Nestin-expressing cell types in the temporal lobe and hippocampus: Morphology, differentiation, and proliferative capacity

Liu, J., Reeves, C., Thomas, J., McEvoy, A., Miserocchi, A., Thompson, P., Sisodiya, S. and Thom, M. 2018. Nestin-expressing cell types in the temporal lobe and hippocampus: Morphology, differentiation, and proliferative capacity. GLIA. 66 (1), pp. 62-77 23211. https://doi.org/10.1002/glia.23211

TitleNestin-expressing cell types in the temporal lobe and hippocampus: Morphology, differentiation, and proliferative capacity
AuthorsLiu, J., Reeves, C., Thomas, J., McEvoy, A., Miserocchi, A., Thompson, P., Sisodiya, S. and Thom, M.
Abstract

Nestin is expressed in immature neuroepithelial and progenitor cell types and transiently upregulated in proliferative neuroglial cells responding to acute brain injury, including following seizures. In 36 temporal lobe specimens from patients with temporal lobe epilepsy (age range 8-60 years) we studied the number, distribution and morphology of nestin-expressing cells in the pes, hippocampus body, parahippocampal gyrus, amygdala, temporal cortex and pole compared to post mortem control tissues from 26 cases (age range 12 gestational weeks to 76 years). The proliferative fraction of nestin-expressing cells was also evaluated in selected regions, including recognized niches, using MCM2. Their differentiation was explored with neuronal (DCX, mushashi, βIII tubulin, NeuN) and glial (GFAP, GFAPdelta, glutamine synthetase , aquaporin4) markers, both in sections and following culture. Findings were correlated with clinical parameters. A stereotypical pattern in the distribution and range of morphologies of nestin-expressing cells was observed, reminiscent of patterns in the developing brain, with increased densities in epilepsy compared to adult controls (p<0.001). Findings included MCM2-positive radial glial-like cells in the periventricular white matter and rows of nestin-expressing cells in the hippocampal fimbria and sulcus. Nestin cells represented 29% of the hippocampal proliferative fraction in epilepsy cases; 20% co-expressed βIII tubulin in culture compared to 28% with GFAP, but they mainly lacked glial maturation (aquaporin 4 or glutamine synthetase expression). Significant correlations were noted between age at surgery, memory deficits and NEC populations. Temporal lobe nestin-expressing cells with ongoing proliferative capacity likely represent vestiges of developmental migratory streams and resident reactive cell populations of potential relevance to hippocampal epileptogenesis, temporal lobe pathology and co-morbidities, including memory decline.

Keywordshippocampal sclerosis, nestin, radial glia, temporal lobe epilepsy, white matter
Article number23211
JournalGLIA
Journal citation66 (1), pp. 62-77
ISSN0894-1491
Year2018
PublisherWiley
Publisher's version
Digital Object Identifier (DOI)https://doi.org/10.1002/glia.23211
Publication dates
Published online19 Sep 2017
Published in printJan 2018
Published19 Sep 2017
LicenseCC BY 4.0

Related outputs

Serotonin transporter in the temporal lobe, hippocampus and amygdala in SUDEP
Patodia, S., Somani, A., Liu, J.Y.W., Cattaneo, A., Paradisco, B., Garcia, M., Othman, M., Diehl, B., Foong, J. and Thom, M. 2022. Serotonin transporter in the temporal lobe, hippocampus and amygdala in SUDEP. Brain Pathology. 32 (5) e13074. https://doi.org/10.1111/bpa.13074

Safety of intracranial electroencephalography during functional electromagnetic resonance imaging in humans at 1.5 tesla using a head transmit RF coil: Histopathological and heat-shock immunohistochemistry observations.
Liu, Joan Y W, Hawsawi, Hassan B, Sharma, Niraj, Carmichael, David W, Diehl, Beate, Thom, Maria and Lemieux, Louis 2022. Safety of intracranial electroencephalography during functional electromagnetic resonance imaging in humans at 1.5 tesla using a head transmit RF coil: Histopathological and heat-shock immunohistochemistry observations. NeuroImage. 254 119129. https://doi.org/10.1016/j.neuroimage.2022.119129

Glial regenerative cell types in the superficial cortex in cortical dysplasia subtypes
Liu, J., Reeves, C., van der Pijl, R. and Thom, M. 2021. Glial regenerative cell types in the superficial cortex in cortical dysplasia subtypes. Epilepsy Research. 169 106529. https://doi.org/10.1016/j.eplepsyres.2020.106529

