Anticonvulsant potential of Grewia tiliaefolia in pentylenetetrazole induced epilepsy: insights from in vivo and in silico studies.
Mice
Animals
Anticonvulsants
/ adverse effects
Pentylenetetrazole
/ toxicity
Grewia
/ chemistry
Hexanes
/ adverse effects
Kaempferols
Antioxidants
/ pharmacology
Methanol
/ adverse effects
Chloroform
/ adverse effects
Receptors, AMPA
Seizures
/ chemically induced
Epilepsy
/ chemically induced
Plant Extracts
/ pharmacology
Gallic Acid
/ therapeutic use
gamma-Aminobutyric Acid
Antioxidant
Epilepsy
GABA
Generalized tonic clonic seizures
Glutamate
In silico
Myoclonic jerks
Journal
Metabolic brain disease
ISSN: 1573-7365
Titre abrégé: Metab Brain Dis
Pays: United States
ID NLM: 8610370
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
16
06
2022
accepted:
07
06
2023
medline:
18
9
2023
pubmed:
12
7
2023
entrez:
12
7
2023
Statut:
ppublish
Résumé
Epilepsy, a chronic neurological condition, impacts millions of individuals globally and remains a significant contributor to both illness and mortality. Available antiepileptic drugs have serious side effects which warrants to explore different medicinal plants used for the management of epilepsy reported in Traditional Indian Medicinal System (TIMS). Therefore, we explored the antiepileptic potential of the Grewia tiliaefolia (Tiliaeceae) which is known for its neuroprotective properties. Aerial parts of G. tiliaefolia were subjected to extraction with increasing order of polarity viz. hexane, chloroform and methanol. Antioxidant potential of hexane, chloroform and methanol extracts of G. tiliaefolia was evaluated by 2,2-diphenyl-1-picryl-hydrazyl-hydrate (DPPH) assay, total antioxidant capacity (TAC) assay, reducing power assay (RPA) and DNA nicking assay. Additionally, quantitative antioxidant assays were also conducted to quantify total phenolic (TPC) and total flavonoid content (TFC). As revealed by in vitro assays, methanol extract was found to contain more phenolic content. Hence, the methanol extract was further explored for its anticonvulsant potential in pentylenetetrazole (PTZ) induced acute seizures in mice. The methanol extract (400 mg/kg) significantly increased the latency to occurrence of myoclonic jerks and generalized tonic clonic seizures (GTCS). Additionally, it also reduced duration and seizure severity score associated with GTCS. The Grewia tiliaefolia methanol extract was further screened by Ultra High-Performance Liquid Chromatography (UHPLC) for presence of polyphenolic compounds, among which gallic acid and kaempferol were present in higher amount and were further analysed by in silico study to predict their possible binding sites and type of interactions these compounds show with gamma amino butyric acid (GABA) receptor and glutamate α amino-3- hydroxyl-5-methyl-4-isoxazolepropionic acid (Glu-AMPA) receptor. It was revealed that gallic acid and kaempferol had shown agonistic interaction for GABA receptor and antagonistic interaction for Glu-AMPA receptor. We concluded that G. tiliaefolia showed anticonvulsant potential possibly because of gallic acid and kaempferol possibly mediated through GABA and Glu-AMPA receptor.
