NG2 glia display wide proliferation and differentiation potential under physiological and pathological conditions. Here, we examined these two features following different types of brain disorders such as focal cerebral ischemia (FCI), cortical stab wound (SW), and demyelination (DEMY) in 3-month-old mice, in which NG2 glia are labeled by tdTomato under the Cspg4 promoter. To compare NG2 glia expression profiles following different CNS injuries, we employed single-cell RT-qPCR and self-organizing Kohonen map analysis of tdTomato-positive cells isolated from the uninjured cortex/corpus callosum and those after specific injury. Such approach enabled us to distinguish two main cell populations (NG2 glia, oligodendrocytes), each of them comprising four distinct subpopulations. The gene expression profiling revealed that a subpopulation of NG2 glia expressing GFAP, a marker of reactive astrocytes, is only present transiently after FCI. However, following less severe injuries, namely the SW and DEMY, subpopulations mirroring different stages of oligodendrocyte maturation markedly prevail. Such injury-dependent incidence of distinct subpopulations was also confirmed by immunohistochemistry. To characterize this unique subpopulation of transient astrocyte-like NG2 glia, we used single-cell RNA-sequencing analysis and to disclose their basic membrane properties, the patch-clamp technique was employed. Overall, we have proved that astrocyte-like NG2 glia are a specific subpopulation of NG2 glia emerging transiently only following FCI. These cells, located in the postischemic glial scar, are active in the cell cycle and display a current pattern similar to that identified in cortical astrocytes. Astrocyte-like NG2 glia may represent important players in glial scar formation and repair processes, following ischemia.

2nd Faculty of Medicine Charles University Prague Czech Republic

Department of Cellular Neurophysiology Institute of Experimental Medicine Czech Academy of Sciences Prague Czech Republic

Faculty of Chemical Technology Laboratory of Informatics and Chemistry University of Chemistry and Technology Prague Czech Republic

Faculty of Science Charles University Prague Czech Republic

Laboratory of Gene Expression Institute of Biotechnology CAS BIOCEV Vestec Czech Republic

Erratum v

Glia. 2022 Dec;70(12):2443. doi: 10.1002/glia.24277. PubMed

Zobrazit více v PubMed

Aguirre, A. , & Gallo, V. (2004). Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2‐expressing progenitors of the subventricular zone. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 24(46), 10530–10541. 10.1523/JNEUROSCI.3572-04.2004 PubMed DOI PMC

Alberdi, E. , Sánchez‐Gómez, M. V. , Marino, A. , & Matute, C. (2002). Ca(2+) influx through AMPA or kainate receptors alone is sufficient to initiate excitotoxicity in cultured oligodendrocytes. Neurobiology of Disease, 9(2), 234–243. 10.1006/nbdi.2001.0457 PubMed DOI

Anderová, M. , Antonova, T. , Petrík, D. , Neprasová, H. , Chvátal, A. , & Syková, E. (2004). Voltage‐dependent potassium currents in hypertrophied rat astrocytes after a cortical stab wound. Glia, 48(4), 311–326. 10.1002/glia.20076 PubMed DOI

Anderová, M. , Kubinová, S. , Jelitai, M. , Neprasová, H. , Glogarová, K. , Prajerová, I. , … Syková, E. (2006). Transplantation of embryonic neuroectodermal progenitor cells into the site of a photochemical lesion: Immunohistochemical and electrophysiological analysis. Journal of Neurobiology, 66(10), 1084–1100. 10.1002/neu.20278 PubMed DOI

Battefeld, A. , Klooster, J. , & Kole, M. H. (2016). Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high‐frequency activity. Nature Communications, 7, 11298. 10.1038/ncomms11298 PubMed DOI PMC

Baxi, E. G. , DeBruin, J. , Jin, J. , Strasburger, H. J. , Smith, M. D. , Orthmann‐Murphy, J. L. , … Calabresi, P. A. (2017). Lineage tracing reveals dynamic changes in oligodendrocyte precursor cells following cuprizone‐induced demyelination. Glia, 65(12), 2087–2098. 10.1002/glia.23229 PubMed DOI PMC

Bergles, D. E. , Roberts, J. D. , Somogyi, P. , & Jahr, C. E. (2000). Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature, 405(6783), 187–191. 10.1038/35012083 PubMed DOI

Boda, E. , Viganò, F. , Rosa, P. , Fumagalli, M. , Labat‐Gest, V. , Tempia, F. , … Buffo, A. (2011). The GPR17 receptor in NG2 expressing cells: Focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia, 59(12), 1958–1973. 10.1002/glia.21237 PubMed DOI

