A strocytic glutamine synthetase is expressed in the neuronal somatic layers and down‐regulated proportionally to neuronal loss in the human epileptic hippocampus
Abstract
Human mesial temporal lobe epilepsy (MTLE) features subregion‐specific hippocampal neurodegeneration and reactive astrogliosis, including up‐regulation of the glial fibrillary acidic protein (GFAP) and down‐regulation of glutamine synthetase (GS). However, the regional astrocytic expression pattern of GFAP and GS upon MTLE‐associated neurodegeneration still remains elusive. We assessed GFAP and GS expression in strict correlation with the local neuronal number in cortical and hippocampal surgical specimens from 16 MTLE patients using immunohistochemistry, stereology and high‐resolution image analysis for digital pathology and whole‐slide imaging. In the cortex, GS‐positive (GS+) astrocytes are dominant in all neuronal layers, with a neuron to GS+ cell ratio of 2:1. GFAP‐positive (GFAP+) cells are widely spaced, with a GS+ to GFAP+ cell ratio of 3:1–5:1. White matter astrocytes, on the contrary, express mainly GFAP and, to a lesser extent, GS. In the hippocampus, the neuron to GS+ cell ratio is approximately 1:1. Hippocampal degeneration is associated with a reduction of GS+ astrocytes, which is proportional to the degree of neuronal loss and primarily present in the hilus. Up‐regulation of GFAP as a classical hallmark of reactive astrogliosis does not follow the GS‐pattern and is prominent in the CA1. Reactive alterations were proportional to the neuronal loss in the neuronal somatic layers (stratum pyramidale and hilus), while observed to a lesser extent in the axonal/dendritic layers (stratum radiatum, molecular layer). We conclude that astrocytic GS is expressed in the neuronal somatic layers and, upon neurodegeneration, is down‐regulated proportionally to the degree of neuronal loss.
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?
In CNT, GS astrocytes were present from layer III onward, whereas in SAD and FAD they increased from layer I.
“As previously described [102], GS astrocytes were present from layer III onward in CNT, whereas in SAD and FAD increased from layer I (Figure 4C).”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp><i>APOE3</i></scp> Christchurch homozygote glioprotection (2023) · cites this paper as [102]
Cites
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
NeuN, a neuronal specific nuclear protein in vertebratesxs
Mullen, R. J., Buck, C. R., & Smith, A. M. (1992) · Development · doi:10.1242/dev.116.1.201 · Cited by 2,351 · see citing works
Fine structural localization of glutamine synthetase in astrocytes of rat brain
Norenberg, M. D., & Martinez-Hernandez, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90071-4 · Cited by 1,349 · see citing works
Glutamine Synthetase: Glial Localization in Brain
Martinez-Hernandez, A., Bell, K. P., & Norenberg, M. D. (1977) · Science · doi:10.1126/science.14400 · Cited by 1,183 · see citing works
Bak, L. K., Schousboe, A., & Waagepetersen, H. S. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03913.x · Cited by 1,114 · see citing works
Glial fibrillary acidic protein: From intermediate filament assembly and gliosis to neurobiomarker
Yang, Z., & Wang, K. K. W. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.003 · Cited by 1,050 · see citing works
Blümcke, I., Thom, M., Aronica, E., Armstrong, D. D., Bartoloméi, F., Bernasconi, A., Bernasconi, N., Bien, C. G., Cendes, F., Coras, R., et al. (2013) · Epilepsia · doi:10.1111/epi.12220 · Cited by 1,010 · see citing works
Astrocyte reactivity and reactive astrogliosis: costs and benefits
Pekny, M., & Pekna, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2013 · Cited by 934 · see citing works
Hol, E. M., & Pekny, M. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.02.004 · Cited by 917 · see citing works
Unbiased Stereology. Three‐Dimensional Measurement in Microscopy.