Identifiants
pubmed: 37436587
doi: 10.1007/s11011-023-01252-0
pii: 10.1007/s11011-023-01252-0
doi:
Substances chimiques
Anticonvulsants
0
Pentylenetetrazole
WM5Z385K7T
n-hexane
2DDG612ED8
Hexanes
0
Kaempferols
0
Antioxidants
0
Methanol
Y4S76JWI15
Chloroform
7V31YC746X
Receptors, AMPA
0
Plant Extracts
0
Gallic Acid
632XD903SP
gamma-Aminobutyric Acid
56-12-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2355-2367Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Adebiyi OE, Olopade FE, Olopade JO, Olayemi FO (2016a) Behavioural studies on the ethanol leaf extract of Grewia carpinifolia in Wistar rats. Afr Health Sci 16(1):339–346
pubmed: 27358651
pmcid: 4915406
doi: 10.4314/ahs.v16i1.45
Adebiyi OE, Olopade JO, Olayemi FO (2016b) Neuroprotective effect of Grewia carpinifolia extract against vanadium induced behavioral impairment. Folia Vet Lat 60(4):5–13
doi: 10.1515/fv-2016-0031
Aguiar CC, Almeida AB, Araújo PV, Abreu RN, Chaves EM, Vale OC, Macêdo DS, Woods DJ, Fonteles MM, Vasconcelos SM (2012) Oxidative stress and epilepsy: literature review. Oxid Med Cellular longev 2012:1–12
Alatorre A, Oviedo-Chávez A, Villalobos N, Ríos A, Barrientos R, Querejeta E (2015) The local application of a flavonoid, (−)-epicatechin, increases the spiking of globus pallidus neurons in a dose-dependent manner and diminishes the catalepsy induced by haloperidol. Behav Pharmacol 26(1 and 2-Special Issue):117–24
pubmed: 25503260
doi: 10.1097/FBP.0000000000000100
Aseervatham GS, Suryakala U, Sundaram S, Bose PC, Sivasudha T (2016) Expression pattern of NMDA receptors reveals antiepileptic potential of apigenin 8-C-glucoside and chlorogenic acid in pilocarpine induced epileptic mice. Biomed Pharmacother 82:54–64
pubmed: 27470339
doi: 10.1016/j.biopha.2016.04.066
Attri S, Kaur P, Singh D, Kaur H, Rashid F, Kumar A, Singh B, Bedi N, Arora S (2021) Induction of apoptosis in A431 cells via ROS generation and p53-mediated pathway by chloroform fraction of Argemone mexicana (Pepaveraceae). E S P R 1–20
Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76
pubmed: 8660627
doi: 10.1006/abio.1996.0292
Berghuis B, Hulst J, Sonsma A, McCormack M, de Haan GJ, Sander JW, Lindhout D, Koeleman BP (2021) Symptomatology of carbamazepine-and oxcarbazepine-induced hyponatremia in people with epilepsy. Epilepsia 62(3):778–784
pubmed: 33576502
pmcid: 8248112
doi: 10.1111/epi.16828
Blume WT, Lüders HO, Mizrahi E, Tassinari C, van Emde Boas W, Engel Jr, Ex-officio J (2001) Glossary of descriptive terminology for ictal semiology: Report of the ILAE task force on classification and terminology. Epilepsia 42(9):1212–8
pubmed: 11580774
doi: 10.1046/j.1528-1157.2001.22001.x
Cárdenas-Rodríguez N, González-Trujano ME, Aguirre-Hernández E, Ruíz-García M, Sampieri A, Coballase-Urrutia E, Carmona-Aparicio L (2014) Anticonvulsant and antioxidant effects of Tilia americana var. mexicana and flavonoids constituents in the pentylenetetrazole-induced seizures. Oxid Med Cell Longev 2014:1–10
doi: 10.1155/2014/759293
Carton L, Auger F, Laloux C, Durieux N, Kyheng M, Potey C, Bergeron S, Rolland B, Deguil J, Bordet R (2022) Effects of acute ethanol and/or diazepam exposure on immediate and delayed hippocampal metabolite levels in rats anesthetized with isoflurane. Fundament Clinic Pharmacol 36(4):687–698
doi: 10.1111/fcp.12764
Chen J, Ye H, Zhang J, Li A, Ni Y (2022) Pathogenesis of seizures and epilepsy after stroke. Acta Epileptologica 1:1–6
Coelho VR, Vieira CG, de Souza LP, Moysés F, Basso C, Papke DK, Pires TR, Siqueira IR, Picada JN, Pereira P (2015) Antiepileptogenic, antioxidant and genotoxic evaluation of rosmarinic acid and its metabolite caffeic acid in mice. Life Sci 122:65–71
