Roles of astrocytes and microglia in seizure-induced aberrant neurogenesis in the hippocampus of adult rats
Abstract
Recent evidence showed that epileptic seizures increase hippocampal neurogenesis in the adult rat, but prolonged seizures result in the aberrant hippocampal neurogenesis that often leads to a recurrent excitatory circuitry and thus contributes to epileptogenesis. However, the mechanism underlying the aberrant neurogenesis after prolonged seizures remains largely unclear. In this study, we examined the role of activated astrocytes and microglia in the aberrant hippocampal neurogenesis induced by status epilepticus. Using a lithium-pilocarpine model to mimic human temporal lobe epilepsy, we found that status epilepticus induced a prominent activation of astrocytes and microglia in the dentate gyrus 3, 7, 14, and 20 days after the initial seizures. Then, we injected fluorocitrate stereotaxicly into the dentate hilus to inhibit astrocytic metabolism and found that fluorocitrate failed to prevent the seizure-induced formation of ectopic hilar basal dendrites but instead promoted the degeneration of dentate granule cells after seizures. In contrast, a selective inhibitor of microglia activation, minocycline, inhibited the aberrant migration of newborn neurons at 14 days after status epilepticus. Furthermore, with stereotaxic injection of lipopolysaccharide into the intact dentate hilus to activate local microglia, we found that lipopolysaccharide promoted the development of ectopic hilar basal dendrites in the hippocampus. These results indicate that the activated microglia in the epileptic hilus may guide the aberrant migration of newborn neurons and that minocycline could be a potential drug to impede seizure-induced aberrant migration of newborn neurons.
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?
Seizures stimulate adult neurogenesis and impair hippocampal function.
“For example, seizures stimulate adult neurogenesis and impair hippocampal function.”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Yang et al., 2010
Seizure-induced reactive astrocytes, reactive microglia, and reduced expression of PNNs around postsynaptic neurons of adult-generated cells likely contribute to the functional impairments.
“Seizure-induced reactive astrocytes (Shapiro et al., 2008; Yang et al., 2010), reactive microglia (Shapiro et al., 2008; Yang et al., 2010), and reduced the expression of PNNs (McRae and Porter, 2012; Rankin-Gee et al., 2015) around postsynaptic neurons of adult-generated cells likely contribute to the functional impairments.”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Yang et al., 2010
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853 · see citing works
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Monje, M. L., Toda, H., & Palmer, T. D. (2003) · Science · doi:10.1126/science.1088417 · Cited by 2,426 · see citing works
Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03727.1997 · Cited by 1,853 · see citing works
Reactive astrocytes: cellular and molecular cues to biological function
Ridet, J., Privat, A., Malhotra, S. K., & Gage, F. H. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01139-9 · Cited by 1,766 · see citing works
Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus
Cameron, H. A., & Mckay, R. D. G. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1040 · Cited by 1,585 · see citing works
Inflammation is detrimental for neurogenesis in adult brain
Ekdahl, C. T., Claasen, J.-H., Bonde, S., Kokaia, Z., & Lindvall, O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234031100 · Cited by 1,559 · see citing works
Streit, W. J., Walter, S. A., & Pennell, N. A. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00069-0 · Cited by 1,096 · see citing works
Liu, B., & Hong, J.-S. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.035048 · Cited by 1,095 · see citing works
THE EPHRINS AND EPH RECEPTORS IN NEURAL DEVELOPMENT
Flanagan, J. G., & Vanderhaeghen, P. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.309 · Cited by 1,088 · see citing works
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P. G., & Carmignoto, G. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.011 · Cited by 970 · see citing works
Tikka, T., Fiebich, B. L., Goldsteins, G., Keinänen, R., & Koistinaho, J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02580.2001 · Cited by 958 · see citing works
Lee, S. C., Liu, W., Dickson, D. W., Brosnan, C., & Berman, J. (1993) · Journal of Immunology · doi:10.4049/jimmunol.150.7.2659 · Cited by 850 · see citing works
Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures
Bengzon, J., Kokaia, Z., Elmér, E., Nanobashvili, A., Kokaia, M., & Lindvall, O. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.19.10432 · Cited by 782 · see citing works
Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., & Croll, S. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.11.016 · Cited by 719 · see citing works
