Remyelination in multiple sclerosis: from basic science to clinical translation

The Lancet Neurology - Tập 19 - Trang 678-688 - 2020
Catherine Lubetzki1,2, Bernard Zalc1, Anna Williams3, Christine Stadelmann4, Bruno Stankoff1,5
1Sorbonne University, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre National de la Recherche Scientifique (CNRS), Institut du Cerveau (ICM), Groupe Hospitalier APHP-Sorbonne University, Paris, France
2Neurology Department Pitié-Salpêtrière, Groupe Hospitalier APHP-Sorbonne University, Paris, France
3Centre for Regenerative Medicine, University of Edinburgh, Edinburgh, UK
4Institute of Neuropathology, University Medical Center Göttingen, Göttingen, Germany
5Neurology Department Saint-Antoine, Groupe Hospitalier APHP-Sorbonne University, Paris, France

Tài liệu tham khảo

Thompson, 2018, Multiple sclerosis, Lancet, 391, 1622, 10.1016/S0140-6736(18)30481-1 Friese, 2014, Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis, Nat Rev Neurol, 10, 225, 10.1038/nrneurol.2014.37 Singh, 2017, Relationship of acute axonal damage, Wallerian degeneration, and clinical disability in multiple sclerosis, J Neuroinflammation, 14, 57, 10.1186/s12974-017-0831-8 Nasrabady, 2018, White matter changes in Alzheimer's disease: a focus on myelin and oligodendrocytes, Acta Neuropathol Commun, 6, 22, 10.1186/s40478-018-0515-3 Caso, 2016, Insights into white matter damage in Alzheimer's disease: from postmortem to in vivo diffusion tensor MRI studies, Neurodegenerative Diseases, 16, 26, 10.1159/000441422 Rajani, 2018, Reversal of endothelial dysfunction reduces white matter vulnerability in cerebral small vessel disease in rats, Sci Transl Med, 10, 10.1126/scitranslmed.aam9507 Fünfschilling, 2012, Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity, Nature, 485, 517, 10.1038/nature11007 Saab, 2017, Myelin dynamics: protecting and shaping neuronal functions, Curr Opin Neurobiol, 47, 104, 10.1016/j.conb.2017.09.013 Lee, 2012, Oligodendroglia metabolically support axons and contribute to neurodegeneration, Nature, 487, 443, 10.1038/nature11314 Schirmer, 2018, Oligodendrocyte-encoded Kir4.1 function is required for axonal integrity, eLife, 7, 10.7554/eLife.36428 Larson, 2018, Oligodendrocytes control potassium accumulation in white matter and seizure susceptibility, eLife, 7, 10.7554/eLife.34829 Dendrou, 2015, Immunopathology of multiple sclerosis, Nat Rev Immunol, 15, 545, 10.1038/nri3871 Waxman, 2004, Na+ channel expression along axons in multiple sclerosis and its models, Trends Pharmacol Sci, 25, 584, 10.1016/j.tips.2004.09.001 Schirmer, 2014, Differential loss of KIR4.1 immunoreactivity in multiple sclerosis lesions, Ann Neurol, 75, 810, 10.1002/ana.24168 Schultz, 2017, Acutely damaged axons are remyelinated in multiple sclerosis and experimental models of demyelination, Glia, 65, 1350, 10.1002/glia.23167 Kornek, 2000, Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions, Am J Pathol, 157, 267, 10.1016/S0002-9440(10)64537-3 Lassmann, 2017, Multiple sclerosis: experimental models and reality, Acta Neuropathol, 133, 223, 10.1007/s00401-016-1631-4 Irvine, 2008, Remyelination protects axons from demyelination-associated axon degeneration, Brain, 131, 1464, 10.1093/brain/awn080 Mei, 2016, Accelerated remyelination during inflammatory demyelination prevents axonal loss and improves functional recovery, eLife, 5, 10.7554/eLife.18246 Duncan, 2009, Extensive remyelination of the CNS leads to functional recovery, Proc Natl Acad Sci USA, 106, 6832, 10.1073/pnas.0812500106 Chang, 2012, Cortical remyelination: a new target for repair therapies in