Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Systematic Review Article

Anti-seizure Effects and Mechanisms of Berberine: A Systematic Review

Author(s): Nahid Jivad, Saeid Heidari-Soureshjani*, Hesamaldin Bagheri, Catherine M.T. Sherwin and Sahar Rostamian

Volume 25, Issue 17, 2024

Published on: 21 February, 2024

Page: [2253 - 2265] Pages: 13

DOI: 10.2174/0113892010283237240107121749

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Epilepsy is one of the most common in all age groups and disabling neurologic disorders around the world.

Objectives: This systematic review was to explore whether berberine (BBR) has any anti-seizure or anti-epileptic effects and also reviewed this possible mechanism.

Methods: The EMBASE, Scopus, Cochrane Library, PubMed, and Web of Science databases were searched before Sep 2023. All types of studies that investigated the effects of BBR on epilepsy or chemical-induced seizures were eligible for inclusion. Two authors independently evaluated and reviewed titles/abstracts to identify publications for potential eligibility, and a third team member resolved discrepancies. Data were extracted in an Excel form, and the outcomes were discussed.

Results: BBR showed its neuroprotective properties by reducing oxidative stress, neuroinflammation, and anti-apoptosis effects. It also increases brain-derived neurotrophic factor (BDNF) release and reduces transforming growth factor-beta (TGF-β1) and hypoxia-inducible factor 1α (HIF-1α). BBR by increasing scavenging reactive oxygen species (ROS), nuclear factor erythroid 2–related factor 2 (Nrf2), endogenous antioxidant enzymes, heme oxygenase-1 (HO-1), and inhibition of lipid peroxidation insert its antioxidant activity. Moreover, BBR showed antiinflammatory activity by reducing Interleukin (IL)-1β, IL-6, and tumor necrosis factor-alpha (TNF-α) levels and through inhibiting cyclooxygenase-2 (COX-2), and including nuclear factor κB (NF-κB). In addition, it modulated c-fos expression and neuronal excitability in the brain.

Conclusion: BBR indicated promising anti-seizure effects with remarkable antioxidant, antiinflammatory, anti-apoptotic, and neuroprotective activity. Future studies should be based on well-designed clinical trial studies that are integrated with new methods related to increasing bioavailability.

Keywords: Epilepsy, seizure, anticonvulsant, anti-epileptic, berberine, alkaloid.

Graphical Abstract
[1]
Beghi, E. The epidemiology of epilepsy. Neuroepidemiology, 2020, 54(2), 185-191.
[http://dx.doi.org/10.1159/000503831] [PMID: 31852003]
[2]
Stafstrom, C.E.; Carmant, L. Seizures and epilepsy: An overview for neuroscientists. Cold Spring Harb. Perspect. Med., 2015, 5(6), a022426.
[http://dx.doi.org/10.1101/cshperspect.a022426] [PMID: 26033084]
[3]
Anwar, H.; Khan, Q.U.; Nadeem, N.; Pervaiz, I.; Ali, M.; Cheema, F.F. Epileptic seizures. Discoveries, 2020, 8(2), e110.
[http://dx.doi.org/10.15190/d.2020.7] [PMID: 32577498]
[4]
Talevi, A. Antiseizure medication discovery: Recent and future paradigm shifts. Epilepsia Open, 2022, 7(S1), S133-S141.
[5]
Kalra, S.; Jiwan, T.; Singh, G.; Gautam, P.L.; Bansal, A. A comparison of the quality of life of people with epilepsy receiving home-based and clinic-based epilepsy care using the european quality of life five-dimension three-level (EQ-5D-3L) scale. Cureus, 2023, 15(2), e35045.
[http://dx.doi.org/10.7759/cureus.35045] [PMID: 36938287]
[6]
Espinosa-Garcia, C.; Zeleke, H.; Rojas, A. Impact of stress on epilepsy: Focus on neuroinflammation—a mini review. Int. J. Mol. Sci., 2021, 22(8), 4061.
[http://dx.doi.org/10.3390/ijms22084061] [PMID: 33920037]
[7]
Ai, X.; Yu, P.; Peng, L.; Luo, L.; Liu, J.; Li, S.; Lai, X.; Luan, F.; Meng, X. Berberine: A review of its pharmacokinetics properties and therapeutic potentials in diverse vascular diseases. Front. Pharmacol., 2021, 12, 762654.