Ernfors, P., Bengzon, J., Kokaia, Z., Persson, H., & Lindvall, O. (1991) · Neuron · doi:10.1016/0896-6273(91)90084-d · Cited by 628 · see citing works
Ito, D., Tanaka, K., Suzuki, S., Dembo, T., & Fukuuchi, Y. (2001) · Stroke · doi:10.1161/01.str.32.5.1208 · Cited by 594 · see citing works
Hatten, M. E., Liem, R. K. H., Shelanski, M. L., & Mason, C. (1991) · Glia · doi:10.1002/glia.440040215 · Cited by 503 · see citing works
Semaphorins and their receptors in vertebrates and invertebrates
Raper, J. A. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00057-4 · Cited by 461 · see citing works
Migration and differentiation of neural precursor cells can be directed by microglia
Aarum, J., Sandberg, K., Haeberlein, S. L. B., & Persson, M. A. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2237050100 · Cited by 450 · see citing works
Targeting leukocyte MMPs and transmigration
Brundula, V., Rewcastle, N. B., Metz, L. M., Bernard, C. C. A., & Yong, V. W. (2002) · Brain · doi:10.1093/brain/awf133 · Cited by 427 · see citing works
Neal, C. R., Mansour, A., Reinscheid, R. K., Nothacker, H., Civelli, O., & Watson, S. J. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990419)406:4 · Cited by 399 · see citing works
The cell biology of neuronal navigation
Song, H., & Poo, M. (2001) · Nature Cell Biology · doi:10.1038/35060164 · Cited by 379 · see citing works
Epigenetic Modulation of Seizure-Induced Neurogenesis and Cognitive Decline
Jessberger, S., Nakashima, K., Clemenson, G. D., Mejia, E., Mathews, E. A., Ure, K., Ogawa, S., Sinton, C. M., Gage, F. H., & Hsieh, J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0110-07.2007 · Cited by 353 · see citing works
Gray, W. P., & Sundström, L. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00030-4 · Cited by 348 · see citing works
Hattiangady, B., Rao, M. S. R., & Shetty, A. K. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.08.008 · Cited by 303 · see citing works
Takeuchi, H., Mizuno, T., Zhang, G., Wang, J., Kawanokuchi, J., Kuno, R., & Suzumura, A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413863200 · Cited by 285 · see citing works
Enhanced Astrocytic Ca2+Signals Contribute to Neuronal Excitotoxicity after Status Epilepticus
Ding, S., Fellin, T., Zhu, Y., Lee, S.-Y., Auberson, Y. P., Meaney, D. F., Coulter, D. A., Carmignoto, G., & Haydon, P. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2001-07.2007 · Cited by 270 · see citing works
Jørgensen, M. B., Finsen, B. R., Jensen, M. B., Castellano, B., Diemer, N. H., & Zimmer, J. (1993) · Experimental Neurology · doi:10.1006/exnr.1993.1041 · Cited by 264 · see citing works
Paulsen, R. E., Contestabile, A., Villani, L., & Fonnum, F. (1987) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1987.tb05674.x · Cited by 262 · see citing works
Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury
Sun, L., Lee, J., & Fine, H. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20001 · Cited by 258 · see citing works
Fluoro-Jade: Novel Fluorochromes for Detecting Toxicant-Induced Neuronal Degeneration
Schmued, L. C., & Hopkins, K. J. (2000) · Toxicologic Pathology · doi:10.1177/019262330002800111 · Cited by 255 · see citing works
Rapid astrocyte and microglial activation following pilocarpine-induced seizures in rats
Shapiro, L. A., Wang, L., & Ribak, C. E. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01491.x · Cited by 242 · see citing works
Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons
Zhu, Y., Yu, T., Zhang, X.-C., Nagasawa, T., Wu, J. Y., & Rao, Y. (2002) · Nature Neuroscience · doi:10.1038/nn881 · Cited by 235 · see citing works
Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury
Sun, L., Lee, J., & Fine, H. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200420001 · Cited by 221 · see citing works
Accelerated Glial Reactivity to Stroke in Aged Rats Correlates with Reduced Functional Recovery
Badan, I., Buchhold, B., Hamm, A. O., Gratz, M., Walker, L. C., Platt, D., Kessler, C., & Popa‐Wagner, A. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000071883.63724.a7 · Cited by 216 · see citing works
Nakamura, Y., Si, Q.-S., & Kataoka, K. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(99)00071-1 · Cited by 216 · see citing works
Turrin, N. P., & Rivest, S. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.03.010 · Cited by 213 · see citing works
Selective inhibition of glial cell metabolism in vivo by fluorocitrate
Hassel, B., Paulsen, R. E., Johnsen, A., & Fonnum, F. (1992) · Brain Research · doi:10.1016/0006-8993(92)90616-h · Cited by 211 · see citing works
Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes
Wong, K. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00343-x · Cited by 210 · see citing works
Macrophages and microglia in central nervous system injury: are they helpful or harmful?
