Origin of New Glial Cells in Intact and Injured Adult Spinal Cord
Open accessAbstract
Several distinct cell types in the adult central nervous system have been suggested to act as stem or progenitor cells generating new cells under physiological or pathological conditions. We have assessed the origin of new cells in the adult mouse spinal cord by genetic fate mapping. Oligodendrocyte progenitors self-renew, give rise to new mature oligodendrocytes, and constitute the dominating proliferating cell population in the intact adult spinal cord. In contrast, astrocytes and ependymal cells, which are restricted to limited self-duplication in the intact spinal cord, generate the largest number of cells after spinal cord injury. Only ependymal cells generate progeny of multiple fates, and neural stem cell activity in the intact and injured adult spinal cord is confined to this cell population. We provide an integrated view of how several distinct cell types contribute in complementary ways to cell maintenance and the reaction to injury.
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?
TAM has been exploited experimentally to induce permanent reporter expression in newly-born neurons in olfactory bulb and dentate gyrus, in physiologically-active neurons throughout the brain, and in progeny of ependymal cells of intact and injured murine spinal cord.
“TAM has been exploited experimentally to induce permanent reporter expression in, for example, newly-born neurons in the olfactory bulb and dentate gyrus [8], in physiologically-active neurons throughout the brain [9], and in progeny of ependymal cells of the intact and injured murine spinal cord [39].”
From Tamoxifen induces cellular stress in the nervous system by inhibiting cholesterol synthesis (2015) · cites this paper as [39]
In Barnabé-Heider et al., five daily treatments of TAM (80 mg/kg) were used to induce recombination in ependymal cells in FoxJ1-CreER mice to determine whether ependymal cells are multipotential in vitro, and in vivo following spinal cord injury.
“Here, five daily treatments of TAM (80 mg/kg) were used to induce recombination in ependymal cells in FoxJ1-CreER mice in order to determine whether ependymal cells are multipotential in vitro, and in vivo following a spinal cord injury.”
From Tamoxifen induces cellular stress in the nervous system by inhibiting cholesterol synthesis (2015) · cites this paper as [39]
In vivo, reporter-expressing ependyma self-renewed and produced astrocytes and oligodendrocyte-lineage cells 5 days following last TAM dose.
“In vivo, reporter-expressing ependyma self-renewed and produced astrocytes and oligodendrocyte-lineage cells 5 days following the last TAM dose.”
From Tamoxifen induces cellular stress in the nervous system by inhibiting cholesterol synthesis (2015) · cites this paper as [39]
The in vitro studies showed that 3 days after cessation of TAM treatment, recombined ependyma could give rise to neurospheres with cells expressing markers for neurons, astrocytes and oligodendrocyte-lineage cells.
“The in vitro studies showed that 3 days after cessation of TAM treatment, recombined ependyma could indeed give rise to neurospheres with cells expressing markers for neurons, astrocytes and oligodendrocyte-lineage cells.”
From Tamoxifen induces cellular stress in the nervous system by inhibiting cholesterol synthesis (2015) · cites this paper as [39]
Cites
Generalized lacZ expression with the ROSA26 Cre reporter strain
Soriano, P. (1999) · Nature Genetics · doi:10.1038/5007 · Cited by 5,237 · see citing works
Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4178-07.2008 · Cited by 3,129 · see citing works
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121 · see citing works
Regeneration beyond the glial scar
Silver, J., & Miller, J. H. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1326 · Cited by 3,090 · see citing works
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation
Dor, Y., Brown, J., Martinez, O. I., & Melton, D. A. (2004) · Nature · doi:10.1038/nature02520 · Cited by 2,219 · see citing works
Identification of a Neural Stem Cell in the Adult Mammalian Central Nervous System
Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U., & Frisén, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80956-3 · Cited by 1,875 · see citing works
Self-citationReactive Astrocytes Protect Tissue and Preserve Function after Spinal Cord Injury
Faulkner, J., Herrmann, J., Woo, M. J., Tansey, K., Doan, N., & Sofroniew, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3547-03.2004 · Cited by 1,600 · 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
Ito, M., Liu, Y., Yang, Z., Nguyen, J., Liang, F., Morris, R. J., & Cotsarelis, G. (2005) · Nature Medicine · doi:10.1038/nm1328 · Cited by 1,317 · see citing works
Multipotent CNS Stem Cells Are Present in the Adult Mammalian Spinal Cord and Ventricular Neuroaxis
Weiss, S., Dunne, C., Hewson, J., Wohl, C. A., Wheatley, M., Peterson, A. C., & Reynolds, B. A. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07599.1996 · Cited by 1,219 · see citing works
Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys
Crowe, M. J., Bresnahan, J. C., Shuman, S. L., Masters, J. N., & Beattie, M. S. (1997) · Nature Medicine · doi:10.1038/nm0197-73 · Cited by 1,153 · see citing works
β Cells Can Be Generated from Endogenous Progenitors in Injured Adult Mouse Pancreas
Xu, X., D’Hoker, J., Stangé, G. M., Bonné, S., Leu, N. D., Xiao, X., de Casteele, M. V., Mellitzer, G., Ling, Z., Pipeleers, D., et al. (2008) · Cell · doi:10.1016/j.cell.2007.12.015 · Cited by 989 · see citing works
Okada, S., Nakamura, M., Katoh, H., Miyao, T., Shimazaki, T., Ishii, K., Yamane, J., Yoshimura, A., Iwamoto, Y., Toyama, Y., et al. (2006) · Nature Medicine · doi:10.1038/nm1425 · Cited by 963 · see citing works
PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice
Rivers, L. E., Young, K. M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A., Kessaris, N., & Richardson, W. D. (2008) · Nature Neuroscience · doi:10.1038/nn.2220 · Cited by 961 · see citing works
Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity
Nishiyama, A., Komitova, M., Suzuki, R., & Zhu, X. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2495 · Cited by 865 · see citing works
Proliferation and Differentiation of Progenitor Cells Throughout the Intact Adult Rat Spinal Cord
Horner, P. J., Power, A. E., Kempermann, G., Kuhn, H. G., Palmer, T. D., Winkler, J., Thal, L. J., & Gage, F. H. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02218.2000 · Cited by 777 · see citing works
Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain
Buffo, A., Rite, I., Tripathi, P., Lepier, A., Colak, D., Horn, A.-P., Mori, T., & Götz, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709002105 · Cited by 766 · see citing works
NG2 cells generate both oligodendrocytes and gray matter astrocytes
Zhu, X., Bergles, D. E., & Nishiyama, A. (2007) · Development · doi:10.1242/dev.004895 · Cited by 678 · see citing works
Neural stem cells and neurospheres—re-evaluating the relationship
Reynolds, B. A., & Rietze, R. L. (2005) · Nature Methods · doi:10.1038/nmeth758 · Cited by 674 · see citing works
Spinal Cord Injury Reveals Multilineage Differentiation of Ependymal Cells
Meletis, K., Barnabé‐Heider, F., Carlén, M., Evergren, E., Tomilin, N. V., Shupliakov, O., & Frisén, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060182 · Cited by 667 · see citing works
Self-citationHofstetter, C. P., Holmström, N., Lilja, J., Schweinhardt, P., Hao, J., Spenger, C., Wiesenfeld‐Hallin, Z., Kurpad, S. N., Frisén, J., & Olson, L. (2005) · Nature Neuroscience · doi:10.1038/nn1405 · Cited by 641 · see citing works
Self-citationDimou, L., Simon, C., Kirchhoff, F., Takebayashi, H., & Götz, M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2831-08.2008 · Cited by 551 · see citing works
Self-citationTakebayashi, H., Nabeshima, Y., Yoshida, S., Chisaka, O., Ikenaka, K., & Nabeshima, Y. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00926-0 · Cited by 500 · see citing works
Self-citationFrisén, J., Johansson, C. B., Török, C., Risling, M., & Lendahl, U. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.2.453 · Cited by 476 · see citing works
Self-citationThe role of extracellular matrix in CNS regeneration
Busch, S. A., & Silver, J. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.004 · Cited by 468 · see citing works
Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke
Carlén, M., Meletis, K., Göritz, C., Darsalia, V., Evergren, E., Tanigaki, K., Amendola, M., Barnabé‐Heider, F., Yeung, M. S. Y., Naldini, L., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2268 · Cited by 453 · see citing works
Self-citationDistinct Stem Cell Populations Regenerate the Follicle and Interfollicular Epidermis
Levy, V., Lindon, C., Harfe, B. D., & Morgan, B. A. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.11.003 · Cited by 419 · see citing works
Nakagawa, T., Nabeshima, Y., & Yoshida, S. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.01.002 · Cited by 402 · see citing works
Nagy, J. I., Patel, D., Ochalski, P. A. Y., & Stelmack, G. L. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00191-2 · Cited by 346 · see citing works
Temporal–Spatial Pattern of Acute Neuronal and Glial Loss after Spinal Cord Contusion
Grossman, S. D., Rosenberg, L. J., & Wrathall, J. R. (2001) · Experimental Neurology · doi:10.1006/exnr.2001.7628 · Cited by 310 · see citing works
FGF-2 Is Sufficient to Isolate Progenitors Found in the Adult Mammalian Spinal Cord
Shihabuddin, L. S., Ray, J., & Gage, F. H. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6697 · Cited by 283 · see citing works
Keirstead, H. S., & Blakemore, W. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199711000-00003 · Cited by 272 · see citing works
Robinson, S. P., Langan-Fahey, S. M., Johnson, D. A., & Jordan, V. C. (1991) · Drug Metabolism and Disposition · doi:10.1016/s0090-9556(25)07102-8 · Cited by 268 · see citing works
Stem Cells for Spinal Cord Repair
Barnabé‐Heider, F., & Frisén, J. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.06.011 · Cited by 265 · see citing works
