Repetitive injury and absence of monocytes promote astrocyte self-renewal and neurological recovery.
TBI
astrocyte topology
cognitive disfunction
inflammation
reactive gliosis
self-renew
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
01
05
2020
revised:
07
07
2020
accepted:
08
07
2020
pubmed:
4
8
2020
medline:
3
2
2022
entrez:
4
8
2020
Statut:
ppublish
Résumé
Unlike microglia and NG2 glia, astrocytes are incapable of migrating to sites of injury in the posttraumatic cerebral cortex, instead relying on proliferation to replenish their numbers and distribution in the affected region. However, neither the spectrum of their proliferative repertoire nor their postinjury distribution has been examined in vivo. Using a combination of different thymidine analogs and clonal analysis in a model of repetitive traumatic brain injury, we show for the first time that astrocytes that are quiescent following an initial injury can be coerced to proliferate after a repeated insult in the cerebral cortex grey matter. Interestingly, this process is promoted by invasion of monocytes to the injury site, as their genetic ablation (using CCR2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
165-181Informations de copyright
© 2020 The Authors. Glia published by Wiley Periodicals LLC .
Références
Anderson, M. A., Burda, J. E., Ren, Y., Ao, Y., O'Shea, T. M., Kawaguchi, R., … Sofroniew, M. V. (2016). Astrocyte scar formation aids central nervous system axon regeneration. Nature, 532(7598), 195-200. https://doi.org/10.1038/nature17623
Araque, A., Carmignoto, G., Haydon, P. G., Oliet, S. H., Robitaille, R., & Volterra, A. (2014). Gliotransmitters travel in time and space. Neuron, 81(4), 728-739. https://doi.org/10.1016/j.neuron.2014.02.007
Bach, M. E., Hawkins, R. D., Osman, M., Kandel, E. R., & Mayford, M. (1995). Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell, 81(6), 905-915. https://doi.org/10.1016/0092-8674(95)90010-1
Bailey, K. R., & Crawley, J. N. (2009). Anxiety-related behaviors in mice. In J. J. Buccafusco (Ed.), Methods of behavior analysis in neuroscience (2nd ed.). Boca Raton, FL: CRC Press/Taylor & Francis.
Bardehle, S., Kruger, M., Buggenthin, F., Schwausch, J., Ninkovic, J., Clevers, H., … Gotz, M. (2013). Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nature Neuroscience, 16(5), 580-586. https://doi.org/10.1038/nn.3371
Barker, J. M., Charlier, T. D., Ball, G. F., & Balthazart, J. (2013). A new method for in vitro detection of bromodeoxyuridine in serum: A proof of concept in a songbird species, the canary. PLoS ONE, 8(5), e63692. https://doi.org/10.1371/journal.pone.0063692
Barnes, C. A. (1979). Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. Journal of Comparative and Physiological Psychology, 93(1), 74-104. https://doi.org/10.1037/h0077579
Batiuk, M. Y., Martirosyan, A., Wahis, J., de Vin, F., Marneffe, C., Kusserow, C., … Holt, M. G. (2020). Identification of region-specific astrocyte subtypes at single cell resolution. Nature Communications, 11(1), 1220. https://doi.org/10.1038/s41467-019-14198-8
Bayraktar, O. A., Bartels, T., Holmqvist, S., Kleshchevnikov, V., Martirosyan, A., Polioudakis, D., … Rowitch, D. H. (2020). Astrocyte layers in the mammalian cerebral cortex revealed by a single-cell in situ transcriptomic map. Nature Neuroscience, 23(4), 500-509. https://doi.org/10.1038/s41593-020-0602-1
Belarbi, K., Jopson, T., Arellano, C., Fike, J. R., & Rosi, S. (2013). CCR2 deficiency prevents neuronal dysfunction and cognitive impairments induced by cranial irradiation. Cancer Research, 73(3), 1201-1210. https://doi.org/10.1158/0008-5472.CAN-12-2989
