A potential role for glia‐derived extracellular matrix remodeling in postinjury epilepsy
Abstract
Head trauma and vascular injuries are known risk factors for acquired epilepsy. The sequence of events that lead from the initial injury to the development of epilepsy involves complex plastic changes and circuit rewiring. In‐depth, comprehensive understanding of the epileptogenic process is critical for the identification of disease‐modifying targets. Here we review the complex interactions of cellular and extracellular components that may promote epileptogenesis, with an emphasis on the role of astrocytes. Emerging evidence demonstrates that astrocytes promptly respond to brain damage and play a critical role in the development of postinjury epilepsy. Astrocytes have been shown to regulate extracellular matrix (ECM) remodeling, which can affect plasticity and stability of synapses and, in turn, contribute to the epileptogenic process. From these separate lines of evidence, we present a hypothesis suggesting a possible role for astrocyte‐regulated remodeling of ECM and perineuronal nets, a specialized ECM structure around fast‐spiking inhibitory interneurons, in the development and progression of posttraumatic epilepsies. © 2016 Wiley Periodicals, Inc.
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?
Several ADAMTs are upregulated following spinal cord injury, stroke, and epilepsy.
“several ADAMTs are upregulated following spinal cord injury, stroke, and epilepsy (Lemarchant et al., 2013; Kim et al., 2016).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Kim et al., 2016
Cites
The blood-brain barrier/neurovascular unit in health and disease
Hawkins, B. T., & Davis, T. P. (2005) · Pharmacological Reviews · doi:10.1124/pr.57.2.4 · Cited by 2,661 · see citing works
Glial and neuronal control of brain blood flow
Attwell, D., Buchan, A. M., Charpak, S., Lauritzen, M., MacVicar, B. A., & Newman, E. A. (2010) · Nature · doi:10.1038/nature09613 · Cited by 2,511 · see citing works
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679 · see citing works
A population-based study of seizures after traumatic brain injuries
Annegers, J. F., Hauser, W. A., Coan, S. P., & Rocca, W. A. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801013380104 · Cited by 1,090 · see citing works
Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W., & Rosenberg, G. A. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600375 · Cited by 1,060 · see citing works
Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors
Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., & Barres, B. A. (2012) · Nature · doi:10.1038/nature11059 · Cited by 764 · see citing works
Perineuronal Nets Protect Fear Memories from Erasure
Gogolla, N., Caroni, P., Lüthi, A., & Herry, C. (2009) · Science · doi:10.1126/science.1174146 · Cited by 760 · see citing works
Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC
Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., Chakraborty, C., Workman, G., Weaver, M., Sage, E. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104977108 · Cited by 642 · see citing works
Perineuronal nets protect fast-spiking interneurons against oxidative stress
Cabungcal, J.-H., Steullet, P., Morishita, H., Kraftsik, R., Cuenod, M., Hensch, T. K., & Do, K. Q. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300454110 · Cited by 512 · see citing works
Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R., & Schachner, M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20361 · Cited by 365 · see citing works
Wang, L., Zhang, Z. G., Zhang, R. L., Gregg, S. R., Hozeska-Solgot, A., LeTourneau, Y., Wang, Y., & Chopp, M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5380-05.2006 · Cited by 316 · see citing works
Wang, X.-B., Bozdagi, O., Nikitczuk, J. S., Zhai, Z. W., Zhou, Q., & Huntley, G. W. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807248105 · Cited by 316 · see citing works
Losartan prevents acquired epilepsy via TGF‐β signaling suppression
Bar‐Klein, G., Cacheaux, L. P., Kamintsky, L., Prager, O., Weissberg, I., Schoknecht, K., Cheng, P., Kim, S. Y., Wood, L., Heinemann, U., et al. (2014) · Annals of Neurology · doi:10.1002/ana.24147 · Cited by 270 · see citing works
