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Promoting remyelination: utilizing a viral model of demyelination to assess cell-based therapies

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References

  • Gage FH. Mammalian neural stem cells. Science 2000;287(5457):1433-8
  • Temple S. Division and differentiation of isolated CNS blast cells in microculture. Nature 1989;340(6233):471-3
  • Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255(5052):1707-10
  • Brustle O, Jones KN, Learish RD, et al. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999;285(5428):754-6
  • Barberi T, Klivenyi P, Calingasan NY, et al. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 2003;21(10):1200-7
  • Onorati M, Camnasio S, Binetti M, et al. Neuropotent self-renewing neural stem (NS) cells derived from mouse induced pluripotent stem (iPS) cells. Mol Cell Neurosci 2010;43(3):287-95
  • Reubinoff BE, Itsykson P, Turetsky T, et al. Neural progenitors from human embryonic stem cells. Nat Biotechnol 2001;19(12):1134-40
  • Kokaia Z, Martino G, Schwartz M, Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair? Nat Neurosci 2012;15(8):1078-87
  • Bergmann CC, Lane TE, Stohlman SA. Coronavirus infection of the central nervous system: host-virus stand-off. Nat Rev Microbiol 2006;4(2):121-32
  • Yajima K, Suzuki K. Demyelination and remyelination in the rat central nervous system following ethidium bromide injection. Lab Invest 1979;41(5):385-92
  • Hall SM. The effect of injections of lysophosphatidyl choline into white matter of the adult mouse spinal cord. J Cell Sci 1972;10(2):535-46
  • Matsushima GK, Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 2001;11(1):107-16
  • Lane TE, Buchmeier MJ. Murine coronavirus infection: a paradigm for virus-induced demyelinating disease. Trends Microbiol 1997;5(1):9-14
  • Templeton SP, Perlman S. Pathogenesis of acute and chronic central nervous system infection with variants of mouse hepatitis virus, strain JHM. Immunol Res 2007;39(1-3):160-72
  • von Herrath MG, Fujinami RS, Whitton JL. Microorganisms and autoimmunity: making the barren field fertile? Nat Rev Microbiol 2003;1(2):151-7
  • Steinman L. Immunology of relapse and remission in multiple sclerosis. Annu Rev Immunol 2014;32:257-81
  • International Multiple Sclerosis Genetics Consortium. Network-based multiple sclerosis pathway analysis with GWAS data from 15,000 cases and 30,000 controls. Am J Hum Genet 2013;92(6):854-65
  • International Multiple Sclerosis Genetics Consortium; Wellcome Trust Case Control Consortium. Sawcer S, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011;476(7359):214-19
  • Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol 2007;61(4):288-99
  • Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part II: noninfectious factors. Ann Neurol 2007;61(6):504-13
  • Haines JL, Terwedow HA, Burgess K, et al. Linkage of the MHC to familial multiple sclerosis suggests genetic heterogeneity. The Multiple Sclerosis Genetics Group. Hum Mol Genet 1998;7(8):1229-34
  • Barcellos LF, Sawcer S, Ramsay PP, et al. Heterogeneity at the HLA-DRB1 locus and risk for multiple sclerosis. Hum Mol Genet 2006;15(18):2813-24
  • Lassmann H, Bruck W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol 2007;17(2):210-18
  • Compston A, Coles A. Multiple sclerosis. Lancet 2002;359(9313):1221-31
  • Kornek B, Storch MK, Weissert R, et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 2000;157(1):267-76
  • Chang A, Tourtellotte WW, Rudick R, Trapp BD. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002;346(3):165-73
  • Chang A, Nishiyama A, Peterson J, et al. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000;20(17):6404-12
  • Traugott U, Reinherz EL, Raine CS. Multiple sclerosis: distribution of T cell subsets within active chronic lesions. Science 1983;219(4582):308-10