[http://dx.doi.org/10.3389/fphar.2021.762654] [PMID: 35370628]
[8]
Gunasekera, C.L.; Sirven, J.I.; Feyissa, A.M. The evolution of antiseizure medication therapy selection in adults: Is artificial intelligence -assisted antiseizure medication selection ready for prime time? J. Cent. Nerv. Syst. Dis., 2023, 15, 11795735231209209.
[http://dx.doi.org/10.1177/11795735231209209] [PMID: 37868934]
[9]
Abou-Khalil, B.W. Update on antiseizure medications 2022. Continuum, 2022, 28(2), 500-535.
[http://dx.doi.org/10.1212/CON.0000000000001104] [PMID: 35393968]
[10]
Sarma, A.K.; Khandker, N.; Kurczewski, L.; Brophy, G.M. Medical management of epileptic seizures: Challenges and solutions. Neuropsychiatr. Dis. Treat., 2016, 12, 467-485.
[PMID: 26966367]
[11]
Khaledifar, A.; Khosravi Farsani, M.R.; Raeisi, E. Berberine efficacy against Doxorubicin-induced cardiotoxicity: A systematic review. J. HerbMed Pharmacol., 2023, 12(2), 187-193.
[http://dx.doi.org/10.34172/jhp.2023.19]
[12]
Amini Chermahini, F.; Raeisi, E.; Aazami, M.H.; Mirzaei, A.; Heidarian, E.; Lemoigne, Y. Does, bromelain-cisplatin combination afford in-vitro synergistic anticancer effects on human prostatic carcinoma cell line PC3? Galen Med. J., 2020, 9, e1749.
[http://dx.doi.org/10.31661/gmj.v9i0.1749] [PMID: 34466585]
[13]
Ekor, M. The growing use of herbal medicines: Issues relating to adverse reactions and challenges in monitoring safety. Front. Pharmacol., 2014, 4, 177.
[http://dx.doi.org/10.3389/fphar.2013.00177] [PMID: 24454289]
[14]
Behl, T.; Singh, S.; Sharma, N.; Zahoor, I.; Albarrati, A.; Albratty, M.; Meraya, A.M.; Najmi, A.; Bungau, S. Expatiating the pharmacological and nanotechnological aspects of the alkaloidal drug berberine: Current and future trends. Molecules, 2022, 27(12), 3705.
[http://dx.doi.org/10.3390/molecules27123705] [PMID: 35744831]
[15]
Berberine. 2004. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/Berberine
[16]
Och, A.; Podgórski, R.; Nowak, R. Biological activity of berberine—a summary update. Toxins, 2020, 12(11), 713.
[http://dx.doi.org/10.3390/toxins12110713] [PMID: 33198257]
[17]
Mohammadzadeh, N.; Mehri, S.; Hosseinzadeh, H. Berberis vulgaris and its constituent berberine as antidotes and protective agents against natural or chemical toxicities. Iran. J. Basic Med. Sci., 2017, 20(5), 538-551.
[PMID: 28656089]
[18]
Feng, X.; Sureda, A.; Jafari, S.; Memariani, Z.; Tewari, D.; Annunziata, G.; Barrea, L.; Hassan, S.T.S.; Šmejkal, K.; Malaník, M.; Sychrová, A.; Barreca, D.; Ziberna, L.; Mahomoodally, M.F.; Zengin, G.; Xu, S.; Nabavi, S.M.; Shen, A.Z. Berberine in cardiovascular and metabolic diseases: From mechanisms to therapeutics. Theranostics, 2019, 9(7), 1923-1951.
[http://dx.doi.org/10.7150/thno.30787] [PMID: 31037148]
[19]
Xia, S.; Ma, L.; Wang, G.; Yang, J.; Zhang, M.; Wang, X.; Su, J.; Xie, M. In vitro antimicrobial activity and the mechanism of berberine against methicillin-resistant staphylococcus aureus isolated from bloodstream infection patients. Infect. Drug Resist., 2022, 15, 1933-1944.
[http://dx.doi.org/10.2147/IDR.S357077] [PMID: 35469308]
[20]
Zheng, Y.M.; Zhang, J.P.; Tang, S.; Song, D.Q. [Establish and use of an epilepsy model in larval zebrafish]. Yao Xue Xue Bao, 2016, 51(4), 580-587.