Self-citationFate of endogenous stem/progenitor cells following spinal cord injury
Horky, L. L., Galimi, F., Gage, F. H., & Horner, P. J. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.21065 · Cited by 258 · see citing works
Proliferation of Parenchymal Neural Progenitors in Response to Injury in the Adult Rat Spinal Cord
Yamamoto, S.-I., Yamamoto, N., Kitamura, T., Nakamura, K., & Nakafuku, M. (2001) · Experimental Neurology · doi:10.1006/exnr.2001.7798 · Cited by 253 · see citing works
Martens, D. J., Seaberg, R. M., & van der Kooy, D. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02181.x · Cited by 237 · see citing works
Ohori, Y., Yamamoto, S.-I., Nagao, M., Sugimori, M., Yamamoto, N., Nakamura, K., & Nakafuku, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3127-06.2006 · Cited by 207 · see citing works
Rash, J. E., Yasumura, T., Davidson, K. G. V., Furman, C. S., Dudek, F. E., & Nagy, J. I. (2001) · Cell Communication & Adhesion · doi:10.3109/15419060109080745 · Cited by 205 · see citing works
Nashmi, R. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00134-5 · Cited by 186 · see citing works
Masahira, N., Takebayashi, H., Ono, K., Watanabe, K., Ding, L., Furusho, M., Ogawa, Y., Nabeshima, Y., Álvarez-Buylla, A., Shimizu, K., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.02.029 · Cited by 182 · see citing works
Self-citationTransgenic mice for conditional gene manipulation in astroglial cells
Ślęzak, M., Göritz, C., Niemiec, A., Frisén, J., Chambon, P., METZGER, D., & Pfrieger, F. W. (2007) · Glia · doi:10.1002/glia.20570 · Cited by 171 · see citing works
Self-citationNG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord.
Zhu, X., Hill, R., & Nishiyama, A. (2008) · Neuron Glia Biology · doi:10.1017/s1740925x09000015 · Cited by 168 · see citing works
Activated Spinal Cord Ependymal Stem Cells Rescue Neurological Function
Moreno‐Manzano, V., Rodríguez-Jiménez, F. J., García-Roselló, M., Laínez, S., Erceg, S., Calvo, M. T., Ronaghi, M., Lloret, M., Planells‐Cases, R., Sánchez-Puelles, J.-M., et al. (2009) · Stem Cells · doi:10.1002/stem.24 · Cited by 163 · see citing works
Demyelination and Remyelination after Spinal Cord Injury
McDonald, J. W., & Belegu, V. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.345 · Cited by 155 · see citing works
Sellers, D. L., Maris, D. O., & Horner, P. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4538-08.2009 · Cited by 130 · see citing works
Glial cell loss, proliferation and replacement in the contused murine spinal cord
Lytle, J. M., & Wrathall, J. R. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05390.x · Cited by 127 · see citing works
Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression
Corti, S. P., Nizzardo, M., Nardini, M., Donadoni, C., Locatelli, F., Papadimitriou, D. A., Salani, S., Bo, R. D., Ghezzi, S., Strazzer, S., et al. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.03.021 · Cited by 125 · see citing works
Hydrogen peroxide-induced apoptosis mediated by p53 protein in glial cells
Kitamura, Y., Ota, T., Matsuoka, Y., Tooyama, I., Kimura, H., Shimohama, S., Nomura, Y., Gebicke‐Haerter, P. J., & Taniguchi, T. (1999) · Glia · doi:10.1002/(sici)1098-1136(19990115)25:2 · Cited by 96 · see citing works
Facultative Endocrine Progenitor Cells in the Adult Pancreas
Dor, Y., & Melton, D. A. (2008) · Cell · doi:10.1016/j.cell.2008.01.004 · Cited by 58 · see citing works
Localisation of the SRY-related HMG box protein, SOX9, in rodent brain
Pompolo, S., & Harley, V. R. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02574-4 · Cited by 58 · see citing works
Xu, Y., Kitada, M., Yamaguchi, M., Dezawa, M., & Idé, C. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.12.051 · Cited by 48 · see citing works
Growth of ascending spinal axons in CNS scar tissue
Frisén, J., Fried, K., Sjögren, A. M., & Risling, M. (1993) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(93)90020-e · Cited by 39 · see citing works
Self-citationGenetic visualization of neurogenesis
Carlén, M., Meletis, K., Barnabé‐Heider, F., & Frisén, J. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.05.012 · Cited by 35 · see citing works
Self-citationA dual role for reactive astrocytes after spinal cord injury
Okada, S., Nakamura, M., Toyama, Y., Iwamoto, Y., & Okano, H. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.06.167 · Cited by 32 · see citing works
Wu, D., Shibuya, S., Miyamoto, O., Itano, T., & Yamamoto, T. (2005) · Journal of Neurocytology · doi:10.1007/s11068-006-8998-4 · Cited by 29 · see citing works
From Stem Cell to Progenitor and Back Again
Simon, A., & Frisén, J. (2007) · Cell · doi:10.1016/j.cell.2007.02.026 · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions
Ming, G.-L., & Song, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.001 · Cited by 2,651 · see citing works
Ahuja, C. S., Wilson, J. R., Nori, S., Kotter, M. R. N., Druschel, C., Curt, A., & Fehlings, M. G. (2017) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2017.18 · Cited by 2,441 · see citing works