Self-citationSlaker, M., Churchill, L., Todd, R. P., Blacktop, J. M., Zuloaga, D. G., Raber, J., Darling, R. A., Brown, T. E., & Sorg, B. A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3592-14.2015 · Cited by 208 · see citing works
Involvement of NOX2 in the Development of Behavioral and Pathologic Alterations in Isolated Rats
Schiavone, S., Sorce, S., Dubois-Dauphin, M., Jaquet, V., Colaianna, M., Zotti, M., Cuomo, V., Trabace, L., & Krause, K.-H. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.04.033 · Cited by 208 · see citing works
Saghatelyan, A. K., Dityatev, A., Schmidt, S., Schuster, T., Bartsch, U., & Schachner, M. (2001) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2000.0922 · Cited by 207 · see citing works
Kann, O., Huchzermeyer, C., Kovács, R., Wirtz, S., & Schuelke, M. (2011) · Brain · doi:10.1093/brain/awq333 · Cited by 189 · see citing works
Evers, M. R., Salmen, B., Bukalo, O., Rollenhagen, A., Bösl, M. R., Morellini, F., Bartsch, U., Dityatev, A., & Schachner, M. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07177.2002 · Cited by 172 · see citing works
de Vivo, L., Landi, S., Panniello, M., Baroncelli, L., Chierzi, S., Mariotti, L., Spolidoro, M., Pizzorusso, T., Maffei, L., & Ratto, G. M. (2013) · Nature Communications · doi:10.1038/ncomms2491 · Cited by 148 · see citing works
The perineuronal net component of the extracellular matrix in plasticity and epilepsy
McRae, P. A., & Porter, B. E. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.08.007 · Cited by 143 · see citing works
Self-citationGeissler, M., Gottschling, C., Aguado, A., Rauch, U., Wetzel, C. H., Hatt, H., & Faissner, A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3275-12.2013 · Cited by 140 · see citing works
Yuan, W., Matthews, R. T., Sandy, J. D., & Gottschall, P. E. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00347-0 · Cited by 109 · see citing works
Persistent decrease in multiple components of the perineuronal net following status epilepticus
McRae, P. A., Baranov, E., Rogers, S. L., & Porter, B. E. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08268.x · Cited by 85 · see citing works
Self-citationKim, G. W., Kim, H.-J., Cho, K.-J., Kim, H.-W., Cho, Y.-J., & Lee, B. I. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.07.008 · Cited by 63 · cited 4× · see citing works
“ADAMTS-4 Reactive astrocytes (Satoh et al., 2000; Hamel et al., 2005; Cross et al., 2006) Increase (Cross et al., 2006) Increase (Yuan et al., 2002) Journal of Neuroscience Research findings highlight the pivotal role of ECM in the regulation of synaptic microenvironment as well as during epileptogenesis.”
InfluentialJenkins, T. A., Harte, M. K., Stenson, G., & Reynolds, G. P. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.07.014 · Cited by 61 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders
Wen, T. H., Binder, D. K., Ethell, I. M., & Razak, K. A. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00270 · Cited by 170 · see citing works
- Authors
- Kim, S. Y., Porter, B. E., Friedman, A., & Kaufer, D.
- Affiliations
- University of California, Berkeley (US)
- Stanford Medicine (US)
- Ben-Gurion University of the Negev (IL)
- Canadian Institute for Advanced Research (CA)
- Corresponding author
- Kaufer, Daniela
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2016-06-05
- Volume
- 94
- Issue
- 9
- Pages
- 794-803
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2416932547
- Cited by
- 47
- References
- 25
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 4 · 2021: 6 · 2020: 2 · 2019: 2 · 2018: 5 · 2017: 7 · 2016: 1
- FWCI
- 0.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NARSAD
- Citizens United for Research in Epilepsy
- National Institute of Neurological Disorders and Stroke (2R56NS066005-05A1)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Keywords
- epileptogenesis, astrocytes, extracellular matrix remodeling, perineuronal nets, head trauma, vascular injury, synaptic plasticity, inhibitory interneurons, fast-spiking interneurons, acquired epilepsy
- MeSH terms
- Brain Injuries, Traumatic, Animals, Epilepsy, Extracellular Matrix, Humans, Neuroglia
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
