Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation
Abstract
Demyelination is the hallmark of numerous neurodegenerative conditions, including multiple sclerosis. Oligodendrocyte progenitors (OPCs), which normally mature into myelin-forming oligodendrocytes, are typically present around demyelinated lesions but do not remyelinate affected axons. Here, we find that the glycosaminoglycan hyaluronan accumulates in demyelinated lesions from individuals with multiple sclerosis and in mice with experimental autoimmune encephalomyelitis. A high molecular weight (HMW) form of hyaluronan synthesized by astrocytes accumulates in chronic demyelinated lesions. This form of hyaluronan inhibits remyelination after lysolecithin-induced white matter demyelination. OPCs accrue and do not mature into myelin-forming cells in demyelinating lesions where HMW hyaluronan is present. Furthermore, the addition of HMW hyaluronan to OPC cultures reversibly inhibits progenitor-cell maturation, whereas degrading hyaluronan in astrocyte-OPC cocultures promotes oligodendrocyte maturation. HMW hyaluronan may therefore contribute substantially to remyelination failure by preventing the maturation of OPCs that are recruited to demyelinating lesions.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The inability to phagocytose myelin debris in the cuprizone model obstructs aspects of oligodendrocyte biology, including differentiation of OPCs into myelin-producing oligodendrocytes.
“The inability to phagocytose myelin debris in the cuprizone model is known to obstruct aspects of oligodendrocyte biology, including the differentiation of oligodendrocyte precursor cells (OPCs) into myelin-producing oligodendrocytes (Back et al., 2005).”
From SYK coordinates neuroprotective microglial responses in neurodegenerative disease (2022) · cites this paper as Back et al., 2005
Cites
CD44: From adhesion molecules to signalling regulators
Ponta, H., Sherman, L. S., & Herrlich, P. A. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1004 · Cited by 2,393 · see citing works
Self-citationHyaluronan: from extracellular glue to pericellular cue
Toole, B. P. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1391 · Cited by 2,125 · see citing works
Oligosaccharides of Hyaluronan Activate Dendritic Cells via Toll-like Receptor 4
Termeer, C., Benedix, F., Sleeman, J., Fieber, C., Voith, U., Ahrens, T., Miyake, K., Freudenberg, M., Galanos, C., & Simon, J. C. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20001858 · Cited by 1,378 · see citing works
Premyelinating Oligodendrocytes in Chronic Lesions of Multiple Sclerosis
Chang, A., Tourtellotte, W. W., Rudick, R., & Trapp, B. D. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa010994 · Cited by 991 · see citing works
Self-citationWhy does remyelination fail in multiple sclerosis?
Franklin, R. J. M. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn917 · Cited by 837 · see citing works
NG2-Positive Oligodendrocyte Progenitor Cells in Adult Human Brain and Multiple Sclerosis Lesions
Chang, A., Nishiyama, A., Peterson, J. W., Prineas, J. W., & Trapp, B. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06404.2000 · Cited by 711 · see citing works
Self-citationNait‐Oumesmar, B., Decker, L., Lachapelle, F., Avellana‐Adalid, V., Bachelin, C., & Van Evercooren, A. B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00873.x · Cited by 560 · see citing works
Wolswijk, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-02-00601.1998 · Cited by 498 · see citing works
Weigel, P. H., Fuller, G. M., & LeBœuf, R. D. (1986) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(86)80076-5 · Cited by 381 · see citing works
Bebo, B. F., Fyfe-Johnson, A., Adlard, K., Beam, A. G., Vandenbark, A. A., & Offner, H. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.3.2080 · Cited by 341 · see citing works
Scolding, N. J. (1998) · Brain · doi:10.1093/brain/121.12.2221 · Cited by 293 · see citing works
Craig, A., Luo, N. L., Beardsley, D. J., Wingate-Pearse, N., Walker, D. W., Hohimer, A. R., & Back, S. A. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00032-3 · Cited by 283 · see citing works
Self-citationOligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord
Wolswijk, G. (2002) · Brain · doi:10.1093/brain/awf031 · Cited by 268 · see citing works
Glycosaminoglycans of brain during development