Traumatic Spinal Cord Injury: An Overview of Pathophysiology, Models and Acute Injury Mechanisms
Alizadeh, A., Dyck, S. M., & Karimi‐Abdolrezaee, S. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00282 · Cited by 1,447 · see citing works
Diversity of astrocyte functions and phenotypes in neural circuits
Khakh, B. S., & Sofroniew, M. V. (2015) · Nature Neuroscience · doi:10.1038/nn.4043 · Cited by 1,239 · see citing works
Cell transplantation therapy for spinal cord injury
Assinck, P., Duncan, G. J., Hilton, B. J., Plemel, J. R., & Tetzlaff, W. (2017) · Nature Neuroscience · doi:10.1038/nn.4541 · Cited by 941 · see citing works
The Biology of Regeneration Failure and Success After Spinal Cord Injury
Tran, A. P., Warren, P. M., & Silver, J. (2018) · Physiological Reviews · doi:10.1152/physrev.00017.2017 · Cited by 883 · see citing works
A Pericyte Origin of Spinal Cord Scar Tissue
Göritz, C., Dias, D. O., Tomilin, N., Barbacid, M., Shupliakov, O., & Frisén, J. (2011) · Science · doi:10.1126/science.1203165 · Cited by 858 · see citing works
Self-citationSpinal cord injury: molecular mechanisms and therapeutic interventions
Hu, X., Xu, W., Ren, Y., Wang, Z., He, X., Huang, R., Ma, B., Zhao, J., Zhu, R., & Cheng, L. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01477-6 · Cited by 823 · see citing works
Sofroniew, M. V. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020420 · Cited by 695 · see citing works
Functional regeneration beyond the glial scar
Cregg, J. M., DePaul, M. A., Filous, A. R., Lang, B. T., Tran, A. P., & Silver, J. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2013.12.024 · Cited by 664 · see citing works
Oligodendrocytes in development, myelin generation and beyond
Kuhn, S., Gritti, L., Crooks, D., & Dombrowski, Y. (2019) · Cells · doi:10.3390/cells8111424 · Cited by 625 · see citing works
Oligodendrocyte Development and PlasticityPreprint
Bergles, D. E., & Richardson, W. D. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020453 · Cited by 573 · see citing works
Dynamics of Oligodendrocyte Generation and Myelination in the Human Brain
Yeung, M. S. Y., Zdunek, S., Bergmann, O., Bernard, S., Salehpour, M., Alkass, K., Perl, S., Tisdale, J., Possnert, G., Brundin, L., et al. (2014) · Cell · doi:10.1016/j.cell.2014.10.011 · Cited by 541 · see citing works
Self-citationMicroenvironment Imbalance of Spinal Cord Injury
Fan, B., Wei, Z., Yao, X. X., Shi, G., Cheng, X., Zhou, X., Zhou, H., Ning, G., Kong, X., & Feng, S. (2018) · Cell Transplantation · doi:10.1177/0963689718755778 · Cited by 535 · see citing works
The stem cell potential of glia: lessons from reactive gliosis
Robel, S., Berninger, B., & Götz, M. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn2978 · Cited by 513 · see citing works
NADPH oxidase in brain injury and neurodegenerative disorders
Ma, M. W., Wang, J., Zhang, Q., Wang, R., Dhandapani, K. M., Vadlamudi, R. K., & Brann, D. W. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0150-7 · Cited by 432 · see citing works
Rat models of spinal cord injury: from pathology to potential therapies
Kjell, J., & Olson, L. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.025833 · Cited by 408 · see citing works
Reducing Pericyte-Derived Scarring Promotes Recovery after Spinal Cord Injury
Dias, D. O., Kim, H., Holl, D., Solnestam, B. W., Lundeberg, J., Carlén, M., Göritz, C., & Frisén, J. (2018) · Cell · doi:10.1016/j.cell.2018.02.004 · Cited by 396 · see citing works
Self-citationReactive Glia in the Injured Brain Acquire Stem Cell Properties in Response to Sonic Hedgehog
Sirko, S., Behrendt, G., Johansson, P. A., Tripathi, P., Costa, M. R., Bek, S., Heinrich, C., Tiedt, S., Colak, D., Dichgans, M., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.01.019 · Cited by 383 · see citing works
SOX9 Is an Astrocyte-Specific Nuclear Marker in the Adult Brain Outside the Neurogenic Regions
Sun, W., Cornwell, A., Li, J., Peng, S., Osorio, M. J., Aalling, N., Wang, S., Benraiss, A., Lou, N., Goldman, S. A., et al. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3199-16.2017 · Cited by 357 · see citing works
Role of Endogenous Neural Stem Cells in Spinal Cord Injury and Repair
Stenudd, M., Sabelström, H., & Frisén, J. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.2927 · Cited by 334 · see citing works
Self-citationReactive Astrogliosis after Spinal Cord Injury—Beneficial and Detrimental Effects
Karimi-Abdolrezaee, S., & Billakanti, R. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8287-4 · Cited by 331 · see citing works
Simon, C., Götz, M., & Dimou, L. (2011) · Glia · doi:10.1002/glia.21156 · Cited by 313 · see citing works
Resident Neural Stem Cells Restrict Tissue Damage and Neuronal Loss After Spinal Cord Injury in Mice
Sabelström, H., Stenudd, M., Réu, P., Dias, D. O., Elfineh, M., Zdunek, S., Damberg, P., Göritz, C., & Frisén, J. (2013) · Science · doi:10.1126/science.1242576 · Cited by 309 · see citing works
Self-citationNG2-glia as multipotent neural stem cells: fact or fantasy?