multiple sclerosis, Ann Neurol, 72, 918, 10.1002/ana.23693 Battefeld, 2016, Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity, Nat Commun, 7, 10.1038/ncomms11298 Manrique-Hoyos, 2012, Late motor decline after accomplished remyelination: impact for progressive multiple sclerosis, Ann Neurol, 71, 227, 10.1002/ana.22681 Chen, 2008, Magnetization transfer ratio evolution with demyelination and remyelination in multiple sclerosis lesions, Ann Neurol, 63, 254, 10.1002/ana.21302 Brown, 2014, Imaging of repeated episodes of demyelination and remyelination in multiple sclerosis, Neuroimage Clin, 6, 20, 10.1016/j.nicl.2014.06.009 Petiet, 2019, Ultrahigh field imaging of myelin disease models: toward specific markers of myelin integrity?, J Comp Neurol, 527, 2179, 10.1002/cne.24598 Fujiyoshi, 2016, Application of q-space diffusion MRI for the visualization of white matter, J Neurosci, 36, 2796, 10.1523/JNEUROSCI.1770-15.2016 Stankoff, 2011, Imaging central nervous system myelin by positron emission tomography in multiple sclerosis using [methyl-11C]-2-(4′-methylaminophenyl)- 6-hydroxybenzothiazole, Ann Neurol, 69, 673, 10.1002/ana.22320 Wu, 2013, Longitudinal positron emission tomography imaging for monitoring myelin repair in the spinal cord, Ann Neurol, 74, 688, 10.1002/ana.23965 Bodini, 2016, Dynamic imaging of individual remyelination profiles in multiple sclerosis, Ann Neurol, 79, 726, 10.1002/ana.24620 Franklin, 2017, Regenerating CNS myelin—from mechanisms to experimental medicines, Nat Rev Neurosci, 18, 753, 10.1038/nrn.2017.136 Zawadzka, 2010, CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination, Cell Stem Cell, 6, 578, 10.1016/j.stem.2010.04.002 Piaton, 2011, Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system, Brain, 134, 1156, 10.1093/brain/awr022 Boyd, 2013, Insufficient OPC migration into demyelinated lesions is a cause of poor remyelination in MS and mouse models, Acta Neuropathol, 125, 841, 10.1007/s00401-013-1112-y Xing, 2014, Adult neural precursor cells from the subventricular zone contribute significantly to oligodendrocyte regeneration and remyelination, J Neurosci, 34, 14128, 10.1523/JNEUROSCI.3491-13.2014 Remaud, 2017, Transient hypothyroidism favors oligodendrocyte generation providing functional remyelination in the adult mouse brain, eLife, 6, 10.7554/eLife.29996 Duncan, 2018, The adult oligodendrocyte can participate in remyelination, Proc Natl Acad Sci USA, 115, e11807, 10.1073/pnas.1808064115 Lubetzki, 1988, Myelination by oligodendrocytes isolated from 4–6-week-old rat central nervous system and transplanted into newborn shiverer brain, J Neurol Sci, 88, 161, 10.1016/0022-510X(88)90214-6 Périer, 1965, Electron microscopic features of multiple sclerosis lesions, Brain, 88, 937, 10.1093/brain/88.5.937 Prineas, 1979, Remyelination in multiple sclerosis, Ann Neurol, 5, 22, 10.1002/ana.410050105 Chang, 2002, Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis, N Engl J Med, 346, 165, 10.1056/NEJMoa010994 Bunge, 1961, Ultrastructural study of remyelination in an experimental lesion in adult cat spinal cord, J Biophys Biochem Cytol, 10, 67, 10.1083/jcb.10.1.67 Blakemore, 1974, Pattern of remyelination in the CNS, Nature, 249, 577, 10.1038/249577a0 Neumann, 2020, Problems and pitfalls of identifying remyelination in multiple sclerosis, Cell Stem Cell, 26, 617, 10.1016/j.stem.2020.03.017 Schmierer, 2004, Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain, Ann Neurol, 56, 407, 10.1002/ana.20202 Fard, 2017, BCAS1 expression defines a population of early myelinating oligodendrocytes in multiple sclerosis lesions, Sci