Multi-omics analysis suggests enhanced epileptogenesis in the Cornu Ammonis 3 of the pilocarpine model of mesial temporal lobe epilepsy.
hippocampus
laser-capture microdissection
proteomics
transcriptomics
Journal
Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
20
05
2020
revised:
04
09
2020
accepted:
26
09
2020
pubmed:
11
10
2020
medline:
25
2
2022
entrez:
10
10
2020
Statut:
ppublish
Résumé
Mesial temporal lobe epilepsy (MTLE) is a chronic neurological disorder characterized by the occurrence of seizures, and histopathological abnormalities in the mesial temporal lobe structures, mainly hippocampal sclerosis (HS). We used a multi-omics approach to determine the profile of transcript and protein expression in the dorsal and ventral hippocampal dentate gyrus (DG) and Cornu Ammonis 3 (CA3) in an animal model of MTLE induced by pilocarpine. We performed label-free proteomics and RNAseq from laser-microdissected tissue isolated from pilocarpine-induced Wistar rats. We divided the DG and CA3 into dorsal and ventral areas and analyzed them separately. We performed a data integration analysis and evaluated enriched signaling pathways, as well as the integrated networks generated based on the gene ontology processes. Our results indicate differences in the transcriptomic and proteomic profiles among the DG and the CA3 subfields of the hippocampus. Moreover, our data suggest that epileptogenesis is enhanced in the CA3 region when compared to the DG, with most abnormalities in transcript and protein levels occurring in the CA3. Furthermore, our results show that the epileptogenesis in the pilocarpine model involves predominantly abnormal regulation of excitatory neuronal mechanisms mediated by N-methyl D-aspartate (NMDA) receptors, changes in the serotonin signaling, and neuronal activity controlled by calcium/calmodulin-dependent protein kinase (CaMK) regulation and leucine-rich repeat kinase 2 (LRRK2)/WNT signaling pathways.
Substances chimiques
Pilocarpine
01MI4Q9DI3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
122-139Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P027849/1
Pays : United Kingdom
Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Ables, J. L., DeCarolis, N. A., Johnson, M. A., Rivera, P. D., Gao, Z., Cooper, D. C., … Eisch, A. J. (2010). Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. Journal of Neuroscience, 30(31), 10484-10492. https://doi.org/10.1523/JNEUROSCI.4721-09.2010
Akiyama, H., Arai, T., Kondo, H., Tanno, E., Haga, C., & Ikeda, K. (2000). Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Disease and Associated Disorders, 14(Suppl 1), S47-S53. https://doi.org/10.1097/00002093-200000001-00008
Balosso, S., Liu, J., Bianchi, M. E., & Vezzani, A. (2014). Disulfide-containing high mobility group Box-1 promotes N -methyl- d -aspartate receptor function and excitotoxicity by activating toll-like receptor 4-dependent signaling in hippocampal neurons. Antioxidants & Redox Signaling, 21(12), 1726-1740. https://doi.org/10.1089/ars.2013.5349
Bardai, F. H., Ordonez, D. G., Bailey, R. M., Hamm, M., Lewis, J., & Feany, M. B. (2018). Lrrk promotes tau neurotoxicity through dysregulation of Actin and mitochondrial dynamics. PLoS Biology, 16(12), e2006265. https://doi.org/10.1371/journal.pbio.2006265
Barel, O., Shalev, S. A., Ofir, R., Cohen, A., Zlotogora, J., Shorer, Z., … Birk, O. S. (2008). Maternally inherited Birk Barel mental retardation Dysmorphism syndrome caused by a mutation in the genomically imprinted potassium channel KCNK9. The American Journal of Human Genetics, 83(2), 193-199. https://doi.org/10.1016/j.ajhg.2008.07.010
Blighe, K., Rana, S., & Lewis, M. (2019). Enhanced Volcano: Publication-ready volcano plots with enhanced coloring and labeling. R package version 1.4.0. https://github.com/kevinblighe/EnhancedVolcano
Blümcke, 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(3), 235-244. https://doi.org/10.1007/s00401-006-0187-0
Blümcke, 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(7), 1315-1329. https://doi.org/10.1111/epi.12220
Brennan, T. J., Seeley, W. W., Kilgard, M., Schreiner, C. E., & Tecott, L. H. (1997). Sound-induced seizures in serotonin 5-HT2c receptor mutant mice. Nature Genetics, 16(4), 387-390. https://doi.org/10.1038/ng0897-387
Cammarota, M., Bevilaqua, L. R. M., Viola, H., Kerr, D. S., Reichmann, B., Teixeira, V., … Medina, J. H. (2002). Participation of CaMKII in neuronal plasticity and memory formation. Cellular and Molecular Neurobiology, 22(3), 259-267.