[PMID: 29859527]
[21]
Wang, X.L.; Jin, G.Z.; Zhou, T.C. [On the central inhibition action of tetrahydroberberine without relevance to GABA receptors]. Sheng Li Xue Bao, 1994, 46(5), 505-508.
[PMID: 7846552]
[22]
Hosseinzadeh, H.; Ramezani, M.; Shafaei, H.; Taghiabadi, E. Anticonvulsant effect of Berberis integerrima L. root extracts in mice. J. Acupunct. Meridian Stud., 2013, 6(1), 12-17.
[http://dx.doi.org/10.1016/j.jams.2012.07.018] [PMID: 23433050]
[23]
Gawel, K.; Kukula-Koch, W.; Nieoczym, D.; Stepnik, K.; van der Ent, W.; Banono, N.S.; Tarabasz, D.; Turski, W.A.; Esguerra, C.V. The influence of palmatine isolated from berberis sibirica radix on pentylenetetrazole-induced seizures in zebrafish. Cells, 2020, 9(5), 1233.
[http://dx.doi.org/10.3390/cells9051233] [PMID: 32429356]
[24]
El-Nahas, A.E.; Elbedaiwy, H.M.; Helmy, M.W.; El-Kamel, A.H. Simultaneous estimation of berberine and piperine in a novel nanoformulation for epilepsy control via HPLC. J. Chromatogr. Sci., 2023, bmad073.
[http://dx.doi.org/10.1093/chromsci/bmad073] [PMID: 37635418]
[25]
Bhutada, P.; Mundhada, Y.; Bansod, K.; Dixit, P.; Umathe, S.; Mundhada, D. Anticonvulsant activity of berberine, an isoquinoline alkaloid in mice. Epilepsy Behav., 2010, 18(3), 207-210.
[http://dx.doi.org/10.1016/j.yebeh.2010.03.007] [PMID: 20638957]
[26]
Gao, F.; Gao, Y.; Liu, Y.; Wang, L.; Li, Y. Berberine exerts an anticonvulsant effect and ameliorates memory impairment and oxidative stress in a pilocarpine-induced epilepsy model in the rat. Neuropsychiatr. Dis. Treat., 2014, 10, 2139-2145.
[http://dx.doi.org/10.2147/NDT.S73210] [PMID: 25419137]
[27]
Mojarad, T.B.; Roghani, M. The anticonvulsant and antioxidant effects of berberine in kainate-induced temporal lobe epilepsy in rats. Basic Clin. Neurosci., 2014, 5(2), 124-130.
[PMID: 25337370]
[28]
Mathew, S.; Faheem, M.; Al-Malki, A.; Kumosani, T.A.; Qadri, I. In silico inhibition of GABARAP activity using antiepileptic medicinal derived compounds. Bioinformation, 2015, 11(4), 189-195.
[http://dx.doi.org/10.6026/97320630011189] [PMID: 26124559]
[29]
Sadeghnia, H.R.; Taji, A.R.; Forouzanfar, F.; Hosseinzadeh, H. Berberine attenuates convulsing behavior and extracellular glutamate and aspartate changes in 4-aminopyridine treated rats. Iran. J. Basic Med. Sci., 2017, 20(5), 588-593.
[PMID: 28656093]
[30]
Sedaghat, R.; Taab, Y.; Kiasalari, Z.; Afshin-Majd, S.; Baluchnejadmojarad, T.; Roghani, M. Berberine ameliorates intrahippocampal kainate-induced status epilepticus and consequent epileptogenic process in the rat: Underlying mechanisms. Biomed. Pharmacother., 2017, 87, 200-208.
[http://dx.doi.org/10.1016/j.biopha.2016.12.109] [PMID: 28061403]
[31]
Guna, V.; Saha, L.; Bhatia, A.; Banerjee, D.; Chakrabarti, A. Anti-oxidant and anti-apoptotic effects of berberine in pentylenetetrazole-induced kindling model in rat. J. Epilepsy Res., 2018, 8(2), 66-73.