Bonfanti, E. , Gelosa, P. , Fumagalli, M. , Dimou, L. , Viganò, F. , Tremoli, E. , … Abbracchio, M. P. (2017). The role of oligodendrocyte precursor cells expressing the GPR17 receptor in brain remodeling after stroke. Cell Death & Disease, 8(6), e2871. 10.1038/cddis.2017.256 PubMed DOI PMC

Boulanger, J. J. , & Messier, C. (2017). Doublecortin in oligodendrocyte precursor cells in the adult mouse brain. Frontiers in Neuroscience, 11, 143. 10.3389/fnins.2017.00143 PubMed DOI PMC

Buffo, A. , Vosko, M. R. , Erturk, D. , Hamann, G. F. , Jucker, M. , Rowitch, D. , & Gotz, M. (2005). Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proceedings of the National Academy of Sciences of the United States of America, 102(50), 18183–18188. 10.1073/pnas.0506535102 PubMed DOI PMC

Butt, A. M. , Vanzulli, I. , Papanikolaou, M. , de la Rocha, I. C. , & Hawkins, V. E. (2017). Metabotropic glutamate receptors protect oligodendrocytes from acute ischemia in the mouse optic nerve. Neurochemical Research, 42(9), 2468–2478. 10.1007/s11064-017-2220-1 PubMed DOI PMC

Cahoy, J. D. , Emery, B. , Kaushal, A. , Foo, L. C. , Zamanian, J. L. , Christopherson, K. S. , … Barres, B. A. (2008). A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28(1), 264–278. 10.1523/jneurosci.4178-07.2008 PubMed DOI PMC

Ceprian, M. , & Fulton, D. (2019). Glial cell AMPA receptors in nervous system health, injury and disease. International Journal of Molecular Sciences, 20(10), 2450. 10.3390/ijms20102450 PubMed DOI PMC

Chamling, X. , Kallman, A. , Fang, W. X. , Berlinicke, C. A. , Mertz, J. L. , Devkota, P. , … Zack, D. J. (2021). Single‐cell transcriptomic reveals molecular diversity and developmental heterogeneity of human stem cell‐derived oligodendrocyte lineage cells. Nat Commun. 12(1), 652. 10.1101/2020.10.07.328971 PubMed DOI PMC

Chittajallu, R. , Aguirre, A. , & Gallo, V. (2004). NG2‐positive cells in the mouse white and grey matter display distinct physiological properties. The Journal of Physiology, 561(Pt 1), 109–122. 10.1113/jphysiol.2004.074252 PubMed DOI PMC

David, F. P. A. , Litovchenko, M. , Deplancke, B. , & Gardeux, V. (2020). ASAP 2020 update: An open, scalable and interactive web‐based portal for (single‐cell) omics analyses. Nucleic Acids Research, 48(W1), W403–w414. 10.1093/nar/gkaa412 PubMed DOI PMC

de Biase, L. M. , Nishiyama, A. , & Bergles, D. E. (2010). Excitability and synaptic communication within the oligodendrocyte lineage. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30(10), 3600–3611. 10.1523/jneurosci.6000-09.2010 PubMed DOI PMC

DeSilva, T. M. , Kabakov, A. Y. , Goldhoff, P. E. , Volpe, J. J. , & Rosenberg, P. A. (2009). Regulation of glutamate transport in developing rat oligodendrocytes. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(24), 7898–7908. 10.1523/jneurosci.6129-08.2009 PubMed DOI PMC

Dewar, D. , Underhill, S. M. , & Goldberg, M. P. (2003). Oligodendrocytes and ischemic brain injury. Journal of Cerebral Blood Flow and Metabolism, 23(3), 263–274. 10.1097/01.WCB.0000053472.41007.F9 PubMed DOI

Dias, D. O. , Kalkitsas, J. , Kelahmetoglu, Y. , Estrada, C. P. , Tatarishvili, J. , Ernst, A. , … Göritz, C. (2020). Pericyte‐derived fibrotic scarring is conserved across diverse central nervous system lesions. bioRxiv, 2020.2004.2030.068965. 10.1101/2020.04.30.068965 PubMed DOI PMC

Dimou, L. , Simon, C. , Kirchhoff, F. , Takebayashi, H. , & Gotz, M. (2008). Progeny of Olig2‐expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28(41), 10434–10442. 10.1523/jneurosci.2831-08.2008 PubMed DOI PMC

Dobin, A. , Davis, C. A. , Schlesinger, F. , Drenkow, J. , Zaleski, C. , Jha, S. , … Gingeras, T. R. (2013). STAR: ultrafast universal RNA‐seq aligner. Bioinformatics, 29(1), 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC

Essers, J. , Theil, A. F. , Baldeyron, C. , van Cappellen, W. A. , Houtsmuller, A. B. , Kanaar, R. , & Vermeulen, W. (2005). Nuclear dynamics of PCNA in DNA replication and repair. Molecular and Cellular Biology, 25(21), 9350–9359. 10.1128/mcb.25.21.9350-9359.2005 PubMed DOI PMC