Sandau, K. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.0429a.x · Cited by 890 · see citing works
Astrocytes Potentiate Transmitter Release at Single Hippocampal Synapses
Perea, G., & Araque, A. (2007) · Science · doi:10.1126/science.1144640 · Cited by 727 · see citing works
Duvernoy, H. M., Cattin, F., & Risold, P. (2013) · Springer eBooks · doi:10.1007/978-3-642-33603-4 · Cited by 567 · see citing works
Review: Hippocampal sclerosis in epilepsy: a neuropathology review
Thom, M. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12150 · Cited by 565 · see citing works
Halama, N., Zoernig, I., Berthel, A., Kahlert, C., Klupp, F., Suarez‐Carmona, M., Sütterlin, T., Brand, K., Krauss, J., Lasitschka, F., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.03.005 · Cited by 497 · see citing works
Self-citationElusive roles for reactive astrocytes in neurodegenerative diseases
Ben Haim, L., Carrillo-de Sauvage, M.-A., Ceyzériat, K., & Escartin, C. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00278 · Cited by 453 · see citing works
Heterogeneity of reactive astrocytes
Anderson, M. A., Ao, Y., & Sofroniew, M. V. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.12.030 · Cited by 449 · see citing works
Eid, T., Thomas, M., Dd, S., Rundén‐Pran, E., Lai, J. C. K., Malthankar, G. V., Kim, J., Danbolt, N. C., Ottersen, O. P., & de Lanerolle, N. C. (2004) · The Lancet · doi:10.1016/s0140-6736(03)15166-5 · Cited by 434 · see citing works
Heterogeneity in astrocyte morphology and physiology
Matyash, V., & Kettenmann, H. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.12.001 · Cited by 413 · see citing works
Kim, K. K., Adelstein, R. S., & Kawamoto, S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.052969 · Cited by 398 · see citing works
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus
Jinno, S., Klausberger, T., Marton, L. F., Dalezios, Y., Roberts, J. D. B., Fuentealba, P., Bushong, E. A., Henze, D., Buzsáki, G., & Somogyi, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1847-07.2007 · Cited by 369 · see citing works
Patterns of gliosis in alzheimer's disease and aging cerebrum
Beach, T. G., Walker, R., & McGeer, E. G. (1989) · Glia · doi:10.1002/glia.440020605 · Cited by 337 · see citing works
Astrocyte uncoupling as a cause of human temporal lobe epilepsy
Bedner, P., Dupper, A., Hüttmann, K., Müller, J., Herde, M. K., Dublin, P., Deshpande, T., Schramm, J., Häussler, U., Haas, C. A., et al. (2015) · Brain · doi:10.1093/brain/awv067 · Cited by 328 · see citing works
Sarnat, H. B., Nochlin, D., & Born, D. E. (1998) · Brain and Development · doi:10.1016/s0387-7604(97)00111-3 · Cited by 308 · see citing works
Kamphuis, W., Mamber, C., Moeton, M., Kooijman, L., Sluijs, J. A., Jansen, A. H. P., Verveer, M., de Groot, L. R., Smith, V. D., Rangarajan, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042823 · Cited by 305 · see citing works
White matter astrocytes in health and disease
Lundgaard, I., Osório, M. J., Kress, B. T., Sanggaard, S., & Nedergaard, M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.050 · Cited by 287 · see citing works
Roles of glutamine in neurotransmission
Albrecht, J., Sidoryk-Węgrzynowicz, M., Zielińska, M., & Aschner, M. (2010) · Neuron Glia Biology · doi:10.1017/s1740925x11000093 · Cited by 273 · see citing works
Role of Astrocytes in EpilepsyPreprint
Coulter, D. A., & Steinhäuser, C. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022434 · Cited by 243 · see citing works
Walls, A. B., Waagepetersen, H. S., Bak, L. K., Schousboe, A., & Sonnewald, U. (2015) · Neurochemical Research · doi:10.1007/s11064-014-1473-1 · Cited by 223 · see citing works
Wyler, A. R., Dohan, F. C., Schweitzer, J. B., & Berry, A. D. (1992) · Journal of Epilepsy · doi:10.1016/s0896-6974(05)80120-3 · Cited by 213 · see citing works
Ammonium and Chloride Extrusion: Hyperpolarizing Synaptic Inhibition in Spinal Motoneurons
