Remyelination alters the pattern of myelin in the cerebral cortex

eLife - Tập 9
Jennifer Orthmann‐Murphy1,2, Cody L. Call2, Gian C Molina-Castro2, Yu-Chen Hsieh2, Matthew N. Rasband3, Peter A. Calabresi4, Dwight E. Bergles5,2
1Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States
2The Solomon Snyder Department of Neuroscience, Johns Hopkins University, Baltimore, United States
3Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, United States
4Department of Neurology Johns Hopkins University, Baltimore, United States
5Johns Hopkins University Kavli Neuroscience Discovery Institute, Baltimore, United States

Tóm tắt

Destruction of oligodendrocytes and myelin sheaths in cortical gray matter profoundly alters neural activity and is associated with cognitive disability in multiple sclerosis (MS). Myelin can be restored by regenerating oligodendrocytes from resident progenitors; however, it is not known whether regeneration restores the complex myelination patterns in cortical circuits. Here, we performed time lapse in vivo two photon imaging in somatosensory cortex of adult mice to define the kinetics and specificity of myelin regeneration after acute oligodendrocyte ablation. These longitudinal studies revealed that the pattern of myelination in cortex changed dramatically after regeneration, as new oligodendrocytes were formed in different locations and new sheaths were often established along axon segments previously lacking myelin. Despite the dramatic increase in axonal territory available, oligodendrogenesis was persistently impaired in deeper cortical layers that experienced higher gliosis. Repeated reorganization of myelin patterns in MS may alter circuit function and contribute to cognitive decline.

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Tài liệu tham khảo

Araújo, 2017, Inflammatory demyelination alters subcortical visual circuits, Journal of Neuroinflammation, 14, 10.1186/s12974-017-0936-0

Auer, 2018, Evidence for myelin sheath remodeling in the CNS revealed by in Vivo Imaging, Current Biology, 28, 549, 10.1016/j.cub.2018.01.017

Back, 2005, Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation, Nature Medicine, 11, 966, 10.1038/nm1279

Bacmeister, 2020, Motor learning promotes remyelination via new and surviving oligodendrocytes, Nature Neuroscience, 378, 10.1038/s41593-020-0637-3

Baxi, 2015, Transfer of myelin-reactive th17 cells impairs endogenous remyelination in the central nervous system of cuprizone-fed mice, The Journal of Neuroscience, 35, 8626, 10.1523/JNEUROSCI.3817-14.2015

Baxi, 2017, Lineage tracing reveals dynamic changes in oligodendrocyte precursor cells following cuprizone-induced demyelination, Glia, 65, 2087, 10.1002/glia.23229

Beck, 2018, Improved visualization of cortical lesions in multiple sclerosis using 7T MP2RAGE, American Journal of Neuroradiology, 39, 459, 10.3174/ajnr.A5534

Biteau, 2011, Maintaining tissue homeostasis: dynamic control of somatic stem cell activity, Cell Stem Cell, 9, 402, 10.1016/j.stem.2011.10.004

Bock, 2011, Network anatomy and in vivo physiology of visual cortical neurons, Nature, 471, 177, 10.1038/nature09802

Calabrese, 2012, Cortical lesion load associates with progression of disability in multiple sclerosis, Brain, 135, 2952, 10.1093/brain/aws246

Call CL. 2020. Orthmann-Murphy_Call_etal_2020_Elife. GitHub. 07e1b08. https://github.com/clcall/Orthmann-Murphy_Call_etal_2020_Elife.

Chang, 2000, NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions, The Journal of Neuroscience, 20, 6404, 10.1523/JNEUROSCI.20-17-06404.2000

Chang, 2012, Cortical remyelination: a new target for repair therapies in multiple sclerosis, Annals of Neurology, 72, 918, 10.1002/ana.23693

Chong, 2012, Neurite outgrowth inhibitor Nogo-A establishes spatial segregation and extent of oligodendrocyte myelination, PNAS, 109, 1299, 10.1073/pnas.1113540109

Coman, 2006, Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis, Brain, 129, 3186, 10.1093/brain/awl144

Craner, 2004, Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger, PNAS, 101, 8168, 10.1073/pnas.0402765101

Czopka, 2013, Individual oligodendrocytes have only a few hours in which to generate new myelin sheaths in vivo, Developmental Cell, 25, 599, 10.1016/j.devcel.2013.05.013

Deshmukh, 2013, A regenerative approach to the treatment of multiple sclerosis, Nature, 502, 327, 10.1038/nature12647

Dimou, 2008, Progeny of Olig2-Expressing progenitors in the gray and white matter of the adult mouse cerebral cortex, Journal of Neuroscience, 28, 10434, 10.1523/JNEUROSCI.2831-08.2008

Dupree, 2004, Oligodendrocytes assist in the maintenance of sodium channel clusters independent of the myelin sheath, Neuron Glia Biology, 1, 179, 10.1017/S1740925X04000304

Dutta, 2018, Regulation of myelin structure and conduction velocity by perinodal astrocytes, PNAS, 115, 11832, 10.1073/pnas.1811013115