Transl Med, 9, 10.1126/scitranslmed.aam7816 Nait-Oumesmar, 2007, Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors, Proc Natl Acad Sci USA, 104, 4694, 10.1073/pnas.0606835104 Yeung, 2014, Dynamics of oligodendrocyte generation and myelination in the human brain, Cell, 159, 766, 10.1016/j.cell.2014.10.011 Yeung, 2019, Dynamics of oligodendrocyte generation in multiple sclerosis, Nature, 566, 538, 10.1038/s41586-018-0842-3 Jäkel, 2019, Altered human oligodendrocyte heterogeneity in multiple sclerosis, Nature, 566, 543, 10.1038/s41586-019-0903-2 Moyon, 2015, Demyelination causes adult CNS progenitors to revert to an immature state and express immune cues that support their migration, J Neurosci, 35, 4, 10.1523/JNEUROSCI.0849-14.2015 Stangel, 2017, Achievements and obstacles of remyelinating therapies in multiple sclerosis, Nat Rev Neurol, 13, 742, 10.1038/nrneurol.2017.139 Woodruff, 2004, Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination, Mol Cell Neurosci, 25, 252, 10.1016/j.mcn.2003.10.014 Wang, 2007, Contrasting effects of mitogenic growth factors on myelination in neuron-oligodendrocyte co-cultures, Glia, 55, 537, 10.1002/glia.20480 Tepavčević, 2014, Early netrin-1 expression impairs central nervous system remyelination, Ann Neurol, 76, 252, 10.1002/ana.24201 Mathieu, 2019, Demyelination-remyelination in the central nervous system: ligand-dependent participation of the Notch signaling pathway, Toxicol Sci, 10.1093/toxsci/kfz130 Mi, 2005, LINGO-1 negatively regulates myelination by oligodendrocytes, Nat Neurosci, 8, 745, 10.1038/nn1460 Fancy, 2009, Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS, Genes Dev, 23, 1571, 10.1101/gad.1806309 Dai, 2014, Stage-specific regulation of oligodendrocyte development by Wnt/β-catenin signaling, J Neurosci, 34, 8467, 10.1523/JNEUROSCI.0311-14.2014 Mei, 2014, Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis, Nat Med, 20, 954, 10.1038/nm.3618 Back, 2005, Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation, Nat Med, 11, 966, 10.1038/nm1279 Pu, 2018, The extracellular matrix: focus on oligodendrocyte biology and targeting CSPGs for remyelination therapies, Glia, 66, 1809, 10.1002/glia.23333 Petersen, 2017, Fibrinogen activates BMP signaling in oligodendrocyte progenitor cells and inhibits remyelination after vascular damage, Neuron, 96, 1003, 10.1016/j.neuron.2017.10.008 Segel, 2019, Niche stiffness underlies the ageing of central nervous system progenitor cells, Nature, 573, 130, 10.1038/s41586-019-1484-9 Huang, 2011, Retinoid X receptor gamma signaling accelerates CNS remyelination, Nat Neurosci, 14, 45, 10.1038/nn.2702 Hartley, 2019, Myelin repair stimulated by CNS-selective thyroid hormone action, JCI Insight, 4, 10.1172/jci.insight.126329 de la Fuente, 2015, Vitamin D receptor-retinoid X receptor heterodimer signaling regulates oligodendrocyte progenitor cell differentiation, J Cell Biol, 211, 975, 10.1083/jcb.201505119 Emery, 2015, Transcriptional and epigenetic regulation of oligodendrocyte development and myelination in the central nervous system, Cold Spring Harb Perspect Biol, 7, 10.1101/cshperspect.a020461 Ulc, 2019, The guanine nucleotide exchange factor Vav3 modulates oligodendrocyte precursor differentiation and supports remyelination in white matter lesions, Glia, 67, 376, 10.1002/glia.23548 Demerens, 1996, Induction of myelination in the central nervous system by electrical activity, Proc Natl Acad Sci USA, 93, 9887, 10.1073/pnas.93.18.9887 Stevens, 1998, Control of myelination by specific patterns of neural impulses, J Neurosci, 18, 9303, 10.1523/JNEUROSCI.18-22-09303.1998 