Lux, H. D. (1971) · Science · doi:10.1126/science.173.3996.555 · Cited by 200 · see citing works
Coras, R., Pauli, E., Li, J., Schwarz, M., Rössler, K., Buchfelder, M., Hamer, H. M., Stefan, H., & Blümcke, I. (2014) · Brain · doi:10.1093/brain/awu100 · Cited by 195 · see citing works
Blümcke, I., Coras, R., Miyata, H., & Özkara, Ç. (2012) · Brain Pathology · doi:10.1111/j.1750-3639.2012.00583.x · Cited by 190 · see citing works
Phenotypic Heterogeneity and Plasticity of Isocortical and Hippocampal Astrocytes in the Human Brain
Sosunov, A. A., Wu, X., Tsankova, N. M., Guilfoyle, E., McKhann, G. M., & Goldman, J. E. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4037-13.2014 · Cited by 185 · see citing works
Gabriel, S., Njunting, M., Pomper, J. K., Merschhemke, M. B., Sanabria, E., Eilers, A., Kivi, A., Zeller, M., Meencke, H., Cavalheiro, É. A., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2074-04.2004 · Cited by 176 · see citing works
Self-citationDerouiche, A., & Frotscher, M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90103-3 · Cited by 164 · see citing works
Blümcke, I., Kistner, I., Clusmann, H., Schramm, J., Becker, A. J., Elger, C. E., Bien, C. G., Merschhemke, M. B., Meencke, H., Lehmann, T. N., et al. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0512-5 · Cited by 142 · see citing works
Kann, O., Kovács, R., Njunting, M., Behrens, C. J., Otáhal, J., Lehmann, T., Gabriel, S., & Heinemann, U. (2005) · Brain · doi:10.1093/brain/awh568 · Cited by 142 · see citing works
Self-citationGriemsmann, S., Höft, S. P., Bedner, P., Zhang, J., von Staden, E., Beinhauer, A., Degen, J., Dublin, P., Cope, D. W., Richter, N., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu157 · Cited by 132 · see citing works
Automated image analysis in histopathology: a valuable tool in medical diagnostics
Mulrane, L., Rexhepaj, E., Penney, S., Callanan, J. J., & Gallagher, W. M. (2008) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.8.6.707 · Cited by 123 · see citing works
Regulation of astrocyte glutamine synthetase in epilepsy
Eid, T., Tu, N., Lee, T.-S. W., & Lai, J. C. K. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.06.008 · Cited by 109 · see citing works
Neuronal Hypertrophy in the Neocortex of Patients with Temporal Lobe Epilepsy
Bothwell, S., Meredith, G. E., Phillips, J. P., Staunton, H., Doherty, C. P., Grigorenko, E. V., Glazier, S. S., Deadwyler, S. A., O’Donovan, C. A., & Farrell, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-13-04789.2001 · Cited by 108 · see citing works
Cytochemical and cytological properties of perineuronal oligodendrocytes in the mouse cortex
Takasaki, C., Yamasaki, M., Uchigashima, M., Konno, K., Yanagawa, Y., & Watanabe, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07377.x · Cited by 106 · see citing works
Glutamine synthetase in the central nervous system is not confined to astrocytes
Cammer, W. (1990) · Journal of Neuroimmunology · doi:10.1016/0165-5728(90)90088-5 · Cited by 95 · see citing works
Hammer, J., Alvestad, S., Osen, K. K., Skare, Ø., Sonnewald, U., & Ottersen, O. P. (2008) · Glia · doi:10.1002/glia.20659 · Cited by 74 · see citing works
Carbamazepine-resistance in the epileptic dentate gyrus of human hippocampal slices
Jandová, K., Päsler, D., Antônio, L. L., Raue, C., Ji, S., Njunting, M., Kann, O., Kovacs, R., Meencke, H. J., Cavalheiro, É. A., et al. (2006) · Brain · doi:10.1093/brain/awl218 · Cited by 69 · see citing works
Self-citationIn vitro seizure like events and changes in ionic concentration
Antônio, L. L., Anderson, M., Angamo, E. A., Gabriel, S., Klaft, Z., Liotta, A., Salar, S., Sandow, N., & Heinemann, U. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.08.014 · Cited by 60 · see citing works
Self-citationDissecting tripartite synapses with STED microscopy
Panatier, A., Arizono, M., & Nägerl, U. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0597 · Cited by 58 · see citing works