pubmed: 25498895
doi: 10.1016/j.lfs.2014.11.009
Dassault Systèmes BIOVIA Discovery Studio Modeling Environment, Release 2020 Dassault Systèmes, San Diego (2020)
Dev R, Kannan V, Kumar MS, Dayal D, Patel R (2019) Grewia Species: Diversity, Distribution, Traditional Knowledge and Utilization. Composition, Nutritional Value and Products, Wild Fruits, pp 395–426
Dhingra D, Jangra A (2014) Antiepileptic activity of ellagic acid, a naturally occurring polyphenolic compound, in mice. J Funct Foods 10:364–9
doi: 10.1016/j.jff.2014.07.011
Dhir A (2020) Natural polyphenols in preclinical models of epilepsy. Phytother Res 34(6):1268–1281
pubmed: 32061189
doi: 10.1002/ptr.6617
Dicson SM, Samuthirapandi M, Govindaraju A, Kasi PD (2015) Evaluation of in vitro and in vivo safety profile of the Indian traditional medicinal plant Grewia tiliaefolia. Regul Toxicol Pharm 73(1):241–247
doi: 10.1016/j.yrtph.2015.07.011
Eastman CL, D’Ambrosio R, Ganesh T (2020) Modulating neuroinflammation and oxidative stress to prevent epilepsy and improve outcomes after traumatic brain injury. Neuropharmacol 172:107907
doi: 10.1016/j.neuropharm.2019.107907
Ferreira A, Rodrigues M, Fortuna A, Falcão A, Alves G (2018) Flavonoid compounds as reversing agents of the P-glycoprotein-mediated multidrug resistance: An in vitro evaluation with focus on antiepileptic drugs. Food Res Int 103:110–120
pubmed: 29389596
doi: 10.1016/j.foodres.2017.10.010
Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, Engel J Jr, Forsgren L, French JA, Glynn M, Hesdorffer DC (2014) ILAE official report: a practical clinical definition of epilepsy. Epilepsia 55(4):475–482
pubmed: 24730690
doi: 10.1111/epi.12550
Geronzi U, Lotti F, Grosso S (2018) Oxidative stress in epilepsy. Expert Rev Neurother 18(5):427–434
pubmed: 29651881
doi: 10.1080/14737175.2018.1465410
Green JL, Dos Santos WF, Fontana AC (2021) Role of glutamate excitotoxicity and glutamate transporter EAAT2 in epilepsy: Opportunities for novel therapeutics development. Biochem Pharmacol 193:114786
pubmed: 34571003
pmcid: 8605998
doi: 10.1016/j.bcp.2021.114786
Han Y, Chen JZ (2012) Oxidative stress induces mitochondrial DNA damage and cytotoxicity through independent mechanisms in human cancer cells. BioMed Res Int 2013:1-8
Hotz AL, Jamali A, Rieser NN, Niklaus S, Aydin E, Myren-Svelstad S, Lalla L, Jurisch-Yaksi N, Yaksi E, Neuhauss SC (2022) Loss of glutamate transporter eaat2a leads to aberrant neuronal excitability, recurrent epileptic seizures, and basal hypoactivity. Glia 70(1):196–214
pubmed: 34716961
doi: 10.1002/glia.24106
Ishola IO, Akinleye MO, Afolayan OO, Okonkwo HE, Animashaun OT, Agbaje EO (2022) Anticonvulsant activity of Nymphaea lotus Linn. extract in mice: The role of GABAergic-glutamatergic neurotransmission and antioxidant defence mechanisms. Epilepsy Res 181:106871.
Jain S, Agarwal NB, Mediratta PK, Sharma KK (2012) Evaluation of anticonvulsant and nootropic effect of ondansetron in mice. Hum Exp Toxicol 31(9):905–912
pubmed: 22354082
doi: 10.1177/0960327112436406
Jastrzembski B, Locke J, Wan MJ (2020) Clinical implications and cost of electroretinography screening for vigabatrin toxicity. Can J Ophthalmol 55(3):e98-100
pubmed: 31879070
doi: 10.1016/j.jcjo.2019.10.014
Jeavons PM, Clark JE (1974) Sodium valproate in treatment of epilepsy. Br Med J 2(5919):584–6
pubmed: 4209500
pmcid: 1610767
doi: 10.1136/bmj.2.5919.584
Jebin R, Molla MI, Chowdhury SM, Rafe MR (2019) Antidepressant and sedative-hypnotic activities of methanolic extract of Grewia asiatica Linn. leaves in mice. Bangladesh J Pharmacol 22(2):185–91
doi: 10.3329/bpj.v22i2.42303
Kim DO, Jeong SW, Lee CY (2003) Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81(3):321–326
