Mossy fiber sprouting into the hippocampal region CA2 in patients with temporal lobe epilepsy.
Ammon's horn
dentate gyrus
granule cell dispersion
hippocampus
kainate
Journal
Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
revised:
23
02
2021
received:
07
10
2020
accepted:
27
02
2021
pubmed:
16
3
2021
medline:
25
2
2022
entrez:
15
3
2021
Statut:
ppublish
Résumé
Hippocampal sclerosis (HS) in Temporal Lobe Epilepsy (TLE) shows neuronal death in cornu ammonis (CA)1, CA3, and CA4. It is known that granule cells and CA2 neurons survive and their axons, the mossy fibers (MF), lose their target cells in CA3 and CA4 and sprout to the granule cell layer and molecular layer. We examined in TLE patients and in a mouse epilepsy model, whether MF sprouting is directed to the dentate gyrus or extends to distant CA regions and whether sprouting is associated with death of target neurons in CA3 and CA4. In 319 TLE patients, HS was evaluated by Wyler grade and International League against Epilepsy (ILAE) types using immunohistochemistry against neuronal nuclei (NeuN). Synaptoporin was used to colocalize MF. In addition, transgenic Thy1-eGFP mice were intrahippocampally injected with kainate and sprouting of eGFP-positive MFs was analyzed together with immunocytochemistry for regulator of G-protein signaling 14 (RGS14). In human HS Wyler III and IV as well as in ILAE 1, 2, and 3 specimens, we found synaptoporin-positive axon terminals in CA2 and even in CA1, associated with the extent of granule cell dispersion. Sprouting was seen in cases with cell death of target neurons in CA3 and CA4 (classical severe HS ILAE type 1) but also without this cell death (atypical HS ILAE type 2). Similarly, in epileptic mice eGFP-positive MFs sprouted to CA2 and beyond. The presence of MF terminals in the CA2 pyramidal cell layer and in CA1 was also correlated with the extent of granule cell dispersion. The similarity of our findings in human specimens and in the mouse model highlights the importance and opens up new chances of using translational approaches to determine mechanisms underlying TLE.
Substances chimiques
RGS Proteins
0
Rgs14 protein, mouse
0
Kainic Acid
SIV03811UC
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
580-592Informations de copyright
© 2021 The Authors. Hippocampus published by Wiley Periodicals LLC.
Références
Althaus, A. L., Zhang, H., & Parent, J. M. (2016). Axonal plasticity of age-defined dentate granule cells in a rat model of mesial temporal lobe epilepsy. Neurobiology of Disease, 86, 187-196. https://doi.org/10.1016/j.nbd.2015.11.024
Blumcke, I., Cross, J. H., & Spreafico, R. (2013). The international consensus classification for hippocampal sclerosis: An important step towards accurate prognosis. Lancet Neurology, 12, 844-846.
Blumcke, I., Pauli, E., Clusmann, H., Schramm, J., Becker, A., Elger, C., … Hildebrandt, M. (2007). A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathologica, 113, 235-244. https://doi.org/10.1007/s00401-006-0187-0
Blumcke, I., Suter, B., Behle, K., Kuhn, R., Schramm, J., Elger, C. E., & Wiestler, O. D. (2000). Loss of hilar mossy cells in Ammon's horn sclerosis. Epilepsia, 41(Suppl 6), S174-S180.
Blumcke, I., Thom, M., Aronica, E., Armstrong, D. D., Bartolomei, F., Bernasconi, A., … Spreafico, R. (2013). International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A Task Force report from the ILAE Commission on diagnostic methods. Epilepsia, 54, 1315-1329.
Blumcke, I., Thom, M., & Wiestler, O. D. (2002). Ammon's horn sclerosis: A maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathology, 12, 199-211.
Braak, E., Strotkamp, B., & Braak, H. (1991). Parvalbumin-immunoreactive structures in the hippocampus of the human adult. Cell and Tissue Research, 264, 33-48. https://doi.org/10.1007/BF00305720
Braak, H. (1974). On the structure of the human archicortex. I. The cornu ammonis. A Golgi and pigmentarchitectonic study. Cell and Tissue Research, 152, 349-383.
Braak H. 1980. Architectonics of the human telencephalic cortex. Berlin Heidelberg: Springer-Verlag. Retreived from: https://www.springer.com/de/book/9783642815249
Engel, J. J., van Nes, P. C., Rasmussen, T. B., & Ojemann, L. M. (1993). Outcome with respect to epileptic seizures in surgical treatment of the epilepsies (pp. 609-621). NY: Raven Press.
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., … Sanes, J. R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 28, 41-51. https://doi.org/10.1016/S0896-6273(00)00084-2
Freiman, T. M., Eismann-Schweimler, J., & Frotscher, M. (2011). Granule cell dispersion in temporal lobe epilepsy is associated with changes in dendritic orientation and spine distribution. Experimental Neurology, 229, 332-338.
Häussler, U., Rinas, K., Kilias, A., Egert, U., & Haas, C. A. (2016). Mossy fiber sprouting and pyramidal cell dispersion in the hippocampal CA2 region in a mouse model of temporal lobe epilepsy. Hippocampus, 26, 577-588. https://doi.org/10.1002/hipo.22543
Heinrich, C., Lähteinen, S., Suzuki, F., Anne-Marie, L., Huber, S., Häussler, U., … Castren, E. (2011). Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy. Neurobiology of Disease, 42, 35-47. https://doi.org/10.1016/j.nbd.2011.01.001
Heinrich, C., Nitta, N., Flubacher, A., Muller, M., Fahrner, A., Kirsch, M., … Haas, C. A. (2006). Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. The Journal of Neuroscience, 26, 4701-4713. https://doi.org/10.1523/JNEUROSCI.5516-05.2006
Houser, C. R. (1990). Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Research, 535, 195-204. https://doi.org/10.1016/0006-8993(90)91601-C
Maglóczky, Z., Acsády, L., & Freund, T. F. (1994). Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus, 4, 322-334. https://doi.org/10.1002/hipo.450040316
Marx, M., Haas, C. A., & Häussler, U. (2013). Differential vulnerability of interneurons in the epileptic hippocampus. Frontiers in Cellular Neuroscience, 7, 167.