Sandow, N., Kim, S., Raue, C., Päsler, D., Klaft, Z., Antônio, L. L., Hollnagel, J., Kovacs, R., Kann, O., Horn, P., et al. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00030 · Cited by 56 · see citing works
Self-citationSkalli, O., Wilhelmsson, U., Örndahl, C., Fekete, B., Malmgren, K., Rydenhag, B., & Pekny, M. (2013) · Human Pathology · doi:10.1016/j.humpath.2013.03.013 · Cited by 54 · see citing works
Blümcke, I., Cross, J. H., & Spreafico, R. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70175-3 · Cited by 54 · see citing works
Rhee, W., Ray, S., Yokoo, H., Hoane, M. E., Lee, C. C., Mikheev, A. M., Horner, P. J., & Rostomily, R. (2008) · Glia · doi:10.1002/glia.20780 · Cited by 46 · see citing works
Glutamine synthetase immunoreactivity in two types of mouse brain glial cells
Miyake, T., & Kitamura, T. (1992) · Brain Research · doi:10.1016/0006-8993(92)91370-t · Cited by 46 · see citing works
Redistribution of astrocytic glutamine synthetase in the hippocampus of chronic epileptic rats
Papageorgiou, I. E., Gabriel, S., Fetani, A. F., Kann, O., & Heinemann, U. (2011) · Glia · doi:10.1002/glia.21217 · Cited by 45 · see citing works
Self-citationSemantic Focusing Allows Fully Automated Single-Layer Slide Scanning of Cervical Cytology Slides
Lahrmann, B., Valous, N. A., Eisenmann, U., Wentzensen, N., & Grabe, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061441 · Cited by 42 · see citing works
Self-citationThe evolution of Olig genes and their roles in myelination
Li, H., & Richardson, W. (2008) · Neuron Glia Biology · doi:10.1017/s1740925x09990251 · Cited by 39 · see citing works
Klaft, Z., Hollnagel, J., Salar, S., Çalışkan, G., Schulz, S., Schneider, U. C., Horn, P., Koch, A., Holtkamp, M., Gabriel, S., et al. (2016) · Epilepsia · doi:10.1111/epi.13360 · Cited by 38 · see citing works
Self-citationPapageorgiou, I. E., Fetani, A. F., Lewen, A., Heinemann, U., & Kann, O. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0802-0 · Cited by 37 · see citing works
Self-citationHalama, N., Zoernig, I., Spille, A., Westphal, K., Schirmacher, P., Jaeger, D., & Grabe, N. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007847 · Cited by 34 · see citing works
Self-citationRapid stereological quantitation of temporal neocortex in TLE
Doherty, C. P., Fitzsimons, M. B., Meredith, G. E., Thornton, J., McMackin, D., Farrell, M., Phillips, J. P., & Staunton, H. (2003) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(03)00078-x · Cited by 28 · see citing works
Intracellular acidification in neurons induced by ammonium depends on KCC2 function
Titz, S., Hormuzdi, S. G., Lewen, A., Monyer, H., & Misgeld, U. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04583.x · Cited by 28 · see citing works
Valous, N. A., Lahrmann, B., Zhou, W., Veltkamp, R. C., & Grabe, N. (2012) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2012.12.017 · Cited by 22 · see citing works
Self-citationST8SIA2 promotes oligodendrocyte differentiation and the integrity of myelin and axons
Szewczyk, Ł. M., Brożko, N., Nagalski, A., Röckle, I., Werneburg, S., Hildebrandt, H., Wisniewska, M. B., & Kuźnicki, J. (2016) · Glia · doi:10.1002/glia.23048 · Cited by 20 · see citing works
Eefsen, R. L., Engelholm, L. H., Alpízar‐Alpízar, W., den Eynden, G. G. E. V., Vermeulen, P. B., Christensen, I. J., Lærum, O. D., Rolff, H. C., Høyer‐Hansen, G., Vainer, B., et al. (2015) · Cancer Microenvironment · doi:10.1007/s12307-015-0172-z · Cited by 20 · see citing works
D'Amelio, F. E., Mehler, W. R., Gibbs, M. A., Eng, L. F., & Wu, J. (1987) · Brain Research · doi:10.1016/0006-8993(87)90320-9 · Cited by 19 · see citing works
KCC2 Mediates NH4+ Uptake in Cultured Rat Brain Neurons
Liu, X., Titz, S., Lewen, A., & Misgeld, U. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00482.2003 · Cited by 16 · see citing works
