013 70
161. J.M. Millward, M. Caruso, I.L. Campbell, J. Gauldie, and T. Owens IFN-gamma-induced chemokines synergize with pertussis toxin to promote T cell entry to the central nervous system J. Immunol. 178 2007 8175 8182
162. B.G. Xiao, and H. Link Immune regulation within the central nervous system J. Neurol. Sci. 157 1998 1 12
163. L. Probert, K. Akassoglou, G. Kassiotis, M. Pasparakis, L. Alexopoulou, and G. Kollias TNF-alpha transgenic and knockout models of CNS inflammation and degeneration J. Neuroimmunol. 72 1997 137 141
164. Y. Dong, and E.N. Benveniste Immune function of astrocytes Glia 36 2001 180 190
165. A. Basu, J.K. Krady, and S.W. Levison Interleukin-1: a master regulator of neuroinflammation J. Neurosci. Res. 78 2004 151 156
166. M. Downen, T.D. Amaral, L.L. Hua, M.L. Zhao, and S.C. Lee Neuronal death in cytokine-activated primary human brain cell culture: role of tumor necrosis factor-alpha Glia 28 1999 114 127
167. P. Thornton, E. Pinteaux, R.M. Gibson, S.M. Allan, and N.J. Rothwell Interleukin-1-induced neurotoxicity is mediated by glia and requires caspase activation and free radical release J. Neurochem. 98 2006 258 266
168. H.S. Suh, C.F. Brosnan, and S.C. Lee Toll-like receptors in CNS viral infections Curr. Top. Microbiol. Immunol. 336 2009 63 81
169. B.J. Baker, L.N. Akhtar, and E.N. Benveniste SOCS1 and SOCS3 in the control of CNS immunity Trends Immunol. 30 2009 392 400
170. L.L. Hua, M.O. Kim, C.F. Brosnan, and S.C. Lee Modulation of astrocyte inducible nitric oxide synthase and cytokine expression by interferon beta is associated with induction and inhibition of interferon gamma-activated sequence binding activity J. Neurochem. 83 2002 1120 1128
171. S. Hashioka, E.G. McGeer, T. Miyaoka, R. Wake, J. Horiguchi, and P.L. McGeer Interferon-gamma-induced neurotoxicity of human astrocytes CNS Neurol. Disord. Drug Targets 14 2015 251 256
172. R. Brambilla, T. Persaud, X. Hu, S. Karmally, V.I. Shestopalov, G. Dvoriantchikova, and et al. Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation J. Immunol. 182 2009 2628 2640
173. L.I. McKay, and J.A. Cidlowski Molecular control of immune/inflammatory responses: interactions between nuclear factor-kappa B and steroid receptor-signaling pathways Endocr. Rev. 20 1999 435 459
174. L. Garidou, S. Laffont, V. Douin-Echinard, C. Coureau, A. Krust, P. Chambon, and et al. Estrogen receptor alpha signaling in inflammatory leukocytes is dispensable for 17beta-estradiol-mediated inhibition of experimental autoimmune encephalomyelitis J. Immunol. 173 2004 2435 2442
175. E. Ambrosini, S. Columba-Cabezas, B. Serafini, A. Muscella, and F. Aloisi Astrocytes are the major intracerebral source of macrophage inflammatory protein-3alpha/CCL20 in relapsing experimental autoimmune encephalomyelitis and in vitro Glia 41 2003 290 300
176. A. Liston, R.E. Kohler, S. Townley, S. Haylock-Jacobs, I. Comerford, A.C. Caon, and et al. Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response J. Immunol. 182 2009 3121 3130
177. G.P. Meares, X. Ma, H. Qin, and E.N. Benveniste Regulation of CCL20 expression in astrocytes by IL-6 and IL-17 Glia 60 2012 771 781
178. R. Li, W. Xu, Y. Chen, W. Qiu, Y. Shu, A. Wu, and et al. Raloxifene suppresses experimental autoimmune encephalomyelitis and NF-kappaB-dependent CCL20 expression in reactive astrocytes PLoS One 9 2014 e94320
179. Y. Hosokawa, I. Hosokawa, S. Shindo, K. Ozaki, and T. Matsuo TLR3 agonist enhances CC chemokine ligand 20 production in IL-1beta-stimulated human gingival fibroblasts Cell Immunol. 283 2013 8 11
180. T. Schlegelmilch, K. Henke, and F. Peri Microglia in the developing brain: from immunity to behaviour Curr. Opin. Neurobiol. 21 2011 5 10