Ferent, J. , Zimmer, C. , Durbec, P. , Ruat, M. , & Traiffort, E. (2013). Sonic Hedgehog signaling is a positive oligodendrocyte regulator during demyelination. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33(5), 1759–1772. 10.1523/jneurosci.3334-12.2013 PubMed DOI PMC

Gudi, V. , Gingele, S. , Skripuletz, T. , & Stangel, M. (2014). Glial response during cuprizone‐induced de‐ and remyelination in the CNS: Lessons learned. Frontiers in Cellular Neuroscience, 8, 73. 10.3389/fncel.2014.00073 PubMed DOI PMC

Guo, F. , Lang, J. , Sohn, J. , Hammond, E. , Chang, M. , & Pleasure, D. (2015). Canonical Wnt signaling in the oligodendroglial lineage: Puzzles remain. Glia, 63(10), 1671–1693. 10.1002/glia.22813 PubMed DOI

Guo, F. , Ma, J. , McCauley, E. , Bannerman, P. , & Pleasure, D. (2009). Early postnatal proteolipid promoter‐expressing progenitors produce multilineage cells in vivo. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(22), 7256–7270. 10.1523/jneurosci.5653-08.2009 PubMed DOI PMC

Hackett, A. R. , Yahn, S. L. , Lyapichev, K. , Dajnoki, A. , Lee, D. H. , Rodriguez, M. , … Lee, J. K. (2018). Injury type‐dependent differentiation of NG2 glia into heterogeneous astrocytes. Experimental Neurology, 308, 72–79. 10.1016/j.expneurol.2018.07.001 PubMed DOI PMC

Haneda, H. , Katabami, M. , Miyamoto, H. , Isobe, H. , Shimizu, T. , Ishiguro, A. , … Kawakami, Y. (1991). The relationship of the proliferating cell nuclear antigen protein to cis‐diamminedichloroplatinum (II) resistance of a murine leukemia cell line P388/CDDP. Oncology, 48(3), 234–238. 10.1159/000226934 PubMed DOI

Hansen, A. J. (1978). The extracellular potassium concentration in brain cortex following ischemia in hypo‐ and hyperglycemic rats. Acta Physiologica Scandinavica, 102(3), 324–329. 10.1111/j.1748-1716.1978.tb06079.x PubMed DOI

Hassannejad, Z. , Shakouri‐Motlagh, A. , Mokhatab, M. , Zadegan, S. A. , Sharif‐Alhoseini, M. , Shokraneh, F. , & Rahimi‐Movaghar, V. (2019). Oligodendrogliogenesis and axon remyelination after traumatic spinal cord injuries in animal studies: A systematic review. Neuroscience, 402, 37–50. 10.1016/j.neuroscience.2019.01.019 PubMed DOI

He, Y. , Liu, X. , & Chen, Z. (2020). Glial scar: A promising target for improving outcomes after CNS injury. Journal of Molecular Neuroscience, 70(3), 340–352. 10.1007/s12031-019-01417-6 PubMed DOI

Hill, R. A. , & Nishiyama, A. (2014). NG2 cells (polydendrocytes): Listeners to the neural network with diverse properties. Glia, 62(8), 1195–1210. 10.1002/glia.22664 PubMed DOI PMC

Honsa, P. , Pivonkova, H. , Dzamba, D. , Filipova, M. , & Anderova, M. (2012). Polydendrocytes display large lineage plasticity following focal cerebral ischemia. PLoS One, 7(5), e36816. 10.1371/journal.pone.0036816 PubMed DOI PMC

Honsa, P. , Valny, M. , Kriska, J. , Matuskova, H. , Harantova, L. , Kirdajova, D. , … Anderova, M. (2016). Generation of reactive astrocytes from NG2 cells is regulated by sonic hedgehog. Glia, 64(9), 1518–1531. 10.1002/glia.23019 PubMed DOI

Huang, W. , Bai, X. , Stopper, L. , Catalin, B. , Cartarozzi, L. P. , Scheller, A. , & Kirchhoff, F. (2018). During development NG2 glial cells of the spinal cord are restricted to the oligodendrocyte lineage, but generate astrocytes upon acute injury. Neuroscience, 385, 154–165. 10.1016/j.neuroscience.2018.06.015 PubMed DOI

Huang, W. , Guo, Q. , Bai, X. , Scheller, A. , & Kirchhoff, F. (2019). Early embryonic NG2 glia are exclusively gliogenic and do not generate neurons in the brain. Glia, 67(6), 1094–1103. 10.1002/glia.23590 PubMed DOI