doi: 10.1016/S0308-8146(02)00423-5
Kumar N, Singh A, Gulati HK, Bhagat K, Kaur K, Kaur J, Dudhal S, Duggal A, Gulati P, Singh H, Singh JV (2021) Phytoconstituents from ten natural herbs as potent inhibitors of main protease enzyme of SARS-COV-2: in silico study. Phytomed Plus 1(4):100083
pubmed: 35403086
pmcid: 8180089
doi: 10.1016/j.phyplu.2021.100083
Kumar Prasad SA, Subrahmanyam EV, Shabaraya AR (2014) Design and biological screening of some novel formazan derivatives from schiff bases of gallic acid. World J Pharm Res 3(2):2741–2752
Lee JC, Kim HR, Kim J, Jang YS (2002) Antioxidant property of an ethanol extract of the stem of Opuntia ficus-indica var. saboten. J Agric Food Chem 50(22):6490–6
doi: 10.1021/jf020388c
Lin TK, Chen SD, Lin KJ, Chuang YC (2020) Seizure-induced oxidative stress in status epilepticus: is antioxidant beneficial? Antioxidants 9(11):1029
pubmed: 33105652
pmcid: 7690410
doi: 10.3390/antiox9111029
Loshali A, Joshi BC, Sundriyal A, Uniyal S (2021) Antiepileptic effects of antioxidant potent extract from Urtica dioica Linn. root on pentylenetetrazole and maximal electroshock induced seizure models. Heliyon 7(2):e06195
pubmed: 33644470
pmcid: 7887401
doi: 10.1016/j.heliyon.2021.e06195
Łukawski K, Czuczwar SJ (2023) Oxidative Stress and Neurodegeneration in Animal Models of Seizures and Epilepsy. Antioxidants 12(5):1049
pubmed: 37237916
pmcid: 10215527
doi: 10.3390/antiox12051049
Madireddy S, Madireddy S (2023) Therapeutic strategies to ameliorate neuronal damage in epilepsy by regulating oxidative stress, mitochondrial dysfunction, and neuroinflammation. Brain Sci 13(5):784
pubmed: 37239256
pmcid: 10216584
doi: 10.3390/brainsci13050784
Maier CM, Chan PH (2002) Book review: role of superoxide dismutases in oxidative damage and neurodegenerative disorders. Neuroscientist 8(4):323–334
pubmed: 12194501
doi: 10.1177/107385840200800408
Mary SJ, Merina AJ (2021) Studies on total antioxidant activity of the extract of Nyctasnthes arbortristis flower extract by DPPH radical-scavenging activity and superoxide anion scavenging activity assay. J Med Plants 9(2):160–164
Meinardi H, Scott RA, Reis R, On Behalf Of The ILAE Commission on the Developing World Sanders J W A S (2001) The treatment gap in epilepsy: the current situation and ways forward. Epilepsia 42(1):136–49
pubmed: 11207798
doi: 10.1046/j.1528-1157.2001.32800.x
Mishra P, Mittal AK, Rajput SK, Sinha JK (2021) Cognition and memory impairment attenuation via reduction of oxidative stress in acute and chronic mice models of epilepsy using antiepileptogenic Nux vomica. J Ethnopharmacol 267:113509
pubmed: 33141053
doi: 10.1016/j.jep.2020.113509
Nieoczym D, Socała K, Raszewski G, Wlaź P (2014) Effect of quercetin and rutin in some acute seizure models in mice. Prog Neuropsychopharmacol Biol 54:50–58
doi: 10.1016/j.pnpbp.2014.05.007
Ojong LJ, Abdou JP, KavayeKandeda A, Yaya AJ, Tchamgoue AD, Tchokouaha LR, Nkantchoua NG, Agbor G, Agbor RS, Ngo EB (2016) Anticonvulsant and in vitro antioxidant activities of Momordica cissoides L.(Cucurbitaceae). J Appl Pharm Sci 6(04):117–23
doi: 10.7324/JAPS.2016.60416
Olowe R, Sandouka S, Saadi A, Shekh-Ahmad T (2020) Approaches for reactive oxygen species and oxidative stress quantification in epilepsy. Antioxidants 9(10):990
pubmed: 33066477
pmcid: 7602129
doi: 10.3390/antiox9100990
Park YS, Jung ST, Kang SG, Heo BG, Arancibia-Avila P, Toledo F, Drzewiecki J, Namiesnik J, Gorinstein S (2008) Antioxidants and proteins in ethylene-treated kiwifruits. Food Chem 107(2):640–648
doi: 10.1016/j.foodchem.2007.08.070
Parsons AL, Bucknor E, Castroflorio E, Soares TR, Oliver PL, Rial D (2022) The interconnected mechanisms of oxidative stress and neuroinflammation in epilepsy. Antioxidants 11(1):157