Margolis, R. U., Margolis, R. K., Chang, L. B., & Preti, C. (1975) · Biochemistry · doi:10.1021/bi00672a014 · Cited by 250 · see citing works
CD44 expression identifies astrocyte-restricted precursor cells
Liu, Y., Han, S. S. W., Wu, Y., Tuohy, T. M. F., Xue, H., Cai, J., Back, S. A., Sherman, L. S., Fischer, I., & Rao, M. S. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.018 · Cited by 215 · see citing works
Self-citationLiu, Y., Wu, Y.-Y., Lee, J., Xue, H., Pevny, L., Kaprielian, Z., & Rao, M. S. (2002) · Glia · doi:10.1002/glia.10111 · Cited by 169 · see citing works
Self-citationMoseley, R., Waddington, R. J., & Embery, G. (1997) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(97)00083-5 · Cited by 159 · see citing works
Reactive Oxygen Species Contribute to Epidermal Hyaluronan Catabolism in Human Skin Organ Culture
Ågren, U. M., Tammi, R., & Tammi, M. (1997) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(97)00098-1 · Cited by 144 · see citing works
Sampson, P. M., Rochester, C. L., Freundlich, B., & Elias, J. A. (1992) · Journal of Clinical Investigation · doi:10.1172/jci116017 · Cited by 139 · see citing works
Struve, J. N., Maher, P. C., Li, Y., Kinney, S. D., Fehlings, M. G., Kuntz, C., & Sherman, L. S. (2005) · Glia · doi:10.1002/glia.20215 · Cited by 137 · see citing works
Self-citationGirgrah, N., Letarte, M., Becker, L. E., Cruz, T. F., Theriault, E., & Moscarello, M. A. (1991) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199111000-00009 · Cited by 126 · see citing works
Ito, M., Blumberg, B. M., Mock, D. J., Goodman, A. D., Moser, A. B., Moser, H. W., Smith, K. D., & Powers, J. M. (2001) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/60.10.1004 · Cited by 125 · see citing works
Generation of oligodendroglial progenitors from neural stem cells
Zhang, S., Lundberg, C. G., Lipsitz, D., O’Connor, L. T., & Duncan, I. D. (1998) · Journal of Neurocytology · doi:10.1023/a:1006953023845 · Cited by 112 · see citing works
Proliferation of Astroglia and Oligodendroglia in Response to Human T Cell-Derived Factors
Merrill, J. E., Kutsunai, S. Y., Mohlstrom, C., Hofman, F. M., Groopman, J. E., & Golde, D. W. (1984) · Science · doi:10.1126/science.6610212 · Cited by 112 · see citing works
Maeda, Y., Solanky, M., Menonna, J., Chapin, J. C., Li, W., & Dowling, P. C. (2001) · Annals of Neurology · doi:10.1002/ana.1015 · Cited by 111 · see citing works
Akiyama, H., Tooyama, I., Kawamata, T., Ikeda, K., & McGeer, P. L. (1993) · Brain Research · doi:10.1016/0006-8993(93)91160-t · Cited by 107 · see citing works
Jiang, H. N., Peterson, R. S., Wang, W., Bartnik, E., Knudson, C. B., & Knudson, W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m108654200 · Cited by 99 · see citing works
Mummert, M. E., Mummert, D. I., Edelbaum, D., Hui, F., Matsue, H., & Takashima, A. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.8.4322 · Cited by 94 · see citing works
Use of Suppression Subtractive Hybridization for Differential Gene Expression in Stroke
Wang, H., Zhan, Y., Xu, L., Feuerstein, G., & Wang, X. (2001) · Stroke · doi:10.1161/01.str.32.4.1020 · Cited by 85 · see citing works
Classification of demyelinating diseases at the interface between etiology and pathogenesis
Lassmann, H. (2001) · Current Opinion in Neurology · doi:10.1097/00019052-200106000-00001 · Cited by 77 · see citing works
Blakemore, W. F., Gilson, J. M., & Crang, A. J. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00347-9 · Cited by 72 · see citing works
Haegel, H., Tölg, C., Hofmann‐Apitius, M., & Ceredig, R. H. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.5.1067 · Cited by 68 · see citing works
CD44 Expression in Human Astrocytes and Oligodendrocytes in Culture
Moretto, G., Xu, R., & Kim, S. U. (1993) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199307000-00009 · Cited by 67 · see citing works
H-CAM expression in the human nervous system: Evidence for a role in diverse glial interactions
Vogel, H., Butcher, E. C., & Picker, L. J. (1992) · Journal of Neurocytology · doi:10.1007/bf01191704 · Cited by 64 · see citing works
Chari, D. M., & Blakemore, W. F. (2002) · Multiple Sclerosis Journal · doi:10.1191/1352458502ms842oa · Cited by 63 · see citing works
Developmental and Age‐Related Changes in Rat Brain Glycosaminoglycans
Jenkins, H. G., & Bachelard, H. S. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb01134.x · Cited by 63 · see citing works