Huang, W. , Zhao, N. , Bai, X. , Karram, K. , Trotter, J. , Goebbels, S. , … Kirchhoff, F. (2014). Novel NG2‐CreERT2 knock‐in mice demonstrate heterogeneous differentiation potential of NG2 glia during development. Glia, 62(6), 896–913. 10.1002/glia.22648 PubMed DOI

Juríková, M. , Danihel, Ľ. , Polák, Š. , & Varga, I. (2016). Ki67, PCNA, and MCM proteins: Markers of proliferation in the diagnosis of breast cancer. Acta Histochemica, 118(5), 544–552. 10.1016/j.acthis.2016.05.002 PubMed DOI

Kang, S. H. , Fukaya, M. , Yang, J. K. , Rothstein, J. D. , & Bergles, D. E. (2010). NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron, 68(4), 668–681. 10.1016/j.neuron.2010.09.009 PubMed DOI PMC

Kantzer, C. G. , Boutin, C. , Herzig, I. D. , Wittwer, C. , Reiß, S. , Tiveron, M. C. , … Bosio, A. (2017). Anti‐ACSA‐2 defines a novel monoclonal antibody for prospective isolation of living neonatal and adult astrocytes. Glia, 65(6), 990–1004. 10.1002/glia.23140 PubMed DOI

Káradóttir, R. , Hamilton, N. B. , Bakiri, Y. , & Attwell, D. (2008). Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nature Neuroscience, 11(4), 450–456. 10.1038/nn2060 PubMed DOI PMC

Khawaja, R. R. , Amit, A. , Fukaya, M. , Jeong, H.‐k. , Gross, S. , Gonzalez‐Fernandez, E. , Soboloff, J. , Bergles, D. E. , & Kang, S. H. (2021). GluA2 overexpression in oligodendrocyte progenitors promotes postinjury oligodendrocyte regeneration. Cell Reports, 35(7), 109147. 10.2139/ssrn.3422305 PubMed DOI PMC

Kirdajova, D. , & Anderova, M. (2020). NG2 cells and their neurogenic potential. Current Opinion in Pharmacology, 50, 53–60. 10.1016/j.coph.2019.11.005 PubMed DOI

Komitova, M. , Serwanski, D. R. , Lu, Q. R. , & Nishiyama, A. (2011). NG2 cells are not a major source of reactive astrocytes after neocortical stab wound injury. Glia, 59(5), 800–809. 10.1002/glia.21152 PubMed DOI PMC

Kukley, M. , Kiladze, M. , Tognatta, R. , Hans, M. , Swandulla, D. , Schramm, J. , & Dietrich, D. (2008). Glial cells are born with synapses. The FASEB Journal, 22(8), 2957–2969. 10.1096/fj.07-090985 PubMed DOI

Kula, B. , Chen, T. J. , & Kukley, M. (2019). Glutamatergic signaling between neurons and oligodendrocyte lineage cells: Is it synaptic or non‐synaptic? Glia, 67(11), 2071–2091. 10.1002/glia.23617 PubMed DOI

Leuchtmann, E. A. , Ratner, A. E. , Vijitruth, R. , Qu, Y. , & McDonald, J. W. (2003). AMPA receptors are the major mediators of excitotoxic death in mature oligodendrocytes. Neurobiology of Disease, 14(3), 336–348. 10.1016/j.nbd.2003.07.004 PubMed DOI

Levine, J. (2016). The reactions and role of NG2 glia in spinal cord injury. Brain Research, 1638, 199–208. 10.1016/j.brainres.2015.07.026 PubMed DOI PMC

Loulier, K. , Ruat, M. , & Traiffort, E. (2006). Increase of proliferating oligodendroglial progenitors in the adult mouse brain upon sonic hedgehog delivery in the lateral ventricle. Journal of Neurochemistry, 98(2), 530–542. 10.1111/j.1471-4159.2006.03896.x PubMed DOI

Lun, A. T. L. , Riesenfeld, S. , Andrews, T. , Dao, T. P. , Gomes, T. , & Marioni, J. C. (2019). EmptyDrops: Distinguishing cells from empty droplets in droplet‐based single‐cell RNA sequencing data. Genome Biology, 20(1), 63. 10.1186/s13059-019-1662-y PubMed DOI PMC

Magaki, S. D. , Williams, C. K. , & Vinters, H. V. (2018). Glial function (and dysfunction) in the normal & ischemic brain. Neuropharmacology, 134, 218–225. 10.1016/j.neuropharm.2017.11.009 PubMed DOI PMC

Marques, S. , van Bruggen, D. , & Castelo‐Branco, G. (2019). Single‐cell RNA sequencing of Oligodendrocyte lineage cells from the mouse central nervous system. Methods in Molecular Biology, 1936, 1–21. 10.1007/978-1-4939-9072-6_1 PubMed DOI