pubmed: 35052661
pmcid: 8772850
doi: 10.3390/antiox11010157
Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269(2):337–341
pubmed: 10222007
doi: 10.1006/abio.1999.4019
Qneibi M, Hanania M, Jaradat N, Emwas N, Radwan S (2021) Inula viscosa (L.) Greuter, phytochemical composition, antioxidant, total phenolic content, total flavonoids content and neuroprotective effects. Eur J Integr Med 42:101291
doi: 10.1016/j.eujim.2021.101291
Rajput A, Sharma P, Kumar N, Kaur S, Arora S (2023a) Neuroprotective activity of novel phenanthrene derivative from Grewia tiliaefolia by in vitro and in silico studies. Sci Rep 13(1):2444
pubmed: 36765125
pmcid: 9918530
doi: 10.1038/s41598-023-29446-7
Rajput A, Sharma P, Singh H, Singh B, Kaur S, Arora S (2023b) Health Promoting Properties of Grewia asiatica and Grewia tenax Berries: A Potential Role in Cancer, Diabetes, and Liver Diseases Prevention. Bioactive Phytochemicals from Himalayas: A Phytotherapeutic Approach 41–48
Redfern J, Kinninmonth M, Burdass D, Verran J (2014) Using soxhlet ethanol extraction to produce and test plant material (essential oils) for their antimicrobial properties. J Microbiol Biol Educ 15(1):45–46
pubmed: 24839520
pmcid: 4004744
doi: 10.1128/jmbe.v15i1.656
Rogawski MA, Löscher W (2004) The neurobiology of antiepileptic drugs. Nat Rev Neurosci 5(7):553–564
pubmed: 15208697
doi: 10.1038/nrn1430
Salem M, El-Bardissy A (2021) Lamotrigine-induced neutropenia after high-dose concomitant initiation with phenytoin. Clin Case Rep 9(11):e05136
pubmed: 34849233
pmcid: 8607801
doi: 10.1002/ccr3.5136
Shamoun MI, Mohamed AH, El-Hadiyah TM (2014) Anticonvulsant and anxiolytic properties of the roots of Grewia bicolor in rats. SJMS 9(3):137–143
Sharma J, Bhardwaj VK, Singh R, Rajendran V, Purohit R, Kumar S (2021) An in-silico evaluation of different bioactive molecules of tea for their inhibition potency against non-structural protein-15 of SARS-CoV-2. Food Chem 346:128933
pubmed: 33418408
doi: 10.1016/j.foodchem.2020.128933
Silva dos Santos J, Goncalves Cirino JP, de Oliveira CP, Ortega MM (2021) The pharmacological action of kaempferol in central nervous system diseases: A review. Front Pharmacol 11:2143
doi: 10.3389/fphar.2020.565700
Singh T, Bagga N, Kaur A, Kaur N, Gawande DY, Goel RK (2017) Agmatine for combined treatment of epilepsy, depression and cognitive impairment in chronic epileptic animals. Biomed Pharmacother 92:720–725
pubmed: 28586743
doi: 10.1016/j.biopha.2017.05.085
Singh T, Mishra A, Goel RK (2021) PTZ kindling model for epileptogenesis, refractory epilepsy, and associated comorbidities: relevance and reliability. Metab Brain Dis 36(7):1573–1590
pubmed: 34427842
doi: 10.1007/s11011-021-00823-3
Tamboli AM, Rub RA, Ghosh P, Bodhankar SL (2012) Antiepileptic activity of lobeline isolated from the leaf of Lobelia nicotianaefolia and its effect on brain GABA level in mice. Asian Pac J Trop Biomed 2(7):537–542
pubmed: 23569966
pmcid: 3609340
doi: 10.1016/S2221-1691(12)60092-6
Ullah W, Uddin G, Siddiqui BS (2012) Ethnic uses, pharmacological and phytochemical profile of genus Grewia. J Asian Natural Products Res 14(2):186–95
doi: 10.1080/10286020.2011.639764
Watanabe Y, Kaida Y, Fukuhara S, Takechi K, Uehara T, Kamei C (2011) Participation of metabotropic glutamate receptors in pentetrazol-induced kindled seizure. Epilepsia 52(1):140–150
pubmed: 21054350
doi: 10.1111/j.1528-1167.2010.02764.x
Zhu F, Li XX, Yang SY, Chen YZ (2018) Clinical success of drug targets prospectively predicted by in silico study. Trends Pharmacol Sci 39(3):229–231
pubmed: 29295742
doi: 10.1016/j.tips.2017.12.002