Richardson, W. D., Young, K. M., Tripathi, R. B., & McKenzie, I. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.013 · Cited by 300 · see citing works
Single-cell analysis of the cellular heterogeneity and interactions in the injured mouse spinal cord
Milich, L. M., Choi, J. S., Ryan, C. B., Cerqueira, S. R., Benavides, S., Yahn, S. L., Tsoulfas, P., & Lee, J. K. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20210040 · Cited by 285 · 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
Type-1 pericytes accumulate after tissue injury and produce collagen in an organ-dependent manner
Birbrair, A., Zhang, T., Files, D. C., Mannava, S., Smith, T. L., Wang, Z., Messi, M. L., Mintz, A., & Delbono, O. (2014) · Stem Cell Research & Therapy · doi:10.1186/scrt512 · Cited by 279 · see citing works
Zukor, K., Belin, S., Wang, C., Keelan, N., Wang, X., & He, Z. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2510-13.2013 · Cited by 281 · see citing works
Fgf-Dependent Glial Cell Bridges Facilitate Spinal Cord Regeneration in Zebrafish
Goldshmit, Y., Sztal, T. E., Jusuf, P. R., Hall, T. E., Chi, M. N., & Currie, P. D. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0758-12.2012 · Cited by 274 · see citing works
Glial Cells as Progenitors and Stem Cells: New Roles in the Healthy and Diseased Brain
Dimou, L., & Götz, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2013 · Cited by 263 · see citing works
NG 2‐glia and their functions in the central nervous system
Dimou, L., & Gallo, V. (2015) · Glia · doi:10.1002/glia.22859 · Cited by 258 · see citing works
Glial cells in amyotrophic lateral sclerosis
Philips, T., & Rothstein, J. D. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.015 · Cited by 255 · see citing works
Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish
Zupanc, G. K. H., & Sîrbulescu, R. F. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07854.x · Cited by 248 · see citing works
Progression in translational research on spinal cord injury based on microenvironment imbalance
Fan, B., Wei, Z., & Feng, S. (2022) · Bone Research · doi:10.1038/s41413-022-00199-9 · Cited by 248 · see citing works
Oligodendrocyte lineage cells and depression
Zhou, B., Zhu, Z., Ransom, B. R., & Tong, X. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00930-0 · Cited by 239 · see citing works
Peroxisome proliferator-activated receptor γ (PPARγ): A master gatekeeper in CNS injury and repair
Cai, W., Yang, T., Liu, H., Han, L., Zhang, K., Hu, X., Zhang, X., Yin, K., Gao, Y., Bennett, M. V. L., et al. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.10.002 · Cited by 238 · 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
Glial Cells Shape Pathology and Repair After Spinal Cord Injury
Gaudet, A. D., & Fonken, L. K. (2018) · Neurotherapeutics · doi:10.1007/s13311-018-0630-7 · Cited by 232 · see citing works
Bioinspired Hydrogel Electrospun Fibers for Spinal Cord Regeneration
Chen, C., Tang, J., Gu, Y., Liu, L., Liu, X., Deng, L., Martins, C., Sarmento, B. F. C. C., Cui, W., & Chen, L. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201806899 · Cited by 224 · see citing works
Götz, M., Sirko, S., Beckers, J., & Irmler, M. (2015) · Glia · doi:10.1002/glia.22850 · Cited by 219 · see citing works
MicroRNA-21 Regulates Astrocytic Response Following Spinal Cord Injury
Bhalala, O. G., Pan, L., Sahni, V., McGuire, T. L., Gruner, K., Tourtellotte, W. G., & Kessler, J. A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3860-12.2012 · Cited by 220 · see citing works
Yang, Z., Zhang, A., Duan, H., Zhang, S., Hao, P., Ye, K., Sun, Y. E., & Li, X. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1510194112 · Cited by 219 · see citing works
Pericyte-derived fibrotic scarring is conserved across diverse central nervous system lesions