Tuohy, T. M. F., Wallingford, N. M., Liu, Y., Chan, F. H., Rizvi, T. A., Xing, R., Bebo, B. F., Rao, M. S., & Sherman, L. S. (2004) · Glia · doi:10.1002/glia.20042 · Cited by 61 · see citing works
Self-citationWang, M.-J., Jeng, K.-C. G., Kuo, J., Chen, H.-L., Huang, H.-Y., Chen, W.-F., & Lin, S. (2003) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.10.034 · Cited by 55 · see citing works
Self-citationLynn, B. D., Li, X., Cattini, P. A., Turley, E. A., & Nagy, J. I. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1353 · Cited by 50 · see citing works
The role of chemokines and chemokine receptors in CNS inflammation
Groot, C. J. A. D., & Woodroofe, M. N. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)32101-5 · Cited by 43 · see citing works
Marret, S., Delpech, B., DELPECH, A., Asou, H., Girard, N., Courel, M., Chauzy, C., Maingonnat, C., & Fessard, C. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.62041285.x · Cited by 42 · see citing works
Alfei, L., Aita, M., Caronti, B., Vita, R. D., Margotta, V., Albani, L. M., & Valente, A. M. (1999) · PubMed · Cited by 36 · see citing works
Glycosaminoglycans in Cortical Autopsy Samples from Alzheimer Brain
Jenkins, H. G., & Bachelard, H. S. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb01135.x · Cited by 36 · see citing works
Perosa, S. R., Porcionatto, M. A., Cukiert, A., Martins, J. R. M., Amado, D., Nader, H. B., Cavalheiro, É. A., Leite, J. P., & Naffah‐Mazzacoratti, M. D. G. (2002) · Epilepsia · doi:10.1046/j.1528-1157.43.s.5.30.x · Cited by 31 · see citing works
CD44H is Expressed by cells of the Oligodendrocyte Lineage and by Oligodendrogliomas in Humans
Bouvier, C., Liprandi, A., Monti, G., Pellissier, J. F., & Figarella-Branger, D. F. (2002) · Journal of Neuro-Oncology · doi:10.1023/a:1020630732625 · Cited by 28 · see citing works
Schwann cell tumors express characteristic patterns of CD44 splice variants
Sherman, L. S., Skroch, P., Moll, J., Schwechheimer, K., Ponta, H., Herrlich, P. A., & Hofmann‐Apitius, M. (1995) · Journal of Neuro-Oncology · doi:10.1007/bf01052620 · Cited by 23 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Remodelling the extracellular matrix in development and disease
Bonnans, C., Chou, J., & Werb, Z. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3904 · Cited by 4,367 · see citing works
Remyelination in the CNS: from biology to therapy
Franklin, R. J. M., & ffrench-Constant, C. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2480 · Cited by 1,544 · see citing works
Hyaluronan fragments: An information-rich system
Stern, R., Asari, A., & Sugahara, K. N. (2006) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2006.05.009 · Cited by 1,142 · see citing works
The bioink: A comprehensive review on bioprintable materials
Hospodiuk, M., Dey, M., Sosnoski, D. M., & Ozbolat, I. T. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.12.006 · Cited by 1,139 · see citing works
Hyaluronan as an Immune Regulator in Human Diseases
Jiang, D., Liang, J., & Noble, P. W. (2011) · Physiological Reviews · doi:10.1152/physrev.00052.2009 · Cited by 1,060 · see citing works
Myelination of the Nervous System: Mechanisms and Functions
Nave, K., & Werner, H. B. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013101 · Cited by 1,000 · see citing works
Stem cells for the treatment of neurological disorders
Lindvall, O., & Kokaia, Z. (2006) · Nature · doi:10.1038/nature04960 · Cited by 829 · see citing works
Myelin in the Central Nervous System: Structure, Function, and Pathology
Stadelmann, C., Timmler, S., Barrantes‐Freer, A., & Simons, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00031.2018 · Cited by 735 · see citing works
Regenerating CNS myelin — from mechanisms to experimental medicines
Franklin, R. J. M., & ffrench-Constant, C. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.136 · Cited by 647 · see citing works
Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNSPreprint
Fancy, S. P. J., Baranzini, S. E., Zhao, C., Yuk, D., Irvine, K., Kaing, S., Sanai, N., Franklin, R. J. M., & Rowitch, D. H. (2009) · Genes & Development · doi:10.1101/gad.1806309 · Cited by 639 · see citing works
Pathophysiology of the brain extracellular matrix: a new target for remyelination