  • Neumann H, Medana IM, Bauer J, Lassmann H. Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases. Trends Neurosci 2002;25(6):313-19
  • Prineas JW, Kwon EE, Goldenberg PZ, et al. Multiple sclerosis. Oligodendrocyte proliferation and differentiation in fresh lesions. Lab Invest 1989;61(5):489-503
  • Lucchinetti C, Bruck W, Parisi J, et al. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 1999;122(Pt 12):2279-95
  • Roy NS, Wang S, Harrison-Restelli C, et al. Identification, isolation, and promoter-defined separation of mitotic oligodendrocyte progenitor cells from the adult human subcortical white matter. J Neurosci 1999;19(22):9986-95
  • Lassmann H. Comparative neuropathology of chronic experimental allergic encephalomyelitis and multiple sclerosis. Schriftenr Neurol 1983;25:1-135
  • Schlesinger H. Zur Frage der akuten multiplen Sklerose und der encephalomyelitis disseminata im Kindesalter. Arb Neurol Inst [Wien] 1909;17:410-32
  • Halfpenny C, Benn T, Scolding N. Cell transplantation, myelin repair, and multiple sclerosis. Lancet neurology 2002;1(1):31-40
  • Kremenchutzky M, Rice GP, Baskerville J, et al. The natural history of multiple sclerosis: a geographically based study 9: observations on the progressive phase of the disease. Brain 2006;129(Pt 3):584-94
  • Antel J, Antel S, Caramanos Z, et al. Primary progressive multiple sclerosis: part of the MS disease spectrum or separate disease entity? Acta Neuropathol 2012;123(5):627-38
  • Trapp BD, Peterson J, Ransohoff RM, et al. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338(5):278-85
  • Peterson JW, Bo L, Mork S, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001;50(3):389-400
  • Bjartmar C, Wujek JR, Trapp BD. Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. J Neurol Sci 2003;206(2):165-71
  • Prineas JW, Wright RG. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 1978;38(4):409-21
  • Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998;18(2):601-9
  • Hauser SL, Chan JR, Oksenberg JR. Multiple sclerosis: prospects and promise. Ann Neurol 2013;74(3):317-27
  • Hochmeister S, Grundtner R, Bauer J, et al. Dysferlin is a new marker for leaky brain blood vessels in multiple sclerosis. J Neuropathol Exp Neurol 2006;65(9):855-65
  • Cristofanilli M, Harris VK, Zigelbaum A, et al. Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice. Stem Cells Dev 2011;20(12):2065-76
  • Harris VK, Yan QJ, Vyshkina T, et al. Clinical and pathological effects of intrathecal injection of mesenchymal stem cell-derived neural progenitors in an experimental model of multiple sclerosis. J Neurol Sci 2012;313(1-2):167-77
  • Harris VK, Faroqui R, Vyshkina T, Sadiq SA. Characterization of autologous mesenchymal stem cell-derived neural progenitors as a feasible source of stem cells for central nervous system applications in multiple sclerosis. Stem cells translational medicine 2012;1(7):536-47
  • Cristofanilli M, Cymring B, Lu A, et al. Cerebrospinal fluid derived from progressive multiple sclerosis patients promotes neuronal and oligodendroglial differentiation of human neural precursor cells in vitro. Neuroscience 2013;250:614-21
  • Gupta N, Henry RG, Strober J, et al. Neural stem cell engraftment and myelination in the human brain. Sci Transl Med 2012;4(155):155ra137
  • Wang FI, Hinton DR, Gilmore W, et al. Sequential infection of glial cells by the murine hepatitis virus JHM strain (MHV-4) leads to a characteristic distribution of demyelination. Lab Invest 1992;66(6):744-54
  • Fleming JO, Trousdale MD, Elzaatari FAK, et al. Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal-antibodies. J Virol 1986;58(3):869-75
  • Parra B, Hinton DR, Lin MT, et al. Kinetics of cytokine mRNA expression in the central nervous system following lethal and nonlethal coronavirus-induced acute encephalomyelitis. Virology 1997;233(2):260-70