Dias, D. O., Kalkitsas, J., Kelahmetoglu, Y., Estrada, C. P., Tatarishvili, J., Holl, D., Jansson, L., Banitalebi, S., Amiry-Moghaddam, M. R., Ernst, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25585-5 · Cited by 214 · see citing works
Self-citationThe glial scar in spinal cord injury and repair
Yuan, Y., & He, C. (2013) · Neuroscience Bulletin · doi:10.1007/s12264-013-1358-3 · Cited by 212 · see citing works
Oligodendrocyte Fate after Spinal Cord Injury
Almad, A., Sahinkaya, F. R., & McTigue, D. M. (2011) · Neurotherapeutics · doi:10.1007/s13311-011-0033-5 · Cited by 210 · see citing works
Regeneration of Spinal Cord Connectivity Through Stem Cell Transplantation and Biomaterial Scaffolds
Katoh, H., Yokota, K., & Fehlings, M. G. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00248 · Cited by 199 · see citing works
Remyelination 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
Shimada, I. S., LeComte, M. D., Granger, J. C., Quinlan, N. J., & Spees, J. L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4303-11.2012 · Cited by 188 · 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
A comparative view of regenerative neurogenesis in vertebrates
Alunni, A., & Bally‐Cuif, L. (2016) · Development · doi:10.1242/dev.122796 · Cited by 189 · see citing works
Neural stem cells in the adult spinal cord
Sabelström, H., Stenudd, M., & Frisén, J. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.01.026 · Cited by 181 · see citing works
Self-citationInhibition of Gli1 mobilizes endogenous neural stem cells for remyelination
Samanta, J., Grund, E. M., Silva, H. M., Lafaille, J. J., Fishell, G., & Salzer, J. L. (2015) · Nature · doi:10.1038/nature14957 · Cited by 170 · see citing works
A latent lineage potential in resident neural stem cells enables spinal cord repair
Llorens-Bobadilla, E., Chell, J. M., Merre, P. L., Wu, Y.-C., Zamboni, M., Bergenstråhle, J., Stenudd, M., Sopova, E., Lundeberg, J., Shupliakov, O., et al. (2020) · Science · doi:10.1126/science.abb8795 · Cited by 143 · see citing works
Self-citationChronic Oligodendrogenesis and Remyelination after Spinal Cord Injury in Mice and Rats
Hesp, Z. C., Goldstein, E. A., Miranda, C. J., Kaspar, B. K., & McTigue, D. M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2568-14.2015 · Cited by 164 · see citing works
Regenerative Therapies for Spinal Cord Injury
Ashammakhi, N. A., Kim, H., Ehsanipour, A., Bierman, R. D., Kaarela, O. I., Xue, C., Khademhosseini, A., & Seidlits, S. K. (2019) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2019.0182 · Cited by 167 · see citing works
Tai, W., Wu, W., Wang, L.-L., Ni, H., Chen, C., Yang, J., Zang, T., Zou, Y., Xu, X., & Zhang, C. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.02.009 · Cited by 162 · see citing works
Astrocyte activation is suppressed in both normal and injured brain by FGF signaling
Kang, W., Balordi, F., Su, N. Y., Chen, L., Fishell, G., & Hébert, J. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320401111 · Cited by 159 · see citing works
Yang, Y., Fan, Y., Zhang, H., Zhang, Q., Zhao, Y., Xiao, Z., Liu, W., Chen, B., Gao, L., Sun, Z., et al. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120479 · Cited by 159 · see citing works
El-Kheir, W. A., Gabr, H. M., Awad, M. R., Ghannam, O. E., Barakat, Y. A. G., Farghali, H. A. M. A., Maadawi, Z. M. E., Ewes, I., & Sabaawy, H. E. (2013) · Cell Transplantation · doi:10.3727/096368913x664540 · Cited by 156 · see citing works
Endogenous neural stem cell responses to stroke and spinal cord injury
Grégoire, C., Goldenstein, B., Floriddia, E. M., Barnabé‐Heider, F., & Fernandes, K. J. L. (2015) · Glia · doi:10.1002/glia.22851 · Cited by 152 · see citing works
Self-citationRen, Y., Ao, Y., O’Shea, T. M., Burda, J. E., Bernstein, A. M., Brumm, A. J., Muthusamy, N., Ghashghaei, H. T., Carmichael, S. T., Cheng, L., et al. (2017) · Scientific Reports · doi:10.1038/srep41122 · Cited by 149 · see citing works