Ong, W., Garey, L. J., Leong, S. K., & Reynolds, R. (1995) · Journal of Neurocytology · doi:10.1007/bf01257375 · Cited by 11 · 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
Advances in the Potential Biomarkers of Epilepsy
Kobylarek, D., Iwanowski, P. S., Lewandowska, Z., Limphaibool, N., Szafranek, S., Labrzycka, A., & Kozubski, W. P. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00685 · Cited by 153 · see citing works
Astrocytes as Guardians of Neuronal Excitability: Mechanisms Underlying Epileptogenesis
Verhoog, Q. P., Holtman, L., Aronica, E., & van Vliet, E. A. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.591690 · Cited by 144 · see citing works
Schirrmacher, V. (2020) · Biomedicines · doi:10.3390/biomedicines8110526 · Cited by 126 · see citing works
The role of glutamate and glutamine metabolism and related transporters in nerve cells
Zhang, D., Hua, Z., & Li, Z. (2024) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14617 · Cited by 102 · see citing works
Oligodendrocytes Support Neuronal Glutamatergic Transmission via Expression of Glutamine Synthetase
Xin, W., Mironova, Y. A., Shen, H., Marino, R. A. M., Waisman, A., Lamers, W. H., Bergles, D. E., & Bonci, A. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.094 · Cited by 100 · see citing works
Glial Glutamine Homeostasis in Health and Disease
Andersen, J. V., & Schousboe, A. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03771-1 · Cited by 88 · see citing works
Gavegnano, C., Haile, W. B., Hurwitz, S. J., Tao, S., Jiang, Y., Schinazi, R. F., & Tyor, W. R. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1565-6 · Cited by 67 · see citing works
Blaszczyk, L., Maître, M., Lesté-Lasserre, T., Clark, S., Cota, D., Oliet, S. H. R., & Fénelon, V. S. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1378-z · Cited by 49 · see citing works
Ribeiro, R. P., Ponz‐Segrelles, G., Bleidorn, C., & Aguado, M. T. (2019) · BMC Genomics · doi:10.1186/s12864-019-6223-y · Cited by 48 · see citing works
Neuronal activity induces glutathione metabolism gene expression in astrocytes
McGann, J. C., & Mandel, G. (2018) · Glia · doi:10.1002/glia.23455 · Cited by 29 · see citing works
Wang, Z., Xie, R., Yang, X., Yin, H., Li, X., Liu, T., Ma, Y., Gao, J., Zang, Z., Ruan, R., et al. (2021) · Theranostics · doi:10.7150/thno.56331 · Cited by 28 · see citing works
Evidence for glutamine synthetase function in mouse spinal cord oligodendrocytes
Haim, L. B., Schirmer, L., Zulji, A., Sabeur, K., Tiret, B., Ribon, M., Chang, S., Lamers, W. H., Boillée, S., Chaumeil, M. M., et al. (2021) · Glia · doi:10.1002/glia.24071 · Cited by 28 · see citing works
Antagomirs targeting miR-142–5p attenuate pilocarpine-induced status epilepticus in mice
Zhang, H., Lian, Y., Xie, N., Cheng, X., Chen, C., Xu, H., & Zheng, Y. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112089 · Cited by 23 · see citing works
Peng, J., Wu, S., Guo, C., Guo, K., Zhang, W., Liu, R., Li, J., & Hu, Z. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02875-5 · Cited by 21 · see citing works
Chameh, H. M., Falby, M. R., Movahed, M., Arbabi, K., Rich, S., Zhang, L., Lefebvre, J., Tripathy, S. J., Pittà, M. D., & Valiante, T. A. (2023) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2023.1250834 · Cited by 14 · see citing works
Tse, K., Beamer, E. H., Simpson, D. M., Beynon, R. J., Sills, G. J., & Thippeswamy, T. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.625017 · Cited by 15 · see citing works
Tse, K., Hammond, D. E., Simpson, D. M., Beynon, R. J., Beamer, E. H., Tymianski, M., Salter, M. W., Sills, G. J., & Thippeswamy, T. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24441 · Cited by 15 · see citing works
He, T., Li, N., Shi, P., Xu, X., Nie, J., Lu, X., Yu, P., Fan, Y., Ge, F., & Guan, X. (2021) · Addiction Biology · doi:10.1111/adb.13068 · Cited by 14 · see citing works
Astrocytic pathology in Alpers’ syndrome