Schwartz, M. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200304000-00001 · Cited by 207 · see citing works
Nakagawa, E., Aimi, Y., Yasuhara, O., Tooyama, I., Shimada, M., McGeer, P. L., & Kimura, H. (2000) · Epilepsia · doi:10.1111/j.1528-1157.2000.tb01498.x · Cited by 200 · see citing works
Physiology of microglial cells
Färber, K., & Kettenmann, H. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.003 · Cited by 195 · see citing works
Menet, V., y Ribotta, M. G., Chauvet, N., Drian, M.-J., Lannoy, J., Colucci‐Guyon, E., & Privat, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06147.2001 · Cited by 181 · see citing works
Cytokine Release from Microglia: Differential Inhibition by Pentoxifylline and Dexamethasone
Chao, C. C., Hu, S., Close, K., Choi, C. S., Molitor, T. W., NOVICK, W. J. J., & Peterson, P. K. (1992) · The Journal of Infectious Diseases · doi:10.1093/infdis/166.4.847 · Cited by 178 · see citing works
Fluoroacetate and fluorocitrate: Mechanism of action
Clarke, D. D. (1991) · Neurochemical Research · doi:10.1007/bf00965850 · Cited by 145 · see citing works
Mechanisms and functional significance of aberrant seizure‐induced hippocampal neurogenesis
Parent, J. M., & Murphy, G. G. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01634.x · Cited by 141 · see citing works
Astrocyte-Derived MCP-1 Mediates Neuroprotective Effects of Noradrenaline
Madrigal, J. L. M., Leza, J. C., Polak, P. E., Kalinin, S., & Feinstein, D. L. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4926-08.2009 · Cited by 138 · see citing works
Scharfman, H. E., Smith, K. L., Goodman, J. H., & Sollas, A. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00132-4 · Cited by 111 · see citing works
Liang, J., Takeuchi, H., Doi, Y., Kawanokuchi, J., Sonobe, Y., Jin, S., Yawata, I., Li, H., Yasuoka, S., Mizuno, T., et al. (2008) · Brain Research · doi:10.1016/j.brainres.2008.03.012 · Cited by 99 · see citing works
Shapiro, L. A., Korn, M. J., & Ribak, C. E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.03.059 · Cited by 92 · see citing works
Rappold, P. M., Lynd‐Balta, E., & Joseph, S. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.040 · Cited by 90 · see citing works
Cytology and Cellular Pathology of the Nervous System.
(1932) · Annals of Internal Medicine · doi:10.7326/0003-4819-6-3-452_2 · Cited by 80 · see citing works
Ajmone‐Cat, M. A., Nicolini, A., & Minghetti, L. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02087.x · Cited by 75 · see citing works
Cell Death in Cortical Development: How Much? Why? So What?