Gibson, 2014, Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain, Science, 344, 10.1126/science.1252304 Koudelka, 2016, Individual neuronal subtypes exhibit diversity in CNS myelination mediated by synaptic vesicle release, Curr Biol, 26, 1447, 10.1016/j.cub.2016.03.070 Mitew, 2018, Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner, Nat Commun, 9, 306, 10.1038/s41467-017-02719-2 Stedehouder, 2018, Activity-dependent myelination of parvalbumin interneurons mediated by axonal morphological plasticity, J Neurosci, 38, 3631, 10.1523/JNEUROSCI.0074-18.2018 Bergles, 2000, Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus, Nature, 405, 187, 10.1038/35012083 Wake, 2015, Nonsynaptic junctions on myelinating glia promote preferential myelination of electrically active axons, Nat Commun, 6, 10.1038/ncomms8844 Wake, 2011, Control of local protein synthesis and initial events in myelination by action potentials, Science, 333, 1647, 10.1126/science.1206998 Fields, 2015, A new mechanism of nervous system plasticity: activity-dependent myelination, Nat Rev Neurosci, 16, 756, 10.1038/nrn4023 Gautier, 2015, Neuronal activity regulates remyelination via glutamate signalling to oligodendrocyte progenitors, Nat Commun, 6, 10.1038/ncomms9518 Ortiz, 2019, Neuronal activity in vivo enhances functional myelin repair, JCI Insight, 5 Jensen, 2018, Multimodal enhancement of remyelination by exercise with a pivotal role for oligodendroglial PGC1α, Cell Rep, 24, 3167, 10.1016/j.celrep.2018.08.060 Lubetzki, 1993, Even in culture, oligodendrocytes myelinate solely axons, Proc Natl Acad Sci USA, 90, 6820, 10.1073/pnas.90.14.6820 Bechler, 2015, CNS myelin sheath lengths are an intrinsic property of oligodendrocytes, Curr Biol, 25, 2411, 10.1016/j.cub.2015.07.056 Bechler, 2018, Intrinsic and adaptive myelination—a sequential mechanism for smart wiring in the brain, Dev Neurobiol, 78, 68, 10.1002/dneu.22518 Bieber, 2003, Efficient central nervous system remyelination requires T cells, Ann Neurol, 53, 680, 10.1002/ana.10578 Dombrowski, 2017, Regulatory T cells promote myelin regeneration in the central nervous system, Nat Neurosci, 20, 674, 10.1038/nn.4528 Baxi, 2015, Transfer of myelin-reactive th17 cells impairs endogenous remyelination in the central nervous system of cuprizone-fed mice, J Neurosci, 35, 8626, 10.1523/JNEUROSCI.3817-14.2015 El Behi, 2017, Adaptive human immunity drives remyelination in a mouse model of demyelination, Brain, 140, 967, 10.1093/brain/awx008 Zrzavy, 2017, Loss of ‘homeostatic’ microglia and patterns of their activation in active multiple sclerosis, Brain, 140, 1900, 10.1093/brain/awx113 Peferoen, 2015, Activation status of human microglia is dependent on lesion formation stage and remyelination in multiple sclerosis, J Neuropathol Exp Neurol, 74, 48, 10.1097/NEN.0000000000000149 Ransohoff, 2016, A polarizing question: do M1 and M2 microglia exist?, Nat Neurosci, 19, 987, 10.1038/nn.4338 Stratoulias, 2019, Microglial subtypes: diversity within the microglial community, EMBO J, 38, 10.15252/embj.2019101997 Masuda, 2019, Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution, Nature, 566, 388, 10.1038/s41586-019-0924-x Kremer, 2019, pHERV-W envelope protein fuels microglial cell-dependent damage of myelinated axons in multiple sclerosis, Proc Natl Acad Sci USA, 116, 15216, 10.1073/pnas.1901283116 Kotter, 2001, Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination, Glia, 35, 204, 10.1002/glia.1085 Lloyd, 2019, The pro-remyelination properties of microglia in the central nervous system, Nat Rev Neurol, 15, 447, 10.1038/s41582-019-0184-2 