Act1 mediates IL-17–induced EAE pathogenesis selectively in NG2+ glial cells (original) (raw)

• Sawcer, S. et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476, 214–219 (2011).
  CAS PubMed PubMed Central Google Scholar
• Becher, B., Bechmann, I. & Greter, M. Antigen presentation in autoimmunity and CNS inflammation: how T lymphocytes recognize the brain. J. Mol. Med. (Berl) 84, 532–543 (2006).
  CAS Google Scholar
• Sospedra, M. & Martin, R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23, 683–747 (2005).
  CAS PubMed Google Scholar
• Steinman, L. Multiple sclerosis: a two-stage disease. Nat. Immunol. 2, 762–764 (2001).
  CAS PubMed Google Scholar
• Ransohoff, R.M. Animal models of multiple sclerosis: the good, the bad and the bottom line. Nat. Neurosci. 15, 1074–1077 (2012).
  CAS PubMed PubMed Central Google Scholar
• Stromnes, I.M., Cerretti, L.M., Liggitt, D., Harris, R.A. & Goverman, J.M. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 14, 337–342 (2008).
  CAS PubMed PubMed Central Google Scholar
• Kroenke, M.A., Carlson, T.J., Andjelkovic, A.V. & Segal, B.M. IL-12– and IL-23–modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile and response to cytokine inhibition. J. Exp. Med. 205, 1535–1541 (2008).
  CAS PubMed PubMed Central Google Scholar
• Cua, D.J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744–748 (2003).
  CAS PubMed Google Scholar
• Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. & Stockinger, B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17–producing T cells. Immunity 24, 179–189 (2006).
  CAS PubMed Google Scholar
• Mangan, P.R. et al. Transforming growth factor–beta induces development of the T(H)17 lineage. Nature 441, 231–234 (2006).
  CAS PubMed Google Scholar
• Komiyama, Y. et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177, 566–573 (2006).
  CAS PubMed Google Scholar
• Hu, Y. et al. IL-17RC is required for IL-17A– and IL-17F–dependent signaling and the pathogenesis of experimental autoimmune encephalomyelitis. J. Immunol. 184, 4307–4316 (2010).
  CAS PubMed Google Scholar
• Li, X. et al. Act1, an NF-kappa B–activating protein. Proc. Natl. Acad. Sci. USA 97, 10489–10493 (2000).
  CAS PubMed PubMed Central Google Scholar
• Leonardi, A., Chariot, A., Claudio, E., Cunningham, K. & Siebenlist, U. CIKS, a connection to Ikappa B kinase and stress-activated protein kinase. Proc. Natl. Acad. Sci. USA 97, 10494–10499 (2000).
  CAS PubMed PubMed Central Google Scholar
• Qian, Y., Zhao, Z., Jiang, Z. & Li, X. Role of NF kappa B activator Act1 in CD40-mediated signaling in epithelial cells. Proc. Natl. Acad. Sci. USA 99, 9386–9391 (2002).
  CAS PubMed PubMed Central Google Scholar
• Qian, Y. et al. The adaptor Act1 is required for interleukin 17–dependent signaling associated with autoimmune and inflammatory disease. Nat. Immunol. 8, 247–256 (2007).
  CAS PubMed Google Scholar
• Kang, Z. et al. Astrocyte-restricted ablation of interleukin-17–induced Act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity 32, 414–425 (2010).
  CAS PubMed PubMed Central Google Scholar
• Raasch, J. et al. IkappaB kinase 2 determines oligodendrocyte loss by non-cell-autonomous activation of NF-kappaB in the central nervous system. Brain 134, 1184–1198 (2011).
  PubMed PubMed Central Google Scholar
• van Loo, G. et al. Inhibition of transcription factor NF-κB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat. Immunol. 7, 954–961 (2006).
  CAS PubMed Google Scholar
• Nishiyama, A., Komitova, M., Suzuki, R. & Zhu, X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9–22 (2009).
  CAS PubMed Google Scholar
• Richardson, W.D., Young, K.M., Tripathi, R.B. & McKenzie, I. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron 70, 661–673 (2011).
  CAS PubMed PubMed Central Google Scholar
• Gold, R., Linington, C. & Lassmann, H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129, 1953–1971 (2006).
  PubMed Google Scholar
• Weaver, A. et al. An elevated matrix metalloproteinase (MMP) in an animal model of multiple sclerosis is protective by affecting Th1/Th2 polarization. FASEB J. 19, 1668–1670 (2005).
  CAS PubMed Google Scholar
• Yan, Y. et al. CNS-specific therapy for ongoing EAE by silencing IL-17 pathway in astrocytes. Mol. Ther. 20, 1338–1348 (2012).
  CAS PubMed PubMed Central Google Scholar
• Siffrin, V. et al. In vivo imaging of partially reversible Th17 cell–induced neuronal dysfunction in the course of encephalomyelitis. Immunity 33, 424–436 (2010).
  CAS PubMed Google Scholar
• Baumann, N. & Pham-Dinh, D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 81, 871–927 (2001).
  CAS PubMed Google Scholar
• Fancy, S.P., Chan, J.R., Baranzini, S.E., Franklin, R.J. & Rowitch, D.H. Myelin regeneration: a recapitulation of development? Annu. Rev. Neurosci. 34, 21–43 (2011).
  CAS PubMed Google Scholar
• Trotter, J., Karram, K. & Nishiyama, A. NG2 cells: Properties, progeny and origin. Brain Res. Rev. 63, 72–82 (2010).