  • Pearce BD, Hobbs MV, McGraw TS, Buchmeier MJ. Cytokine induction during T-cell-mediated clearance of mouse hepatitis virus from neurons in vivo. J Virol 1994;68(9):5483-95
  • Ireland DD, Stohlman SA, Hinton DR, et al. Type I interferons are essential in controlling neurotropic coronavirus infection irrespective of functional CD8 T cells. J Virol 2008;82(1):300-10
  • Smith AL, Barthold SW, Beck DS. Intranasally administered alpha/beta interferon prevents extension of mouse hepatitis virus, strain JHM, into the brains of BALB/cByJ mice. Antiviral Res 1987;8(5-6):239-45
  • Minagawa H, Takenaka A, Mohri S, Mori R. Protective effect of recombinant murine interferon beta against mouse hepatitis virus infection. Antiviral Res 1987;8(2):85-95
  • Yong VW, Zabad RK, Agrawal S, et al. Elevation of matrix metalloproteinases (MMPs) in multiple sclerosis and impact of immunomodulators. J Neurol Sci 2007;259(1-2):79-84
  • Hosking MP, Liu L, Ransohoff RM, Lane TE. A protective role for ELR+ chemokines during acute viral encephalomyelitis. PLoS Pathog 2009;5(11):e1000648
  • Savarin C, Stohlman SA, Atkinson R, et al. Monocytes regulate T cell migration through the glia limitans during acute viral encephalitis. J Virol 2010;84(10):4878-88
  • Zhou J, Stohlman SA, Atkinson R, et al. Matrix metalloproteinase expression correlates with virulence following neurotropic mouse hepatitis virus infection. J Virol 2002;76(15):7374-84
  • Zhou J, Stohlman SA, Hinton DR, Marten NW. Neutrophils promote mononuclear cell infiltration during viral-induced encephalitis. J Immunol 2003;170(6):3331-6
  • Phares TW, Stohlman SA, Hwang M, et al. CD4 T Cells Promote CD8 T Cell Immunity at the Priming and Effector Site during Viral Encephalitis. J Virol 2012;86(5):2416-27
  • Zhou J, Hinton DR, Stohlman SA, et al. Maintenance of CD8+ T cells during acute viral infection of the central nervous system requires CD4+ T cells but not interleukin-2. Viral Immunol 2005;18(1):162-9
  • Bergmann CC, Parra B, Hinton DR, et al. Perforin-mediated effector function within the central nervous system requires IFN-gamma-mediated MHC up-regulation. J Immunol 2003;170(6):3204-13
  • Ramakrishna C, Stohlman SA, Atkinson RA, et al. Differential regulation of primary and secondary CD8(+) T cells in the central nervous system. J Immunol 2004;173(10):6265-73
  • Parra B, Hinton DR, Marten NW, et al. IFN-gamma is required for viral clearance from central nervous system oligodendroglia. J Immunol 1999;162(3):1641-7
  • Gonzalez JM, Bergmann CC, Ramakrishna C, et al. Inhibition of interferon-gamma signaling in oligodendroglia delays coronavirus clearance without altering demyelination. Am J Pathol 2006;168(3):796-804
  • Lin MT, Stohlman SA, Hinton DR. Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis. J Virol 1997;71(1):383-91
  • Bergmann CC, Parra B, Hinton DR, et al. Perforin and gamma interferon-mediated control of coronavirus central nervous system infection by CD8 T cells in the absence of CD4 T cells. J Virol 2004;78(4):1739-50
  • Parra B, Lin MT, Stohlman SA, et al. Contributions of Fas-Fas ligand interactions to the pathogenesis of mouse hepatitis virus in the central nervous system. J Virol 2000;74(5):2447-50
  • Stohlman SA, Hinton DR. Viral induced demyelination. Brain Pathol 2001;11(1):92-106
  • Wu GF, Perlman S. Macrophage infiltration, but not apoptosis, is correlated with immune-mediated demyelination following murine infection with a neurotropic coronavirus. J Virol 1999;73(10):8771-80
  • Redwine JM, Buchmeier MJ, Evans CF. In vivo expression of major histocompatibility complex molecules on oligodendrocytes and neurons during viral infection. Am J Pathol 2001;159(4):1219-24
  • Fleming JO, Adami C, Pooley J, et al. Mutations associated with viral sequences isolated from mice persistently infected with MHV-JHM. Adv Exp Med Biol 1995;380:591-5