Myelinogenic Plasticity of Oligodendrocyte Precursor Cells following Spinal Cord Contusion Injury
Assinck, P., Duncan, G. J., Plemel, J. R., Lee, M. J., Stratton, J. A., Manesh, S. B., Liu, J., Ramer, L. M., Kang, S. H., Bergles, D. E., et al. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2409-16.2017 · Cited by 151 · see citing works
Cell-based transplantation strategies to promote plasticity following spinal cord injury
Ruff, C. A., Wilcox, J. T., & Fehlings, M. G. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.02.010 · Cited by 149 · see citing works
“Targeting astrocytes in CNS injury and disease: A translational research approach”
Filous, A. R., & Silver, J. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.03.009 · Cited by 149 · see citing works
Bioactive DNA-Peptide Nanotubes Enhance the Differentiation of Neural Stem Cells Into Neurons
Stephanopoulos, N., Freeman, R., North, H. A., Sur, S., Jeong, S. J., Tantakitti, F., Kessler, J. A., & Stupp, S. I. (2015) · Nano Letters · doi:10.1021/nl504079q · Cited by 138 · see citing works
A modified collagen scaffold facilitates endogenous neurogenesis for acute spinal cord injury repair
Fan, C., Li, X., Xiao, Z., Zhao, Y., Liang, H., Wang, B., Han, S., Li, X., Bai, X., Wang, N., et al. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.01.009 · Cited by 143 · see citing works
Ahuja, C. S., Mothe, A. J., Khazaei, M., Badhiwala, J. H., Gilbert, E. A. B., van der Kooy, D., Morshead, C. M., Tator, C. H., & Fehlings, M. G. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0135 · Cited by 143 · see citing works
Signaling Pathways in Reactive Astrocytes, a Genetic Perspective
Kang, W., & Hébert, J. M. (2011) · Molecular Neurobiology · doi:10.1007/s12035-011-8163-7 · Cited by 123 · see citing works
Tien, A., Tsai, H., Molofsky, A. V., McMahon, M., Foo, L. C., Kaul, A., Dougherty, J. D., Heintz, N., Gutmann, D. H., Barres, B. A., et al. (2012) · Development · doi:10.1242/dev.077214 · Cited by 137 · see citing works
Li, X., Zhao, Y., Cheng, S., Han, S., Shu, M., Chen, B., Chen, X., Tang, F., Wang, N., Tu, Y., et al. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.05.027 · Cited by 138 · see citing works
Multimodal treatment for spinal cord injury: a sword of neuroregeneration upon neuromodulation
Zheng, Y., Mao, Y.-R., Yuan, T., Xu, D., & Cheng, L. (2020) · Neural Regeneration Research · doi:10.4103/1673-5374.274332 · Cited by 138 · see citing works
Reciprocal Modulation Between Microglia and Astrocyte in Reactive Gliosis Following the CNS Injury
Gao, Z., Zhu, Q., Zhang, Y., Zhao, Y., Cai, L., Shields, C. B., & Cai, J. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8460-4 · Cited by 139 · see citing works
Zhu, R., Zhu, X., Zhu, Y., Wang, Z., He, X., Wu, Z., Xue, L., Fan, W., Huang, R., Xu, Z. Q., et al. (2021) · ACS Nano · doi:10.1021/acsnano.0c08727 · Cited by 133 · see citing works
Neurogenesis in the Developing and Adult Brain—Similarities and Key DifferencesPreprint
Götz, M., Nakafuku, M., & Petřík, D. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018853 · Cited by 131 · see citing works
Hosseini, S. M., Borys, B., & Karimi‐Abdolrezaee, S. (2023) · Brain · doi:10.1093/brain/awad392 · Cited by 134 · see citing works
Zhu, Y., Lyapichev, K. A., Lee, D. H., Motti, D., Ferraro, N. M., Zhang, Y., Yahn, S. L., Soderblom, C., Zha, J., Bethea, J. R., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2751-16.2017 · Cited by 128 · see citing works
Karimi‐Abdolrezaee, S., Schut, D., Wang, J., & Fehlings, M. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037589 · Cited by 126 · see citing works
Concise Review: Reactive Astrocytes and Stem Cells in Spinal Cord Injury: Good Guys or Bad Guys?