Lau, L. W., Cua, R., Keough, M. B., Haylock-Jacobs, S., & Yong, V. W. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3550 · Cited by 549 · see citing works
Seidlits, S. K., Khaing, Z. Z., Petersen, R. R., Nickels, J. D., Vanscoy, J. E., Shear, J. B., & Schmidt, C. E. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.01.125 · Cited by 528 · see citing works
Neurovascular and Cognitive Dysfunction in Hypertension
Iadecola, C., & Gottesman, R. F. (2019) · Circulation Research · doi:10.1161/circresaha.118.313260 · Cited by 518 · see citing works
White matter injury in the preterm infant: pathology and mechanisms
Back, S. A. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1718-6 · Cited by 509 · see citing works
Self-citationShen, S., Sandoval, J., Swiss, V. A., Li, J., Dupree, J. L., Franklin, R. J. M., & Casaccia‐Bonnefil, P. (2008) · Nature Neuroscience · doi:10.1038/nn.2172 · Cited by 486 · see citing works
The cuprizone animal model: new insights into an old story
Kipp, M., Clarner, T., Dang, J., Copray, S., & Beyer, C. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0591-3 · Cited by 481 · see citing works
Non–cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology
Ballas, N., Lioy, D. T., Grunseich, C., & Mandel, G. (2009) · Nature Neuroscience · doi:10.1038/nn.2275 · Cited by 466 · see citing works
The life, death, and replacement of oligodendrocytes in the adult CNS
McTigue, D. M., & Tripathi, R. B. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05570.x · Cited by 455 · see citing works
Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants
Buser, J. R., Maire, J. J., Riddle, A., Gong, X., Nguyen, T. D., Nelson, K., Luo, N. L., Ren, J., Struve, J. N., Sherman, L. S., et al. (2011) · Annals of Neurology · doi:10.1002/ana.22627 · Cited by 447 · see citing works
Self-citationOligodendrocyte, Astrocyte, and Microglia Crosstalk in Myelin Development, Damage, and Repair
Domingues, H. S., Portugal, C. C., Socodato, R., & Relvas, J. B. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00071 · Cited by 438 · see citing works
van der Knaap, M. S., & Bugiani, M. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1739-1 · Cited by 403 · see citing works
The developing oligodendrocyte: key cellular target in brain injury in the premature infant
Volpe, J. J., Kinney, H. C., Jensen, F. E., & Rosenberg, P. A. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.02.012 · Cited by 394 · see citing works
Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy?
Fleiss, B., & Gressèns, P. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70058-3 · Cited by 367 · see citing works
Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through TLR2
Sloane, J. A., Batt, C. E., Ma, Y. C., Harris, Z. M., Trapp, B. D., & Vartanian, T. K. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006496107 · Cited by 362 · see citing works
Self-citationBrain injury in premature neonates: A primary cerebral dysmaturation disorder?
Back, S. A., & Miller, S. P. (2014) · Annals of Neurology · doi:10.1002/ana.24132 · Cited by 360 · see citing works
Self-citationRemyelination in multiple sclerosis: From basic science to clinical translation
Lubetzki, C., Zalc, B., Williams, A., Stadelmann, C., & Stankoff, B. (2020) · The Lancet Neurology · doi:10.1016/s1474-4422(20)30140-x · Cited by 350 · see citing works
Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury
Segovia, K. N., McClure, M., Moravec, M., Luo, N. L., Wan, Y., Gong, X., Riddle, A., Craig, A., Struve, J., Sherman, L. S., et al. (2008) · Annals of Neurology · doi:10.1002/ana.21359 · Cited by 340 · see citing works
Self-citationToll-like receptors in the pathogenesis of neuroinflammation
Kumar, V. (2019) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2019.03.012 · Cited by 331 · see citing works
SYK coordinates neuroprotective microglial responses in neurodegenerative disease
Ennerfelt, H., Frost, E. L., Shapiro, D. A., Holliday, C., Zengeler, K. E., Voithofer, G., Bolte, A. C., Lammert, C. R., Kulas, J. A., Ulland, T. K., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.030 · Cited by 329 · see citing works
“The inability to phagocytose myelin debris in the cuprizone model is known to obstruct aspects of oligodendrocyte biology, including the differentiation of oligodendrocyte precursor cells (OPCs) into myelin-producing oligodendrocytes (Back et al., 2005).”
Myelin Regeneration: A Recapitulation of Development?