Marques, S. , van Bruggen, D. , Vanichkina, D. P. , Floriddia, E. M. , Munguba, H. , Varemo, L. , … Castelo‐Branco, G. (2018). Transcriptional convergence of oligodendrocyte lineage progenitors during development. Developmental Cell, 46(4), 504–517.e507. 10.1016/j.devcel.2018.07.005 PubMed DOI PMC

Marques, S. , Zeisel, A. , Codeluppi, S. , van Bruggen, D. , Mendanha Falcao, A. , Xiao, L. , … Castelo‐Branco, G. (2016). Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science, 352(6291), 1326–1329. 10.1126/science.aaf6463 PubMed DOI PMC

Martinez‐Lozada, Z. , Waggener, C. T. , Kim, K. , Zou, S. , Knapp, P. E. , Hayashi, Y. , … Fuss, B. (2014). Activation of sodium‐dependent glutamate transporters regulates the morphological aspects of oligodendrocyte maturation via signaling through calcium/calmodulin‐dependent kinase IIβ's actin‐binding/‐stabilizing domain. Glia, 62(9), 1543–1558. 10.1002/glia.22699 PubMed DOI PMC

McDonald, J. W. , Bhattacharyya, T. , Sensi, S. L. , Lobner, D. , Ying, H. S. , Canzoniero, L. M. , & Choi, D. W. (1998). Extracellular acidity potentiates AMPA receptor‐mediated cortical neuronal death. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 18(16), 6290–6299. 10.1523/jneurosci.18-16-06290.1998 PubMed DOI PMC

Milosevic, A. , Liebmann, T. , Knudsen, M. , Schintu, N. , Svenningsson, P. , & Greengard, P. (2017). Cell‐ and region‐specific expression of depression‐related protein p11 (S100a10) in the brain. The Journal of Comparative Neurology, 525(4), 955–975. 10.1002/cne.24113 PubMed DOI PMC

Mori, T. , Tan, J. , Arendash, G. W. , Koyama, N. , Nojima, Y. , & Town, T. (2008). Overexpression of human S100B exacerbates brain damage and periinfarct gliosis after permanent focal ischemia. Stroke, 39(7), 2114–2121. 10.1161/strokeaha.107.503821 PubMed DOI PMC

Nawashiro, H. , Brenner, M. , Fukui, S. , Shima, K. , & Hallenbeck, J. M. (2000). High susceptibility to cerebral ischemia in GFAP‐null mice. Journal of Cerebral Blood Flow & Metabolism, 20(7), 1040–1044. 10.1097/00004647-200007000-00003 PubMed DOI

Neprasova, H. , Anderova, M. , Petrik, D. , Vargova, L. , Kubinova, S. , Chvatal, A. , & Sykova, E. (2007). High extracellular K(+) evokes changes in voltage‐dependent K(+) and Na (+) currents and volume regulation in astrocytes. Pflügers Archiv, 453(6), 839–849. 10.1007/s00424-006-0151-9 PubMed DOI

Nishiyama, A. , Boshans, L. , Goncalves, C. M. , Wegrzyn, J. , & Patel, K. D. (2016). Lineage, fate, and fate potential of NG2‐glia. Brain Research, 1638, 116–128. 10.1016/j.brainres.2015.08.013 PubMed DOI PMC

Nishiyama, A. , Watanabe, M. , Yang, Z. , & Bu, J. (2002). Identity, distribution, and development of polydendrocytes: NG2‐expressing glial cells. Journal of Neurocytology, 31(6–7), 437–455. PubMed

Nolte, C. , Matyash, M. , Pivneva, T. , Schipke, C. G. , Ohlemeyer, C. , Hanisch, U. K. , … Kettenmann, H. (2001). GFAP promoter‐controlled EGFP‐expressing transgenic mice: A tool to visualize astrocytes and astrogliosis in living brain tissue. Glia, 33(1), 72–86. PubMed

Notomi, T. , & Shigemoto, R. (2004). Immunohistochemical localization of Ih channel subunits, HCN1‐4, in the rat brain. The Journal of Comparative Neurology, 471(3), 241–276. 10.1002/cne.11039 PubMed DOI

Ozerdem, U. , Grako, K. A. , Dahlin‐Huppe, K. , Monosov, E. , & Stallcup, W. B. (2001). NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Developmental Dynamics, 222(2), 218–227. 10.1002/dvdy.1200 PubMed DOI

Pablo, Y. , Nilsson, M. , Pekna, M. , & Pekny, M. (2013). Intermediate filaments are important for astrocyte response to oxidative stress induced by oxygen‐glucose deprivation and reperfusion. Histochemistry and Cell Biology, 140(1), 81–91. 10.1007/s00418-013-1110-0 PubMed DOI