[http://dx.doi.org/10.14581/jer.18011] [PMID: 30809499]
[32]
Zheng, Y.M.; Chen, B.; Jiang, J.D.; Zhang, J.P. Syntaxin 1B mediates berberine’s roles in epilepsy-like behavior in a pentylenetetrazole-induced seizure zebrafish model. Front. Mol. Neurosci., 2018, 11, 378.
[http://dx.doi.org/10.3389/fnmol.2018.00378] [PMID: 30534049]
[33]
Senthilvel, C.K.; Karuppaiyan, K.; Moideen, M.M.J. Development of capsules filled with phenytoin and berberine loaded nanoparticles- a new approach to improve anticonvulsant efficacy. IJPER, 2019, 53(3), 468-479.
[http://dx.doi.org/10.5530/ijper.53.3.79]
[34]
Zhang, B.; Wang, L.; Ji, X.; Zhang, S.; Sik, A.; Liu, K.; Jin, M. Anti-inflammation associated protective mechanism of berberine and its derivatives on attenuating pentylenetetrazole-induced seizures in zebrafish. J. Neuroimmune Pharmacol., 2020, 15(2), 309-325.
[http://dx.doi.org/10.1007/s11481-019-09902-w] [PMID: 31909440]
[35]
Ghanem, H.B.; Emam, M.N.; Ali, D.A.M.; Abd-Ellatif, R.N. Impact of berberine on some epigenetic, transcription regulation and inflammatory biomarkers in a mice model of epilepsy. Rep. Biochem. Mol. Biol., 2021, 10(3), 362-372.
[http://dx.doi.org/10.52547/rbmb.10.3.362] [PMID: 34981012]
[36]
Asadollah-salmanpour, Y.; Hassanpour, S.; Vazir, B. Effects of berberine on pentylenetetrazole-induced seizures during estrus cycle in rats. Comp. Clin. Pathol., 2023, 32(6), 919-924.
[http://dx.doi.org/10.1007/s00580-023-03502-0]
[37]
El-Nahas, A.E.; Elbedaiwy, H.M.; Masoud, I.M.; Aly, R.G.; Helmy, M.W.; El-Kamel, A.H. Berberine-loaded zein/hyaluronic acid composite nanoparticles for efficient brain uptake to alleviate neuro-degeneration in the pilocarpine model of epilepsy. Eur. J. Pharm. Biopharm., 2023, 188, 182-200.
[http://dx.doi.org/10.1016/j.ejpb.2023.04.008] [PMID: 37068561]
[38]
Saha, L.; Kumari, P.; Rawat, K.; Gautam, V.; Sandhu, A.; Singh, N.; Bhatia, A.; Bhattacharya, S.; Sinha, V.R.; Chakrabarti, A. Neuroprotective effect of berberine nanoparticles against seizures in pentylenetetrazole induced kindling model of epileptogenesis: Role of anti-oxidative, anti-inflammatory, and anti-apoptotic mechanisms. Neurochem. Res., 2023, 48(10), 3055-3072.
[http://dx.doi.org/10.1007/s11064-023-03967-z] [PMID: 37329447]
[39]
Cheng, Z.; Kang, C.; Che, S.; Su, J.; Sun, Q.; Ge, T.; Guo, Y.; Lv, J.; Sun, Z.; Yang, W.; Li, B.; Li, X.; Cui, R. Berberine: A promising treatment for neurodegenerative diseases. Front. Pharmacol., 2022, 13, 845591.
[http://dx.doi.org/10.3389/fphar.2022.845591] [PMID: 35668943]
[40]
Sharma, A. Neuroprotective agents. In: Advances in Structure and Activity Relationship of Coumarin Derivatives; Penta, S., Ed.; Academic Press: Boston, 2016; pp. 77-99.
[http://dx.doi.org/10.1016/B978-0-12-803797-3.00004-7]
[41]
Fabisiak, T.; Patel, M. Crosstalk between neuroinflammation and oxidative stress in epilepsy. Front. Cell Dev. Biol., 2022, 10, 976953.
[http://dx.doi.org/10.3389/fcell.2022.976953] [PMID: 36035987]
[42]
Sadeghnia, H.R.; Kolangikhah, M.; Asadpour, E.; Forouzanfar, F.; Hosseinzadeh, H. Berberine protects against glutamate-induced oxidative stress and apoptosis in PC12 and N2a cells. Iran. J. Basic Med. Sci., 2017, 20(5), 594-603.
