Ginsenoside Re protects against kainate-induced neurotoxicity in mice by attenuating mitochondrial dysfunction through activation of the signal transducers and activators of transcription 3 signaling

References

• Liu L, Cao Q, Gao W, et al. Melatonin protects against focal cerebral ischemia-reperfusion injury in diabetic mice by ameliorating mitochondrial impairments: involvement of the Akt-SIRT3-SOD2 signaling pathway. Aging. 2021;13(12):16105–16123. doi: 10.18632/aging.203137.
   PubMedGoogle Scholar
• Kunz WS, Kudin AP, Vielhaber S, et al. Mitochondrial complex I deficiency in the epileptic focus of patients with temporal lobe epilepsy. Ann Neurol. 2000;48(5):766–773. doi: 10.1002/1531-8249(200011)48:5<766::AID-ANA10>3.0.CO;2-M.
   PubMed Web of Science ®Google Scholar
• Shin EJ, Jeong JH, Chung YH, et al. Role of oxidative stress in epileptic seizures. Neurochem Int. 2011;59(2):122–137. doi: 10.1016/j.neuint.2011.03.025.
   PubMed Web of Science ®Google Scholar
• Waldbaum S, Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res. 2010;88(1):23–45. doi: 10.1016/j.eplepsyres.2009.09.020.
   PubMed Web of Science ®Google Scholar
• Sperk G. Kainic acid seizures in the rat. Prog Neurobiol. 1994;42(1):1–32. doi: 10.1016/0301-0082(94)90019-1.
   PubMed Web of Science ®Google Scholar
• Melov S, Coskun P, Patel M, et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci U S A. 1999;96(3):846–851. doi: 10.1073/pnas.96.3.846.
   PubMed Web of Science ®Google Scholar
• Shin E-J, Jeong JH, Bing G, et al. Kainate-induced mitochondrial oxidative stress contributes to hippocampal degeneration in senescence-accelerated mice. Cell Signal. 2008;20(4):645–658. doi: 10.1016/j.cellsig.2007.11.014.
   PubMed Web of Science ®Google Scholar
• Shin E-J, Jeong JH, Kim AY, et al. Protection against kainate neurotoxicity by ginsenosides: attenuation of convulsive behavior, mitochondrial dysfunction, and oxidative stress. J Neurosci Res. 2009;87(3):710–722. doi: 10.1002/jnr.21880.
   PubMed Web of Science ®Google Scholar
• Sultana B, Panzini M-A, Veilleux Carpentier A, et al. Incidence and prevalence of drug-resistant epilepsy: a systematic review and meta-analysis. Neurology. 2021;96(17):805–817. doi: 10.1212/WNL.0000000000011839.
   PubMed Web of Science ®Google Scholar
• Prakash S, Rathore C, Rana K, et al. Antiepileptic drugs and serotonin syndrome- A systematic review of case series and case reports. Seizure. 2021;91:117–131. doi: 10.1016/j.seizure.2021.06.004.
   PubMed Web of Science ®Google Scholar
• Zaccara G, Franciotta D, Perucca E. Idiosyncratic adverse reactions to antiepileptic drugs. Epilepsia. 2007;48(7):1223–1244. doi: 10.1111/j.1528-1167.2007.01041.x.
   PubMed Web of Science ®Google Scholar
• Tu T-HT, Sharma N, Shin E-J, et al. Ginsenoside re protects trimethyltin-induced neurotoxicity via activation of IL-6-mediated phosphoinositol 3-kinase/akt signaling in mice. Neurochem Res. 2017;42(11):3125–3139. doi: 10.1007/s11064-017-2349-y.
   PubMed Web of Science ®Google Scholar
• Tran H-YP, Shin E-J, Saito K, et al. Protective potential of IL-6 against trimethyltin-induced neurotoxicity in vivo. Free Radic Biol Med. 2012;52(7):1159–1174. doi: 10.1016/j.freeradbiomed.2011.12.008.
   PubMed Web of Science ®Google Scholar
• Shin E-J, Shin SW, Nguyen T-TL, et al. Ginsenoside re rescues methamphetamine-induced oxidative damage, mitochondrial dysfunction, microglial activation, and dopaminergic degeneration by inhibiting the protein kinase Cδ gene. Mol Neurobiol. 2014;49(3):1400–1421. doi: 10.1007/s12035-013-8617-1.