Voyvodic, J. T. (1996) · Neuron · doi:10.1016/s0896-6273(00)80089-6 · Cited by 74 · see citing works
Lian, X., & Stringer, J. L. (2004) · Brain Research · doi:10.1016/j.brainres.2004.04.011 · Cited by 68 · see citing works
Dentate granule cell neurogenesis after seizures induced by pentylenetrazol in rats
Jiang, W., Wan, Q., Zhang, Z., Wang, W., Huang, Y., Rao, Z., & Zhang, X. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02438-7 · Cited by 66 · see citing works
Weller, M. L., Stone, I. M., Goss, A., Rau, T., Rova, C. R. L., & Poulsen, D. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.059 · Cited by 62 · see citing works
Different effects of mild and severe seizures on hippocampal neurogenesis in adult rats
Yang, F., Wang, J., Han, J., Zhao, G., & Jiang, W. (2008) · Hippocampus · doi:10.1002/hipo.20409 · Cited by 60 · see citing works
Characterization of Reactive Astrocytes in the Chronic Phase of the Pilocarpine Model of Epilepsy
Garzillo, C. L., & Mello, L. E. (2002) · Epilepsia · doi:10.1046/j.1528-1157.43.s.5.40.x · Cited by 57 · see citing works
Berg–Johnsen, J., Paulsen, R. E., Fonnum, F., & Langmoen, I. A. (1993) · Experimental Brain Research · doi:10.1007/bf00227104 · Cited by 46 · see citing works
He, J., Yang, Y., Xu, H., Zhang, X., & Li, X. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300757 · Cited by 43 · see citing works
Expression of Heat Shock Protein‐70 and Limbic Seizure‐induced Neuronal Death in the Rat Brain
Zhang, X., Boulton, A. A., & Yu, P. H. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01605.x · Cited by 42 · see citing works
Endogenous Glutamate Levels Regulate Nerve Growth Factor mRNA Expression in the Rat Dentate Gyrus
Gwag, B. J., Sessler, F. M., Robine, V., & Springer, J. E. (1997) · Molecules and Cells · doi:10.1016/s1016-8478(23)13316-4 · Cited by 27 · see citing works
Okere, C. O., & Kaba, H. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02656-1 · Cited by 24 · see citing works
Inhibition of aconitase in astrocytes increases the sensitivity to chemical convulsants
Lian, X., & Stringer, J. L. (2004) · Epilepsy Research · doi:10.1016/j.eplepsyres.2004.05.003 · Cited by 17 · see citing works
Blockade of AMPA receptors by nickel in cultured rat astrocytes
Telgkamp, P., Backus, K. H., & Deitmer, J. W. (1996) · Glia · doi:10.1002/(sici)1098-1136(199602)16:2 · Cited by 16 · see citing works
Effects of glial toxins on extracellular acidification in the hippocampal CA1 region in vivo
Stringer, J. L., & Aribi, A. M. (2003) · Epilepsy Research · doi:10.1016/s0920-1211(03)00064-0 · Cited by 13 · see citing works
Stringer, J. L., Mukherjee, K., Xiang, T., & Xu, K. (2007) · Epilepsy Research · doi:10.1016/j.eplepsyres.2007.03.005 · Cited by 5 · see citing works
Glucose transporter proteins in brain: Delivery of glucose to neurons and glia
Vannucci, S. J., Maher, F., & Simpson, I. A. (1997) · Glia · doi:10.1002/(sici)1098-1136(199709)21:1
Flagged first, then by citations
Cited by
Sorted by citations
Microglia–Neuron Communication in Epilepsy
Eyo, U. B., Murugan, M., & Wu, L. (2016) · Glia · doi:10.1002/glia.23006 · Cited by 290 · see citing works
Seizure-Induced Oxidative Stress in Temporal Lobe Epilepsy
Puttachary, S., Sharma, S., Stark, S., & Thippeswamy, T. (2015) · BioMed Research International · doi:10.1155/2015/745613 · Cited by 262 · see citing works
Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
The changing phenotype of microglia from homeostasis to disease
Luo, X., & Chen, S. (2012) · Translational Neurodegeneration · doi:10.1186/2047-9158-1-9 · Cited by 233 · see citing works
The effects of microglia‐ and astrocyte‐derived factors on neurogenesis in health and disease
Araki, T., Ikegaya, Y., & Koyama, R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14969 · Cited by 177 · see citing works
Amanollahi, M., Jameie, M., Heidari, A., & Rezaei, N. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03102-z · Cited by 171 · see citing works