Early, 2018, An automated high-resolution in vivo screen in zebrafish to identify chemical regulators of myelination, eLife, 7, 10.7554/eLife.35136

England, 1990, Changed distribution of sodium channels along demyelinated axons, PNAS, 87, 6777, 10.1073/pnas.87.17.6777

Filippi, 2014, Ultra-high-field MR imaging in multiple sclerosis, Journal of Neurology, Neurosurgery & Psychiatry, 85, 60, 10.1136/jnnp-2013-305246

Gibson, 2014, Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain, Science, 344, 10.1126/science.1252304

Goebbels, 2017, A neuronal PI(3,4,5)P3-dependent program of oligodendrocyte precursor recruitment and myelination, Nature Neuroscience, 20, 10, 10.1038/nn.4425

Gouw, 2008, Heterogeneity of white matter hyperintensities in Alzheimer's disease: post-mortem quantitative MRI and neuropathology, Brain, 131, 3286, 10.1093/brain/awn265

Gudi, 2009, Regional differences between grey and white matter in cuprizone induced demyelination, Brain Research, 1283, 127, 10.1016/j.brainres.2009.06.005

Gudi, 2017, Synaptophysin is a reliable marker for axonal damage, Journal of Neuropathology & Experimental Neurology, 76, 109, 10.1093/jnen/nlw114

Herranz, 2019, Profiles of cortical inflammation in multiple sclerosis by 11 C-PBR28 MR-PET and 7 tesla imaging, Multiple Sclerosis Journal, 1, 10.1177/1352458519867320

Hill, 2018, Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain, Nature Neuroscience, 21, 683, 10.1038/s41593-018-0120-6

Holtmaat, 2012, Imaging neocortical neurons through a chronic cranial window, Cold Spring Harbor Protocols, 2012, 10.1101/pdb.prot069617

Howell, 2011, Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis, Brain, 134, 2755, 10.1093/brain/awr182

Hughes, 2013, Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain, Nature Neuroscience, 16, 668, 10.1038/nn.3390

Hughes, 2018, Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex, Nature Neuroscience, 21, 696, 10.1038/s41593-018-0121-5

Ihara, 2010, Quantification of myelin loss in frontal lobe white matter in vascular dementia, Alzheimer's disease, and dementia with Lewy bodies, Acta Neuropathologica, 119, 579, 10.1007/s00401-009-0635-8

Jeffery, 1995, Remyelination of mouse spinal cord axons demyelinated by local injection of lysolecithin, Journal of Neurocytology, 24, 775, 10.1007/BF01191213

Kang, 2010, NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration, Neuron, 68, 668, 10.1016/j.neuron.2010.09.009

Kang, 2013, Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis, Nature Neuroscience, 16, 571, 10.1038/nn.3357

Kidd, 1999, Cortical lesions in multiple sclerosis, Brain, 122 ( Pt 1, 17, 10.1093/brain/122.1.17

Kilsdonk, 2013, Multicontrast MR imaging at 7T in multiple sclerosis: highest lesion detection in cortical gray matter with 3D-FLAIR, American Journal of Neuroradiology, 34, 791, 10.3174/ajnr.A3289

Kirby, 2019, Oligodendrocyte precursor cells present antigen and are cytotoxic targets in inflammatory demyelination, Nature Communications, 10, 10.1038/s41467-019-11638-3

Klingseisen, 2019, Oligodendrocyte neurofascin independently regulates both myelin targeting and sheath growth in the CNS, Developmental Cell, 51, 730, 10.1016/j.devcel.2019.10.016

Kotter, 2006, Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation, Journal of Neuroscience, 26, 328, 10.1523/JNEUROSCI.2615-05.2006

Kutzelnigg, 2005, Cortical demyelination and diffuse white matter injury in multiple sclerosis, Brain, 128, 2705, 10.1093/brain/awh641

Lassmann, 1997, Remyelination in multiple sclerosis, Multiple Sclerosis Journal, 3, 133, 10.1177/135245859700300213

Lau, 2012, Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination, Annals of Neurology, 72, 419, 10.1002/ana.23599

Lodato, 2015, Generating neuronal diversity in the mammalian cerebral cortex, Annual Review of Cell and Developmental Biology, 31, 699, 10.1146/annurev-cellbio-100814-125353

Longair, 2011, Simple neurite tracer: open source software for reconstruction, visualization and analysis of neuronal processes, Bioinformatics, 27, 2453, 10.1093/bioinformatics/btr390

Lucchinetti, 2011, Inflammatory cortical demyelination in early multiple sclerosis, New England Journal of Medicine, 365, 2188, 10.1056/NEJMoa1100648

Magliozzi, 2007, Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology, Brain, 130, 1089, 10.1093/brain/awm038

Magliozzi, 2018, MRI of cortical lesions and its use in studying their role in MS pathogenesis and disease course, Brain Pathology, 28, 735, 10.1111/bpa.12642