Ben Haim, L., & Rowitch, D. H. (2017). Functional diversity of astrocytes in neural circuit regulation. Nature Reviews. Neuroscience, 18(1), 31-41. https://doi.org/10.1038/nrn.2016.159
Biernaskie, J., Chernenko, G., & Corbett, D. (2004). Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. The Journal of Neuroscience, 24(5), 1245-1254. https://doi.org/10.1523/JNEUROSCI.3834-03.2004
Boring, L., Gosling, J., Cleary, M., & Charo, I. F. (1998). Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis. Nature, 394(6696), 894-897. https://doi.org/10.1038/29788
Brizzi, M. F., Tarone, G., & Defilippi, P. (2012). Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Current Opinion in Cell Biology, 24(5), 645-651. https://doi.org/10.1016/j.ceb.2012.07.001
Buffo, A., Rite, I., Tripathi, P., Lepier, A., Colak, D., Horn, A. P., … Gotz, M. (2008). Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proceedings of the National Academy of Sciences of the United States of America, 105(9), 3581-3586. https://doi.org/10.1073/pnas.0709002105
Bylicky, M. A., Mueller, G. P., & Day, R. M. (2018). Mechanisms of endogenous Neuroprotective effects of astrocytes in brain injury. Oxidative Medicine and Cellular Longevity, 2018, 6501031. https://doi.org/10.1155/2018/6501031
Calzolari, F., Michel, J., Baumgart, E. V., Theis, F., Gotz, M., & Ninkovic, J. (2015). Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nature Neuroscience, 18(4), 490-492. https://doi.org/10.1038/nn.3963
Chai, H., Diaz-Castro, B., Shigetomi, E., Monte, E., Octeau, J. C., Yu, X., … Khakh, B. S. (2017). Neural circuit-specialized astrocytes: Transcriptomic, proteomic, morphological, and functional evidence. Neuron, 95(3), 531-549 e539. https://doi.org/10.1016/j.neuron.2017.06.029
Chandrasekar, A., Heuvel, F. O., Tar, L., Hagenston, A. M., Palmer, A., Linkus, B., … Roselli, F. (2019). Parvalbumin interneurons shape neuronal vulnerability in blunt TBI. Cerebral Cortex, 29(6), 2701-2715. https://doi.org/10.1093/cercor/bhy139
Chopp, M., Zhang, Z. G., & Jiang, Q. (2007). Neurogenesis, angiogenesis, and MRI indices of functional recovery from stroke. Stroke, 38(2 Suppl), 827-831. https://doi.org/10.1161/01.STR.0000250235.80253.e9
Chu, H. X., Arumugam, T. V., Gelderblom, M., Magnus, T., Drummond, G. R., & Sobey, C. G. (2014). Role of CCR2 in inflammatory conditions of the central nervous system. Journal of Cerebral Blood Flow and Metabolism, 34(9), 1425-1429. https://doi.org/10.1038/jcbfm.2014.120
Clark, D., Brazina, S., Yang, F., Hu, D., Hsieh, C. L., Niemi, E. C., … Marcucio, R. (2020). Age-related changes to macrophages are detrimental to fracture healing in mice. Aging Cell, 19(3), e13112. https://doi.org/10.1111/acel.13112
Clark, R. A. (2008). Synergistic signaling from extracellular matrix-growth factor complexes. The Journal of Investigative Dermatology, 128(6), 1354-1355. https://doi.org/10.1038/jid.2008.75
Cramer, S. C., & Riley, J. D. (2008). Neuroplasticity and brain repair after stroke. Current Opinion in Neurology, 21(1), 76-82. https://doi.org/10.1097/WCO.0b013e3282f36cb6
Dallerac, G., & Rouach, N. (2016). Astrocytes as new targets to improve cognitive functions. Progress in Neurobiology, 144, 48-67. https://doi.org/10.1016/j.pneurobio.2016.01.003
Dimou, L., & Gotz, M. (2014). Glial cells as progenitors and stem cells: New roles in the healthy and diseased brain. Physiological Reviews, 94(3), 709-737. https://doi.org/10.1152/physrev.00036.2013
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, 28(41), 10434-10442. https://doi.org/10.1523/JNEUROSCI.2831-08.2008
Domann, R., Hagemann, G., Kraemer, M., Freund, H. J., & Witte, O. W. (1993). Electrophysiological changes in the surrounding brain tissue of photochemically induced cortical infarcts in the rat. Neuroscience Letters, 155(1), 69-72. https://doi.org/10.1016/0304-3940(93)90675-b