[PMID: 28656094]
[43]
Falcicchia, C.; Paolone, G.; Emerich, D.F.; Lovisari, F.; Bell, W.J.; Fradet, T.; Wahlberg, L.U.; Simonato, M. Seizure-suppressant and neuroprotective effects of encapsulated BDNF-producing cells in a rat model of temporal lobe epilepsy. Mol. Ther. Methods Clin. Dev., 2018, 9, 211-224.
[http://dx.doi.org/10.1016/j.omtm.2018.03.001] [PMID: 29766029]
[44]
Gliwińska, A.; Czubilińska-Łada, J.; Więckiewicz, G.; Świętochowska, E.; Badeński, A.; Dworak, M.; Szczepańska, M. The role of brain-derived neurotrophic factor (BDNF) in diagnosis and treatment of epilepsy, depression, schizophrenia, anorexia nervosa and alzheimer’s disease as highly drug-resistant diseases: A narrative review. Brain Sci., 2023, 13(2), 163.
[http://dx.doi.org/10.3390/brainsci13020163] [PMID: 36831706]
[45]
Iughetti, L.; Lucaccioni, L.; Fugetto, F.; Predieri, B.; Berardi, A.; Ferrari, F. Brain-derived neurotrophic factor and epilepsy: A systematic review. Neuropeptides, 2018, 72, 23-29.
[http://dx.doi.org/10.1016/j.npep.2018.09.005] [PMID: 30262417]
[46]
Spiers, J.G.; Steinert, J.R. Nitrergic modulation of ion channel function in regulating neuronal excitability. Channels, 2021, 15(1), 666-679.
[http://dx.doi.org/10.1080/19336950.2021.2002594] [PMID: 34802368]
[47]
Khazipov, R. GABAergic synchronization in epilepsy. Cold Spring Harb. Perspect. Med., 2016, 6(2), a022764.
[http://dx.doi.org/10.1101/cshperspect.a022764] [PMID: 26747834]
[48]
Chen, S.; Sang, N. Hypoxia-inducible factor-1: A critical player in the survival strategy of stressed cells. J. Cell. Biochem., 2016, 117(2), 267-278.
[http://dx.doi.org/10.1002/jcb.25283] [PMID: 26206147]
[49]
Zalpoor, H.; Akbari, A.; Nabi-Afjadi, M.; Forghaniesfidvajani, R.; Tavakol, C.; Barzegar, Z.; Iravanpour, F.; Hosseini, M.; Mousavi, S.R.; Farrokhi, M.R. Hypoxia‐inducible factor 1 alpha (HIF‐1α) stimulated and P2X7 receptor activated by COVID-19, as a potential therapeutic target and risk factor for epilepsy. Hum. Cell, 2022, 35(5), 1338-1345.
[http://dx.doi.org/10.1007/s13577-022-00747-9] [PMID: 35831562]
[50]
Feast, A.; Martinian, L.; Liu, J.; Catarino, C.B.; Thom, M.; Sisodiya, S.M. Investigation of hypoxia‐inducible factor‐1α in hippocampal sclerosis: A postmortem study. Epilepsia, 2012, 53(8), 1349-1359.
[http://dx.doi.org/10.1111/j.1528-1167.2012.03591.x] [PMID: 22812626]
[51]
Long, Q.; Fan, C.; Kai, W.; Luo, Q.; Xin, W.; Wang, P.; Wang, A.; Wang, Z.; Han, R.; Fei, Z.; Qiu, B.; Liu, W. Hypoxia inducible factor-1α expression is associated with hippocampal apoptosis during epileptogenesis. Brain Res., 2014, 1590, 20-30.
[http://dx.doi.org/10.1016/j.brainres.2014.09.028] [PMID: 25242614]
[52]
Yang, J.; He, F.; Meng, Q.; Sun, Y.; Wang, W.; Wang, C. Inhibiting HIF-1α decreases expression of TNF-α and caspase-3 in specific brain regions exposed kainic acid-induced status epilepticus. Cell. Physiol. Biochem., 2016, 38(1), 75-82.
[http://dx.doi.org/10.1159/000438610] [PMID: 26741705]
[53]
Kukec, E.; Goričar, K.; Dolžan, V.; Rener-Primec, Z. HIF1A polymorphisms do not modify the risk of epilepsy nor cerebral palsy after neonatal hypoxic-ischemic encephalopathy. Brain Res., 2021, 1757, 147281.