  • Rowe CL, Baker SC, Nathan MJ, Fleming JO. Evolution of mouse hepatitis virus: detection and characterization of spike deletion variants during persistent infection. J Virol 1997;71(4):2959-69
  • Adami C, Pooley J, Glomb J, et al. Evolution of mouse hepatitis virus (MHV) during chronic infection: quasispecies nature of the persisting MHV RNA. Virology 1995;209(2):337-46
  • Dandekar AA, Wu GF, Pewe L, Perlman S. Axonal damage is T cell mediated and occurs concomitantly with demyelination in mice infected with a neurotropic coronavirus. J Virol 2001;75(13):6115-20
  • Das Sarma J, Kenyon LC, Hingley ST, Shindler KS. Mechanisms of primary axonal damage in a viral model of multiple sclerosis. J Neurosci 2009;29(33):10272-80
  • Pewe L, Perlman S. Cutting edge: CD8 T cell-mediated demyelination is IFN-gamma dependent in mice infected with a neurotropic coronavirus. J Immunol 2002;168(4):1547-51
  • Lane TE, Liu MT, Chen BP, et al. A central role for CD4(+) T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J Virol 2000;74(3):1415-24
  • Horiuchi M, Itoh A, Pleasure D, Itoh T. MEK-ERK signaling is involved in interferon-gamma-induced death of oligodendroglial progenitor cells. J Biol Chem 2006;281(29):20095-106
  • Chew LJ, King WC, Kennedy A, Gallo V. Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 2005;52(2):127-43
  • Balabanov R, Strand K, Kemper A, et al. Suppressor of cytokine signaling 1 expression protects oligodendrocytes from the deleterious effects of interferon-gamma. J Neurosci 2006;26(19):5143-52
  • Baerwald KD, Popko B. Developing and mature oligodendrocytes respond differently to the immune cytokine interferon-gamma. J Neurosci Res 1998;52(2):230-9
  • Wang Y, Ren Z, Tao D, et al. STAT1/IRF-1 signaling pathway mediates the injurious effect of interferon-gamma on oligodendrocyte progenitor cells. Glia 2010;58(2):195-208
  • Lin WS, Kunkler PE, Harding HP, et al. Enhanced Integrated Stress Response Promotes Myelinating Oligodendrocyte Survival in Response to Interferon-gamma. Am. J. Pathol 2008;173(5):1508-17
  • Vartanian T, Li Y, Zhao M, Stefansson K. Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol Med 1995;1(7):732-43
  • Fleury HJA, Sheppard RD, Bornstein MB, Raine CS. Further ultrastructural observations of virus morphogenesis and myelin pathology in JHM virus encephalomyelitis. Neuropathol Appl Neurobiol 1980;6(3):165-79
  • Templeton SP, Kim TS, O’Malley K, Perlman S. Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathol 2008;18(1):40-51
  • Das Sarma J. Microglia-mediated neuroinflammation is an amplifier of virus-induced neuropathology. J Neurovirol 2014;20(2):122-36
  • Yamasaki R, Lu H, Butovsky O, et al. J Exp Med 2014;211(8):1533-49
  • Armstrong RC, Le TQ, Flint NC, et al. Endogenous cell repair of chronic demyelination. J Neuropathol Exp Neurol 2006(65(3):245-56
  • Keirstead HS, Blakemore WF. The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Adv Exp Med Biol 1999;468:183-97
  • Blakemore WF, Keirstead HS. The origin of remyelinating cells in the central nervous system. J Neuroimmunol 1999;98(1):69-76
  • Liu L, Darnall L, Hu T, et al. Myelin repair is accelerated by inactivating CXCR2 on nonhematopoietic cells. J Neurosci 2010;30(27):9074-83
  • Murtie JC, Zhou YX, Le TQ, et al. PDGF and FGF2 pathways regulate distinct oligodendrocyte lineage responses in experimental demyelination with spontaneous remyelination. Neurobiol Dis 2005;19(1-2):171-82
  • McTigue DM, Tripathi RB. The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem 2008;107(1):1-19
  • Carbajal KS, Miranda JL, Tsukamoto MR, Lane TE. CXCR4 signaling regulates remyelination by endogenous oligodendrocyte progenitor cells in a viral model of demyelination. Glia 2011;59(12):1813-21
  • Tsai HH, Frost E, To V, et al. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 2002;110(3):373-83
  • Armstrong RC, Le TQ, Frost EE, et al. Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J Neurosci 2002;22(19):8574-85