181. J.J. Rodriguez, and A. Verkhratsky Neuroglial roots of neurodegenerative diseases? Mol. Neurobiol. 43 2011 87 96
182. L. Mayo, S.A. Trauger, M. Blain, M. Nadeau, B. Patel, J.I. Alvarez, and et al. Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation Nat. Med. 20 2014 1147 1156
183. M. Lindner, K. Thummler, A. Arthur, S. Brunner, C. Elliott, D. McElroy, and et al. Fibroblast growth factor signalling in multiple sclerosis: inhibition of myelination and induction of pro-inflammatory environment by FGF9 Brain 138 Pt. 7 2015 1875 1893
184. H.Y. Hsiao, Y.C. Chen, H.M. Chen, P.H. Tu, and Y. Chern A critical role of astrocyte-mediated nuclear factor-kappaB-dependent inflammation in Huntington's disease Hum. Mol. Genet. 22 2013 1826 1842
185. J.Y. Shin, Z.H. Fang, Z.X. Yu, C.E. Wang, S.H. Li, and X.J. Li Expression of mutant huntingtin in glial cells contributes to neuronal excitotoxicity J. Cell Biol. 171 2005 1001 1012
186. M. Vila, V. Jackson-Lewis, C. Guegan, D.C. Wu, P. Teismann, D.K. Choi, and et al. The role of glial cells in Parkinson's disease Curr. Opin. Neurol. 14 2001 483 489
187. F. Endo, O. Komine, N. Fujimori-Tonou, M. Katsuno, S. Jin, S. Watanabe, and et al. Astrocyte-derived TGF-beta1 accelerates disease progression in ALS mice by interfering with the neuroprotective functions of microglia and T cells Cell Rep. 11 2015 592 604
188. V. Rusnakova, P. Honsa, D. Dzamba, A. Stahlberg, M. Kubista, and M. Anderova Heterogeneity of astrocytes: from development to injury - single cell gene expression PLoS One 8 2013 e69734
189. J.L. Zamanian, L. Xu, L.C. Foo, N. Nouri, L. Zhou, R.G. Giffard, and et al. Genomic analysis of reactive astrogliosis J. Neurosci. 32 2012 6391 6410
190. S.S. Kang, M.P. Keasey, J. Cai, and T. Hagg Loss of neuron-astroglial interaction rapidly induces protective CNTF expression after stroke in mice J. Neurosci. 32 2012 9277 9287
191. M.D. LeComte, I.S. Shimada, C. Sherwin, and J.L. Spees Notch1-STAT3-ETBR signaling axis controls reactive astrocyte proliferation after brain injury Proc. Natl. Acad. Sci. U. S. A. 112 2015 8726 8731
192. H. Min, J. Hong, I.H. Cho, Y.H. Jang, H. Lee, D. Kim, and et al. TLR2-induced astrocyte MMP9 activation compromises the blood brain barrier and exacerbates intracerebral hemorrhage in animal models Mol. Brain 8 2015 23
193. C.D. Cuevas, and S.R. Ross Toll-like receptor 2-mediated innate immune responses against Junin virus in mice lead to antiviral adaptive immune responses during systemic infection and do not affect viral replication in the brain J. Virol. 88 2014 7703 7714
194. S.C. Tang, T.V. Arumugam, X. Xu, A. Cheng, M.R. Mughal, D.G. Jo, and et al. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits Proc. Natl. Acad. Sci. U. S. A. 104 2007 13798 13803
195. L. Qian, L. Ding, L. Cheng, X. Zhu, H. Zhao, J. Jin, and et al. Early biomarkers for post-stroke cognitive impairment J. Neurol. 259 2012 2111 2118
196. Q.W. Yang, F.L. Lu, Y. Zhou, L. Wang, Q. Zhong, S. Lin, and et al. HMBG1 mediates ischemia-reperfusion injury by TRIF-adaptor independent Toll-like receptor 4 signaling J. Cereb. Blood Flow Metab. 31 2011 593 605
197. T. Jiang, F. Yin, J. Yao, R.D. Brinton, and E. Cadenas Lipoic acid restores age-associated impairment of brain energy metabolism through the modulation of Akt/JNK signaling and PGC1alpha transcriptional pathway Aging Cell 12 2013 1021 1031
198. F. Yin, T. Jiang, and E. Cadenas Metabolic triad in brain aging: mitochondria, insulin/IGF-1 signalling and JNK signalling Biochem. Soc. Trans. 41 2013 101 105
199. J.P. Bolanos, A. Almeida, and S. Moncada Glycolysis: a bioenergetic or a survival pathway? Trends Biochem. Sci. 35 2010 145 149
200. G.A. Dienel, and L. Hertz Glucose and lactate metabolism during brain activation J. Neurosci. Res. 66 2001 824 838