   PubMed Web of Science ®Google Scholar
• Tran NKC, Jeong JH, Sharma N, et al. Ginsenoside re blocks Bay k-8644-induced neurotoxicity via attenuating mitochondrial dysfunction and PKCδ activation in the hippocampus of mice: involvement of antioxidant potential. Food Chem Toxicol. 2023;178:113869. doi: 10.1016/j.fct.2023.113869.
   PubMed Web of Science ®Google Scholar
• Hernández-Echeagaray E, González N, Ruelas A, et al. Low doses of 3-nitropropionic acid in vivo induce damage in mouse skeletal muscle. Neurol Sci. 2011;32(2):241–254. doi: 10.1007/s10072-010-0394-2.
   PubMed Web of Science ®Google Scholar
• Lemoine S, Pillot B, Augeul L, et al. Dose and timing of injections for effective cyclosporine a pretreatment before renal ischemia reperfusion in mice. PLoS One. 2017;12(8):e0182358. doi: 10.1371/journal.pone.0182358.
   PubMed Web of Science ®Google Scholar
• Mai HN, Nguyen LTT, Shin E-J, et al. Astrocytic mobilization of glutathione peroxidase-1 contributes to the protective potential against cocaine kindling behaviors in mice via activation of JAK2/STAT3 signaling. Free Radic Biol Med. 2019;131:408–431. doi: 10.1016/j.freeradbiomed.2018.12.027.
   PubMed Web of Science ®Google Scholar
• Schauwecker PE, Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc Natl Acad Sci U S A. 1997;94(8):4103–4108. doi: 10.1073/pnas.94.8.4103.
   PubMed Web of Science ®Google Scholar
• Shin E-J, Jeong JH, Nguyen B-T, et al. Ginsenoside re protects against serotonergic behaviors evoked by 2,5-dimethoxy-4-iodo-amphetamine in mice via inhibition of PKCδ-mediated mitochondrial dysfunction. Int J Mol Sci. 2021;22(13):7219. doi: 10.3390/ijms22137219.
   PubMed Web of Science ®Google Scholar
• Tran H-Q, Park SJ, Shin E-J, et al. Clozapine attenuates mitochondrial burdens and abnormal behaviors elicited by phencyclidine in mice via inhibition of p47 phox; possible involvements of phosphoinositide 3-kinase/akt signaling. J Psychopharmacol. 2018;32(11):1233–1251. doi: 10.1177/0269881118795244.
   PubMed Web of Science ®Google Scholar
• Lebel CP, Bondy SC. Sensitive and rapid quantitation of oxygen reactive species formation in rat synaptosomes. Neurochem Int. 1990;17(3):435–440. doi: 10.1016/0197-0186(90)90025-o.
   PubMed Web of Science ®Google Scholar
• Oliver CN, Ahn BW, Moerman EJ, et al. Age-related changes in oxidized proteins. J Biol Chem. 1987;262(12):5488–5491. doi: 10.1016/S0021-9258(18)45598-6.
   PubMed Web of Science ®Google Scholar
• Xiong Y, Gu Q, Peterson PL, et al. Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J Neurotrauma. 1997;14(1):23–34. doi: 10.1089/neu.1997.14.23.
   PubMed Web of Science ®Google Scholar
• Kurobe N, Suzuki F, Kato K, et al. Sensitive immunoassay of rat Cu/Zn superoxide dismutase consentrations in the brain, liver, and kidney are not affected by aging. Biomed. Res. 1990;11(3):187–194. doi: 10.2220/biomedres.11.187.
   Web of Science ®Google Scholar
• Hwang Y, Kim H-C, Shin E-J. Repeated exposure to microcystin-leucine-arginine potentiates excitotoxicity induced by a low dose of kainate. Toxicology. 2021;460:152887. doi: 10.1016/j.tox.2021.152887.
   PubMed Web of Science ®Google Scholar
• Hwang Y, Kim H-C, Shin E-J. Effect of rottlerin on astrocyte phenotype polarization after trimethyltin insult in the dentate gyrus of mice. J Neuroinflammation. 2022;19(1):142. doi: 10.1186/s12974-022-02507-w.
   PubMed Web of Science ®Google Scholar
• Hwang Y, Kim H-C, Shin E-J. Enhanced neurogenesis is involved in neuroprotection provided by rottlerin against trimethyltin-induced delayed apoptotic neuronal damage. Life Sci. 2020;262:118494. doi: 10.1016/j.lfs.2020.118494.