Fancy, S. P. J., Chan, J. R., Baranzini, S. E., Franklin, R. J. M., & Rowitch, D. H. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113629 · Cited by 321 · see citing works
Tissue mechanics regulate brain development, homeostasis and disease
Barnes, J. M., Przybyla, L., & Weaver, V. M. (2017) · Journal of Cell Science · doi:10.1242/jcs.191742 · Cited by 313 · see citing works
Astrocytes in multiple sclerosis: A product of their environment
Nair, A., Frederick, T., & Miller, S. D. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8059-5 · Cited by 312 · see citing works
Meinl, E., Krumbholz, M., & Hohlfeld, R. (2006) · Annals of Neurology · doi:10.1002/ana.20890 · Cited by 308 · see citing works
Brain Extracellular Matrix in Neurodegeneration
Bonneh‐Barkay, D., & Wiley, C. A. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00195.x · Cited by 303 · see citing works
Pathology of multiple sclerosis and related inflammatory demyelinating diseases
Kutzelnigg, A., & Lassmann, H. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52001-2.00002-9 · Cited by 302 · see citing works
Astrocytes—Friends or foes in multiple sclerosis?
Williams, A., Piaton, G., & Lubetzki, C. (2007) · Glia · doi:10.1002/glia.20546 · Cited by 301 · see citing works
Mi, S., Miller, R. H., Tang, W., Lee, X., Hu, B., Wu, W., Zhang, Y., Shields, C. B., Zhang, Y., Miklasz, S., et al. (2009) · Annals of Neurology · doi:10.1002/ana.21581 · Cited by 300 · see citing works
van Tilborg, E., de Theije, C. G. M., van Hal, M., Wagenaar, N., de Vries, L. S., Benders, M. J. N. L., Rowitch, D. H., & Nijboer, C. H. A. (2017) · Glia · doi:10.1002/glia.23256 · Cited by 292 · see citing works
White matter astrocytes in health and disease
Lundgaard, I., Osório, M. J., Kress, B. T., Sanggaard, S., & Nedergaard, M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.050 · Cited by 287 · see citing works
Remyelination therapies: a new direction and challenge in multiple sclerosis
Plemel, J. R., Liu, W., & Yong, V. W. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.115 · Cited by 281 · see citing works
Nagy, N., Kuipers, H. F., Frymoyer, A. R., Ishak, H. D., Bollyky, J., Wight, T. N., & Bollyky, P. L. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00123 · Cited by 280 · see citing works
Gene therapy: can neural stem cells deliver?
Müller, F.-J., Snyder, E. Y., & Loring, J. F. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1829 · Cited by 275 · see citing works
Neurobiology of premature brain injury
Salmaso, N., Jablonska, B., Scafidi, J., Vaccarino, F. M., & Gallo, V. (2014) · Nature Neuroscience · doi:10.1038/nn.3604 · Cited by 271 · see citing works
The Role of Astrocytes in Multiple Sclerosis Progression
Correale, J. D., & Farez, M. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00180 · Cited by 261 · see citing works
Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination
Lau, L. W., Keough, M. B., Haylock‐Jacobs, S., Cua, R., Döring, A., Sloka, S., Stirling, D. P., Rivest, S., & Yong, V. W. (2012) · Annals of Neurology · doi:10.1002/ana.23599 · Cited by 248 · see citing works
Is multiple sclerosis a mitochondrial disease?
Mao, P., & Reddy, P. H. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.07.002 · Cited by 242 · see citing works
Gadea, A., Schinelli, S., & Gallo, V. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5652-07.2008 · Cited by 241 · see citing works
Myelin damage and repair in pathologic CNS: challenges and prospects
Alizadeh, A., Dyck, S. M., & Karimi‐Abdolrezaee, S. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00035 · Cited by 230 · see citing works
Nicaise, A., Wagstaff, L., Willis, C. M., Paisie, C., Chandok, H., Robson, P., Fossati, V., Williams, A. C., & Crocker, S. (2019) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1818348116 · Cited by 216 · see citing works
Natrajan, M. S., de la Fuente, A. G., Crawford, A. H., Linehan, E., Núñez, V., Johnson, K. R., Wu, T., Fitzgerald, D. C., Ricote, M., Bielekova, B., et al. (2015) · Brain · doi:10.1093/brain/awv289 · Cited by 217 · see citing works