[http://dx.doi.org/10.1016/j.brainres.2021.147281] [PMID: 33515534]
[54]
Bar-Klein, G.; Cacheaux, L.P.; Kamintsky, L.; Prager, O.; Weissberg, I.; Schoknecht, K.; Cheng, P.; Kim, S.Y.; Wood, L.; Heinemann, U.; Kaufer, D.; Friedman, A. Losartan prevents acquired epilepsy via TGF‐β signaling suppression. Ann. Neurol., 2014, 75(6), 864-875.
[http://dx.doi.org/10.1002/ana.24147] [PMID: 24659129]
[55]
Qian, L.; Wei, S.J.; Zhang, D.; Hu, X.; Xu, Z.; Wilson, B.; El-Benna, J.; Hong, J.S.; Flood, P.M. Potent anti-inflammatory and neuroprotective effects of TGF-beta1 are mediated through the inhibition of ERK and p47phox-Ser345 phosphorylation and translocation in microglia. J. Immunol., 2008, 181(1), 660-668.
[http://dx.doi.org/10.4049/jimmunol.181.1.660] [PMID: 18566433]
[56]
Chitra, P.; Saiprasad, G.; Manikandan, R.; Sudhandiran, G. Berberine attenuates bleomycin induced pulmonary toxicity and fibrosis via suppressing NF-κB dependant TGF-β activation: A biphasic experimental study. Toxicol. Lett., 2013, 219(2), 178-193.
[http://dx.doi.org/10.1016/j.toxlet.2013.03.009] [PMID: 23523906]
[57]
Borowicz-Reutt, K.K.; Czuczwar, S.J. Role of oxidative stress in epileptogenesis and potential implications for therapy. Pharmacol. Rep., 2020, 72(5), 1218-1226.
[http://dx.doi.org/10.1007/s43440-020-00143-w] [PMID: 32865811]
[58]
Shou, J.W.; Shaw, P.C. Therapeutic efficacies of berberine against neurological disorders: An update of pharmacological effects and mechanisms. Cells, 2022, 11(5), 796.
[http://dx.doi.org/10.3390/cells11050796] [PMID: 35269418]
[59]
Su, L.J.; Zhang, J.H.; Gomez, H.; Murugan, R.; Hong, X.; Xu, D.; Jiang, F.; Peng, Z.Y. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid. Med. Cell. Longev., 2019, 2019, 1-13.
[http://dx.doi.org/10.1155/2019/5080843] [PMID: 31737171]
[60]
Kaspar, J.W.; Niture, S.K.; Jaiswal, A.K. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic. Biol. Med., 2009, 47(9), 1304-1309.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.07.035] [PMID: 19666107]
[61]
Carmona-Aparicio, L.; Pérez-Cruz, C.; Zavala-Tecuapetla, C.; Granados-Rojas, L.; Rivera-Espinosa, L.; Montesinos-Correa, H.; Hernández- Damián, J.; Pedraza-Chaverri, J.; Sampieri, A., III; Coballase-Urrutia, E.; Cárdenas-Rodríguez, N. Overview of Nrf2 as therapeutic target in epilepsy. Int. J. Mol. Sci., 2015, 16(8), 18348-18367.
[http://dx.doi.org/10.3390/ijms160818348] [PMID: 26262608]
[62]
Wagener, F.A.D.T.G.; van Beurden, H.E.; von den Hoff, J.W.; Adema, G.J.; Figdor, C.G. The heme-heme oxygenase system: A molecular switch in wound healing. Blood, 2003, 102(2), 521-528.
[http://dx.doi.org/10.1182/blood-2002-07-2248] [PMID: 12649161]
[63]
Itoh, K.; Wakabayashi, N.; Katoh, Y.; Ishii, T.; O’Connor, T.; Yamamoto, M. Keap1 regulates both cytoplasmic‐nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells, 2003, 8(4), 379-391.
[http://dx.doi.org/10.1046/j.1365-2443.2003.00640.x] [PMID: 12653965]
[64]
Lin, T.K.; Chen, S.D.; Lin, K.J.; Chuang, Y.C. Seizure-induced oxidative stress in status epilepticus: Is antioxidant beneficial? Antioxidants, 2020, 9(11), 1029.