Matsushima, 2001, The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system, Brain Pathology, 11, 107, 10.1111/j.1750-3639.2001.tb00385.x

McKenzie, 2014, Motor skill learning requires active central myelination, Science, 346, 318, 10.1126/science.1254960

Mei, 2014, Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis, Nature Medicine, 20, 954, 10.1038/nm.3618

Mei, 2016, Accelerated remyelination during inflammatory demyelination prevents axonal loss and improves functional recovery, eLife, 5, 10.7554/eLife.18246

Mi, 2005, LINGO-1 negatively regulates myelination by oligodendrocytes, Nature Neuroscience, 8, 745, 10.1038/nn1460

Micheva, 2016, A large fraction of neocortical myelin ensheathes axons of local inhibitory neurons, eLife, 5, 10.7554/eLife.15784

Miron, 2013, M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination, Nature Neuroscience, 16, 1211, 10.1038/nn.3469

Murtie, 2007, Morphometric analysis of oligodendrocytes in the adult mouse frontal cortex, Journal of Neuroscience Research, 85, 2080, 10.1002/jnr.21339

Neumann, 2019, Metformin restores CNS remyelination capacity by rejuvenating aged stem cells, Cell Stem Cell, 25, 473, 10.1016/j.stem.2019.08.015

Nicaise, 2019, Cellular senescence in progenitor cells contributes to diminished remyelination potential in progressive multiple sclerosis, PNAS, 116, 9030, 10.1073/pnas.1818348116

Nielsen, 2013, Contribution of cortical lesion subtypes at 7T MRI to physical and cognitive performance in MS, Neurology, 81, 641, 10.1212/WNL.0b013e3182a08ce8

Oh, 2019, Imaging outcome measures of neuroprotection and repair in MS, Neurology, 11, 10.1212/WNL.0000000000007099

Parslow, 2014, Sample drift correction following 4D confocal Time-lapse imaging, Journal of Visualized Experiments, 86, 10.3791/51086

Peterson, 2001, Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions, Annals of Neurology, 50, 389, 10.1002/ana.1123

Rankin, 2019, Selective estrogen receptor modulators enhance CNS remyelination independent of estrogen receptors, The Journal of Neuroscience, 39, 2184, 10.1523/JNEUROSCI.1530-18.2019

Ruckh, 2012, Rejuvenation of regeneration in the aging central nervous system, Cell Stem Cell, 10, 96, 10.1016/j.stem.2011.11.019

Samanta, 2015, Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination, Nature, 526, 448, 10.1038/nature14957

Skripuletz, 2008, Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent, The American Journal of Pathology, 172, 1053, 10.2353/ajpath.2008.070850

Snaidero, 2019, Precision in a sea of profusion: myelin replacement triggered by single-cell cortical demyelination, bioRxiv, 10.1101/2019.12.16.877597

Stedehouder, 2017, Fast-spiking parvalbumin interneurons are frequently myelinated in the cerebral cortex of mice and humans, Cerebral Cortex, 27, 5001, 10.1093/cercor/bhx203

Stedehouder, 2017, Myelination of parvalbumin interneurons: a parsimonious locus of pathophysiological convergence in schizophrenia, Molecular Psychiatry, 22, 4, 10.1038/mp.2016.147

Su, 2011, Reactive astrocytes inhibit the survival and differentiation of oligodendrocyte precursor cells by secreted TNF-α, Journal of Neurotrauma, 28, 1089, 10.1089/neu.2010.1597

Susuki, 2016, Submembranous cytoskeletons stabilize nodes of ranvier, Experimental Neurology, 283, 446, 10.1016/j.expneurol.2015.11.012

Tomassy, 2014, Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex, Science, 344, 319, 10.1126/science.1249766

Trapp, 1997, Differentiation and Death of Premyelinating Oligodendrocytes in Developing Rodent Brain, Journal of Cell Biology, 137, 459, 10.1083/jcb.137.2.459

Vega-Riquer, 2019, Five decades of cuprizone, an updated model to replicate demyelinating diseases, Current Neuropharmacology, 17, 129, 10.2174/1570159X15666170717120343

Walhovd, 2014, Unraveling the secrets of white matter--bridging the gap between cellular, animal and human imaging studies, Neuroscience, 276, 2, 10.1016/j.neuroscience.2014.06.058

Werneburg, 2020, Targeted complement inhibition at synapses prevents microglial synaptic engulfment and synapse loss in demyelinating disease, Immunity, 52, 167, 10.1016/j.immuni.2019.12.004

Xiao, 2016, Rapid production of new oligodendrocytes is required in the earliest stages of motor-skill learning, Nature Neuroscience, 19, 1210, 10.1038/nn.4351

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

Young, 2013, Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling, Neuron, 77, 873, 10.1016/j.neuron.2013.01.006

Zhang, 2010, TGFbeta1 induces Jagged1 expression in astrocytes via ALK5 and Smad3 and regulates the balance between oligodendrocyte progenitor proliferation and differentiation, Glia, 58, 964, 10.1002/glia.20978

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Tập 9

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