Mathern, G. W., Babb, T. L., Micevych, P. E., Blanco, C. E., & Pretorius, J. K. (1997). Granule cell mRNA levels for BDNF, NGF, and NT-3 correlate with neuron losses or supragranular mossy fiber sprouting in the chronically damaged and epileptic human hippocampus. Molecular and Chemical Neuropathology, 30, 53-76. https://doi.org/10.1007/BF02815150
Mouritzen Dam, A. (1979). The density of neurons in the human hippocampus. Neuropathology and Applied Neurobiology, 5, 249-264.
Piskorowski, R. A., & Chevaleyre, V. (2012). Synaptic integration by different dendritic compartments of hippocampal CA1 and CA2 pyramidal neurons. Cellular and Molecular Life Sciences, 69, 75-88. https://doi.org/10.1007/s00018-011-0769-4
Proper, E. A., Jansen, G. H., van Veelen, C. W., van Rijen, P. C., Gispen, W. H., & de Graan, P. N. (2001). A grading system for hippocampal sclerosis based on the degree of hippocampal mossy fiber sprouting. Acta Neuropathologica, 101, 405-409. https://doi.org/10.1007/s004010000301
Proper, E. A., Oestreicher, A. B., Jansen, G. H., Veelen, C. W., van Rijen, P. C., Gispen, W. H., & de Graan, P. N. (2000). Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain: A Journal of Neurology, 123(Pt 1), 19-30.
R Development Core Team. (2015). A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Schmeiser, B., Li, J., Brandt, A., Zentner, J., Doostkam, S., & Freiman, T. M. (2017). Different mossy fiber sprouting patterns in ILAE hippocampal sclerosis types. Epilepsy Research, 136, 115-122.
Schmeiser, B., Zentner, J., Prinz, M., Brandt, A., & Freiman, T. M. (2017). Extent of mossy fiber sprouting in patients with mesiotemporal lobe epilepsy correlates with neuronal cell loss and granule cell dispersion. Epilepsy Research, 129, 51-58.
Singec, I., Knoth, R., Ditter, M., Hagemeyer, C. E., Rosenbrock, H., Frotscher, M., & Volk, B. (2002). Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. The Journal of Comparative Neurology, 452, 139-153. https://doi.org/10.1002/cne.10371
Sloviter, R. S., Sollas, A. L., Barbaro, N. M., & Laxer, K. D. (1991). Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. The Journal of Comparative Neurology, 308, 381-396. https://doi.org/10.1002/cne.903080306
Sutula, T., Cascino, G., Cavazos, J., Parada, I., & Ramirez, L. (1989). Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Annals of Neurology, 26, 321-330. https://doi.org/10.1002/ana.410260303
Sutula, T., He, X. X., Cavazos, J., & Scott, G. (1988). Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science, 239, 1147-1150. https://doi.org/10.1126/science.2449733
Thom, M. (2014). Review: Hippocampal sclerosis in epilepsy: A neuropathology review. Neuropathology and Applied Neurobiology, 40, 520-543. https://doi.org/10.1111/nan.12150
Thom, M., Zhou, J., Martinian, L., & Sisodiya, S. (2005). Quantitative post-mortem study of the hippocampus in chronic epilepsy: Seizures do not inevitably cause neuronal loss. Brain, 128, 1344-1357. https://doi.org/10.1093/brain/awh475
Tulke, S., Haas, C. A., & Häussler, U. (2019). Expression of brain-derived neurotrophic factor and structural plasticity in the dentate gyrus and CA2 region correlate with epileptiform activity. Epilepsia, 60, 1234-1247.
Wittner, L., Eross, L., Czirják, S., Halász, P., Freund, T. F., & Maglóczky, Z. (2005). Surviving CA1 pyramidal cells receive intact perisomatic inhibitory input in the human epileptic hippocampus. Brain: A Journal of Neurology, 128, 138-152.
Wittner, L., Huberfeld, G., Clémenceau, S., Eross, L., Dezamis, E., Entz, L., … Miles, R. (2009). The epileptic human hippocampal cornu ammonis 2 region generates spontaneous interictal-like activity in vitro. Brain: A Journal of Neurology, 132, 3032-3046. https://doi.org/10.1093/brain/awp238
Wittner, L., Maglóczky, Z., Borhegyi, Z., Halász, P., Tóth, S., Eross, L., … Freund, T. F. (2001). Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience, 108, 587-600. https://doi.org/10.1016/S0306-4522(01)00446-8
Wyler, A. R., Dohan, F. C., Schweitzer, J. B., & Berry, A. D. (1992). A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporallobectomy. Journal of Epilepsy, 5, 220-225.
Zentner, J., Hufnagel, A., Wolf, H. K., Ostertun, B., Behrens, E., Campos, M. G., … Schramm, J. (1995). Surgical treatment of temporal lobe epilepsy: Clinical, radiological, and histopathological findings in 178 patients. Journal of Neurology, Neurosurgery, and Psychiatry, 58, 666-673. https://doi.org/10.1136/jnnp.58.6.666