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CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Research Article

Neuroprotective Potential of Bacopa monnieri: Modulation of Inflammatory Signals

Author(s): Erica Costantini, Srinivas Jarlapoodi, Federica Serra, Lisa Aielli, Haroon Khan, Tarun Belwal, Katia Falasca and Marcella Reale*

Volume 22, Issue 3, 2023

Published on: 11 March, 2022

Page: [441 - 451] Pages: 11

DOI: 10.2174/1871527321666220111124047

Price: $65

Abstract

Background: To date, much evidence has shown the increased interest in natural molecules and traditional herbal medicine as alternative bioactive compounds to fight many inflammatory conditions, both in relation to immunomodulation and in terms of their wound healing potential. Bacopa monnieri is a herb that is used in the Ayurvedic medicine tradition for its anti-inflammatory activity.

Objective: In this study, we evaluate the anti-inflammatory and regenerative properties of the Bacopa monnieri extract (BME) in vitro model of neuroinflammation.

Methods: Neuronal SH-SY5Y cells were stimulated with TNFα and IFNγ and used to evaluate the effect of BME on cell viability, cytotoxicity, cytokine gene expression, and healing rate.

Results: Our results showed that BME protects against the Okadaic acid-induced cytotoxicity in SH-SY5Y cells. Moreover, in TNFα and IFNγ primed cells, BME reduces IL-1β, IL-6, COX-2, and iNOS, mitigates the mechanical trauma injury-induced damage, and accelerates the healing of wounds.

Conclusion: This study indicates that BME might become a promising candidate for the treatment of neuroinflammation.

Keywords: Neuroprotection, inflammation, cytokines, metalloproteinases, cyclooxygenase, inducible nitric oxide synthase.