Cortical remyelination: A new target for repair therapies in multiple sclerosis
Chang, A., Staugaitis, S. M., Dutta, R., Batt, C. E., Easley, K. E., Chomyk, A. M., Yong, V. W., Fox, R. J., Kidd, G. J., & Trapp, B. D. (2012) · Annals of Neurology · doi:10.1002/ana.23693 · Cited by 216 · see citing works
Self-citationKochlamazashvili, G., Henneberger, C., Bukalo, O., Dvoretskova, E., Senkov, O., Lievens, P. M.-J., Westenbroek, R., Engel, A. K., Catterall, W. A., Rusakov, D. A., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.030 · Cited by 215 · see citing works
Keough, M. B., Rogers, J. A., Zhang, P., Jensen, S. K., Stephenson, E. L., Chen, T., Hurlbert, M. G., Lau, L. W., Rawji, K. S., Plemel, J. R., et al. (2016) · Nature Communications · doi:10.1038/ncomms11312 · Cited by 212 · see citing works
Baer, A. S., Syed, Y. A., Kang, S. U., Mitteregger, D., Vig, R., ffrench-Constant, C., Franklin, R. J. M., Altmann, F., Lubec, G., & Kotter, M. R. (2009) · Brain · doi:10.1093/brain/awn334 · Cited by 211 · see citing works
Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination
Zhang, Y., Argaw, A. T., Gurfein, B. T., Zameer, A., Snyder, B. J., Ge, C., Lu, Q. R., Rowitch, D. H., Raine, C. S., Brosnan, C. F., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902834106 · Cited by 210 · see citing works
Glia Disease and Repair—RemyelinationPreprint
Franklin, R. J. M., & Goldman, S. A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020594 · Cited by 208 · see citing works
Fibronectin aggregation in multiple sclerosis lesions impairs remyelination
Stoffels, J. M. J., de Jonge, J. C., Stancic, M., Nomden, A., van Strien, M. E., Ma, D., Šišková, Z., Maier, O., ffrench‐Constant, C., Franklin, R. J. M., et al. (2013) · Brain · doi:10.1093/brain/aws313 · Cited by 206 · see citing works
Pathophysiology of glia in perinatal white matter injury
Back, S. A., & Rosenberg, P. A. (2014) · Glia · doi:10.1002/glia.22658 · Cited by 202 · see citing works
Self-citationRemyelination after spinal cord injury: Is it a target for repair?
Plemel, J. R., Keough, M. B., Duncan, G. J., Sparling, J. S., Yong, V. W., Stys, P. K., & Tetzlaff, W. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.02.006 · Cited by 197 · see citing works
Zhang, J., Buller, B., Zhang, Z. G., Zhang, Y., Lü, M., Rosene, D. L., Medalla, M., Moore, T. L., & Chopp, M. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113895 · Cited by 195 · see citing works
Dyck, S. M., & Karimi‐Abdolrezaee, S. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.04.006 · Cited by 189 · see citing works
Astrocytes and Microglia as Major Players of Myelin Production in Normal and Pathological Conditions
Traiffort, É., Kassoussi, A., Zahaf, A., & Laouarem, Y. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00079 · Cited by 189 · see citing works
The extracellular matrix as modifier of neuroinflammation and remyelination in multiple sclerosis
Ghorbani, S., & Yong, V. W. (2021) · Brain · doi:10.1093/brain/awab059 · Cited by 189 · see citing works
Protective effects of caffeine on chronic hypoxia‐induced perinatal white matter injury
Back, S. A., Craig, A., Luo, N. L., Ren, J., Akundi, R. S., Ribeiro, I., & Rivkees, S. A. (2006) · Annals of Neurology · doi:10.1002/ana.21008 · Cited by 187 · see citing works
Self-citationCNS remyelination and inflammation: From basic mechanisms to therapeutic opportunities
Franklin, R. J. M., & Simons, M. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.023 · Cited by 184 · see citing works
CD44: molecular interactions, signaling and functions in the nervous system
Dzwonek, J., & Wilczynski, G. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00175 · Cited by 180 · see citing works
Multiple sclerosis: Prospects and promise
Hauser, S. L., Chan, J. R., & Oksenberg, J. R. (2013) · Annals of Neurology · doi:10.1002/ana.24009 · Cited by 179 · see citing works
Enhancing remyelination in disease--can we wrap it up?