  • Robinson S, Tani M, Strieter RM, et al. The chemokine growth-regulated oncogene-alpha promotes spinal cord oligodendrocyte precursor proliferation. J Neurosci 1998;18(24):10457-63
  • Williams JL, Patel JR, Daniels BP, Klein RS. Targeting CXCR7/ACKR3 as a therapeutic strategy to promote remyelination in the adult central nervous system. J Exp Med 2014;211(5):791-9
  • Totoiu MO, Nistor GI, Lane TE, Keirstead HS. Remyelination, axonal sparing, and locomotor recovery following transplantation of glial-committed progenitor cells into the MHV model of multiple sclerosis. Exp Neurol 2004;187(2):254-65
  • Carbajal KS, Schaumburg C, Strieter R, et al. Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proc Natl Acad Sci USA 2010;107(24):11068-73
  • Hardison JL, Nistor G, Gonzalez R, et al. Transplantation of glial-committed progenitor cells into a viral model of multiple sclerosis induces remyelination in the absence of an attenuated inflammatory response. Exp Neurol 2006;197(2):420-9
  • Whitman LM, Blanc CA, Schaumburg CS, et al. Olig1 function is required for remyelination potential of transplanted neural progenitor cells in a model of viral-induced demyelination. Exp Neurol 2012;235(1):380-7
  • Greenberg ML, Weinger JG, Matheu MP, et al. Two-photon imaging of remyelination of spinal cord axons by engrafted neural precursor cells in a viral model of multiple sclerosis. Proc Natl Acad Sci USA 2014;111(22):E2349-55
  • Faulkner J, Keirstead HS. Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transpl Immunol 2005;15(2):131-42
  • Asterias. Safety Study of GRNOPC1 in Spinal Cord Injury. 2010. Available from: http://clinicaltrials.gov/ct2/show/NCT01217008
  • Chen Z, Phillips LK, Gould E, et al. MHC mismatch inhibits neurogenesis and neuron maturation in stem cell allografts. PLoS One 2011;6(3):e14787
  • Phillips LK, Gould EA, Babu H, et al. Natural killer cell-activating receptor NKG2D mediates innate immune targeting of allogeneic neural progenitor cell grafts. Stem Cells 2013;31(9):1829-39
  • Weinger JG, Weist BM, Plaisted WC, et al.C mismatch results in neural progenitor cell rejection following spinal cord transplantation in a model of viral-induced demyelination. Stem Cells 2012;30(11):2584-95
  • Weinger JG, Plaisted WC, Maciejewski SM, et al. Activating Receptor NKG2D Targets RAE-1-expressing allogeneic neural precursor cells in a viral model of multiple sclerosis stem cells. Stem Cells 2014. [Epub ahead of print]
  • Plaisted WC, Weinger JG, Walsh CM, Lane TE. T cell mediated suppression of neurotropic coronavirus replication in neural precursor cells. Virology 2014;449:235-43
  • Hatch MN, Schaumburg CS, Lane TE, Keirstead HS. Endogenous remyelination is induced by transplant rejection in a viral model of multiple sclerosis. J Neuroimmunol 2009;212(1-2):74-81
  • Keirstead HS, Nistor G, Bernal G, et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 2005;25(19):4694-705
  • Aharonowiz M, Einstein O, Fainstein N, et al. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS One 2008;23(9):e3145
  • Pluchino S, Gritti A, Blezer E, et al. Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates. Ann Neurol 2009;66(3):343-54
  • Chen L, Coleman R, Leang R, et al. Human neural precursor cells promote neurologic recovery in a viral model of multiple sclerosis. Stem Cell Reports 2014;2(6):825-37
  • Marie JC, Letterio JJ, Gavin M, Rudensky AY. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J Exp Med 2005;201(7):1061-1067
  • Anghelina D, Zhao J, Trandem K, Perlman S. Role of regulatory T cells in coronavirus-induced acute encephalitis. Virology 2009;385(2):358-67
  • Trandem K, Anghelina D, Zhao J, Perlman S. Regulatory T cells inhibit T cell proliferation and decrease demyelination in mice chronically infected with a coronavirus. J Immunol 2010;184(8):4391-400

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