Pivonkova, H. , Benesova, J. , Butenko, O. , Chvatal, A. , & Anderova, M. (2010). Impact of global cerebral ischemia on K+ channel expression and membrane properties of glial cells in the rat hippocampus. Neurochemistry International, 57(7), 783–794. 10.1016/j.neuint.2010.08.016 PubMed DOI

Polito, A. , & Reynolds, R. (2005). NG2‐expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. Journal of Anatomy, 207(6), 707–716. 10.1111/j.1469-7580.2005.00454.x PubMed DOI PMC

Rivers, L. E. , Young, K. M. , Rizzi, M. , Jamen, F. , Psachoulia, K. , Wade, A. , … Richardson, W. D. (2008). PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nature Neuroscience, 11(12), 1392–1401. 10.1038/nn.2220 PubMed DOI PMC

Rusnakova, V. , Honsa, P. , Dzamba, D. , Ståhlberg, A. , Kubista, M. , & Anderova, M. (2013). Heterogeneity of astrocytes: From development to injury ‐ single cell gene expression. PLoS One, 8(8), e69734. 10.1371/journal.pone.0069734 PubMed DOI PMC

Saab, A. S. , Tzvetavona, I. D. , Trevisiol, A. , Baltan, S. , Dibaj, P. , Kusch, K. , … Nave, K. A. (2016). Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron, 91(1), 119–132. 10.1016/j.neuron.2016.05.016 PubMed DOI PMC

Sanchez‐Gomez, M. V. , Alberdi, E. , Perez‐Navarro, E. , Alberch, J. , & Matute, C. (2011). Bax and calpain mediate excitotoxic oligodendrocyte death induced by activation of both AMPA and kainate receptors. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(8), 2996–3006. 10.1523/JNEUROSCI.5578-10.2011 PubMed DOI PMC

Schools, G. P. , Zhou, M. , & Kimelberg, H. K. (2003). Electrophysiologically “complex” glial cells freshly isolated from the hippocampus are immunopositive for the chondroitin sulfate proteoglycan NG2. Journal of Neuroscience Research, 73(6), 765–777. 10.1002/jnr.10680 PubMed DOI

Shao, X. , Liao, J. , Lu, X. , Xue, R. , Ai, N. , & Fan, X. (2020). scCATCH: Automatic annotation on cell types of clusters from single‐cell RNA sequencing data. iScience, 23(3), 100882. 10.1016/j.isci.2020.100882 PubMed DOI PMC

Shivji, K. K. , Kenny, M. K. , & Wood, R. D. (1992). Proliferating cell nuclear antigen is required for DNA excision repair. Cell, 69(2), 367–374. 10.1016/0092-8674(92)90416-a PubMed DOI

Simons, M. , & Nave, K. A. (2015). Oligodendrocytes: Myelination and axonal support. Cold Spring Harbor Perspectives in Biology, 8(1), a020479. 10.1101/cshperspect.a020479 PubMed DOI PMC

Skripuletz, T. , Gudi, V. , Hackstette, D. , & Stangel, M. (2011). De‐ and remyelination in the CNS white and grey matter induced by cuprizone: The old, the new, and the unexpected. Histology and Histopathology, 26(12), 1585–1597. PubMed

Sofroniew, M. V. , & Vinters, H. V. (2010). Astrocytes: Biology and pathology. Acta Neuropathologica, 119(1), 7–35. 10.1007/s00401-009-0619-8 PubMed DOI PMC

Song, F. E. , Huang, J. L. , Lin, S. H. , Wang, S. , Ma, G. F. , & Tong, X. P. (2017). Roles of NG2‐glia in ischemic stroke. CNS Neuroscience & Therapeutics, 23(7), 547–553. 10.1111/cns.12690 PubMed DOI PMC

Spitzer, S. , Volbracht, K. , Lundgaard, I. , & Karadottir, R. T. (2016). Glutamate signalling: A multifaceted modulator of oligodendrocyte lineage cells in health and disease. Neuropharmacology, 110, 574–585. 10.1016/j.neuropharm.2016.06.014 PubMed DOI

Spitzer, S. O. , Sitnikov, S. , Kamen, Y. , Evans, K. A. , Kronenberg‐Versteeg, D. , Dietmann, S. , … Karadottir, R. T. (2019). Oligodendrocyte progenitor cells become regionally diverse and heterogeneous with age. Neuron, 101(3), 459–471.e455. 10.1016/j.neuron.2018.12.020 PubMed DOI PMC

Streitberg, A. , Jäkel, S. , Eugenin von Bernhardi, J. , Straube, C. , Buggenthin, F. , Marr, C. , & Dimou, L. (2021). NG2‐glia transiently overcome their homeostatic network and contribute to wound closure after brain injury. Frontiers in Cell and Developmental Biology, 9, 662056–662056. 10.3389/fcell.2021.662056 PubMed DOI PMC