Doyle, K. P., Simon, R. P., & Stenzel-Poore, M. P. (2008). Mechanisms of ischemic brain damage. Neuropharmacology, 55(3), 310-318. https://doi.org/10.1016/j.neuropharm.2008.01.005
Faiz, M., Sachewsky, N., Gascon, S., Bang, K. W., Morshead, C. M., & Nagy, A. (2015). Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell, 17(5), 624-634. https://doi.org/10.1016/j.stem.2015.08.002
Faulkner, J. R., Herrmann, J. E., Woo, M. J., Tansey, K. E., Doan, N. B., & Sofroniew, M. V. (2004). Reactive astrocytes protect tissue and preserve function after spinal cord injury. The Journal of Neuroscience, 24(9), 2143-2155. https://doi.org/10.1523/JNEUROSCI.3547-03.2004
Frik, J., Merl-Pham, J., Plesnila, N., Mattugini, N., Kjell, J., Kraska, J., … Gotz, M. (2018). Cross-talk between monocyte invasion and astrocyte proliferation regulates scarring in brain injury. EMBO Reports, 19(5), 20. https://doi.org/10.15252/embr.201745294
Gotz, M., Sirko, S., Beckers, J., & Irmler, M. (2015). Reactive astrocytes as neural stem or progenitor cells: in vivo lineage, in vitro potential, and genome-wide expression analysis. GLIA, 63(8), 1452-1468. https://doi.org/10.1002/glia.22850
Gyoneva, S., Kim, D., Katsumoto, A., Kokiko-Cochran, O. N., Lamb, B. T., & Ransohoff, R. M. (2015). Ccr2 deletion dissociates cavity size and tau pathology after mild traumatic brain injury. Journal of Neuroinflammation, 12, 228. https://doi.org/10.1186/s12974-015-0443-0
Halassa, M. M., & Haydon, P. G. (2010). Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior. Annual Review of Physiology, 72, 335-355. https://doi.org/10.1146/annurev-physiol-021909-135843
Heimann, G., Canhos, L. L., Frik, J., Jager, G., Lepko, T., Ninkovic, J., … Sirko, S. (2017). Changes in the proliferative program limit astrocyte homeostasis in the aged post-traumatic murine cerebral cortex. Cerebral Cortex, 27(8), 4213-4228. https://doi.org/10.1093/cercor/bhx112
Heimann, G., & Sirko, S. (2019). Investigating age-related changes in proliferation and the cell division repertoire of parenchymal reactive astrocytes. Methods in Molecular Biology, 1938, 277-292. https://doi.org/10.1007/978-1-4939-9068-9_20
Heintz, N. (2004). Gene expression nervous system atlas (GENSAT). Nature Neuroscience, 7(5), 483. https://doi.org/10.1038/nn0504-483
Hirrlinger, J., Scheller, A., Hirrlinger, P. G., Kellert, B., Tang, W., Wehr, M. C., … Kirchhoff, F. (2009). Split-cre complementation indicates coincident activity of different genes in vivo. PLoS ONE, 4(1), e4286. https://doi.org/10.1371/journal.pone.0004286
Hol, E. M., & Pekny, M. (2015). Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Current Opinion in Cell Biology, 32, 121-130. https://doi.org/10.1016/j.ceb.2015.02.004
Hsieh, C. L., Niemi, E. C., Wang, S. H., Lee, C. C., Bingham, D., Zhang, J., … Nakamura, M. C. (2014). CCR2 deficiency impairs macrophage infiltration and improves cognitive function after traumatic brain injury. Journal of Neurotrauma, 31(20), 1677-1688. https://doi.org/10.1089/neu.2013.3252
Huemmeke, M., Eysel, U. T., & Mittmann, T. (2004). Lesion-induced enhancement of LTP in rat visual cortex is mediated by NMDA receptors containing the NR2B subunit. The Journal of Physiology, 559(Pt 3), 875-882. https://doi.org/10.1113/jphysiol.2004.069534
Hynes, R. O. (2009). The extracellular matrix: Not just pretty fibrils. Science, 326(5957), 1216-1219. https://doi.org/10.1126/science.1176009
Imbrosci, B., Eysel, U. T., & Mittmann, T. (2010). Metaplasticity of horizontal connections in the vicinity of focal laser lesions in rat visual cortex. The Journal of Physiology, 588(Pt 23), 4695-4703. https://doi.org/10.1113/jphysiol.2010.198192