Granule Cell Dispersion in Human Temporal Lobe Epilepsy: Proteomics investigation of neurodevelopmental migratory pathways
Liu, J., Dzurova, N., Al-Kaaby, B., Millks, K., Sisodiya, S.M. and Thom, M. 2020. Granule Cell Dispersion in Human Temporal Lobe Epilepsy: Proteomics investigation of neurodevelopmental migratory pathways. Frontiers in Cellular Neuroscience. 14 53. https://doi.org/10.3389/fncel.2020.00053

Spatiotemporal dynamics of PDGFRβ expression in pericytes and glial scar formation in penetrating brain injuries in adults
Reeves, C., Jardim, A.P., Sisodiya, S.M., Thom, M. and Liu, J. 2019. Spatiotemporal dynamics of PDGFRβ expression in pericytes and glial scar formation in penetrating brain injuries in adults. Neuropathology and Applied Neurobiology. 45 (6), pp. 609-627 NAN-2018-0107.R1. https://doi.org/10.1111/nan.12539

Multinodular and vacuolating neuronal tumors in epilepsy: dysplasia or neoplasia?
Thom, M., Liu, J., Bongaarts, A., Reinten, R., Paradiso, B., Jäger, H., Reeves, C., Somani, A., An, S., Marsdon, D., McEvoy, A., Miserocchi, A., Thorne, L., Newman, F., Bucur, S., Honavar, M., Jacques, T. and Aronica, E. 2018. Multinodular and vacuolating neuronal tumors in epilepsy: dysplasia or neoplasia? Brain Pathology. 28 (2), pp. 155-171. https://doi.org/10.1111/bpa.12555

Characterising subtypes of hippocampal sclerosis and reorganization: correlation with pre and postoperative memory deficit
Prada Jardim, A., Liu, J., Baber, J., Michalak, Z., Reeves, C., Ellis, M., Novy, J., de Tisi, J., McEvoy, A., Miserocchi, A., Targas Yacubian, E., Sisodiya, S., Thompson, P. and Thom, M. 2018. Characterising subtypes of hippocampal sclerosis and reorganization: correlation with pre and postoperative memory deficit. Brain Pathology. 28 (2), pp. 143-154. https://doi.org/10.1111/BPA.12514

The ventrolateral medulla and medullary raphe in sudden unexpected death in epilepsy
Patodia, S., Somani, A., O’Hare, M., Venkateswaran, R., Liu, J., Michalak, Z., Ellis, M., Scheffer, I., Diehl, B., Sisodiya, S. and Thom, M. 2018. The ventrolateral medulla and medullary raphe in sudden unexpected death in epilepsy. Brain. 141 (6), pp. 1719-1733. https://doi.org/10.1093/brain/awy078

Doublecortin-expressing cell types in temporal lobe epilepsy
Liu, J.Y.W., Matarin, M., Reeves, C., McEvoy, A.W., Miserocchi, A., Thompson, P., Sisodiya, S.M. and Thom, M. 2018. Doublecortin-expressing cell types in temporal lobe epilepsy. Acta Neuropathologica Communications. 6, p. 60 60. https://doi.org/10.1186/s40478-018-0566-5

Pathology-MRI correlations in diffuse low-grade epilepsy associated tumors
Al-Hajri, A., Al-Mughairi, S., Somani, A., An, S., Liu, J.Y.W., Miserocchi, A., McEvoy, A.W., Yousry, T., Hoskote, C. and Thom, M. 2017. Pathology-MRI correlations in diffuse low-grade epilepsy associated tumors. Journal of Neuropathology and Experimental Neurology. 76 (12), pp. 1023-1033. https://doi.org/10.1093/jnen/nlx090

PAX6, brain structure and function in human adults: Advanced MRI in aniridia
Yogarajah, M., Matarin, M., Vollmar, C., Thompson, P.J., Duncan, J.S., Symms, M., Moore, A.T., Liu, J.Y.W., Thom, M., van Heyningen, V. and Sisodiya, S.M. 2016. PAX6, brain structure and function in human adults: Advanced MRI in aniridia. Annals of Clinical and Translational Neurology. 3 (5), pp. 314-330. https://doi.org/10.1002/acn3.297

Combined Ex Vivo 9.4T MRI and Quantitative Histopathological Study in Normal and Pathological Neocortical Resections in Focal Epilepsy
Reeves, C., Tachrount, M., Thomas, D., Michalak, Z., Liu, J.Y.W., Ellis, M., Diehl, B., Miserocchi, A., McEvoy, A.W., Eriksson, S., Yousry, T. and Thom, M. 2016. Combined Ex Vivo 9.4T MRI and Quantitative Histopathological Study in Normal and Pathological Neocortical Resections in Focal Epilepsy. Brain Pathology. 26 (3), pp. 319-333. https://doi.org/10.1111/bpa.12298

Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections
Tai, X., Koepp, M., Duncan, J., Fox, N., Thompson, P., Baxendale, S., Liu, J., Reeves, C., Michalak, Z. and Thom, M. 2016. Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections. Brain. 139 (9), pp. 2441-55. https://doi.org/10.1093/brain/aww187

Early lipofuscin accumulation in Frontal Lobe Epilepsy
Liu, J., Reeves, C., Diehl, B., Coppola, A., Al-Hajri, A., Hoskote, C., Mughairy, S., Tachrount, M., Groves, M., Michalak, Z., Mills, K., McEvoy, A., Miserocchi, A., Sisodiya, S. and Thom, M. 2016. Early lipofuscin accumulation in Frontal Lobe Epilepsy. Annals of Neurology. 80, pp. 882-895. https://doi.org/10.1002/ana.24803

A cautionary note in the interpretation of human papillomavirus E6 immunohistochemistry in focal cortical dysplasia
Thom, M., Liu, J., Reeves, C., Stopps, V., Sisodiya, S.M. and Liu, J.Y.W. 2015. A cautionary note in the interpretation of human papillomavirus E6 immunohistochemistry in focal cortical dysplasia. Annals of Neurology. 77 (2), pp. 352-353. https://doi.org/10.1002/ana.24330

A comparative study of the dentate gyrus in hippocampal sclerosis in epilepsy and dementia
Bandopadhyay, R., Liu, J.Y.W., Sisodiya, S.M. and Thom, M. 2014. A comparative study of the dentate gyrus in hippocampal sclerosis in epilepsy and dementia. Neuropathology and Applied Neurobiology. 40 (2), pp. 177-190. https://doi.org/10.1111/nan.12087

High-throughput, automated quantification of white matter neurons in mild malformation of cortical development in epilepsy
Liu, J.Y.W., Ellis, M., Brooke-Ball, H., de Tisi, J., Eriksson, S.H., Brandner, S., Sisodiya, S.M. and Thom, M. 2014. High-throughput, automated quantification of white matter neurons in mild malformation of cortical development in epilepsy. Acta Neuropathologica Communications. 2 72. https://doi.org/10.1186/2051-5960-2-72

Evidence for mTOR pathway activation in a spectrum of epilepsy-associated pathologies
Liu, J.Y.W., Reeves, C., Michalak, Z., Coppola, A., Diehl, B., Sisodiya, S.M. and Thom, M. 2014. Evidence for mTOR pathway activation in a spectrum of epilepsy-associated pathologies. Acta Neuropathologica Communications. 2 71. https://doi.org/10.1186/2051-5960-2-71

In vivo P-glycoprotein function before and after epilepsy surgery
Bauer, M., Karch, R., Zeitlinger, M., Liu, J.Y.W., Koepp, M.J., Asselin, M.-C., Sisodiya, S.M., Hainfellner, J.A., Wadsak, W., Mitterhauser, M., Müller, M., Pataraia, E. and Langer, O. 2014. In vivo P-glycoprotein function before and after epilepsy surgery. Neurology. 83 (15). https://doi.org/10.1212/wnl.0000000000000858

Interictal psychosis following temporal lobe surgery: dentate gyrus pathology
Thom, M., Kensche, M., Maynard, J., Liu, J.Y.W., Reeves, C., Goc, J., Marsdon, D., Fluegel, D. and Foong, J. 2014. Interictal psychosis following temporal lobe surgery: dentate gyrus pathology. Psychological Medicine. 44 (14), pp. 3037-3049. https://doi.org/10.1017/s0033291714000452

A spatiotemporal study of gliosis in relation to depth electrode tracks in drug-resistant epilepsy
Goc, J., Liu, J.Y.W., Sisodiya, S.M. and Thom, M. 2014. A spatiotemporal study of gliosis in relation to depth electrode tracks in drug-resistant epilepsy. European Journal of Neuroscience. 39 (12), pp. 2151-2162. https://doi.org/10.1111/ejn.12548