   PubMed Web of Science ®Google Scholar
• Finsterer J, Zarrouk Mahjoub S. Mitochondrial toxicity of antiepileptic drugs and their tolerability in mitochondrial disorders. Expert Opin Drug Metab Toxicol. 2012;8(1):71–79. doi: 10.1517/17425255.2012.644535.
   PubMed Web of Science ®Google Scholar
• Gao J, Chi Z-F, Liu X-W, et al. Mitochondrial dysfunction and ultrastructural damage in the hippocampus of pilocarpine-induced epileptic rat. Neurosci Lett. 2007;411(2):152–157. doi: 10.1016/j.neulet.2006.10.022.
   PubMed Web of Science ®Google Scholar
• Rowley S, Patel M. Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radic Biol Med. 2013;62:121–131. doi: 10.1016/j.freeradbiomed.2013.02.002.
   PubMed Web of Science ®Google Scholar
• Hu Q-P, Yan H-X, Peng F, et al. Genistein protects epilepsy-induced brain injury through regulating the JAK2/STAT3 and Keap1/Nrf2 signaling pathways in the developing rats. Eur J Pharmacol. 2021;912:174620. doi: 10.1016/j.ejphar.2021.174620.
   PubMed Web of Science ®Google Scholar
• Kim BK, Tran H-YP, Shin E-J, et al. IL-6 attenuates trimethyltin-induced cognitive dysfunction via activation of JAK2/STAT3, M1 mAChR and ERK signaling network. Cell Signal. 2013;25(6):1348–1360. doi: 10.1016/j.cellsig.2013.02.017.
   PubMed Web of Science ®Google Scholar
• Sayed RH, Ghazy AH, Yammany MFE. Recombinant human erythropoietin and interferon-β-1b protect against 3-nitropropionic acid-induced neurotoxicity in rats: possible role of JAK/STAT signaling pathway. Inflammopharmacology. 2022;30(2):667–681. doi: 10.1007/s10787-022-00935-x.
   PubMed Web of Science ®Google Scholar
• Jung JE, Kim GS, Chan PH. Neuroprotection by interleukin-6 is mediated by signal transducer and activator of transcription 3 and antioxidative signaling in ischemic stroke. Stroke. 2011;42(12):3574–3579. doi: 10.1161/STROKEAHA.111.626648.
   PubMed Web of Science ®Google Scholar
• Mai HN, Sharma N, Jeong JH, et al. P53 knockout mice are protected from cocaine-induced kindling behaviors via inhibiting mitochondrial oxidative burdens, mitochondrial dysfunction, and proapoptotic changes. Neurochem Int. 2019;124:68–81. doi: 10.1016/j.neuint.2018.12.017.
   PubMed Web of Science ®Google Scholar
• Kim HC, Jhoo WK, Kim WK, et al. An immunocytochemical study of mitochondrial manganese-superoxide dismutase in the rat hippocampus after kainate administration. Neurosci Lett. 2000;281(1):65–68. doi: 10.1016/s0304-3940(99)00969-6.
   PubMed Web of Science ®Google Scholar
• Jung JE, Kim GS, Narasimhan P, et al. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci. 2009;29(21):7003–7014. doi: 10.1523/JNEUROSCI.1110-09.2009.
   PubMed Web of Science ®Google Scholar
• Mai HN, Chung YH, Shin E-J, et al. IL-6 knockout mice are protected from cocaine-induced kindling behaviors; possible involvement of JAK2/STAT3 and PACAP signalings. Food Chem Toxicol. 2018;116(Pt B):249–263. doi: 10.1016/j.fct.2018.04.031.
   PubMedGoogle Scholar
• Castillo PE, Malenka RC, Nicoll RA. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature. 1997;388(6638):182–186. doi: 10.1038/40645.
   PubMed Web of Science ®Google Scholar
• Ruiz A. Kainate receptors with a metabotropic signature enhance hippocampal excitability by regulating the slow after-hyperpolarization in CA3 pyramidal neurons. Adv Exp Med Biol. 2011;717:59–68. doi: 10.1007/978-1-4419-9557-5_6.
   PubMed Web of Science ®Google Scholar
• Shin E-J, Ko KH, Kim W-K, et al. Role of glutathione peroxidase in the ontogeny of hippocampal oxidative stress and kainate seizure sensitivity in the genetically epilepsy-prone rats. Neurochem Int. 2008;52(6):1134–1147. doi: 10.1016/j.neuint.2007.12.003.