Stuart, T. , Butler, A. , Hoffman, P. , Hafemeister, C. , Papalexi, E. , Mauck, W. M., 3rd , … Satija, R. (2019). Comprehensive integration of single‐cell data. Cell, 177(7), 1888–1902.e1821. 10.1016/j.cell.2019.05.031 PubMed DOI PMC

Suárez‐Pozos, E. , Thomason, E. J. , & Fuss, B. (2020). Glutamate transporters: expression and function in oligodendrocytes. Neurochemical Research, 45(3), 551–560. 10.1007/s11064-018-02708-x PubMed DOI PMC

Tamura, Y. , Kataoka, Y. , Cui, Y. , Takamori, Y. , Watanabe, Y. , & Yamada, H. (2007). Multi‐directional differentiation of doublecortin‐ and NG2‐immunopositive progenitor cells in the adult rat neocortex in vivo. The European Journal of Neuroscience, 25(12), 3489–3498. 10.1111/j.1460-9568.2007.05617.x PubMed DOI

Tanner, D. C. , Cherry, J. D. , & Mayer‐Pröschel, M. (2011). Oligodendrocyte progenitors reversibly exit the cell cycle and give rise to astrocytes in response to interferon‐γ. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(16), 6235–6246. 10.1523/jneurosci.5905-10.2011 PubMed DOI PMC

Tripathi, R. B. , Rivers, L. E. , Young, K. M. , Jamen, F. , & Richardson, W. D. (2010). NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30(48), 16383–16390. 10.1523/jneurosci.3411-10.2010 PubMed DOI PMC

Tsoa, R. W. , Coskun, V. , Ho, C. K. , & de Vellis, J. (2014). Spatiotemporally different origins of NG2 progenitors produce cortical interneurons versus glia in the mammalian forebrain. Proceedings of the National Academy of Sciences of the United States of America, 111(20), 7444–7449. 10.1073/pnas.1400422111 PubMed DOI PMC

Valny, M. , Honsa, P. , Kirdajova, D. , Kamenik, Z. , & Anderova, M. (2016). Tamoxifen in the mouse brain: Implications for fate‐mapping studies using the Tamoxifen‐inducible Cre‐loxP system. Frontiers in Cellular Neuroscience, 10, 243. 10.3389/fncel.2016.00243 PubMed DOI PMC

Valny, M. , Honsa, P. , Waloschkova, E. , Matuskova, H. , Kriska, J. , Kirdajova, D. , … Anderova, M. (2018). A single‐cell analysis reveals multiple roles of oligodendroglial lineage cells during post‐ischemic regeneration. Glia, 66(5), 1068–1081. 10.1002/glia.23301 PubMed DOI

Vigano, F. , & Dimou, L. (2016). The heterogeneous nature of NG2‐glia. Brain Research, 1638, 129–137. 10.1016/j.brainres.2015.09.012 PubMed DOI

Viganò, F. , Möbius, W. , Götz, M. , & Dimou, L. (2013). Transplantation reveals regional differences in oligodendrocyte differentiation in the adult brain. Nature Neuroscience, 16(10), 1370–1372. 10.1038/nn.3503 PubMed DOI

Wallraff, A. , Odermatt, B. , Willecke, K. , & Steinhäuser, C. (2004). Distinct types of astroglial cells in the hippocampus differ in gap junction coupling. Glia, 48(1), 36–43. 10.1002/glia.20040 PubMed DOI

Wang, L. C. , & Almazan, G. (2016). Role of sonic hedgehog signaling in oligodendrocyte differentiation. Neurochemical Research, 41(12), 3289–3299. 10.1007/s11064-016-2061-3 PubMed DOI

Wanner, I. B. , Anderson, M. A. , Song, B. , Levine, J. , Fernandez, A. , Gray‐Thompson, Z. , … Sofroniew, M. V. (2013). Glial scar Borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3‐dependent mechanisms after spinal cord injury. Journal of Neuroscience, 33(31), 12870–12886. 10.1523/jneurosci.2121-13.2013 PubMed DOI PMC

Wu, Y. E. , Pan, L. , Zuo, Y. , Li, X. , & Hong, W. (2017). Detecting activated cell populations using single‐cell RNA‐Seq. Neuron, 96(2), 313–329.e316. 10.1016/j.neuron.2017.09.026 PubMed DOI

Xia, W. , Liu, Y. , & Jiao, J. (2015). GRM7 regulates embryonic neurogenesis via CREB and YAP. Stem Cell Reports, 4(5), 795–810. 10.1016/j.stemcr.2015.03.004 PubMed DOI PMC