201. P.J. Magistretti Neuron-glia metabolic coupling and plasticity Exp. Physiol. 96 2011 407 410
202. A. Suzuki, S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti, and et al. Astrocyte-neuron lactate transport is required for long-term memory formation Cell 144 2011 810 823
203. F. Boumezbeur, G.F. Mason, R.A. de Graaf, K.L. Behar, G.W. Cline, G.I. Shulman, and et al. Altered brain mitochondrial metabolism in healthy aging as assessed by in vivo magnetic resonance spectroscopy J. Cereb. Blood Flow Metab. 30 2010 211 221
204. O. Campuzano, M.M. Castillo-Ruiz, L. Acarin, B. Castellano, and B. Gonzalez Increased levels of proinflammatory cytokines in the aged rat brain attenuate injury-induced cytokine response after excitotoxic damage J. Neurosci. Res. 87 2009 2484 2497
205. G. Zhang, J. Li, S. Purkayastha, Y. Tang, H. Zhang, Y. Yin, and et al. Hypothalamic programming of systemic ageing involving IKK-beta, NF-kappaB and GnRH Nature 497 2013 211 216
206. M.S. Han, D.Y. Jung, C. Morel, S.A. Lakhani, J.K. Kim, R.A. Flavell, and et al. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation Science 339 2013 218 222
207. S. Mehan, H. Meena, D. Sharma, and R. Sankhla JNK: a stress-activated protein kinase therapeutic strategies and involvement in Alzheimer's and various neurodegenerative abnormalities J. Mol. Neurosci. 43 2011 376 390
208. M. Belanger, and P.J. Magistretti The role of astroglia in neuroprotection Dialogues Clin. Neurosci. 11 2009 281 295
209. M. Pekny, and M. Pekna Astrocyte reactivity and reactive astrogliosis: costs and benefits Physiol. Rev. 94 2014 1077 1098
210. M. Pekny, U. Wilhelmsson, and M. Pekna The dual role of astrocyte activation and reactive gliosis Neurosci. Lett. 565 2014 30 38
211. N. Gregori, C. Proschel, M. Noble, and M. Mayer-Proschel The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function J. Neurosci. 22 2002 248 256
212. M.S. Rao, and M. Mayer-Proschel Glial-restricted precursors are derived from multipotent neuroepithelial stem cells Dev. Biol. 188 1997 48 63
213. J. Herrera, H. Yang, S.C. Zhang, C. Proschel, P. Tresco, I.D. Duncan, and et al. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo Exp. Neurol. 171 2001 11 21
214. G. Criste, B. Trapp, and R. Dutta Axonal loss in multiple sclerosis: causes and mechanisms Handb. Clin. Neurol. 122 2014 101 113
215. J.R. Patel, E.E. McCandless, D. Dorsey, and R.S. Klein CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination Proc. Natl. Acad. Sci. U. S. A. 107 2010 11062 11067
216. H.A. Arnett, S.P. Fancy, J.A. Alberta, C. Zhao, S.R. Plant, S. Kaing, and et al. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS Science 306 2004 2111 2115
217. P.J. Horner, A.E. Power, G. Kempermann, H.G. Kuhn, T.D. Palmer, J. Winkler, and et al. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord J. Neurosci. 20 2000 2218 2228
218. S. Bramow, J.M. Frischer, H. Lassmann, N. Koch-Henriksen, C.F. Lucchinetti, P.S. Sorensen, and et al. Demyelination versus remyelination in progressive multiple sclerosis Brain 133 2010 2983 2998
219. E.P. Mensah-Brown, A. Shahin, M. Al Shamisi, and M.L. Lukic Early influx of macrophages determines susceptibility to experimental allergic encephalomyelitis in Dark Agouti (DA) rats J. Neuroimmunol. 232 2011 68 74
220. C. Trebst, F. Konig, R. Ransohoff, W. Bruck, and M. Stangel CCR5 expression on macrophages/microglia is associated with early remyelination in multiple sclerosis lesions Mult. Scler. 14 2008 728 733
221. V.W. Yong Promoting remyelination by reducing an inhibitory microenvironment Rinsho Shinkeigaku 50 2010 869
222. E. Ydens, G. Lornet, V. Smits, S. Goethals, V. Timmerman, and S. Janssens The neuroinflammatory role of Schwann cells in disease Neurobiol. Dis. 55 2013 95 103