Inflammatory aspects of epileptogenesis: contribution of molecular inflammatory mechanisms
Alyu, F., & Dikmen, M. (2016) · Acta Neuropsychiatrica · doi:10.1017/neu.2016.47 · Cited by 147 · see citing works
Abraham, J., Fox, P. D., Condello, C., Bartolini, A., & Koh, S. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.02.006 · Cited by 140 · see citing works
Wang, N., Mi, X., Gao, B., Gu, J., Wang, W., Zhang, Y., & Wang, X. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.021 · Cited by 140 · see citing works
Neuroinflammation in epileptogenesis: from pathophysiology to therapeutic strategies
Li, W., Wu, J., Zeng, Y., & Zheng, W. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1269241 · Cited by 141 · see citing works
Ye, R., Yang, Q., Kong, X., Han, J., Zhang, X., Zhang, Y., Li, P., Liu, J., Shi, M., Xiong, L., et al. (2010) · Neurochemistry International · doi:10.1016/j.neuint.2010.12.015 · Cited by 131 · see citing works
Synaptic Pruning by Microglia in Epilepsy
Andoh, M., Ikegaya, Y., & Koyama, R. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8122170 · Cited by 128 · see citing works
Ye, R., Kong, X., Yang, Q., Zhang, Y., Han, J., & Zhao, G. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.05.029 · Cited by 117 · see citing works
Ye, R., Zhang, X., Kong, X., Han, J., Yang, Q., Zhang, Y., Chen, Y., Li, P., Liu, J., Shi, M., et al. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.007 · Cited by 108 · see citing works
Mirrione, M. M., Konomos, D. K., Gravanis, I., Dewey, S. L., Aguzzi, A., Heppner, F. L., & Tsirka, S. E. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.04.001 · Cited by 103 · see citing works
Microglial P2Y12 Receptor Regulates Seizure-Induced Neurogenesis and Immature Neuronal Projections
Mo, M., Eyo, U. B., Xie, M., Peng, J., Bosco, D. B., Umpierre, A. D., Zhu, X., Tian, D., Xu, P., & Wu, L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0487-19.2019 · Cited by 93 · see citing works
Microglia engulf viable newborn cells in the epileptic dentate gyrus
Luo, C., Koyama, R., & Ikegaya, Y. (2016) · Glia · doi:10.1002/glia.23018 · Cited by 94 · see citing works
Glial cell-expressed mechanosensitive channel TRPV4 mediates infrasound-induced neuronal impairment
Shi, M., Du, F., Liu, Y., Li, L., Cai, J., Zhang, G.-F., Xu, X.-F., Lin, T., Cheng, H.-R., Liu, X.-D., et al. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1166-x · Cited by 87 · see citing works
Gao, F., Liu, Y., Li, X., Wang, Y., Wei, D., & Jiang, W. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.08.025 · Cited by 86 · see citing works
Minocycline- and tetracycline-class antibiotics are protective against partial seizures in vivo
Wang, D. D., Englot, D. J., Garcia, P. A., Lawton, M. T., & Young, W. L. (2012) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2012.03.035 · Cited by 73 · see citing works
Ma, L., Cui, X., Wang, Y., Li, X., Yang, F., Wei, D., & Jiang, W. (2012) · Brain Research · doi:10.1016/j.brainres.2012.05.058 · Cited by 71 · see citing works
Astrocyte Hypertrophy Contributes to Aberrant Neurogenesis after Traumatic Brain Injury
Robinson, C., Apgar, C. J., & Shapiro, L. A. (2016) · Neural Plasticity · doi:10.1155/2016/1347987 · Cited by 71 · see citing works
Lipopolysaccharide potentiates hyperthermia-induced seizures
Eun, B., Abraham, J., Mlsna, L. M., Kim, M. J., & Koh, S. (2015) · Brain and Behavior · doi:10.1002/brb3.348 · Cited by 63 · see citing works
Lu, D. C.-T., Zador, Z. E., Yao, J., Fazlollahi, F., & Manley, G. T. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2011.2114 · Cited by 68 · see citing works
Cao, J., Tang, C. C., Gao, M., Rui, Y., Zhang, J., Wang, L., Wang, Y., Xu, B., & Yan, B. C. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.112884 · Cited by 62 · see citing works