Cappuccio, I., Calderone, A., Busceti, C. L., Biagioni, F., Pontarelli, F., Bruno, V., … Caricasole, A. (2005). Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is required for the development of ischemic neuronal death. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25(10), 2647-2657. https://doi.org/10.1523/JNEUROSCI.5230-04.2005
Cavalheiro, E. A., Leite, J. P., Bortolotto, Z. A., Turski, W. A., Ikonomidou, C., & Turski, L. (1991). Long-term effects of pilocarpine in rats: Structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia, 32(6), 778-782. https://doi.org/10.1111/j.1528-1157.1991.tb05533.x
Chen, B., Khodadoust, M. S., Liu, C. L., Newman, A. M., & Alizadeh, A. A. (2018). Profiling tumor infiltrating immune cells with CIBERSORT. In L. von Stechow (Ed.), Cancer systems biology (Vol. 1711, pp. 243-259). New York, NY: Springer. https://doi.org/10.1007/978-1-4939-7493-1_12
Cho, K.-O., Lybrand, Z. R., Ito, N., Brulet, R., Tafacory, F., Zhang, L., … Hsieh, J. (2015). Aberrant hippocampal neurogenesis contributes to epilepsy and associated cognitive decline. Nature Communications, 6(1), 6606. https://doi.org/10.1038/ncomms7606
Citraro, R., Leo, A., Constanti, A., Russo, E., & De Sarro, G. (2016). MTOR pathway inhibition as a new therapeutic strategy in epilepsy and epileptogenesis. Pharmacological Research, 107, 333-343. https://doi.org/10.1016/j.phrs.2016.03.039
Civelek, M., & Lusis, A. J. (2014). Systems genetics approaches to understand complex traits. Nature Reviews Genetics, 15(1), 34-48. https://doi.org/10.1038/nrg3575
Cloix, J.-F., & Hévor, T. (2009). Epilepsy, regulation of brain energy metabolism and neurotransmission. Current Medicinal Chemistry, 16(7), 841-853.
Conover, J. C., Doetsch, F., Garcia-Verdugo, J. M., Gale, N. W., Yancopoulos, G. D., & Alvarez-Buylla, A. (2000). Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nature Neuroscience, 3(11), 1091-1097. https://doi.org/10.1038/80606
Conway, J. R., Lex, A., & Gehlenborg, N. (2017). UpSetR: An R package for the visualization of intersecting sets and their properties. Bioinformatics, 33(18), 2938-2940. https://doi.org/10.1093/bioinformatics/btx364
Crotti, A., & Glass, C. K. (2015). The choreography of neuroinflammation in Huntington's disease. Trends in Immunology, 36(6), 364-373. https://doi.org/10.1016/j.it.2015.04.007
da Fonseca, N. C., Joaquim, H. P. G., Talib, L. L., de Vincentiis, S., Gattaz, W. F., & Valente, K. D. (2015). Hippocampal serotonin depletion is related to the presence of generalized tonic-clonic seizures, but not to psychiatric disorders in patients with temporal lobe epilepsy. Epilepsy Research, 111, 18-25. https://doi.org/10.1016/j.eplepsyres.2014.12.013
de Sousa Abreu, R., Penalva, L. O., Marcotte, E. M., & Vogel, C. (2009). Global signatures of protein and mRNA expression levels. Molecular BioSystems, 5(12), 1512-1526. https://doi.org/10.1039/b908315d
Delgado-Escueta, A. V., Wilson, W. A., Olsen, R. W., & Porter, R. J. (1999). New waves of research in the epilepsies: Crossing into the third millennium. Advances in Neurology, 79, 3-58.
Devinsky, O., Vezzani, A., Najjar, S., De Lanerolle, N. C., & Rogawski, M. A. (2013). Glia and epilepsy: Excitability and inflammation. Trends in Neurosciences, 36(3), 174-184. https://doi.org/10.1016/j.tins.2012.11.008
do Canto, A. M., Vieira, A. S., Matos, H. B., Carvalho, B. S., Henning, B., Norwood, B. A., … Lopes-Cendes, I. (2020). Laser microdissection-based microproteomics of the hippocampus of a rat epilepsy model reveals regional differences in protein abundances. Scientific Reports, 10(1), 4412. https://doi.org/10.1038/s41598-020-61401-8
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., … Gingeras, T. R. (2013). STAR: Ultrafast universal RNA-seq aligner. Bioinformatics, 29(1), 15-21. https://doi.org/10.1093/bioinformatics/bts635
Engel, J. (1996). Excitation and inhibition in epilepsy. Canadian Journal of Neurological Sciences/Journal Canadien des Sciences Neurologiques, 23(3), 167-174. https://doi.org/10.1017/S0317167100038464
Everett, K. V., Chioza, B., Aicardi, J., Aschauer, H., Brouwer, O., Callenbach, P., … Gardiner, M. (2007). Linkage and association analysis of CACNG3 in childhood absence epilepsy. European Journal of Human Genetics, 15(4), 463-472. https://doi.org/10.1038/sj.ejhg.5201783
Fabene, P. F., Bramanti, P., & Constantin, G. (2010). The emerging role for chemokines in epilepsy. Journal of Neuroimmunology, 224(1-2), 22-27. https://doi.org/10.1016/j.jneuroim.2010.05.016
Fanselow, M. S., & Dong, H.-W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1), 7-19. https://doi.org/10.1016/j.neuron.2009.11.031
Fisher, R. S., Acevedo, C., Arzimanoglou, A., Bogacz, A., Cross, J. H., Elger, C. E., … Wiebe, S. (2014). ILAE official report: A practical clinical definition of epilepsy. Epilepsia, 55(4), 475-482. https://doi.org/10.1111/epi.12550
Gales, J. M., & Prayson, R. A. (2017). Chronic inflammation in refractory hippocampal sclerosis-related temporal lobe epilepsy. Annals of Diagnostic Pathology, 30, 12-16. https://doi.org/10.1016/j.anndiagpath.2017.05.009
Glickman, M. E., Rao, S. R., & Schultz, M. R. (2014). False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. Journal of Clinical Epidemiology, 67(8), 850-857. https://doi.org/10.1016/j.jclinepi.2014.03.012
Greene, J. G., Borges, K., & Dingledine, R. (2009). Quantitative transcriptional neuroanatomy of the rat hippocampus: Evidence for wide-ranging, pathway-specific heterogeneity among three principal cell layers. Hippocampus, 19(3), 253-264. https://doi.org/10.1002/hipo.20502
Grone, B. P., & Baraban, S. C. (2015). Animal models in epilepsy research: Legacies and new directions. Nature Neuroscience, 18(3), 339-343. https://doi.org/10.1038/nn.3934
Guyon, A., Skrzydelsi, D., Rovère, C., Rostène, W., Parsadaniantz, S. M., & Nahon, J. L. (2006). Stromal cell-derived factor-1? Modulation of the excitability of rat substantia nigra dopaminergic neurones: Presynaptic mechanisms. Journal of Neurochemistry, 96(6), 1540-1550. https://doi.org/10.1111/j.1471-4159.2006.03659.x
Harvey, K., & Outeiro, T. F. (2019). The role of LRRK2 in cell signalling. Biochemical Society Transactions, 47(1), 197-207. https://doi.org/10.1042/BST20180464
Hasin, Y., Seldin, M., & Lusis, A. (2017). Multi-omics approaches to disease. Genome Biology, 18(1), 83. https://doi.org/10.1186/s13059-017-1215-1
Hodges, S. L., & Lugo, J. N. (2018). Wnt/β-catenin signaling as a potential target for novel epilepsy therapies. Epilepsy Research, 146, 9-16. https://doi.org/10.1016/j.eplepsyres.2018.07.002
Hulsen, T., Jamuar, S. S., Moody, A. R., Karnes, J. H., Varga, O., Hedensted, S., … McKinney, E. F. (2019). From big data to precision medicine. Frontiers in Medicine, 6, 34. https://doi.org/10.3389/fmed.2019.00034
Ihaka, R., & Gentleman, R. (1996). R: A language for data analysis and graphics. Journal of Computational and Graphical Statistics, 5(3), 299. https://doi.org/10.2307/1390807
Iori, V., Maroso, M., Rizzi, M., Iyer, A. M., Vertemara, R., Carli, M., … Vezzani, A. (2013). Receptor for advanced glycation Endproducts is upregulated in temporal lobe epilepsy and contributes to experimental seizures. Neurobiology of Disease, 58, 102-114. https://doi.org/10.1016/j.nbd.2013.03.006
Joseph, A., & Turrigiano, G. G. (2017). All for one but not one for all: Excitatory synaptic scaling and intrinsic excitability are Coregulated by CaMKIV, whereas inhibitory synaptic scaling is under independent control. The Journal of Neuroscience, 37(28), 6778-6785. https://doi.org/10.1523/JNEUROSCI.0618-17.2017
Kaczmarek, L. K. (2013). Slack, slick, and sodium-activated potassium channels. ISRN Neuroscience, 2013, 1-14. https://doi.org/10.1155/2013/354262
Karczewski, K. J., & Snyder, M. P. (2018). Integrative omics for health and disease. Nature Reviews Genetics, 19(5), 299-310. https://doi.org/10.1038/nrg.2018.4
Kawahara, R., Lima, R. N., Domingues, R. R., Pauletti, B. A., Meirelles, G. V., Assis, M., … Paes Leme, A. F. (2014). Deciphering the role of the ADAM17-dependent secretome in cell signaling. Journal of Proteome Research, 13(4), 2080-2093. https://doi.org/10.1021/pr401224u
Khan, Z., Ford, M. J., Cusanovich, D. A., Mitrano, A., Pritchard, J. K., & Gilad, Y. (2013). Primate transcript and protein expression levels evolve under compensatory selection pressures. Science (New York, N.Y.), 342(6162), 1100-1104. https://doi.org/10.1126/science.1242379
Kutlu, M. G., & Gould, T. J. (2016). Nicotinic modulation of hippocampal cell signaling and associated effects on learning and memory. Physiology & Behavior, 155, 162-171. https://doi.org/10.1016/j.physbeh.2015.12.008
Lauro, C., Di Angelantonio, S., Cipriani, R., Sobrero, F., Antonilli, L., Brusadin, V., … Limatola, C. (2008). Activity of adenosine receptors type 1 is required for CX 3 CL1-mediated neuroprotection and neuromodulation in hippocampal neurons. The Journal of Immunology, 180(11), 7590-7596. https://doi.org/10.4049/jimmunol.180.11.7590
Lee, H., Deignan, J. L., Dorrani, N., Strom, S. P., Kantarci, S., Quintero-Rivera, F., … Nelson, S. F. (2014). Clinical exome sequencing for genetic identification of rare Mendelian disorders. Jama, 312(18), 1880. https://doi.org/10.1001/jama.2014.14604
Leite, J. P., Bortolotto, Z. A., & Cavalheiro, E. A. (1990). Spontaneous recurrent seizures in rats: An experimental model of partial epilepsy. Neuroscience and Biobehavioral Reviews, 14(4), 511-517.
Li, J., Ma, Z., Shi, M., Malty, R. H., Aoki, H., Minic, Z., … Snyder, M. (2015). Identification of human neuronal protein complexes reveals biochemical activities and convergent mechanisms of action in autism Spectrum disorders. Cell Systems, 1(5), 361-374. https://doi.org/10.1016/j.cels.2015.11.002
Liao, Y., Smyth, G. K., & Shi, W. (2014). featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics (Oxford, England), 30(7), 923-930. https://doi.org/10.1093/bioinformatics/btt656
Lie, D.-C., Colamarino, S. A., Song, H.-J., Désiré, L., Mira, H., Consiglio, A., … Gage, F. H. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature, 437(7063), 1370-1375. https://doi.org/10.1038/nature04108
Lisman, J., Schulman, H., & Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Reviews. Neuroscience, 3(3), 175-190. https://doi.org/10.1038/nrn753
Liu, Y., Cui, L., Schwarz, M. K., Dong, Y., & Schlüter, O. M. (2017). Adrenergic gate release for spike timing-dependent synaptic potentiation. Neuron, 93(2), 394-408. https://doi.org/10.1016/j.neuron.2016.12.039
Liu, Y., Beyer, A., & Aebersold, R. (2016). On the dependency of cellular protein levels on mRNA abundance. Cell, 165(3), 535-550. https://doi.org/10.1016/j.cell.2016.03.014
Löscher, W., & Brandt, C. (2010). Prevention or modification of Epileptogenesis after brain insults: Experimental approaches and translational research. Pharmacological Reviews, 62(4), 668-700. https://doi.org/10.1124/pr.110.003046
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8
Maia, G. H., Soares, J. I., Almeida, S. G., Leite, J. M., Baptista, H. X., Lukoyanova, A. N., … Lukoyanov, N. V. (2019). Altered serotonin innervation in the rat epileptic brain. Brain Research Bulletin, 152, 95-106. https://doi.org/10.1016/j.brainresbull.2019.07.009
Maia, G. H., Soares, J. I., Andrade, P. A., Leite, J. F., Luz, L. L., Andrade, J. P., & Lukoyanov, N. V. (2016). Altered taste preference and loss of limbic-projecting serotonergic neurons in the dorsal raphe nucleus of chronically epileptic rats. Behavioural Brain Research, 297, 28-36. https://doi.org/10.1016/j.bbr.2015.10.010
Mazarati, A., Siddarth, P., Baldwin, R. A., Shin, D., Caplan, R., & Sankar, R. (2008). Depression after status epilepticus: Behavioural and biochemical deficits and effects of fluoxetine. Brain, 131(8), 2071-2083. https://doi.org/10.1093/brain/awn117
Onore, C., Careaga, M., & Ashwood, P. (2012). The role of immune dysfunction in the pathophysiology of autism. Brain, Behavior, and Immunity, 26(3), 383-392. https://doi.org/10.1016/j.bbi.2011.08.007
Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 17(10), 3727-3738.
Payne, H. L. (2008). The role of transmembrane AMPA receptor regulatory proteins (TARPs) in neurotransmission and receptor trafficking (review). Molecular Membrane Biology, 25(4), 353-362. https://doi.org/10.1080/09687680801986480
Payne, S. H. (2015). The utility of protein and mRNA correlation. Trends in Biochemical Sciences, 40(1), 1-3. https://doi.org/10.1016/j.tibs.2014.10.010
Pitkänen, A., Kharatishvili, I., Karhunen, H., Lukasiuk, K., Immonen, R., Nairismägi, J., … Nissinen, J. (2007). Epileptogenesis in experimental models. Epilepsia, 48(s2), 13-20. https://doi.org/10.1111/j.1528-1167.2007.01063.x
Pitkänen, A., Löscher, W., Vezzani, A., Becker, A. J., Simonato, M., Lukasiuk, K., … Beck, H. (2016). Advances in the development of biomarkers for epilepsy. The Lancet Neurology, 15(8), 843-856. https://doi.org/10.1016/S1474-4422(16)00112-5
Price, N. D., Magis, A. T., Earls, J. C., Glusman, G., Levy, R., Lausted, C., … Hood, L. (2017). A wellness study of 108 individuals using personal, dense, dynamic data clouds. Nature Biotechnology, 35(8), 747-756. https://doi.org/10.1038/nbt.3870
Pun, R. Y. K., Rolle, I. J., Lasarge, C. L., Hosford, B. E., Rosen, J. M., Uhl, J. D., … Danzer, S. C. (2012). Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron, 75(6), 1022-1034. https://doi.org/10.1016/j.neuron.2012.08.002
Ragozzino, D., Renzi, M., Giovannelli, A., & Eusebi, F. (2002). Stimulation of chemokine CXC receptor 4 induces synaptic depression of evoked parallel fibers inputs onto Purkinje neurons in mouse cerebellum. Journal of Neuroimmunology, 127(1-2), 30-36.
Ravizza, T., Balosso, S., & Vezzani, A. (2011). Inflammation and prevention of epileptogenesis. Neuroscience Letters, 497(3), 223-230. https://doi.org/10.1016/j.neulet.2011.02.040
Ray, R., Juranek, J. K., & Rai, V. (2016). RAGE axis in neuroinflammation, neurodegeneration and its emerging role in the pathogenesis of amyotrophic lateral sclerosis. Neuroscience and Biobehavioral Reviews, 62, 48-55. https://doi.org/10.1016/j.neubiorev.2015.12.006
Rowley, S., & Patel, M. (2013). Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radical Biology and Medicine, 62, 121-131. https://doi.org/10.1016/j.freeradbiomed.2013.02.002
Ryan, C. J., Cimermančič, P., Szpiech, Z. A., Sali, A., Hernandez, R. D., & Krogan, N. J. (2013). High-resolution network biology: Connecting sequence with function. Nature Reviews Genetics, 14(12), 865-879. https://doi.org/10.1038/nrg3574
Sarnyai, Z., Sibille, E. L., Pavlides, C., Fenster, R. J., McEwen, B. S., & Toth, M. (2000). Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin1A receptors. Proceedings of the National Academy of Sciences, 97(26), 14731-14736. https://doi.org/10.1073/pnas.97.26.14731
Scharfman, H. E. (2002). Epilepsy as an example of neural plasticity. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry, 8(2), 154-173. https://doi.org/10.1177/107385840200800211
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., … Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature, 473(7347), 337-342. https://doi.org/10.1038/nature10098
Shah, K., & Lahiri, D. K. (2017). A tale of the good and bad: Remodeling of the microtubule network in the brain by Cdk5. Molecular Neurobiology, 54(3), 2255-2268. https://doi.org/10.1007/s12035-016-9792-7
Shapiro, M. S., Roche, J. P., Kaftan, E. J., Cruzblanca, H., Mackie, K., & Hille, B. (2000). Reconstitution of muscarinic modulation of the KCNQ2/KCNQ3 K(+) channels that underlie the neuronal M current. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 20(5), 1710-1721.
Storey, N. M., Gómez-Angelats, M., Bortner, C. D., Armstrong, D. L., & Cidlowski, J. A. (2003). Stimulation of Kv1.3 potassium channels by death receptors during apoptosis in Jurkat T lymphocytes. Journal of Biological Chemistry, 278(35), 33319-33326. https://doi.org/10.1074/jbc.M300443200
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nature Reviews. Neuroscience, 15(10), 655-669. https://doi.org/10.1038/nrn3785
Szabo, I., Bock, J., Grassme, H., Soddemann, M., Wilker, B., Lang, F., … Gulbins, E. (2008). Mitochondrial potassium channel Kv1.3 mediates Bax-induced apoptosis in lymphocytes. Proceedings of the National Academy of Sciences, 105(39), 14861-14866. https://doi.org/10.1073/pnas.0804236105
Tomasello, D. L., Hurley, E., Wrabetz, L., & Bhattacharjee, A. (2017). Slick (Kcnt2) sodium-activated potassium channels limit Peptidergic nociceptor excitability and hyperalgesia. Journal of Experimental Neuroscience, 11, 117906951772699. https://doi.org/10.1177/1179069517726996
Vieira, A. S., de Matos, A. H., do Canto, A. M., Rocha, C. S., Carvalho, B. S., Pascoal, V. D. B., … Lopes-Cendes, I. (2016). RNA sequencing reveals region-specific molecular mechanisms associated with epileptogenesis in a model of classical hippocampal sclerosis. Scientific Reports, 6, 22416. https://doi.org/10.1038/srep22416
Vigil, F. A., Mizuno, K., Lucchesi, W., Valls-Comamala, V., & Giese, K. P. (2017). Prevention of long-term memory loss after retrieval by an endogenous CaMKII inhibitor. Scientific Reports, 7(1), 4040. https://doi.org/10.1038/s41598-017-04355-8
Wu, L., Candille, S. I., Choi, Y., Xie, D., Jiang, L., Li-Pook-Than, J., … Snyder, M. (2013). Variation and genetic control of protein abundance in humans. Nature, 499(7456), 79-82. https://doi.org/10.1038/nature12223
Zhang, Y., Sloan, S. A., Clarke, L. E., Caneda, C., Plaza, C. A., Blumenthal, P. D., … Barres, B. A. (2016). Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron, 89(1), 37-53. https://doi.org/10.1016/j.neuron.2015.11.013
Zhao, H., Lin, Y., Chen, S., Li, X., & Huo, H. (2017). 5-HT3 receptors: A potential therapeutic target for epilepsy. Current Neuropharmacology, 16(1), 29-36. https://doi.org/10.2174/1570159X15666170508170412
Zhou, Y., Zhou, B., Pache, L., Chang, M., Khodabakhshi, A. H., Tanaseichuk, O., … Chanda, S. K. (2019). Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nature Communications, 10(1), 1523. https://doi.org/10.1038/s41467-019-09234-6