Ruckh, 2012, Rejuvenation of regeneration in the aging central nervous system, Cell Stem Cell, 10, 96, 10.1016/j.stem.2011.11.019 Lloyd, 2019, Central nervous system regeneration is driven by microglia necroptosis and repopulation, Nat Neurosci, 22, 1046, 10.1038/s41593-019-0418-z Miron, 2017, Microglia-driven regulation of oligodendrocyte lineage cells, myelination, and remyelination, J Leukoc Biol, 101, 1103, 10.1189/jlb.3RI1116-494R Miron, 2013, M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination, Nat Neurosci, 16, 1211, 10.1038/nn.3469 Arnett, 2001, TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination, Nat Neurosci, 4, 1116, 10.1038/nn738 Cunha, 2020, Pro-inflammatory activation following demyelination is required for myelin clearance and oligodendrogenesis, J Exp Med, 217, 10.1084/jem.20191390 Nörenberg, 2011, Clemastine potentiates the human P2X7 receptor by sensitizing it to lower ATP concentrations, J Biol Chem, 286, 11067, 10.1074/jbc.M110.198879 Wang, 2015, Quetiapine inhibits microglial activation by neutralizing abnormal STIM1-mediated intercellular calcium homeostasis and promotes myelin repair in a cuprizone-induced mouse model of demyelination, Front Cell Neurosci, 9, 492, 10.3389/fncel.2015.00492 Deshmukh, 2013, A regenerative approach to the treatment of multiple sclerosis, Nature, 502, 327, 10.1038/nature12647 Najm, 2015, Drug-based modulation of endogenous stem cells promotes functional remyelination in vivo, Nature, 522, 216, 10.1038/nature14335 Stankoff, 2002, Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules, J Neurosci, 22, 9221, 10.1523/JNEUROSCI.22-21-09221.2002 Mei, 2014, Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis, Nat Med, 20, 954, 10.1038/nm.3618 Buckley, 2010, Drug reprofiling using zebrafish identifies novel compounds with potential pro-myelination effects, Neuropharmacology, 59, 149, 10.1016/j.neuropharm.2010.04.014 Mannioui, 2018, The Xenopus tadpole: an in vivo model to screen drugs favoring remyelination, Mult Scler, 24, 1421, 10.1177/1352458517721355 Hubler, 2018, Accumulation of 8,9-unsaturated sterols drives oligodendrocyte formation and remyelination, Nature, 560, 372, 10.1038/s41586-018-0360-3 Rankin, 2019, Selective estrogen receptor modulators enhance CNS remyelination independent of estrogen receptors, J Neurosci, 39, 2184, 10.1523/JNEUROSCI.1530-18.2019 Neumann, 2019, Metformin restores CNS remyelination capacity by rejuvenating aged stem cells, Cell Stem Cell, 25, 473, 10.1016/j.stem.2019.08.015 Diebold, 2019, The monoclonal antibody GNbAC1: targeting human endogenous retroviruses in multiple sclerosis, Ther Adv Neurol Disord, 12, 10.1177/1756286419833574 Schwartzbach, 2017, Lesion remyelinating activity of GSK239512 versus placebo in patients with relapsing-remitting multiple sclerosis: a randomised, single-blind, phase II study, J Neurol, 264, 304, 10.1007/s00415-016-8341-7 Cadavid, 2019, Safety and efficacy of opicinumab in patients with relapsing multiple sclerosis (SYNERGY): a randomised, placebo-controlled, phase 2 trial, Lancet Neurol, 18, 845, 10.1016/S1474-4422(19)30137-1 Cadavid, 2017, Safety and efficacy of opicinumab in acute optic neuritis (RENEW): a randomised, placebo-controlled, phase 2 trial, Lancet Neurol, 16, 189, 10.1016/S1474-4422(16)30377-5 Green, 2017, Clemastine fumarate as a remyelinating therapy for multiple sclerosis (ReBUILD): a randomised, controlled, double-blind, crossover trial, Lancet, 390, 2481, 10.1016/S0140-6736(17)32346-2 Zhang, 2019, Evolution of clinical trials in multiple sclerosis, Ther Adv Neurol Disord, 12, 10.1177/1756286419826547