Kotter, M., Stadelmann, C., & Hartung, H. ‐. (2011) · Brain · doi:10.1093/brain/awr014 · Cited by 179 · see citing works
Wang, Y., Cheng, X., He, Q., Zheng, Y., Kim, D., Whittemore, S. R., & Cao, Q. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5524-09.2011 · Cited by 172 · see citing works
How factors secreted from astrocytes impact myelin repair
Moore, C. S., Abdullah, S. L., Brown, A. D., Arulpragasam, A. R., & Crocker, S. J. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22482 · Cited by 172 · see citing works
Kwok, J. C. F., Afshari, F. T., García‐Alías, G., & Fawcett, J. W. (2008) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2008-00439 · Cited by 170 · see citing works
Blocking LINGO-1 as a Therapy to Promote CNS Repair: From Concept to the Clinic
Mi, S., Pepinsky, R. B., & Cadavid, D. (2013) · CNS Drugs · doi:10.1007/s40263-013-0068-8 · Cited by 168 · see citing works
Sen, M. K., Mahns, D. A., Coorssen, J. R., & Shortland, P. J. (2022) · Glia · doi:10.1002/glia.24148 · Cited by 166 · see citing works
Voskuhl, R. R., Itoh, N., Tassoni, A., Matsukawa, M. A., Ren, E., Tse, V., Jang, E., Suen, T. T., & Itoh, Y. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821306116 · Cited by 162 · see citing works
Piaton, G., Aigrot, M., Williams, A., Moyon, S., Tepavčević, V., Moutkine, I., Gras, J., Matho, K. S., Schmitt, A., Soellner, H., et al. (2011) · Brain · doi:10.1093/brain/awr022 · Cited by 162 · see citing works
Neural stem cell niches: Roles for the hyaluronan-based extracellular matrix
Preston, M. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/218 · Cited by 160 · see citing works
Mohan, H., Krumbholz, M., Sharma, R. D., Eisele, S. C., Junker, A., Sixt, M., Newcombe, J., Wekerle, H., Hohlfeld, R., Lassmann, H., et al. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2010.00399.x · Cited by 160 · see citing works
Dysfunction of Cerebrovascular Endothelial Cells: Prelude to Vascular Dementia
Wang, F., Cao, Y., Ma, L., Pei, H., Rausch, W., & Li, H. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00376 · Cited by 160 · see citing works
Zhang, Q., Zhu, W., Xu, F., Dai, X., Shi, L., Cai, W., Mu, H., Hitchens, T. K., Foley, L. M., Liu, X., et al. (2019) · PLOS Biology · doi:10.1371/journal.pbio.3000330 · Cited by 160 · see citing works
Astrocytes are central in the pathomechanisms of vanishing white matter
Dooves, S., Bugiani, M., Postma, N. L., Polder, E., Land, N., Horan, S. T., van Deijk, A. F., van de Kreeke, A., Jacobs, G., Vuong, C., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci83908 · Cited by 159 · see citing works
Reed, M. J., Damodarasamy, M., & Banks, W. A. (2019) · Tissue Barriers · doi:10.1080/21688370.2019.1651157 · Cited by 158 · see citing works
Burnside, E. R., & Bradbury, E. J. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12114 · Cited by 153 · see citing works
Chondroitin Sulfate Proteoglycans in the Nervous System: Inhibitors to Repair
Siebert, J. R., Conta, A. C., & Osterhout, D. J. (2014) · BioMed Research International · doi:10.1155/2014/845323 · Cited by 151 · see citing works
Myelin Recovery in Multiple Sclerosis: The Challenge of Remyelination
Podbielska, M., Banik, N. L., Kurowska, E., & Hogan, E. (2013) · Brain Sciences · doi:10.3390/brainsci3031282 · Cited by 149 · see citing works
Impaired oligodendrocyte maturation in preterm infants: Potential therapeutic targets
van Tilborg, E., Heijnen, C. J., Benders, M. J. N. L., van Bel, F., Fleiss, B., Gressèns, P., & Nijboer, C. H. A. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.11.002 · Cited by 148 · see citing works
The role of immune cells, glia and neurons in white and gray matter pathology in multiple sclerosis
Mallucci, G., Peruzzotti‐Jametti, L., Bernstock, J. D., & Pluchino, S. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.02.003 · Cited by 143 · see citing works
Remyelination In Multiple Sclerosis
Chari, D. M. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(07)79026-8 · Cited by 140 · see citing works
Kohama, S. G., Rosene, D. L., & Sherman, L. S. (2011) · AGE · doi:10.1007/s11357-011-9357-7 · Cited by 139 · see citing works
Self-citationRiddle, A., Dean, J. M., Buser, J. R., Gong, X., Maire, J. J., Chen, K., Ahmad, T., Cai, V., Nguyen, T. D., Kroenke, C. D., et al. (2011) · Annals of Neurology · doi:10.1002/ana.22501 · Cited by 139 · see citing works
Self-citationInterleukin-11 Potentiates Oligodendrocyte Survival and Maturation, and Myelin Formation
Zhang, Y., Taveggia, C., Melendez‐Vasquez, C. V., Einheber, S., Raine, C. S., Salzer, J. L., Brosnan, C. F., & John, G. R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2289-06.2006 · Cited by 138 · see citing works
Is Alzheimer’s a disease of the white matter?