A quantitative study of white matter hypomyelination and oligodendroglial maturation in focal cortical dysplasia type II
Shepherd, C., Liu, J., Goc, J., Martinian, L., Jacques, T.S., Sisodiya, S.M., Thom, M. and Liu, J.Y.W. 2013. A quantitative study of white matter hypomyelination and oligodendroglial maturation in focal cortical dysplasia type II. Epilepsia. 54 (5), pp. 898-908. https://doi.org/10.1111/epi.12143

P-glycoprotein expression and function in patients with temporal lobe epilepsy: A case-control study
Feldmann, M., Asselin, M.-C., Wang, S., McMahon, A., Anton-Rodriguez, J., Walker, M., Symms, M., Brown, G., Hinz, R., Matthews, J., Bauer, M., Langer, O., Thom, M., Jones, T., Vollmar, C., Duncan, J.S., Sisodiya, S.M., Koepp, M.J. and Liu, J.Y.W. 2013. P-glycoprotein expression and function in patients with temporal lobe epilepsy: A case-control study. The Lancet Neurology. 12 (8), pp. 777-785. https://doi.org/10.1016/s1474-4422(13)70109-1

Neuropathology of 16p13.11 deletion in epilepsy
Liu, J.Y.W., Kasperavičiute, D., Martinian, L., Thom, M. and Sisodiya, S.M. 2012. Neuropathology of 16p13.11 deletion in epilepsy. PLoS ONE. 7 (4). https://doi.org/10.1371/journal.pone.0034813

Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy
Liu, J.Y.W., Thom, M., Catarino, C.B., Martinian, L., Figarella-Branger, D., Bartolomei, F., Koepp, M. and Sisodiya, S.M. 2012. Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy. Brain. 135 (10), p. 3115–3133. https://doi.org/10.1093/brain/aws147

Investigation of hypoxia-inducible factor-1α in hippocampal sclerosis: A postmortem study
Feast, A., Martinian, L., Liu, J.Y.W., Catarino, C.B., Thom, M. and Sisodiya, S.M. 2012. Investigation of hypoxia-inducible factor-1α in hippocampal sclerosis: A postmortem study. Epilepsia. 53 (8), pp. 1349-1359. https://doi.org/10.1111/j.1528-1167.2012.03591.x

Variability of sclerosis along the longitudinal hippocampal axis in epilepsy: A post mortem study
Thom, M., Liagkouras, I., Martinian, L., Catarino, C.B., Sisodiya, S.M. and Liu, J.Y.W. 2012. Variability of sclerosis along the longitudinal hippocampal axis in epilepsy: A post mortem study. Epilepsy Research. 102 (1-2), pp. 45-59. https://doi.org/10.1016/j.eplepsyres.2012.04.015

Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: A post-mortem study
Thom, M., Liu, J.Y.W., Thompson, P., Phadke, R., Narkiewicz, M., Martinian, L., Marsdon, D., Koepp, M., Caboclo, L., Catarino, C.B. and Sisodiya, S.M. 2011. Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: A post-mortem study. Brain. 134 (10), pp. 2969-2981. https://doi.org/10.1093/brain/awr209

Dravet syndrome as epileptic encephalopathy: Evidence from long-term course and neuropathology
Catarino, C.B., Liu, J.Y.W., Liagkouras, I., Gibbons, V.S., Labrum, R.W., Ellis, R., Woodward, C., Davis, M.B., Smith, S.J., Cross, J.H., Appleton, R.E., Yendle, S.C., McMahon, J.M., Bellows, S.T., Jacques, T.S., Zuberi, S.M., Koepp, M.J., Martinian, L., Scheffer, I.E., Thom, M. and Sisodiya, S.M. 2011. Dravet syndrome as epileptic encephalopathy: Evidence from long-term course and neuropathology. Brain. 134 (10), pp. 2982-3010. https://doi.org/10.1093/brain/awr129

Immunolabeling recovery in archival, post-mortem, human brain tissue using modified antigen retrieval and the catalyzed signal amplification system
Liu, J.Y.W., Martinian, L., Thom, M. and Sisodiya, S.M. 2010. Immunolabeling recovery in archival, post-mortem, human brain tissue using modified antigen retrieval and the catalyzed signal amplification system. Journal of Neuroscience Methods. 190 (1), pp. 49-56. https://doi.org/10.1016/j.jneumeth.2010.04.020

Permalink - https://westminsterresearch.westminster.ac.uk/item/q27y9/nestin-expressing-cell-types-in-the-temporal-lobe-and-hippocampus-morphology-differentiation-and-proliferative-capacity


Share this

Usage statistics

80 total views
169 total downloads
These values cover views and downloads from WestminsterResearch and are for the period from September 2nd 2018, when this repository was created.