   PubMed Web of Science ®Google Scholar
• Shin EJ, Jeong JH, Chung CK, et al. Ceruloplasmin is an endogenous protectant against kainate neurotoxicity. Free Radic Biol Med. 2015;84:355–372. doi: 10.1016/j.freeradbiomed.2015.03.031.
   PubMed Web of Science ®Google Scholar
• Angelova PR, Vinogradova D, Neganova ME, et al. Pharmacological sequestration of mitochondrial calcium uptake protects neurons against glutamate excitotoxicity. Mol Neurobiol. 2019; 56(3):2244–2255. doi: 10.1007/s12035-018-1204-8.
   PubMed Web of Science ®Google Scholar
• Calvo-Rodriguez M, Bacskai BJ. Mitochondria and calcium in alzheimer’s disease: from cell signaling to neuronal cell death. Trends Neurosci. 2021; 44(2):136–151. doi: 10.1016/j.tins.2020.10.004.
   PubMed Web of Science ®Google Scholar
• Nam Y, Wie MB, Shin E-J, et al. Ginsenoside re protects methamphetamine-induced mitochondrial burdens and proapoptosis via genetic inhibition of protein kinase C δ in human neuroblastoma dopaminergic SH-SY5Y cell lines. J Appl Toxicol. 2015;35(8):927–944. doi: 10.1002/jat.3093.
   PubMed Web of Science ®Google Scholar
• Akaneya Y, Takahashi M, Hatanaka H. Interleukin-1 beta enhances survival and interleukin-6 protects against MPP + neurotoxicity in cultures of fetal rat dopaminergic neurons. Exp Neurol. 1995;136(1):44–52. doi: 10.1006/exnr.1995.1082.
   PubMed Web of Science ®Google Scholar
• Hama T, Kushima Y, Miyamoto M, et al. Interleukin-6 improves the survival of mesencephalic catecholaminergic and septal cholinergic neurons from postnatal, two-week-old rats in cultures. Neuroscience. 1991;40(2):445–452. doi: 10.1016/0306-4522(91)90132-8.
   PubMed Web of Science ®Google Scholar
• Yamada M, Hatanaka H. Interleukin-6 protects cultured rat hippocampal neurons against glutamate-induced cell death. Brain Res. 1994;643(1-2):173–180. doi: 10.1016/0006-8993(94)90023-x.
   PubMed Web of Science ®Google Scholar
• Tu TT, Sharma N, Shin EJ, et al. Treatment with mountain-cultivated ginseng alleviates trimethyltin-induced cognitive impairments in mice via IL-6-dependent JAK2/STAT3/ERK signaling. Planta Med. 2017; 83(17):1342–1350. doi: 10.1055/s-0043-111896.
   PubMed Web of Science ®Google Scholar
• Chang Q, Bournazou E, Sansone P, et al. The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis. Neoplasia. 2013;15(7):848–862. doi: 10.1593/neo.13706.
   PubMed Web of Science ®Google Scholar
• Huang W-L, Yeh H-H, Lin C-C, et al. Signal transducer and activator of transcription 3 activation up-regulates interleukin-6 autocrine production: a biochemical and genetic study of established cancer cell lines and clinical isolated human cancer cells. Mol Cancer. 2010;9(1):309. doi: 10.1186/1476-4598-9-309.
   PubMedGoogle Scholar
• Yoon S, Woo SU, Kang JH, et al. STAT3 transcriptional factor activated by reactive oxygen species induces IL6 in starvation-induced autophagy of cancer cells. Autophagy. 2010;6(8):1125–1138. doi: 10.4161/auto.6.8.13547.
   PubMed Web of Science ®Google Scholar
• Guo Z, Jiang H, Xu X, et al. Leptin-mediated cell survival signaling in hippocampal neurons mediated by JAK STAT3 and mitochondrial stabilization. J Biol Chem. 2008;283(3):1754–1763. doi: 10.1074/jbc.M703753200.
   PubMed Web of Science ®Google Scholar
• Pinteaux E, Copin JC, Ledig M, et al. Modulation of oxygen-radical-scavenging enzymes by oxidative stress in primary cultures of rat astroglial cells. Dev Neurosci. 1996;18(5-6):397–404. doi: 10.1159/000111433.