Imbrosci, B., & Mittmann, T. (2011). Functional consequences of the disturbances in the GABA-mediated inhibition induced by injuries in the cerebral cortex. Neural Plasticity, 2011, 614329. https://doi.org/10.1155/2011/614329
Ito, U., Kuroiwa, T., Nagasao, J., Kawakami, E., & Oyanagi, K. (2006). Temporal profiles of axon terminals, synapses and spines in the ischemic penumbra of the cerebral cortex: Ultrastructure of neuronal remodeling. Stroke, 37(8), 2134-2139. https://doi.org/10.1161/01.STR.0000231875.96714.b1
Izikson, L., Klein, R. S., Charo, I. F., Weiner, H. L., & Luster, A. D. (2000). Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. The Journal of Experimental Medicine, 192(7), 1075-1080. https://doi.org/10.1084/jem.192.7.1075
Jahn, H. M., Scheller, A., & Kirchhoff, F. (2015). Genetic control of astrocyte function in neural circuits. Frontiers in Cellular Neuroscience, 9, 310. https://doi.org/10.3389/fncel.2015.00310
Jakel, S., & Dimou, L. (2017). Glial cells and their function in the adult brain: A journey through the history of their ablation. Frontiers in Cellular Neuroscience, 11, 24. https://doi.org/10.3389/fncel.2017.00024
Jukkola, P., Guerrero, T., Gray, V., & Gu, C. (2013). Astrocytes differentially respond to inflammatory autoimmune insults and imbalances of neural activity. Acta Neuropathologica Communications, 1, 70. https://doi.org/10.1186/2051-5960-1-70
Khakh, B. S., & Deneen, B. (2019). The emerging nature of astrocyte diversity. Annual Review of Neuroscience, 42, 187-207. https://doi.org/10.1146/annurev-neuro-070918-050443
Khakh, B. S., & Sofroniew, M. V. (2015). Diversity of astrocyte functions and phenotypes in neural circuits. Nature Neuroscience, 18(7), 942-952. https://doi.org/10.1038/nn.4043
Kjell, J., & Gotz, M. (2020). Filling the gaps - a call for comprehensive analysis of extracellular matrix of the glial scar in region- and injury-specific contexts. Frontiers in Cellular Neuroscience, 14, 32. https://doi.org/10.3389/fncel.2020.00032
Kolb, B., Gibb, R., & Gorny, G. (2000). Cortical plasticity and the development of behavior after early frontal cortical injury. Developmental Neuropsychology, 18(3), 423-444. https://doi.org/10.1207/S1532694208Kolb
Komitova, M., Zhu, X., Serwanski, D. R., & Nishiyama, A. (2009). NG2 cells are distinct from neurogenic cells in the postnatal mouse subventricular zone. The Journal of Comparative Neurology, 512(5), 702-716. https://doi.org/10.1002/cne.21917
Lanjakornsiripan, D., Pior, B. J., Kawaguchi, D., Furutachi, S., Tahara, T., Katsuyama, Y., … Gotoh, Y. (2018). Layer-specific morphological and molecular differences in neocortical astrocytes and their dependence on neuronal layers. Nature Communications, 9(1), 1623. https://doi.org/10.1038/s41467-018-03940-3
Laviola, G., Macri, S., Morley-Fletcher, S., & Adriani, W. (2003). Risk-taking behavior in adolescent mice: Psychobiological determinants and early epigenetic influence. Neuroscience and Biobehavioral Reviews, 27(1-2), 19-31. https://doi.org/10.1016/s0149-7634(03)00006-x
Li, L., Jiang, Q., Zhang, L., Ding, G., Gang Zhang, Z., Li, Q., … Chopp, M. (2007). Angiogenesis and improved cerebral blood flow in the ischemic boundary area detected by MRI after administration of sildenafil to rats with embolic stroke. Brain Research, 1132(1), 185-192. https://doi.org/10.1016/j.brainres.2006.10.098
Liu, B., Teschemacher, A. G., & Kasparov, S. (2017). Neuroprotective potential of astroglia. Journal of Neuroscience Research, 95(11), 2126-2139. https://doi.org/10.1002/jnr.24140
Liu, C. Y., Yang, Y., Ju, W. N., Wang, X., & Zhang, H. L. (2018). Emerging roles of astrocytes in neuro-vascular unit and the tripartite synapse with emphasis on reactive gliosis in the context of Alzheimer's disease. Frontiers in Cellular Neuroscience, 12, 193. https://doi.org/10.3389/fncel.2018.00193
Luhmann, H. J., Mittmann, T., Schmidt-Kastner, R., Eysel, U. T., Mudrick-Donnon, L. A., & Heinemann, U. (1996). Hyperexcitability after focal lesions and transient ischemia in rat neocortex. Epilepsy Research. Supplement, 12, 119-128. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/9302510
Martin-Lopez, E., Garcia-Marques, J., Nunez-Llaves, R., & Lopez-Mascaraque, L. (2013). Clonal astrocytic response to cortical injury. PLoS ONE, 8(9), e74039. https://doi.org/10.1371/journal.pone.0074039
Maxwell, W. L., MacKinnon, M. A., Stewart, J. E., & Graham, D. I. (2010). Stereology of cerebral cortex after traumatic brain injury matched to the Glasgow outcome score. Brain, 133(Pt 1), 139-160. https://doi.org/10.1093/brain/awp264
Morel, L., Men, Y., Chiang, M. S. R., Tian, Y., Jin, S., Yelick, J., … Yang, Y. (2019). Intracortical astrocyte subpopulations defined by astrocyte reporter mice in the adult brain. GLIA, 67(1), 171-181. https://doi.org/10.1002/glia.23545
Morganti, J. M., Jopson, T. D., Liu, S., Riparip, L. K., Guandique, C. K., Gupta, N., … Rosi, S. (2015). CCR2 antagonism alters brain macrophage polarization and ameliorates cognitive dysfunction induced by traumatic brain injury. The Journal of Neuroscience, 35(2), 748-760. https://doi.org/10.1523/JNEUROSCI.2405-14.2015
Mori, T., Tanaka, K., Buffo, A., Wurst, W., Kuhn, R., & Gotz, M. (2006). Inducible gene deletion in astroglia and radial glia- -a valuable tool for functional and lineage analysis. GLIA, 54(1), 21-34. https://doi.org/10.1002/glia.20350
Murphy, T. H., & Corbett, D. (2009). Plasticity during stroke recovery: From synapse to behaviour. Nature Reviews. Neuroscience, 10(12), 861-872. https://doi.org/10.1038/nrn2735
Nahmani, M., & Turrigiano, G. G. (2014). Adult cortical plasticity following injury: Recapitulation of critical period mechanisms? Neuroscience, 283, 4-16. https://doi.org/10.1016/j.neuroscience.2014.04.029
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. https://doi.org/10.1016/j.brainres.2015.08.013
Nudo, R. J., Plautz, E. J., & Frost, S. B. (2001). Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle & Nerve, 24(8), 1000-1019. https://doi.org/10.1002/mus.1104
Oberheim, N. A., Goldman, S. A., & Nedergaard, M. (2012). Heterogeneity of astrocytic form and function. Methods in Molecular Biology, 814, 23-45. https://doi.org/10.1007/978-1-61779-452-0_3
Ohab, J. J., Fleming, S., Blesch, A., & Carmichael, S. T. (2006). A neurovascular niche for neurogenesis after stroke. The Journal of Neuroscience, 26(50), 13007-13016. https://doi.org/10.1523/JNEUROSCI.4323-06.2006
Ouyang, W., Yan, Q., Zhang, Y., & Fan, Z. (2017). Moderate injury in motor-sensory cortex causes behavioral deficits accompanied by electrophysiological changes in mice adulthood. PLoS ONE, 12(2), e0171976. https://doi.org/10.1371/journal.pone.0171976
Overman, J. J., & Carmichael, S. T. (2014). Plasticity in the injured brain: More than molecules matter. The Neuroscientist, 20(1), 15-28. https://doi.org/10.1177/1073858413491146
Palpagama, T. H., Waldvogel, H. J., Faull, R. L. M., & Kwakowsky, A. (2019). The role of microglia and astrocytes in Huntington's disease. Frontiers in Molecular Neuroscience, 12, 258. https://doi.org/10.3389/fnmol.2019.00258
Pekny, M., & Pekna, M. (2016). Reactive gliosis in the pathogenesis of CNS diseases. Biochimica et Biophysica Acta, 1862(3), 483-491. https://doi.org/10.1016/j.bbadis.2015.11.014
Pekny, M., Wilhelmsson, U., Tatlisumak, T., & Pekna, M. (2019). Astrocyte activation and reactive gliosis-a new target in stroke? Neuroscience Letters, 689, 45-55. https://doi.org/10.1016/j.neulet.2018.07.021
Petraglia, A. L., Plog, B. A., Dayawansa, S., Chen, M., Dashnaw, M. L., Czerniecka, K., … Huang, J. H. (2014). The spectrum of neurobehavioral sequelae after repetitive mild traumatic brain injury: A novel mouse model of chronic traumatic encephalopathy. Journal of Neurotrauma, 31(13), 1211-1224. https://doi.org/10.1089/neu.2013.3255
Popper, B., Demleitner, A., Bolivar, V. J., Kusek, G., Snyder-Keller, A., Schieweck, R., … Kiebler, M. A. (2018). Staufen2 deficiency leads to impaired response to novelty in mice. Neurobiology of Learning and Memory, 150, 107-115. https://doi.org/10.1016/j.nlm.2018.02.027
Qu, M., Mittmann, T., Luhmann, H. J., Schleicher, A., & Zilles, K. (1998). Long-term changes of ionotropic glutamate and GABA receptors after unilateral permanent focal cerebral ischemia in the mouse brain. Neuroscience, 85(1), 29-43. https://doi.org/10.1016/s0306-4522(97)00656-8
Robel, S., Berninger, B., & Gotz, M. (2011). The stem cell potential of glia: Lessons from reactive gliosis. Nature Reviews. Neuroscience, 12(2), 88-104. https://doi.org/10.1038/nrn2978
Robel, S., & Sontheimer, H. (2016). Glia as drivers of abnormal neuronal activity. Nature Neuroscience, 19(1), 28-33. https://doi.org/10.1038/nn.4184
Rodgers, R. J., Cao, B. J., Dalvi, A., & Holmes, A. (1997). Animal models of anxiety: An ethological perspective. Brazilian Journal of Medical and Biological Research, 30(3), 289-304. https://doi.org/10.1590/s0100-879x1997000300002
Roll, L., & Faissner, A. (2014). Influence of the extracellular matrix on endogenous and transplanted stem cells after brain damage. Frontiers in Cellular Neuroscience, 8, 219. https://doi.org/10.3389/fncel.2014.00219
Saederup, N., Cardona, A. E., Croft, K., Mizutani, M., Cotleur, A. C., Tsou, C. L., … Charo, I. F. (2010). Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE, 5(10), e13693. https://doi.org/10.1371/journal.pone.0013693
Santello, M., Toni, N., & Volterra, A. (2019). Astrocyte function from information processing to cognition and cognitive impairment. Nature Neuroscience, 22(2), 154-166. https://doi.org/10.1038/s41593-018-0325-8
Seibenhener, M. L., & Wooten, M. C. (2015). Use of the open field maze to measure locomotor and anxiety-like behavior in mice. Journal of Visualized Experiments, 96, e52434. https://doi.org/10.3791/52434
Simon, C., Gotz, M., & Dimou, L. (2011). Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury. GLIA, 59(6), 869-881. https://doi.org/10.1002/glia.21156
Siracusa, R., Fusco, R., & Cuzzocrea, S. (2019). Astrocytes: Role and functions in brain pathologies. Frontiers in Pharmacology, 10, 1114. https://doi.org/10.3389/fphar.2019.01114
Sirko, S., Behrendt, G., Johansson, P. A., Tripathi, P., Costa, M., Bek, S., … Gotz, M. (2013). Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [corrected]. Cell Stem Cell, 12(4), 426-439. https://doi.org/10.1016/j.stem.2013.01.019
Sirko, S., Irmler, M., Gascon, S., Bek, S., Schneider, S., Dimou, L., … Gotz, M. (2015). Astrocyte reactivity after brain injury-: The role of galectins 1 and 3. GLIA, 63(12), 2340-2361. https://doi.org/10.1002/glia.22898
Sirko, S., Neitz, A., Mittmann, T., Horvat-Brocker, A., von Holst, A., Eysel, U. T., & Faissner, A. (2009). Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain, 132(Pt 8), 2252-2264. https://doi.org/10.1093/brain/awp043
Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., … Clevers, H. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell, 143(1), 134-144. https://doi.org/10.1016/j.cell.2010.09.016
Sun, W., Cornwell, A., Li, J., Peng, S., Osorio, M. J., Aalling, N., … Nedergaard, M. (2017). SOX9 is an astrocyte-specific nuclear marker in the adult brain outside the neurogenic regions. The Journal of Neuroscience, 37(17), 4493-4507. https://doi.org/10.1523/JNEUROSCI.3199-16.2017
Takano, T., Tian, G. F., Peng, W., Lou, N., Libionka, W., Han, X., & Nedergaard, M. (2006). Astrocyte-mediated control of cerebral blood flow. Nature Neuroscience, 9(2), 260-267. https://doi.org/10.1038/nn1623
Takata, N., & Hirase, H. (2008). Cortical layer 1 and layer 2/3 astrocytes exhibit distinct calcium dynamics in vivo. PLoS ONE, 3(6), e2525. https://doi.org/10.1371/journal.pone.0002525
Taupin, P. (2007). BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Research Reviews, 53(1), 198-214. https://doi.org/10.1016/j.brainresrev.2006.08.002
Tay, T. L., Mai, D., Dautzenberg, J., Fernandez-Klett, F., Lin, G., Sagar, … Prinz, M. (2017). A new fate mapping system reveals context-dependent random or clonal expansion of microglia. Nature Neuroscience, 20(6), 793-803. https://doi.org/10.1038/nn.4547
Toledo-Rodriguez, M., & Sandi, C. (2011). Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats. Frontiers in Behavioral Neuroscience, 5, 17. https://doi.org/10.3389/fnbeh.2011.00017
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, 30(48), 16383-16390. https://doi.org/10.1523/JNEUROSCI.3411-10.2010
Van Den Herrewegen, Y., Denewet, L., Buckinx, A., Albertini, G., Van Eeckhaut, A., Smolders, I., & De Bundel, D. (2019). The Barnes maze task reveals specific impairment of spatial learning strategy in the Intrahippocampal Kainic acid model for temporal lobe epilepsy. Neurochemical Research, 44(3), 600-608. https://doi.org/10.1007/s11064-018-2610-z
van Dijk, B. J., Vergouwen, M. D., Kelfkens, M. M., Rinkel, G. J., & Hol, E. M. (2016). Glial cell response after aneurysmal subarachnoid hemorrhage - functional consequences and clinical implications. Biochimica et Biophysica Acta, 1862(3), 492-505. https://doi.org/10.1016/j.bbadis.2015.10.013
Verkhratsky, A., & Nedergaard, M. (2016). The homeostatic astroglia emerges from evolutionary specialization of neural cells. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 371(1700), 20150428. https://doi.org/10.1098/rstb.2015.0428
Verkhratsky, A., Rodriguez, J. J., & Parpura, V. (2014). Neuroglia in ageing and disease. Cell and Tissue Research, 357(2), 493-503. https://doi.org/10.1007/s00441-014-1814-z
Verkhratsky, A., & Zorec, R. (2019). Astroglial signalling in health and disease. Neuroscience Letters, 689, 1-4. https://doi.org/10.1016/j.neulet.2018.07.026
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. The Journal of Neuroscience, 33(31), 12870-12886. https://doi.org/10.1523/JNEUROSCI.2121-13.2013
Westergard, T., & Rothstein, J. D. (2020). Astrocyte diversity: Current insights and future directions. Neurochemical Research, 45, 1298-1305. https://doi.org/10.1007/s11064-020-02959-7
Wieloch, T., & Nikolich, K. (2006). Mechanisms of neural plasticity following brain injury. Current Opinion in Neurobiology, 16(3), 258-264. https://doi.org/10.1016/j.conb.2006.05.011
Wilhelmsson, U., Pozo-Rodrigalvarez, A., Kalm, M., de Pablo, Y., Widestrand, A., Pekna, M., & Pekny, M. (2019). The role of GFAP and vimentin in learning and memory. Biological Chemistry, 400(9), 1147-1156. https://doi.org/10.1515/hsz-2019-0199
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. https://doi.org/10.1016/j.stem.2010.04.002
Zhang, S., Boyd, J., Delaney, K., & Murphy, T. H. (2005). Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. The Journal of Neuroscience, 25(22), 5333-5338. https://doi.org/10.1523/JNEUROSCI.1085-05.2005
Zhao, X., Ahram, A., Berman, R. F., Muizelaar, J. P., & Lyeth, B. G. (2003). Early loss of astrocytes after experimental traumatic brain injury. GLIA, 44(2), 140-152. https://doi.org/10.1002/glia.10283