Lukovic, D., Stojković, M., Moreno‐Manzano, V., Jendelová, P., Syková, E., Bhattacharya, S. S., & Erceg, S. (2015) · Stem Cells · doi:10.1002/stem.1959 · Cited by 123 · see citing works
Stem Cells Therapy for Spinal Cord Injury
Gazdic, M., Volarević, V., Harrell, C. R., Fellabaum, C., Jovicic, N. U., Arsenijević, N., & Stojković, M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041039 · Cited by 121 · see citing works
Advances in Biomaterial‐Based Spinal Cord Injury Repair
Shen, H., Fan, C., You, Z., Xiao, Z., Zhao, Y., & Dai, J. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202110628 · Cited by 119 · see citing works
O’Shea, T. M., Ao, Y., Wang, S., Ren, Y., Cheng, A. L., Kawaguchi, R., Shi, Z., Swarup, V., & Sofroniew, M. V. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01684-6 · Cited by 123 · see citing works
Li, X., Liu, D., Xiao, Z., Zhao, Y., Han, S., Chen, B., & Dai, J. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.01.012 · Cited by 117 · see citing works
The fate and function of oligodendrocyte progenitor cells after traumatic spinal cord injury
Duncan, G. J., Manesh, S. B., Hilton, B. J., Assinck, P., Plemel, J. R., & Tetzlaff, W. (2019) · Glia · doi:10.1002/glia.23706 · Cited by 117 · see citing works
Decimo, I., Bifari, F., Rodríguez, F. J., Malpeli, G., Dolci, S., Lavarini, V., Pretto, S., Vásquez, S., Sciancalepore, M., Montalbano, A., et al. (2011) · Stem Cells · doi:10.1002/stem.766 · Cited by 117 · see citing works
From demyelination to remyelination: The road toward therapies for spinal cord injury
Papastefanaki, F., & Matsas, R. (2015) · Glia · doi:10.1002/glia.22809 · Cited by 113 · see citing works
Duncan, G. J., Manesh, S. B., Hilton, B. J., Assinck, P., Liu, J., Moulson, A., Plemel, J. R., & Tetzlaff, W. (2018) · Nature Communications · doi:10.1038/s41467-018-05473-1 · Cited by 113 · see citing works
Mitochondrial function in spinal cord injury and regeneration
Slater, P. G., Domínguez-Romero, M. E., Villarreal, M., Eisner, V., & Larraı́n, J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04261-x · Cited by 110 · see citing works
Neural Stem Cells and Neurogenesis in the Adult
Göritz, C., & Frisén, J. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.04.005 · Cited by 110 · see citing works
Self-citationOligodendrocytes in the aging brain
Sams, E. C. (2021) · Neuronal Signaling · doi:10.1042/ns20210008 · Cited by 107 · see citing works
Spinal cord regeneration: Lessons for mammals from non‐mammalian vertebrates
Lee‐Liu, D., Edwards‐Faret, G., Tapia, V. S., & Larraı́n, J. (2013) · genesis · doi:10.1002/dvg.22406 · Cited by 105 · see citing works
Lin, R., Cai, J., Nathan, C. L., Wei, X., Schleidt, S. S., Rosenwasser, R. H., & Iacovitti, L. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.11.016 · Cited by 106 · see citing works
Quraishe, S., Forbes, L. H., & Andrews, M. R. (2018) · Neural Plasticity · doi:10.1155/2018/2952386 · Cited by 105 · see citing works
Khazaei, M., Ahuja, C. S., Nakashima, H., Nagoshi, N., Li, L., Wang, J., Chio, J. C. T., Badner, A., Seligman, D., Ichise, A., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aau3538 · Cited by 106 · see citing works
Ma, D., Zhao, Y., Huang, L., Xiao, Z., Chen, B., Shi, Y., Shen, H., & Dai, J. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.119830 · Cited by 104 · see citing works
The glial scar is more than just astrocytes
Silver, J. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.06.018 · Cited by 102 · see citing works
Falk, S., & Götz, M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.025 · Cited by 99 · see citing works
Understanding the NG2 Glial Scar after Spinal Cord Injury
Hackett, A. R., & Lee, J. K. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00199 · Cited by 103 · see citing works
Neuronal Regeneration from Ependymo-Radial Glial Cells: Cook, Little Pot, Cook!
Becker, C. G., & Becker, T. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.001 · Cited by 97 · see citing works
Neural Stem Cell Niches in Health and Diseases
Decimo, I., Bifari, F., Krampera, M., & Fumagalli, G. F. (2012) · Current Pharmaceutical Design · doi:10.2174/138161212799859611 · Cited by 97 · see citing works
- Authors
- Barnabé-Heider, F., Göritz, C., Sabelström, H., Takebayashi, H., Pfrieger, F. W., Meletis, K., & Frisén, J.
- Affiliations
- Karolinska Institutet (SE)
- Kumamoto University (JP)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Frisén, Jonas
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2010-10
- Volume
- 7
- Issue
- 4
- Pages
- 470-482
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W2128475302
- Cited by
- 628
- References
- 58
- Citations by year
- 2026: 28 · 2025: 33 · 2024: 34 · 2023: 44 · 2022: 40 · 2021: 64 · 2020: 35 · 2019: 37 · 2018: 46 · 2017: 48 · 2016: 42 · 2015: 44 · 2014: 48 · 2013: 33 · 2012: 24
- FWCI
- 8.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- adult spinal cord, glial cell origin, spinal cord injury, oligodendrocyte progenitors, astrocytes, ependymal cells, neural stem cells, cell proliferation, self-renewal, genetic fate mapping
- MeSH terms
- Animals, Immunohistochemistry, Mice, Transgenic, Neuroglia, Spinal Cord Injuries, Stem Cells, Mice, Spinal Cord Regeneration
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