   PubMed Web of Science ®Google Scholar
• Thakur N, Pandey RK, Mehrotra S. Signal transducer and activator of transcription-3 mediated neuroprotective effect of interleukin-6 on cobalt chloride mimetic hypoxic cell death in R28 cells. Mol Biol Rep. 2021;48(8):6197–6203. doi: 10.1007/s11033-021-06586-5.
   PubMed Web of Science ®Google Scholar
• Dugan LL, Bruno VM, Amagasu SM, et al. Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J Neurosci. 1995;15(6):4545–4555. doi: 10.1523/JNEUROSCI.15-06-04545.1995.
   PubMed Web of Science ®Google Scholar
• Rosenberg PA, Aizenman E. Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci Lett. 1989;103(2):162–168. doi: 10.1016/0304-3940(89)90569-7.
   PubMed Web of Science ®Google Scholar
• Xu L, Emery JF, Ouyang Y-B, et al. Astrocyte targeted overexpression of Hsp72 or SOD2 reduces neuronal vulnerability to forebrain ischemia. Glia. 2010;58(9):1042–1049. doi: 10.1002/glia.20985.
   PubMed Web of Science ®Google Scholar
• Rodríguez MJ, Martínez-Sánchez M, Bernal F, et al. Heterogeneity between hippocampal and septal astroglia as a contributing factor to differential in vivo AMPA excitotoxicity. J Neurosci Res. 2004;77(3):344–353. doi: 10.1002/jnr.20177.
   PubMed Web of Science ®Google Scholar
• Kim H, Bing G, Jhoo W, et al. Changes of hippocampal Cu/Zn-superoxide dismutase after kainate treatment in the rat. Brain Res. 2000;853(2):215–226. doi: 10.1016/s0006-8993(99)02254-4.
   PubMed Web of Science ®Google Scholar
• Penkowa M, Giralt M, Carrasco J, et al. Impaired inflammatory response and increased oxidative stress and neurodegeneration after brain injury in interleukin-6-deficient mice. Glia. 2000;32(3):271–285. doi: 10.1002/1098-1136(200012)32:3<271::AID-GLIA70>3.0.CO;2-5.
   PubMed Web of Science ®Google Scholar
• Park HJ, Kim SK, Chung J-H, et al. Protective effect of carbamazepine on kainic acid-induced neuronal cell death through activation of signal transducer and activator of transcription-3. J Mol Neurosci. 2013;49(1):172–181. doi: 10.1007/s12031-012-9854-x.
   PubMed Web of Science ®Google Scholar
• Khurgel M, Koo AC, Ivy GO. Selective ablation of astrocytes by intracerebral injections of alpha-aminoadipate. Glia. 1996;16(4):351–358. doi: 10.1002/(SICI)1098-1136(199604)16:4<351::AID-GLIA7>3.0.CO;2-2.
   PubMed Web of Science ®Google Scholar
• Galoczova M, Coates P, Vojtesek B. STAT3, stem cells, cancer stem cells and p63. Cell Mol Biol Lett. 2018;23(1):12. doi: 10.1186/s11658-018-0078-0.
   PubMedGoogle Scholar
• Mao M, Zhang T, Wang Z, et al. Glaucocalyxin A-induced oxidative stress inhibits the activation of STAT3 signaling pathway and suppresses osteosarcoma progression in vitro and in vivo. Biochim Biophys Acta Mol Basis Dis. 2019; 1865(6):1214–1225. doi: 10.1016/j.bbadis.2019.01.016.
   PubMed Web of Science ®Google Scholar
• Lee B, Shim I, Lee H, et al. Effect of ginsenoside re on depression- and anxiety-like behaviors and cognition memory deficit induced by repeated immobilization in rats. J Microbiol Biotechnol. 2012; 22(5):708–720. doi: 10.4014/jmb.1112.12046.
   PubMed Web of Science ®Google Scholar
• Wang H, Lv J, Jiang N, et al. Ginsenoside re protects against chronic restraint stress-induced cognitive deficits through regulation of NLRP3 and Nrf2 pathways in mice. Phytother Res. 2021;35(5):2523–2535. doi: 10.1002/ptr.6947.
   PubMed Web of Science ®Google Scholar
• Nguyen BT, Shin E-J, Jeong JH, et al. Ginsenoside re attenuates memory impairments in aged klotho deficient mice via interactive modulations of angiotensin II AT1 receptor, Nrf2 and GPx-1 gene. Free Radic Biol Med. 2022;189:2–19. doi: 10.1016/j.freeradbiomed.2022.07.003.
   PubMed Web of Science ®Google Scholar