Wang, R.-F., Xue, G., Hölscher, C., Tian, M.-J., Feng, P., Zheng, J.-Y., & Li, D. (2018) · Epilepsy Research · doi:10.1016/j.eplepsyres.2018.03.009 · Cited by 54 · see citing works
Role of glia in epilepsy-associated neuropathology, neuroinflammation and neurogenesis
Foresti, M. L., Arisi, G. M., & Shapiro, L. A. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.09.002 · Cited by 51 · see citing works
Vizuete, A. F. K., Hansen, F., Negri, E., Leite, M. C., de Oliveira, D. L., & Gonçalves, C. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1109-5 · Cited by 50 · see citing works
Schmidt, S. I., Bogetofte, H., Ritter, L., Agergaard, J. B., Hammerich, D., Kabiljagic, A. A., Włodarczyk, A., López, S. G., Sørensen, M. D., Jørgensen, M. L., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.12.011 · Cited by 51 · see citing works
The epilepsies: Complex challenges needing complex solutions
Tejada, J., Costa, K. M., Bertti, P., & Garcia‐Cairasco, N. (2012) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2012.09.029 · Cited by 46 · see citing works
Li, X., Han, X., Yang, J., Bao, J., Di, X., Zhang, G., & Liu, H. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0278-4 · Cited by 46 · see citing works
Astrocytic Acid-Sensing Ion Channel 1a Contributes to the Development of Chronic Epileptogenesis
Yang, F., Sun, X., Ding, Y., Ma, H., Ou-Yang, T.-P., Ma, Y., Wei, D., Li, W., Xu, T., & Jiang, W. (2016) · Scientific Reports · doi:10.1038/srep31581 · Cited by 44 · see citing works
Haj‐Mirzaian, A., Ramezanzadeh, K., Tafazolimoghadam, A., Kazemi, K., Nikbakhsh, R., Nikbakhsh, R., Amini-Khoei, H., Afshari, K., Haddadi, N., Shakiba, S., et al. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172446 · Cited by 43 · see citing works
Mechanism of NLRP3 Inflammasome in Epilepsy and Related Therapeutic Agents
Chen, J., Gao, Y., Liu, N., Hai, D., Wei, W., Liu, Y., Lan, X., Jin, X., Yu, J., & Ma, L. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.03.029 · Cited by 41 · see citing works
Inflammation in Epileptic Encephalopathies
Shandra, O. O., Moshé, S. L., & Galanopoulou, A. S. (2017) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2017.01.005 · Cited by 39 · see citing works
Wang, Q., Zhu, L., Xian-hong, W., Zuo, J., He, H., Tian, M., Wang, L., Liang, G.-L., & Wang, Y. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0736-5 · Cited by 30 · see citing works
Microglia modulate the structure and function of the hippocampus after early-life seizures
Andoh, M., Ikegaya, Y., & Koyama, R. (2020) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2020.09.003 · Cited by 27 · see citing works
Neurologic impairment following closed head injury predicts post-traumatic neurogenesis
Villasana, L., Westbrook, G. L., & Schnell, E. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.016 · Cited by 27 · see citing works
Transient extracellular application of gold nanostars increases hippocampal neuronal activity
Salinas, K., Kereselidze, Z., DeLuna, F., Peralta, X. G., & Santamarı́a, F. (2014) · Journal of Nanobiotechnology · doi:10.1186/preaccept-7863745011292633 · Cited by 27 · see citing works
Synaptic Dysfunction in Epilepsy
Zaitsev, A. V., Amakhin, D. V., Dyomina, A. V., Zakharova, M. V., Ergina, J. L., Postnikova, T. Y., Diespirov, G. P., & Magazanik, L. G. (2021) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s002209302103008x · Cited by 28 · see citing works
Progranulin promotes activation of microglia/macrophage after pilocarpine-induced status epilepticus
Zhu, S., Tai, C., Petkau, T. L., Zhang, S., Liao, C., Dong, Z., Wen, W., Chang, Q., Wang, Y. T., MacVicar, B. A., et al. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.023 · Cited by 26 · see citing works
Clinical and Genetic Aspects of Epilepsy
Heron, S., & Mulley, J. (2011) · InTech eBooks · doi:10.5772/1138 · Cited by 24 · see citing works
Astrocyte Alterations in the Hippocampus Following Pilocarpine-induced Seizures in Aged Rats.