223. P.J. Armati, and E.K. Mathey Clinical implications of Schwann cell biology J. Peripher. Nerv. Syst. 19 2014 14 23
224. M. Bremer, F. Frob, T. Kichko, P. Reeh, E.R. Tamm, U. Suter, and et al. Sox10 is required for Schwann-cell homeostasis and myelin maintenance in the adult peripheral nerve Glia 59 2011 1022 1032
225. P. Dubovy, R. Jancalek, and T. Kubek Role of inflammation and cytokines in peripheral nerve regeneration Int. Rev. Neurobiol. 108 2013 173 206
226. R. Fledrich, R.M. Stassart, A. Klink, L.M. Rasch, T. Prukop, L. Haag, and et al. Soluble neuregulin-1 modulates disease pathogenesis in rodent models of Charcot-Marie-Tooth disease 1A Nat. Med. 20 2014 1055 1061
227. D. Klein, J. Groh, J. Wettmarshausen, and R. Martini Nonuniform molecular features of myelinating Schwann cells in models for CMT1: distinct disease patterns are associated with NCAM and c-Jun upregulation Glia 62 2014 736 750
228. A. Doring, and V.W. Yong The good, the bad and the ugly. Macrophages/microglia with a focus on myelin repair Front. Biosci. (Sch. Ed.) 3 2011 846 856
229. R. Martini, D. Klein, and J. Groh Similarities between inherited demyelinating neuropathies and Wallerian degeneration: an old repair program may cause myelin and axon perturbation under nonlesion conditions Am. J. Pathol. 183 2013 655 660
230. J. Groh, I. Klein, C. Hollmann, J. Wettmarshausen, D. Klein, and R. Martini CSF-1-activated macrophages are target-directed and essential mediators of Schwann cell dedifferentiation and dysfunction in Cx32-deficient mice Glia 63 2015 977 986
231. D. Klein, J. Groh, A. Weishaupt, and R. Martini Endogenous antibodies contribute to macrophage-mediated demyelination in a mouse model for CMT1B J. Neuroinflamm. 12 2015 49
232. M. Takeda, M. Takahashi, and S. Matsumoto Contribution of the activation of satellite glia in sensory ganglia to pathological pain Neurosci. Biobehav. Rev. 33 2009 784 792
233. R.A. Warwick, and M. Hanani The contribution of satellite glial cells to chemotherapy-induced neuropathic pain Eur. J. Pain 17 2013 571 580
234. M. Hanani, E. Blum, S. Liu, L. Peng, and S. Liang Satellite glial cells in dorsal root ganglia are activated in streptozotocin-treated rodents J. Cell. Mol. Med. 18 2014 2367 2371
235. S. Liu, Q. Shi, Q. Zhu, T. Zou, G. Li, A. Huang, and et al. P2X(7) receptor of rat dorsal root ganglia is involved in the effect of moxibustion on visceral hyperalgesia Purinergic Signal. 11 2015 161 169
236. D.D. Song, Y. Li, D. Tang, L.Y. Huang, and Y.Z. Yuan Neuron-glial communication mediated by TNF-alpha and glial activation in dorsal root ganglia in visceral inflammatory hypersensitivity Am. J. Physiol. Gastrointest. Liver Physiol. 306 2014 G788 95
237. N.P. Goncalves, S. Costelha, and M.J. Saraiva Glial cells in familial amyloidotic polyneuropathy Acta Neuropathol. Commun. 2 2014 177
238. M. Hanani Satellite glial cells in sensory ganglia: from form to function Brain Res. Brain Res. Rev. 48 2005 457 476
239. P.T. Ohara, J.P. Vit, A. Bhargava, M. Romero, C. Sundberg, A.C. Charles, and et al. Gliopathic pain: when satellite glial cells go bad Neuroscientist 15 2009 450 463
240. M. Hanani, T.Y. Huang, P.S. Cherkas, M. Ledda, and E. Pannese Glial cell plasticity in sensory ganglia induced by nerve damage Neuroscience 114 2002 279 283
241. S. Ohtori, K. Takahashi, H. Moriya, and R.R. Myers TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord Spine (Phila. PA 1976) 29 2004 1082 1088
242. M.F. Vesin, Y. Urade, O. Hayaishi, and B. Droz Neuronal and glial prostaglandin D synthase isozymes in chick dorsal root ganglia: a light and electron microscopic immunocytochemical study J. Neurosci. 15 1995 470 476