[http://dx.doi.org/10.3390/antiox9111029] [PMID: 33105652]
[65]
Vezzani, A.; Lang, B.; Aronica, E. Immunity and inflammation in epilepsy. Cold Spring Harb. Perspect. Med., 2016, 6(2), a022699.
[http://dx.doi.org/10.1101/cshperspect.a022699] [PMID: 26684336]
[66]
Gakharia, T.; Bakhtadze, S.; Lim, M.; Khachapuridze, N.; Kapanadze, N. Alterations of plasma pro-inflammatory cytokine levels in children with refractory epilepsies. Children, 2022, 9(10), 1506.
[http://dx.doi.org/10.3390/children9101506] [PMID: 36291442]
[67]
Youn, Y.; Sung, I.K.; Lee, I.G. The role of cytokines in seizures: Interleukin (IL)-1β, IL-1Ra, IL-8, and IL-10. Korean J. Pediatr., 2013, 56(7), 271-274.
[http://dx.doi.org/10.3345/kjp.2013.56.7.271] [PMID: 23908665]
[68]
Riazi, K.; Galic, M.A.; Kuzmiski, J.B.; Ho, W.; Sharkey, K.A.; Pittman, Q.J. Microglial activation and TNFα production mediate altered CNS excitability following peripheral inflammation. Proc. Natl. Acad. Sci., 2008, 105(44), 17151-17156.
[http://dx.doi.org/10.1073/pnas.0806682105] [PMID: 18955701]
[69]
Rawat, C.; Kukal, S.; Dahiya, U.R.; Kukreti, R. Cyclooxygenase-2 (COX-2) inhibitors: Future therapeutic strategies for epilepsy management. J. Neuroinflammation, 2019, 16(1), 197.
[http://dx.doi.org/10.1186/s12974-019-1592-3] [PMID: 31666079]
[70]
Kenney, M.J.; Ganta, C.K. Autonomic nervous system and immune system interactions. Compr. Physiol., 2014, 4(3), 1177-1200.
[http://dx.doi.org/10.1002/cphy.c130051] [PMID: 24944034]
[71]
Li, L.; Yu, Y.; Hou, R.; Hao, J.; Jiang, J. Inhibiting the PGE 2 receptor EP2 mitigates excitotoxicity and ischemic injury. ACS Pharmacol. Transl. Sci., 2020, 3(4), 635-643.
[http://dx.doi.org/10.1021/acsptsci.0c00040] [PMID: 32832866]
[72]
Domitrović, R.; Jakovac, H.; Blagojević, G. Hepatoprotective activity of berberine is mediated by inhibition of TNF-α, COX-2, and iNOS expression in CCl4-intoxicated mice. Toxicology, 2011, 280(1-2), 33-43.
[http://dx.doi.org/10.1016/j.tox.2010.11.005] [PMID: 21095217]
[73]
Hayatdavoudi, P.; Hosseini, M.; Hajali, V.; Hosseini, A.; Rajabian, A. The role of astrocytes in epileptic disorders. Physiol. Rep., 2022, 10(6), e15239.
[http://dx.doi.org/10.14814/phy2.15239] [PMID: 35343625]
[74]
Sanz, P.; Garcia-Gimeno, M.A. Reactive glia inflammatory signaling pathways and epilepsy. Int. J. Mol. Sci., 2020, 21(11), 4096.
[http://dx.doi.org/10.3390/ijms21114096] [PMID: 32521797]
[75]
Cai, M.; Lin, W. The function of NF-kappa B during epilepsy, a potential therapeutic target. Front. Neurosci., 2022, 16, 851394.
[http://dx.doi.org/10.3389/fnins.2022.851394] [PMID: 35360161]
[76]
Staba, R.J.; Stead, M.; Worrell, G.A. Electrophysiological biomarkers of epilepsy. Neurotherapeutics, 2014, 11(2), 334-346.
[http://dx.doi.org/10.1007/s13311-014-0259-0] [PMID: 24519238]
[77]
Bertram, E. Electrophysiology in epilepsy surgery: Roles and limitations. Ann. Indian Acad. Neurol., 2014, 17(5), 40.