Smith, L. A., Chen, C., Lax, N. Z., Taylor, R. W., Erskine, D., & McFarland, R. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01579-w · Cited by 13 · see citing works
Henao‐Restrepo, J., López‐Murillo, C., Valderrama‐Carmona, P., Orozco‐Santa, N., Gomez, J., Gutiérrez‐Vargas, J., Moraga, R., Toledo, J., Littau, J. L., Härtel, S., et al. (2023) · Brain Pathology · doi:10.1111/bpa.13119 · Cited by 11 · see citing works
Halder, A., Yadav, K., Aggarwal, A., Singhal, N. K., & Sandhir, R. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109714 · Cited by 9 · see citing works
Gómez-Oliver, F., de la Rosa, R. F., Brackhan, M., Bascuñana, P., Pozo, M. A., & García‐García, L. (2025) · Biomolecules · doi:10.3390/biom15091242 · Cited by 6 · see citing works
Kalirin is involved in epileptogenesis by modulating the activity of the Rac1 signaling pathway
Chen, L., Luo, T., Cui, W., Zhu, M., Xu, Z., & Huang, H. (2023) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2023.102289 · Cited by 6 · see citing works
Panayotacopoulou, M. T., Papageorgiou, I. E., Pagida, M. A., Katsogridaki, A. E., Chrysanthou‐Piterou, M., Valous, N. A., Halama, N., Patsouris, E., & Konstantinidou, A. E. (2022) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlab135 · Cited by 5 · see citing works
Self-citationGüler, B. E., Zorin, M., Linnert, J., Nagel‐Wolfrum, K., & Uwe Wolfrum, B. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.25.591120 · Cited by 4 · see citing works
The adhesion GPCR ADGRV1 controls glutamate homeostasis in hippocampal astrocytes supporting neurons
Güler, B. E., Zorin, M., Linnert, J., Nagel‐Wolfrum, K., & Wolfrum, U. (2026) · Acta Neuropathologica Communications · doi:10.1186/s40478-026-02282-2 · Cited by 7 · see citing works
Gavegnano, C., Haile, W. B., Koneru, R., Hurwitz, S. J., Kohler, J. J., Tyor, W. R., & Schinazi, R. F. (2020) · Journal of NeuroVirology · doi:10.1007/s13365-020-00842-3 · Cited by 3 · see citing works
Albrecht, J., Czuczwar, S. J., Zielińska, M., & Miziak, B. (2025) · Neurochemical Research · doi:10.1007/s11064-024-04329-z · Cited by 2 · see citing works
Nosova, O., Суфиева, Д. А., & Korzhevsky, D. E. (2021) · Cell and Tissue Biology · doi:10.1134/s1990519x21030081 · Cited by 2 · see citing works
Kalirin is Involved in the Epiliptogenesis by Modulating the Activity of Rac1 Signaling PathwayPreprint
Chen, L., Luo, T., Cui, W., Zhu, M., Xu, Z., & Huang, H. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4166320
Li, C., Hao, L.-L., Liu, X.-Y., Zhou, J., & Ma, W.-N. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1966487
- Authors
- Papageorgiou, I. E., Valous, N. A., Lahrmann, B., Janova, H., Klaft, Z., Koch, A., Schneider, U. C., Vajkoczy, P., Heppner, F. L., Grabe, N., Halama, N., Heinemann, U., & Kann, O.
- Affiliations
- Heidelberg University (DE)
- German Cancer Research Center (DE)
- Division of Clinical Neuroscience Max Planck Institute of Experimental Medicine, Hermann‐Rein‐str. 3 Göttingen D‐37075 Germany
- Charité – Universitätsmedizin Berlin (DE)
- Corresponding author
- Heinemann, Uwe
- Kann, Oliver
- ORCID
- Venue
- Glia
- Publisher
- Wiley
- Published
- 2018-01-19
- Volume
- 66
- Issue
- 5
- Pages
- 920-933
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- OpenAlex
- W2790693017
- Cited by
- 31
- References
- 67
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 5 · 2019: 6 · 2018: 2
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- glutamine synthetase, mesial temporal lobe epilepsy, hippocampal neurodegeneration, reactive astrogliosis, glial fibrillary acidic protein, astrocytes, neuronal loss, CA1, hippocampal hilus, white matter astrocytes
- MeSH terms
- Drug Resistant Epilepsy, Adult, Astrocytes, Cerebral Cortex, Epilepsy, Temporal Lobe, Female, Glial Fibrillary Acidic Protein, Gliosis, Glutamate-Ammonia Ligase, Humans, Immunohistochemistry, Male, Neurons, Cell Death, Neurodegenerative Diseases, White Matter
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