Arisi, G. M., Ruch, M., Foresti, M. L., Mukherjee, S., Ribak, C. E., & Shapiro, L. A. (2011) · Europe PMC (PubMed Central) · Cited by 23 · see citing works
Minocycline fails to exert antiepileptogenic effects in a rat status epilepticus model
Russmann, V., Goc, J., Boes, K., Ongerth, T., Salvamoser, J. D., Siegl, C., & Potschka, H. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.12.002 · Cited by 23 · see citing works
Xiong, T., Chen, L.-M., Tan, B., Guo, C., Li, Y., Zhang, Y.-F., Li, S.-L., Zhao, H., & Li, Y. (2018) · Epilepsy Research · doi:10.1016/j.eplepsyres.2018.01.007 · Cited by 22 · see citing works
Reconnoitering the transformative journey of minocycline from an antibiotic to an antiepileptic drug
Singh, T., Thapliyal, S., Bhatia, S., Singh, V., Singh, M., Singh, H. B., Kumar, A., & Mishra, A. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120346 · Cited by 21 · see citing works
Wulsin, A. C., Kraus, K. L., Gaitonde, K. D., Suru, V., Arafa, S. R., Packard, B. A., Herman, J. P., & Danzer, S. C. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113703 · Cited by 18 · see citing works
Estrada, F. S., Hernández, V. S., López-Hernández, E., Corona-Morales, A. A., Solís, H., Escobar, A., & Zhang, L. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.02.055 · Cited by 19 · see citing works
Seizure-induced hilar ectopic granule cells in the adult dentate gyrus
Kasahara, Y., Nakashima, H., & Nakashima, K. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1150283 · Cited by 17 · see citing works
de Aquino, P. É. A., Bezerra, J. R., Nascimento, T. D. S., Tavares, J., Lustosa, Í. R., Filho, A. J. M. C., Mottin, M., Macêdo, D. S., de Andrade, G. M., Neves, K. R. T., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114188 · Cited by 17 · see citing works
Immunity and neuroinflammation in early stages of life and epilepsy
García, A. V., López‐Meraz, M. L., González, M. I., Rocha, L., Peixoto-Santos, J. E., & Cavalheiro, É. A. (2025) · Epilepsia · doi:10.1111/epi.18361 · Cited by 17 · see citing works
Li, X., Yang, F., Wang, Y., Wang, J., Ma, L., & Jiang, W. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.11.007 · Cited by 16 · see citing works
The Role of Aquaporins in Epileptogenesis—A Systematic Review
Bonosi, L., Benigno, U. E., Musso, S., Giardina, K., Gerardi, R. M., Brunasso, L., Costanzo, R., Paolini, F., Buscemi, F., Avallone, C., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241511923 · Cited by 14 · see citing works
Xiong, T., Liu, J., Dai, G., Hou, Y., Tan, B., Zhang, Y.-F., Li, S., Song, Y., Liu, H., Li, Y., et al. (2015) · Epilepsy Research · doi:10.1016/j.eplepsyres.2015.11.002 · Cited by 14 · see citing works
Kegler, A., Cardoso, A. S., Caprara, A. L. F., Pascotini, E. T., Arend, J., Gabbi, P., Duarte, M. M. M. F., da Cruz, I. B. M., Furian, A. F., Oliveira, M. S., et al. (2019) · Gene · doi:10.1016/j.gene.2019.06.014 · Cited by 13 · see citing works
Peng, S., Zhuang, Q., Zhang, Y., Zhang, X., Wang, J., & Zhu, J. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23745 · Cited by 13 · see citing works
Vizuete, A. F. K., Leal, M. B., Moreira, A. P., Seady, M., Taday, J., & Gonçalves, C. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110704 · Cited by 11 · see citing works
Coupled Oscillators Model of Hyperexcitable Neuroglial Networks
Farah, F. H., Grigorovsky, V., & Bardakjian, B. L. (2018) · International Journal of Neural Systems · doi:10.1142/s0129065718500417 · Cited by 11 · see citing works
A Functional Role for Microglia in Epilepsy
Martine, M. E. M., & Stella, E. (2011) · InTech eBooks · doi:10.5772/17778 · Cited by 9 · see citing works
Microglia: The Bodyguard and the Hunter of the Adult Neurogenic Niche
Valero, J., Eiriz, M. F., Santos, T., Neiva, I., Ferreira, R., & Malva, J. O. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-940-2_14 · Cited by 9 · see citing works