[http://dx.doi.org/10.4103/0972-2327.128649] [PMID: 24791088]
[78]
Mikkilineni, S.; Cantuti-Castelvetri, I.; Cahill, C.M.; Balliedier, A.; Greig, N.H.; Rogers, J.T. The anticholinesterase phenserine and its enantiomer posiphen as 5'untranslated-region-directed translation blockers of the Parkinson’s alpha synuclein expression. Parkinsons Dis., 2012, 2012, 1-13.
[http://dx.doi.org/10.1155/2012/142372] [PMID: 22693681]
[79]
Zhou, G.; Yan, M.; Guo, G.; Tong, N. Ameliorative effect of berberine on neonatally induced type 2 diabetic neuropathy via modulation of BDNF, IGF-1, PPAR-γ, and AMPK expressions. Dose Response, 2019, 17(3)
[http://dx.doi.org/10.1177/1559325819862449] [PMID: 31360147]
[80]
Mittli, D. Inflammatory processes in the prefrontal cortex induced by systemic immune challenge: Focusing on neurons. Brain Behav. Immun Health, 2023, 34, 100703.
[http://dx.doi.org/10.1016/j.bbih.2023.100703] [PMID: 38033612]
[81]
Chawla, M.K.; Penner, M.R.; Olson, K.M.; Sutherland, V.L.; Mittelman-Smith, M.A.; Barnes, C.A. Spatial behavior and seizure-induced changes in c-fos mRNA expression in young and old rats. Neurobiol. Aging, 2013, 34(4), 1184-1198.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.10.017] [PMID: 23158763]
[82]
Baraban, S.C.; Taylor, M.R.; Castro, P.A.; Baier, H. Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience, 2005, 131(3), 759-768.
[http://dx.doi.org/10.1016/j.neuroscience.2004.11.031] [PMID: 15730879]
[83]
Wang, S.; Zhou, L.; He, C.; Wang, D.; Cai, X.; Yu, Y.; Chen, L.; Lu, D.; Bian, L.; Du, S.; Wu, Q.; Han, Y. The association between STX1B polymorphisms and treatment response in patients with epilepsy. Front. Pharmacol., 2021, 12, 701575.
[http://dx.doi.org/10.3389/fphar.2021.701575] [PMID: 34305610]
[84]
Ye, Y.; Liu, X.; Wu, N.; Han, Y.; Wang, J.; Yu, Y.; Chen, Q. Efficacy and safety of berberine alone for several metabolic disorders: A systematic review and meta-analysis of randomized clinical trials. Front. Pharmacol., 2021, 12, 653887.
[http://dx.doi.org/10.3389/fphar.2021.653887] [PMID: 33981233]
[85]
Chang, C.F.; Lee, Y.C.; Lee, K.H.; Lin, H.C.; Chen, C.L.; Shen, C.K.J.; Huang, C.C. Therapeutic effect of berberine on TDP-43-related pathogenesis in FTLD and ALS. J. Biomed. Sci., 2016, 23(1), 72.
[http://dx.doi.org/10.1186/s12929-016-0290-z] [PMID: 27769241]
[86]
Singh, N.; Sharma, B. Toxicological effects of berberine and sanguinarine. Front. Mol. Biosci., 2018, 5, 21.
[http://dx.doi.org/10.3389/fmolb.2018.00021] [PMID: 29616225]
[87]
Rad, S.Z.K.; Rameshrad, M.; Hosseinzadeh, H. Toxicology effects of Berberis vulgaris (barberry) and its active constituent, berberine: A review. Iran. J. Basic Med. Sci., 2017, 20(5), 516-529.
[PMID: 28656087]
[88]
Kwon, I.H.; Choi, H.S.; Shin, K.S.; Lee, B.K.; Lee, C.K.; Hwang, B.Y.; Lim, S.C.; Lee, M.K. Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson’s disease. Neurosci. Lett., 2010, 486(1), 29-33.
[http://dx.doi.org/10.1016/j.neulet.2010.09.038] [PMID: 20851167]
[89]
Kysenius, K.; Brunello, C.A.; Huttunen, H.J. Mitochondria and NMDA receptor-dependent toxicity of berberine sensitizes neurons to glutamate and rotenone injury. PLoS One, 2014, 9(9), e107129.
[http://dx.doi.org/10.1371/journal.pone.0107129] [PMID: 25192195]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy