Scavenger Receptor Class B Type I Modulates Epileptic Seizures and Receptor α2δ-1 Expression.
Epilepsy
NMDA receptor
SR-BI
Synapse
Α2δ-1
Journal
Neurochemical research
ISSN: 1573-6903
Titre abrégé: Neurochem Res
Pays: United States
ID NLM: 7613461
Informations de publication
Date de publication:
17 Jul 2024
17 Jul 2024
Historique:
received:
30
03
2024
accepted:
08
07
2024
revised:
30
06
2024
medline:
17
7
2024
pubmed:
17
7
2024
entrez:
17
7
2024
Statut:
aheadofprint
Résumé
Scavenger receptor class B type I (SR-BI) is abundant in adult mouse and human brains, but its function in the central nervous system (CNS) remains unclear. This study explored the role of SR-BI in epilepsy and its possible underlying mechanism. Expression patterns of SR-BI in the brains of mice with kainic acid (KA)-induced epilepsy were detected using immunofluorescence staining, quantitative real-time polymerase chain reaction (qPCR), and Western blotting(WB). Behavioral analysis was performed by 24-hour video monitoring and hippocampal local field potential (LFP) recordings were employed to verify the role of SR-BI in epileptogenesis. RNA sequencing (RNA-seq) was used to obtain biological information on SR-BI in the CNS. WB, qPCR, and co-immunoprecipitation (Co-IP) were performed to identify the relationship between SR-BI and the gabapentin receptor α2δ-1.The results showed that SR-BI was primarily co-localized with astrocytes and its expression was down-regulated in the hippocampus of KA mice. Notably, overexpressing SR-BI alleviated the epileptic behavioral phenotype in KA mice. Hippocampal transcriptomic analysis revealed 1043 differentially expressed genes (DEGs) in the SR-BI-overexpressing group. Most DEGs confirmed by RNA-seq analysis were associated with synapses, neuronal projections, neuron development, and ion binding. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis demonstrated that the DEGs were enriched in the glutamatergic synapse pathway. Furthermore, the gabapentin receptor α2δ-1 decreased with SR-BI overexpression in epileptic mice. Overall, these findings highlight the important role of SR-BI in regulating epileptogenesis and that the gabapentin receptor α2δ-1 is a potential downstream target of SR-BI.
Identifiants
pubmed: 39017956
doi: 10.1007/s11064-024-04209-6
pii: 10.1007/s11064-024-04209-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : the National Natural Science Foundations of China
ID : 82071458
Organisme : the National Natural Science Foundations of China
ID : 82071458
Organisme : the National Natural Science Foundations of China
ID : 82071458
Organisme : the National Natural Science Foundations of China
ID : 82071458
Organisme : the National Natural Science Foundations of China
ID : 82071458
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Thijs RD, Surges R, O’Brien TJ et al (2019) Epilepsy in adults. Lancet 393(10172):689–701. https://doi.org/10.1016/S0140-6736
doi: 10.1016/S0140-6736
pubmed: 30686584
Sills GJ, Rogawski MA (2020) Mechanisms of action of currently used antiseizure drugs. Neuropharmacology 168:107966. https://doi.org/10.1016/j.neuropharm.2020.107966 . PMID: 32120063
Morimoto K, Fahnestock M, Racine RJ (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73(1):1–60. https://doi.org/10.1016/j.pneurobio.2004.03.009 . PMID: 15193778
Eyo UB, Murugan M, Wu LJ (2017) Microglia-Neuron communication in Epilepsy. Glia 65(1):5–18. https://doi.org/10.1002/glia.23006 . PMID: 27189853; PMCID: PMC5116010
doi: 10.1002/glia.23006
pubmed: 27189853
Ferlazzo E, Sueri C, Gasparini S et al (2017) Methodological issues associated with clinical trials in epilepsy. Expert Rev Clin Pharmacol 10(10):1103–1108. https://doi.org/10.1080/17512433.2017.1356720 . PMID: 28715945
Husemann J, Loike JD, Anankov R et al (2002) Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system. Glia 40(2):195–205. https://doi.org/10.1002/glia.10148 . PMID: 12379907
Srivastava RA (2003) Scavenger receptor class B type I expression in murine brain and regulation by estrogen and dietary cholesterol. J Neurol Sci 210(1–2):11–18. https://doi.org/10.1016/s0022-510x(03)00006-6 . PMID: 12736081
doi: 10.1016/s0022-510x
pubmed: 12736081
Prior R, Wihl G, Urmoneit B, Apolipoprotein E (2000) smooth muscle cells and the pathogenesis of cerebral amyloid angiopathy: the potential role of impaired cerebrovascular A beta clearance. Ann N Y Acad Sci 903:180-6. https://doi.org/10.1111/j.1749-6632.2000.tb06367.x . PMID: 10818506
Ohgami N 1, Nagai R, Miyazaki A et al (2001) Scavenger receptor class B type I-mediated reverse cholesterol transport is inhibited by advanced glycation end products. J Biol Chem 276(16):13348–13355. https://doi.org/10.1074/jbc.M011613200 . Epub 2001 Jan 17. PMID: 11278947
Tran-Dinh A, Levoye A, Couret D et al (2020) High-Density Lipoprotein Therapy in Stroke: Evaluation of Endothelial SR-BI-Dependent Neuroprotective Effects. Int J Mol Sci 22(1):106. https://doi.org/10.3390/ijms22010106 . PMID: 33374266
Chang EH, Rigotti A, Huerta PT (2009) Age-related influence of the HDL receptor SR-BI on synaptic plasticity and cognition. Neurobiol Aging 30(3): 407 – 19. https://doi.org/10.1016/j.neurobiolaging.2007.07.006 . Epub 2007 Aug 23. PMID: 17719144
Koudinov AR, Koudinova NV (2001) Essential role for cholesterol in synaptic plasticity and neuronal degeneration. Faseb J 15(10):1858-60. https://doi.org/10.1096/fj.00-0815fje . PMID: 11481254
Rusina E, Bernard C, Williamson A (2021) The Kainic Acid Models of Temporal Lobe Epilepsy. eNeuro 8(2):ENEURO.0337-20.2021. https://doi.org/10.1523/ENEURO.0337-20.2021 . PMID: 33658312
Lévesque M, Avoli M (2013) The kainic acid model of temporal lobe epilepsy. Neurosci Biobehav Rev 37(10 Pt 2):2887-99. https://doi.org/10.1016/j.neubiorev.2013.10.011 . PMID: 24184743
Nagisa Sada S, Lee T, Katsu et al (2015) Epilepsy treatment. Targeting LDH enzymes with a stiripentol analog to treat epilepsy. Science 347(6228):1362-7. https://doi.org/10.1126/science.aaa1299 . PMID: 25792327
Yang Y, Tian X, Xu D et al (2018) GPR40 modulates epileptic seizure and NMDA receptor function. Sci Adv 4(10):eaau2357. https://doi.org/10.1126/sciadv.aau2357 . PMID: 30345361
Gardoni F, Stanic J, Scheggia D et al (2021) NMDA and AMPA Receptor Autoantibodies in Brain Disorders: From Molecular Mechanisms to Clinical Features. Cells 10(1):77. https://doi.org/10.3390/cells10010077 . PMID: 33466431
Gardoni F, Di Luca M (2006) New targets for pharmacological intervention in the glutamatergic synapse. Eur J Pharmacol 545(1):2–10. https://doi.org/10.1016/j.ejphar.2006.06.022 . PMID: 16831414
Lee JH, Kim JY, Noh S et al (2021) Astrocytes phagocytose adult hippocampal synapses for circuit homeostasis. Nature 590(7847):612–617. https://doi.org/10.1038/s41586-020-03060-3 . PMID: 33361813
doi: 10.1038/s41586-020-03060-3PMID
pubmed: 33361813
Zhu Y, Huang D, Zhao Z et al (2021) Bioinformatic analysis identifies potential key genes of epilepsy. PLoS One 16(9):e0254326. https://doi.org/10.1371/journal.pone.0254326 . PMID: 34555062
Wolinski P, Ksiazek-Winiarek D, Glabinski A (2022) Cytokines and Neurodegeneration in Epileptogenesis. Brain Sci 12(3):380. https://doi.org/10.3390/brainsci12030380 . PMID: 35326336
Han T et al (2021) Analysis and Construction of a Molecular Diagnosis Model of Drug-Resistant Epilepsy Based on Bioinformatics. Front Mol Biosci 8:683032. https://doi.org/10.3389/fmolb.2021.683032 . PMID: 34805265
Runtz L, Girard B, Toussenot M et al (2018) Hepatic and hippocampal cytochrome P450 enzyme overexpression during spontaneous recurrent seizures. Epilepsia 59(1):123–134. https://doi.org/10.1111/epi.13942 . PMID: 29125184
Kondratiuk I, Plucinska G, Miszczuk D et al (2015) Epileptogenesis following Kainic Acid-Induced Status Epilepticus in Cyclin D2 Knock-Out Mice with Diminished Adult Neurogenesis. PLoS One 10(5):e0128285. https://doi.org/10.1371/journal.pone.0128285 . PMID: 26020770
Fu Y, Liu D, Guo J et al (2020) Dynamic Change of Shanks Gene mRNA Expression and DNA Methylation in Epileptic Rat Model and Human Patients. Mol Neurobiol 57(9):3712–3726. https://doi.org/10.1007/s12035-020-01968-5 . PMID: 32564287
Monteiro P, Feng G (2017) SHANK proteins: roles at the synapse and in autism spectrum disorder. Nat Rev Neurosci 18(3):147–157. https://doi.org/10.1038/nrn.2016.183 . PMID: 28179641
Celli R, Santolini I, Guiducci M et al (2017) The α2δ Subunit and Absence Epilepsy: Beyond Calcium Channels? Curr Neuropharmacol 15(6):918–925. https://doi.org/10.2174/1570159X15666170309105451 . PMID: 28290248
Schöpf CL, Ablinger C, Geisler SM et al (2021) Presynaptic α2δ subunits are key organizers of glutamatergic synapses. Proc Natl Acad Sci U S A 118(14):e1920827118. https://doi.org/10.1073/pnas.1920827118 . PMID: 33782113
Van Hoeymissen E, Held K, Nogueira Freitas AC et al (2020) Gain of channel function and modified gating properties in TRPM3 mutants causing intellectual disability and epilepsy. Elife 9:e57190. https://doi.org/10.7554/eLife.57190 . PMID: 32427099
Holter J, Carter D, Leresche N et al (2005) A TASK3 channel (KCNK9) mutation in a genetic model of absence epilepsy. J Mol Neurosci 25(1):37–51. https://doi.org/10.1385/JMN:25:1:037 . PMID: 15781965
doi: 10.1385/JMN:25:1:037
pubmed: 15781965
Kim JE, Lee DS, Kang TC (2022) Sp1-Mediated Prdx6 Upregulation Leads to Clasmatodendrosis by Increasing Its aiPLA2 Activity in the CA1 Astrocytes in Chronic Epilepsy Rats. Antioxidants (Basel) 11(10):1883. https://doi.org/10.3390/antiox11101883 . PMID: 36290607
Wang XD, Liu S, Lu H et al (2021) Analysis of Shared Genetic Regulatory Networks for Alzheimer’s Disease and Epilepsy. Biomed Res Int 2021:6692974. https://doi.org/10.1155/2021/6692974 . PMID: 34697589
Tang S, Terzic B, Wang IJ et al (2019) Altered NMDAR signaling underlies autistic-like features in mouse models of CDKL5 deficiency disorder. Nat Commun 10(1):2655. https://doi.org/10.1038/s41467-019-10689-w . PMID: 31201320
Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823 – 47. https://doi.org/10.1146/annurev.biochem.76.060805.160029 . PMID: 17243894
Beamer E, Kuchukulla M, Boison D et al (2021) ATP and adenosine-two players in the control of seizures and epilepsy development. Prog Neurobiol 204:102105. https://doi.org/10.1016/j.pneurobio.2021.102105 . Epub 2021 Jun 16. PMID: 34144123
doi: 10.1016/j.pneurobio.2021.102105
pubmed: 34144123
pmcid: 10237002
Riquelme J, Wellmann M, Sotomayor-Zárate R et al (2020) Gliotransmission: a Novel Target for the development of antiseizure drugs. Neuroscientist 26(4):293–309. https://doi.org/10.1177/1073858420901474 . Epub 2020 Jan 24. PMID: 31976817
doi: 10.1177/1073858420901474
pubmed: 31976817
Vezzani A, Balosso S, Ravizza T (2019) Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy. Nat Rev Neurol 15(8):459–472. https://doi.org/10.1038/s41582-019-0217-x . PMID: 31263255
Purnell BS, Alves M, Boison D (2023) Astrocyte-neuron circuits in epilepsy. Neurobiol Dis 179:106058. https://doi.org/10.1016/j.nbd.2023.106058 . PMID: 36868484
Andrade A, Brennecke A, Mallat S et al (2019) Genetic Associations between Voltage-Gated Calcium Channels and Psychiatric Disorders. Int J Mol Sci 20(14):3537. https://doi.org/10.3390/ijms20143537 . PMID: 31331039
Bourinet E, Francois A, Laffray S (2016) T-type calcium channels in neuropathic pain. Pain 157(Suppl 1):S15-S22. https://doi.org/10.1097/j.pain.0000000000000469 . PMID: 26785151
Heyes S, Pratt WS, Rees E et al (2015) Genetic disruption of voltage-gated calcium channels in psychiatric and neurological disorders. Prog Neurobiol 134:36–54. https://doi.org/10.1016/j.pneurobio.2015.09.002 . PMID: 26386135
Pietrobon D (2013) Calcium channels and migraine. Biochim Biophys Acta 1828(7):1655-65. https://doi.org/10.1016/j.bbamem.2012.11.012 . PMID: 23165010
Rajakulendran S, Hanna MG (2016) The Role of Calcium Channels in Epilepsy. Cold Spring Harb Perspect Med 6(1):a022723. https://doi.org/10.1101/cshperspect.a022723 . PMID: 26729757
Striessnig J (2016) Voltage-gated calcium channels - from basic mechanisms to disease. J Physiol 594(20):5817–5821. https://doi.org/10.1113/JP272619 . PMID: 27739079
Surmeier DJ (2007) Calcium, ageing, and neuronal vulnerability in Parkinson’s disease. Lancet Neurol 6(10):933-8. https://doi.org/10.1016/S1474-4422(07)70246-6 . PMID: 17884683
Zamponi GW (2016) Targeting voltage-gated calcium channels in neurological and psychiatric diseases. Nat Rev Drug Discov 15(1):19–34. https://doi.org/10.1038/nrd.2015.5 . PMID: 26542451
Rebecca L, Cole 1 SM, Lechner, Mark E, Williams (2005) Differential distribution of voltage-gated calcium channel alpha-2 delta (alpha2delta) subunit mRNA-containing cells in the rat central nervous system and the dorsal root ganglia. J Comp Neurol 491(3):246 – 69. https://doi.org/10.1002/cne.20693 . PMID: 16134135
Gee NS, Brown JP, Dissanayake VU et al (1996) The novel anticonvulsant drug, gabapentin (Neurontin), binds to the alpha2delta subunit of a calcium channel. J Biol Chem 271(10):5768-76. https://doi.org/10.1074/jbc.271.10.5768 . PMID: 8621444
Kurshan PT, Oztan A, Schwarz TL (2009) Presynaptic alpha2delta-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat Neurosci 12(11):1415-23. https://doi.org/10.1038/nn.2417 . PMID: 19820706
Eroglu C, Allen NJ, Susman MW et al (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139(2):380 – 92. https://doi.org/10.1016/j.cell.2009.09.025 . PMID: 19818485
Risher WC, Kim N, Koh S et al (2018) Thrombospondin receptor α2δ-1 promotes synaptogenesis and spinogenesis via postsynaptic Rac1. J Cell Biol 217(10):3747–3765. https://doi.org/10.1083/jcb.201802057 . PMID: 30054448
Faria LC, Gu F, Parada I et al (2017) Epileptiform activity and behavioral arrests in mice overexpressing the calcium channel subunit α2δ-1. Neurobiol Dis 102:70–80. https://doi.org/10.1016/j.nbd.2017.01.009 . PMID: 28193459
Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11(10):682 – 96. https://doi.org/10.1038/nrn2911 . PMID: 20842175
Paoletti P, Bellone C, Zhou Q (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14(6):383–400. https://doi.org/10.1038/nrn3504 . PMID: 23686171
Alim I, Teves L, Li R et al (2013) Modulation of NMDAR subunit expression by TRPM2 channels regulates neuronal vulnerability to ischemic cell death. J Neurosci 33(44):17264–17277. https://doi.org/10.1523/JNEUROSCI.1729-13.2013
doi: 10.1523/JNEUROSCI.1729-13.2013
pubmed: 24174660
pmcid: 6618359
Zhang H, Tian X, Lu X et al (2019) TMEM25 modulates neuronal excitability and NMDA receptor subunit NR2B degradation. J Clin Invest 129(9):3864–3876. https://doi.org/10.1172/JCI122599 . PMID: 31424425
Parsons MP, Raymond LA (2014) Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82(2):279 – 93. https://doi.org/10.1016/j.neuron.2014.03.030 . PMID: 24742457