Zhang, W., Yin, J., Gao, B., Lu, X., Duan, Y.-J., Liu, X.-Y., Li, M.-Z., & Jiang, S. (2023) · Behavioral and Brain Functions · doi:10.1186/s12993-023-00226-7 · Cited by 7 · see citing works
Postnikova, T. Y., Diespirov, G. P., Griflyuk, A. V., & Zaitsev, A. V. (2026) · Life Sciences · doi:10.1016/j.lfs.2026.124193 · Cited by 7 · see citing works
Hung, Y.-W., Lu, G.-L., Chen, H.-H., Tung, H., & Lee, S. (2023) · Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie · doi:10.1016/j.biopha.2023.115270 · Cited by 5 · see citing works
Neurogenesis in a Young Dog With Epileptic Seizures
Borschensky, C. M., Woolley, J., Kipar, A., & Herden, C. (2011) · Veterinary Pathology · doi:10.1177/0300985811429308 · Cited by 6 · see citing works
Kelemen, K., Sárosi, M., Csüdör, Á., Orbán-Kis, K., Kelemen, H., Bába, L., Gáll, Z., Horváth, E., Katona, I., & Szilágyi, T. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1553545 · Cited by 4 · see citing works
Nguyen, D. A., Niquet, J., Marrero-Rosado, B. M., Schultz, C. R., Stone, M. F., Furtado, M. D. A., Biney, A. K., & Lumley, L. A. (2024) · Experimental Neurology · doi:10.1016/j.expneurol.2024.115122 · Cited by 3 · see citing works
de Melo, I. S., Silva, R. S., Costa, M. A. P. D. C., Vaz, E. R., Anselmo-e-Silva, C. I., Mendonça, T. D. P. S., Oliveira, K. B., de Souza, F. M. A., dos Santos, Y. M. O., Pacheco, A. L. D., et al. (2023) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-023-01410-z · Cited by 2 · see citing works
Microglia in Epilepsy: From Molecular Mechanism to Therapeutic Strategy
Paudel, Y. N., Angelopoulou, E., Kulkarni, S., Blair, R. E., & Deshpande, L. S. (2026) · Cells · doi:10.3390/cells15090835 · Cited by 1 · see citing works
Järvelä, J. (2011) · UTUPub (University of Turku) · Cited by 1 · see citing works
Santos, J. E. P. (2014) · doi:10.11606/t.17.2014.tde-19122014-154406
Factors in glutamate excitotoxicity, inflammation and epilepsy
Zhu, S. (2012) · cIRcle (University of British Columbia) · doi:10.14288/1.0072497
Microglial Location, Morphology, and Cognitive Performance in Mold-Exposed Mice
Marmon, K. (2017) · CUNY Academic Works (City University of New York)
Siddiqui, T. A. (2016) · TSpace (University of Toronto)
Role of Midline Thalamic Circuits in Limbic Seizures
Sloan, D. M. (2010) · doi:10.18130/v30v9b
Wu, Q., Wang, H., Liu, X., Zhao, Y., Zhao, X., Su, P., & Miao, J. (2022) · Research Square · doi:10.21203/rs.3.rs-1733117/v1
Kempermann, G. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780197519233.003.0012
Hens, J. R., Brown, S. N., Licznerski, P., Suarez, J., Jonas, E. A., & Wysolmerski, J. J. (2025) · PLoS ONE · doi:10.1371/journal.pone.0318760
Zhang, W., Yin, J., Gao, B.-Y., Lu, X., Duan, Y.-J., Liu, X.-Y., Li, M., & Jiang, S. (2024) · Figshare · doi:10.6084/m9.figshare.26655517
Zhang, W., Yin, J., Gao, B.-Y., Lu, X., Duan, Y.-J., Liu, X.-Y., Li, M., & Jiang, S. (2024) · Figshare · doi:10.6084/m9.figshare.26655520
- Authors
- Yang, F., Liu, Z., Chen, J., Zhang, S., Quan, Q., Huang, Y., & Jiang, W.
- Affiliations
- Xijing Hospital (CN)
- Corresponding author
- Jiang, Wen
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2009-09-22
- Volume
- 88
- Issue
- 3
- Pages
- 519-529
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2056705288
- Cited by
- 80
- References
- 69
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 5 · 2018: 4 · 2017: 2 · 2016: 9 · 2015: 4 · 2014: 4 · 2013: 2 · 2012: 10
- FWCI
- 4.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- astrocytes, microglia, status epilepticus, epileptogenesis, lithium-pilocarpine model, temporal lobe epilepsy, dentate gyrus, fluorocitrate, minocycline, lipopolysaccharide, microglial activation
- MeSH terms
- Aging, Animals, Astrocytes, Cell Movement, Dendrites, Disease Models, Animal, Epilepsy, Temporal Lobe, Male, Nerve Degeneration, Neurons, Random Allocation, Seizures, Status Epilepticus, Time Factors, Rats, Sprague-Dawley, Microglia, Dentate Gyrus, Rats, Neurogenesis
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