Xin, W. , Mironova, Y. A. , Shen, H. , Marino, R. A. M. , Waisman, A. , Lamers, W. H. , … Bonci, A. (2019). Oligodendrocytes support neuronal glutamatergic transmission via expression of glutamine synthetase. Cell Reports, 27(8), 2262–2271 e2265. 10.1016/j.celrep.2019.04.094 PubMed DOI PMC

Ye, J. , Coulouris, G. , Zaretskaya, I. , Cutcutache, I. , Rozen, S. , & Madden, T. L. (2012). Primer‐BLAST: A tool to design target‐specific primers for polymerase chain reaction. BMC Bioinformatics, 13, 134. 10.1186/1471-2105-13-134 PubMed DOI PMC

Young, K. M. , Psachoulia, K. , Tripathi, R. B. , Dunn, S. J. , Cossell, L. , Attwell, D. , … Richardson, W. D. (2013). Oligodendrocyte dynamics in the healthy adult CNS: Evidence for myelin remodeling. Neuron, 77(5), 873–885. 10.1016/j.neuron.2013.01.006 PubMed DOI PMC

Zawadzka, M. , Rivers, L. E. , Fancy, S. P. , Zhao, C. , Tripathi, R. , Jamen, F. , … Franklin, R. J. (2010). CNS‐resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell, 6(6), 578–590. 10.1016/j.stem.2010.04.002 PubMed DOI PMC

Zeisel, A. , Hochgerner, H. , Lonnerberg, P. , Johnsson, A. , Memic, F. , van der Zwan, J. , … Linnarsson, S. (2018). Molecular architecture of the mouse nervous system. Cell, 174(4), 999–1014.e1022. 10.1016/j.cell.2018.06.021 PubMed DOI PMC

Zhang, L. , Chopp, M. , Zhang, R. L. , Wang, L. , Zhang, J. , Wang, Y. , … Zhang, Z. G. (2010). Erythropoietin amplifies stroke‐induced oligodendrogenesis in the rat. PLoS One, 5(6), e11016. 10.1371/journal.pone.0011016 PubMed DOI PMC

Zhang, S. , Zhu, X. , Gui, X. , Croteau, C. , Song, L. , Xu, J. , … Guo, F. (2018). Sox2 is essential for oligodendroglial proliferation and differentiation during postnatal brain myelination and CNS Remyelination. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 38(7), 1802–1820. 10.1523/JNEUROSCI.1291-17.2018 PubMed DOI PMC

Zhang, Y. , Chen, K. , Sloan, S. A. , Bennett, M. L. , Scholze, A. R. , O'Keeffe, S. , … Guarnieri, P. (2014). An RNA‐sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. Journal of Neuroscience, 34(36), 11929–11947. 10.1523/jneurosci.1860-14.2014 PubMed DOI PMC

Zhao, C. , Ma, D. , Zawadzka, M. , Fancy, S. P. J. , Elis‐Williams, L. , Bouvier, G. , … Franklin, R. J. M. (2015). Sox2 sustains recruitment of Oligodendrocyte progenitor cells following CNS demyelination and primes them for differentiation during Remyelination. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 35(33), 11482–11499. 10.1523/JNEUROSCI.3655-14.2015 PubMed DOI PMC

Zhou, M. , Schools, G. P. , & Kimelberg, H. K. (2006). Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: Mature astrocytes are electrophysiologically passive. Journal of Neurophysiology, 95(1), 134–143. 10.1152/jn.00570.2005 PubMed DOI

Zhou, M. , Xu, G. , Xie, M. , Zhang, X. , Schools, G. P. , Ma, L. , … Chen, H. (2009). TWIK‐1 and TREK‐1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(26), 8551–8564. 10.1523/jneurosci.5784-08.2009 PubMed DOI PMC

Zhu, H. , & Dahlström, A. (2007). Glial fibrillary acidic protein‐expressing cells in the neurogenic regions in normal and injured adult brains. Journal of Neuroscience Research, 85(12), 2783–2792. 10.1002/jnr.21257 PubMed DOI

Zhu, X. , Bergles, D. E. , & Nishiyama, A. (2008). NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development, 135(1), 145–157. 10.1242/dev.004895 PubMed DOI

Zhu, X. , Hill, R. A. , Dietrich, D. , Komitova, M. , Suzuki, R. , & Nishiyama, A. (2011). Age‐dependent fate and lineage restriction of single NG2 cells. Development, 138(4), 745–753. 10.1242/dev.047951 PubMed DOI PMC

A view of the genetic and proteomic profile of extracellular matrix molecules in aging and stroke

Astrocytic TRPV4 Channels and Their Role in Brain Ischemia

On the Common Journey of Neural Cells through Ischemic Brain Injury and Alzheimer's Disease