  CAS PubMed PubMed Central Google Scholar
• Menn, B. et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907–7918 (2006).
  CAS PubMed PubMed Central Google Scholar
• Zhu, X., Bergles, D.E. & Nishiyama, A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145–157 (2008).
  CAS PubMed Google Scholar
• Emery, B. et al. Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138, 172–185 (2009).
  CAS PubMed PubMed Central Google Scholar
• Zhou, Q., Wang, S. & Anderson, D.J. Identification of a novel family of oligodendrocyte lineage–specific basic helix-loop-helix transcription factors. Neuron 25, 331–343 (2000).
  CAS PubMed Google Scholar
• Schüller, U. et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14, 123–134 (2008).
  PubMed PubMed Central Google Scholar
• Yu, W.P., Collarini, E.J., Pringle, N.P. & Richardson, W.D. Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12, 1353–1362 (1994).
  CAS PubMed Google Scholar
• Lappe-Siefke, C. et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33, 366–374 (2003).
  CAS PubMed Google Scholar
• Dugas, J.C. et al. Dicer1 and miR-219 are required for normal oligodendrocyte differentiation and myelination. Neuron 65, 597–611 (2010).
  CAS PubMed PubMed Central Google Scholar
• Kaga, Y. et al. Mice with conditional inactivation of fibroblast growth factor receptor-2 signaling in oligodendrocytes have normal myelin, but display dramatic hyperactivity when combined with Cnp1 inactivation. J. Neurosci. 26, 12339–12350 (2006).
  CAS PubMed PubMed Central Google Scholar
• Paintlia, M.K., Paintlia, A.S., Singh, A.K. & Singh, I. Synergistic activity of interleukin-17 and tumor necrosis factor-alpha enhances oxidative stress-mediated oligodendrocyte apoptosis. J. Neurochem. 116, 508–521 (2011).
  CAS PubMed PubMed Central Google Scholar
• Furuta, S. et al. IL-25 causes apoptosis of IL-25R–expressing breast cancer cells without toxicity to nonmalignant cells. Sci. Transl. Med. 3, 78ra31 (2011).
  PubMed PubMed Central Google Scholar
• Simon, C., Gotz, M. & Dimou, L. Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59, 869–881 (2011).
  PubMed Google Scholar
• Nishiyama, A., Chang, A. & Trapp, B.D. NG2+ glial cells: a novel glial cell population in the adult brain. J. Neuropathol. Exp. Neurol. 58, 1113–1124 (1999).
  CAS PubMed Google Scholar
• Lee, Y. et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487, 443–448 (2012).
  CAS PubMed PubMed Central Google Scholar
• Fünfschilling, U. et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485, 517–521 (2012).
  PubMed PubMed Central Google Scholar
• Butts, B.D., Houde, C. & Mehmet, H. Maturation-dependent sensitivity of oligodendrocyte lineage cells to apoptosis: implications for normal development and disease. Cell Death Differ. 15, 1178–1186 (2008).
  CAS PubMed Google Scholar
• Franklin, R.J. & Ffrench-Constant, C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9, 839–855 (2008).
  CAS PubMed Google Scholar
• Lev, N., Barhum, Y., Melamed, E. & Offen, D. Bax-ablation attenuates experimental autoimmune encephalomyelitis in mice. Neurosci. Lett. 359, 139–142 (2004).
  CAS PubMed Google Scholar
• Hisahara, S., Okano, H. & Miura, M. Caspase-mediated oligodendrocyte cell death in the pathogenesis of autoimmune demyelination. Neurosci. Res. 46, 387–397 (2003).
  CAS PubMed Google Scholar
• Mc Guire, C., Beyaert, R. & van Loo, G. Death receptor signaling in central nervous system inflammation and demyelination. Trends Neurosci. 34, 619–628 (2011).
  CAS PubMed Google Scholar
• Hara, H., Nanri, Y., Tabata, E., Mitsutake, S. & Tabira, T. Identification of astrocyte-derived immune suppressor factor that induces apoptosis of autoreactive T cells. J. Neuroimmunol. 233, 135–146 (2011).
  CAS PubMed Google Scholar
• Patel, J. & Balabanov, R. Molecular mechanisms of oligodendrocyte injury in multiple sclerosis and experimental autoimmune encephalomyelitis. Int. J. Mol. Sci. 13, 10647–10659 (2012).
  CAS PubMed PubMed Central Google Scholar
• Qian, Y. et al. Act1, a negative regulator in CD40- and BAFF-mediated B cell survival. Immunity 21, 575–587 (2004).
  CAS PubMed Google Scholar
• Bajenaru, M.L. et al. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol. Cell. Biol. 22, 5100–5113 (2002).
  CAS PubMed PubMed Central Google Scholar
• Frugier, T. et al. Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum. Mol. Genet. 9, 849–858 (2000).
  CAS PubMed Google Scholar
• Pedraza, C.E., Monk, R., Lei, J., Hao, Q. & Macklin, W.B. Production, characterization and efficient transfection of highly pure oligodendrocyte precursor cultures from mouse embryonic neural progenitors. Glia 56, 1339–1352 (2008).
  PubMed PubMed Central Google Scholar
• Chen, Y. et al. Isolation and culture of rat and mouse oligodendrocyte precursor cells. Nat. Protoc. 2, 1044–1051 (2007).
  CAS PubMed Google Scholar