Sachdev, P. S., Zhuang, L., Braidy, N., & Wen, W. (2013) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e32835ed6e8 · Cited by 137 · see citing works
Mechanobiology of the brain in ageing and Alzheimer's disease
Hall, C. M., Moeendarbary, E., & Sheridan, G. K. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14766 · Cited by 137 · see citing works
Hyaluronic Acid Biomaterials for Central Nervous System Regenerative Medicine
Jensen, G., Holloway, J. L., & Stabenfeldt, S. E. (2020) · Cells · doi:10.3390/cells9092113 · Cited by 137 · see citing works
Inhibition of CNS Remyelination by the Presence of Semaphorin 3A
Syed, Y. A., Hand, E., Möbius, W., Zhao, C., Hofer, M., Nave, K. A., & Kotter, M. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4930-10.2011 · Cited by 134 · see citing works
Oestrogen receptor β ligand: a novel treatment to enhance endogenous functional remyelination
Crawford, D. K., Mangiardi, M., Song, B., Patel, R., Du, S., Sofroniew, M. V., Voskuhl, R. R., & Tiwari-Woodruff, S. K. (2010) · Brain · doi:10.1093/brain/awq237 · Cited by 134 · see citing works
Cheng, X., Wang, Y., He, Q., Qiu, M. S., Whittemore, S. R., & Cao, Q. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0284 · Cited by 132 · see citing works
RASSF1A controls tissue stiffness and cancer stem‐like cells in lung adenocarcinoma
Paňková, D., Jiang, Y., Chatzifrangkeskou, M., Vendrell, I., Buzzelli, J. N., Ryan, A. J., Brown, C., & O’Neill, E. E. (2019) · The EMBO Journal · doi:10.15252/embj.2018100532 · Cited by 132 · see citing works
Shiow, L. R., Favrais, G., Schirmer, L., Schang, A., Cipriani, S., Andres, C., Wright, J. N., Nobuta, H., Fleiss, B., Gressens, P., et al. (2017) · Glia · doi:10.1002/glia.23212 · Cited by 130 · see citing works
The complex world of oligodendroglial differentiation inhibitors
Kremer, D., Aktaş, O., Hartung, H., & Küry, P. (2011) · Annals of Neurology · doi:10.1002/ana.22415 · Cited by 129 · see citing works
Intrauterine growth restriction affects the maturation of myelin
Tolcos, M., Bateman, E., O'Dowd, R., Markwick, R., Vrijsen, K., Rehn, A., & Rees, S. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.08.002 · Cited by 125 · see citing works
- Authors
- Back, S. A., Tuohy, T. M. F., Chen, H., Wallingford, N., Craig, A., Struve, J., Luo, N. L., Banine, F., Liu, Y., Chang, A., Trapp, B. D., Bebo, Rao, M. S., & Sherman, L. S.
- Affiliations
- Oregon Health & Science University (US)
- Oregon National Primate Research Center (US)
- National Institutes of Health (US)
- Cleveland Clinic (US)
- Corresponding author
- Sherman, Larry S
- ORCID
- Venue
- Nature Medicine
- Published
- 2005-08-07
- Volume
- 11
- Issue
- 9
- Pages
- 966-972
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2108005154
- Cited by
- 612
- References
- 46
- Citations by year
- 2026: 20 · 2025: 16 · 2024: 33 · 2023: 17 · 2022: 32 · 2021: 31 · 2020: 39 · 2019: 41 · 2018: 33 · 2017: 49 · 2016: 24 · 2015: 33 · 2014: 34 · 2013: 46 · 2012: 30
- FWCI
- 11.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (7r01ns039550-04)
- National Institute of Neurological Disorders and Stroke (NS 39550)
- National Center for Research Resources (RR-00163.)
- National Center for Complementary and Integrative Health (AT001517, R01AT001517)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hyaluronic acid, demyelination, oligodendrocyte precursor cells, remyelination, oligodendrocyte maturation, multiple sclerosis, experimental autoimmune encephalomyelitis, astrocytes, high molecular weight hyaluronic acid, glycosaminoglycans, white matter demyelination, lysolecithin-induced demyelination
- MeSH terms
- Animals, Astrocytes, Demyelinating Diseases, Encephalomyelitis, Autoimmune, Experimental, Humans, Hyaluronic Acid, Multiple Sclerosis, Oligodendroglia, Stem Cells, Hyaluronan Receptors, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review