Graphical Abstract
[1]
Crutcher KA, Gendelman HE, Kipnis J, et al. Debate: “is increasing neuroinflammation beneficial for neural repair?”. J Neuroimmune Pharmacol 2006; 1(3): 195-211.
[http://dx.doi.org/10.1007/s11481-006-9021-7] [PMID: 18040798]
[2]
Chitnis T, Weiner HL. CNS inflammation and neurodegeneration. J Clin Invest 2017; 127(10): 3577-87.
[http://dx.doi.org/10.1172/JCI90609] [PMID: 28872464]
[3]
Behl T, Makkar R, Sehgal A, et al. Current trends in neurodegeneration: Cross talks between oxidative stress, cell death, and inflammation. Int J Mol Sci 2021; 22(14): 7432.
[http://dx.doi.org/10.3390/ijms22147432]
[4]
Lee Y, Lee S, Chang SC, Lee J. Significant roles of neuroinflammation in Parkinson’s disease: Therapeutic targets for PD prevention. Arch Pharm Res 2019; 42(5): 416-25.
[http://dx.doi.org/10.1007/s12272-019-01133-0] [PMID: 30830660]
[5]
Regen F, Hellmann-Regen J, Costantini E, Reale M. Neuroinflammation and Alzheimer’s disease: Implications for microglial activation. Curr Alzheimer Res 2017; 14(11): 1140-8.
[http://dx.doi.org/10.2174/1567205014666170203141717] [PMID: 28164764]
[6]
Irollo E, Luchetta J, Ho C, Nash B, Meucci O. Mechanisms of neuronal dysfunction in HIV-associated neurocognitive disorders. Cell Mol Life Sci 2021; 78(9): 4283-303.
[http://dx.doi.org/10.1007/s00018-021-03785-y] [PMID: 33585975]
[7]
Heaton RK, Franklin DR, Ellis RJ, et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. J Neurovirol 2011; 17(1): 3-16.
[http://dx.doi.org/10.1007/s13365-010-0006-1] [PMID: 21174240]
[8]
Falasca K, Reale M, Ucciferri C, et al. Cytokines, hepatic fibrosis, and antiretroviral therapy role in neurocognitive disorders HIV related. AIDS Res Hum Retroviruses 2017; 33(3): 246-53.
[http://dx.doi.org/10.1089/aid.2016.0138] [PMID: 27615271]
[9]
Knoblach SM, Fan L, Faden AI. Early neuronal expression of tumor necrosis factor-alpha after experimental brain injury contributes to neurological impairment. J Neuroimmunol 1999; 95(1-2): 115-25.
[http://dx.doi.org/10.1016/S0165-5728(98)00273-2] [PMID: 10229121]
[10]
Shohami E, Bass R, Wallach D, Yamin A, Gallily R. Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury. J Cereb Blood Flow Metab 1996; 16(3): 378-84.
[http://dx.doi.org/10.1097/00004647-199605000-00004] [PMID: 8621742]
[11]
Erta M, Quintana A, Hidalgo J. Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci 2012; 8(9): 1254-66.
[http://dx.doi.org/10.7150/ijbs.4679] [PMID: 23136554]
[12]
Morganti-Kossmann MC, Rancan M, Stahel PF, Kossmann T. Inflammatory response in acute traumatic brain injury: A double-edged sword. Curr Opin Crit Care 2002; 8(2): 101-5.
[http://dx.doi.org/10.1097/00075198-200204000-00002] [PMID: 12386508]
[13]
Goldman SM, Tanner CM, Oakes D, Bhudhikanok GS, Gupta A, Langston JW. Head injury and Parkinson’s disease risk in twins. Ann Neurol 2006; 60(1): 65-72.
[http://dx.doi.org/10.1002/ana.20882] [PMID: 16718702]
[14]
Nordström P, Michaëlsson K, Gustafson Y, Nordström A. Traumatic brain injury and young onset dementia: A nationwide cohort study. Ann Neurol 2014; 75(3): 374-81.
[http://dx.doi.org/10.1002/ana.24101] [PMID: 24812697]
[15]
Vázquez-Fresno R, Rosana ARR, Sajed T, Onookome-Okome T, Wishart NA, Wishart DS. Herbs and spices- Biomarkers of intake based on human intervention studies - A systematic review. Genes Nutr 2019; 14: 18.
[http://dx.doi.org/10.1186/s12263-019-0636-8] [PMID: 31143299]
[16]
Lai PK, Roy J. Antimicrobial and chemopreventive properties of herbs and spices. Curr Med Chem 2004; 11(11): 1451-60.
[http://dx.doi.org/10.2174/0929867043365107] [PMID: 15180577]
[17]
Shahidi F, Ambigaipalan P. Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects-a review. J Funct Foods 2015; 18 Part B: 820-97.
[http://dx.doi.org/10.1016/j.jff.2015.06.018]
[18]
Ahammed S, Afrin R, Uddin N, et al. Acetylcholinesterase inhibitory and antioxidant activity of the compounds isolated from Vanda roxburghii. Adv Pharmacol Pharm Sci 2021; 2021: 5569054.
[http://dx.doi.org/10.1155/2021/5569054] [PMID: 33855299]
[19]
Jeyasri R, Muthuramalingam P, Suba V, Ramesh M, Chen JT. Bacopa monnieri and their bioactive compounds inferred multi-target treatment strategy for neurological diseases: A cheminformatics and system pharmacology approach. Biomolecules 2020; 10(4): 536.
[http://dx.doi.org/10.3390/biom10040536] [PMID: 32252235]
[20]
Le XT, Nguyet Pham HT, Van Nguyen T, et al. Protective effects of Bacopa monnieri on ischemia-induced cognitive deficits in mice: The possible contribution of bacopaside I and underlying mechanism. J Ethnopharmacol 2015; 164: 37-45.
[http://dx.doi.org/10.1016/j.jep.2015.01.041] [PMID: 25660331]
[21]
Mathew M, Subramanian S. Evaluation of anti-amyloidogenic potential of nootropic herbal extracts in vitro. Int J Pharmaceutic Sci Res 2012; 3(11): 4276-80.
[22]
Bhattacharya SK, Bhattacharya A, Kumar A, Ghosal S. Antioxidant activity of Bacopa monniera in rat frontal cortex, striatum and hippocampus. Phytother Res 2000; 14(3): 174-9.
[http://dx.doi.org/10.1002/(SICI)1099-1573(200005)14:3<174::AID-PTR624>3.0.CO;2-O] [PMID: 10815010]
[23]
Limpeanchob N, Jaipan S, Rattanakaruna S, Phrompittayarat W, Ingkaninan K. Neuroprotective effect of Bacopa monnieri on beta-amyloid-induced cell death in primary cortical culture. J Ethnopharmacol 2008; 120(1): 112-7.
[http://dx.doi.org/10.1016/j.jep.2008.07.039] [PMID: 18755259]
[24]
Kovalevich J, Langford D. Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology. Methods Mol Biol 2013; 1078: 9-21.
[http://dx.doi.org/10.1007/978-1-62703-640-5_2] [PMID: 23975817]
[25]
Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the MTT assay. Cold Spring Harb Protoc 2018; 2018(6)
[http://dx.doi.org/10.1101/pdb.prot095505] [PMID: 29858338]
[26]
Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the lactate dehydrogenase assay. Cold Spring Harb Protoc 2018; 2018(6)
[http://dx.doi.org/10.1101/pdb.prot095497] [PMID: 29858337]
[27]
Licastro F, Hrelia S, Porcellini E, et al. Peripheral inflammatory markers and antioxidant response during the post-acute and chronic phase after severe traumatic brain injury. Front Neurol 2016; 7: 189.
[http://dx.doi.org/10.3389/fneur.2016.00189] [PMID: 27853449]
[28]
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25(4): 402-8.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[29]
Chhabra A, Rani V. Gel-based gelatin Zymography to examine matrix metalloproteinase activity in cell culture. Methods Mol Biol 2018; 1731: 83-96.
[http://dx.doi.org/10.1007/978-1-4939-7595-2_9] [PMID: 29318546]
[30]
Dhillon SS, Mastropaolo LA, Murchie R, et al. Higher activity of the inducible nitric oxide synthase contributes to very early onset inflammatory bowel disease. Clin Transl Gastroenterol 2014; 5(1): e46.
[http://dx.doi.org/10.1038/ctg.2013.17] [PMID: 24430113]
[31]
Ziebell JM, Morganti-Kossmann MC. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 2010; 7(1): 22-30.
[http://dx.doi.org/10.1016/j.nurt.2009.10.016] [PMID: 20129494]
[32]
Xicoy H, Wieringa B, Martens GJ. The SH-SY5Y cell line in Parkinson’s disease research: A systematic review. Mol Neurodegener 2017; 12(1): 10.
[http://dx.doi.org/10.1186/s13024-017-0149-0] [PMID: 28118852]
[33]
Saponaro C, Cianciulli A, Calvello R, Dragone T, Iacobazzi F, Panaro MA. The PI3K/Akt pathway is required for LPS activation of microglial cells. Immunopharmacol Immunotoxicol 2012; 34(5): 858-65.
[http://dx.doi.org/10.3109/08923973.2012.665461] [PMID: 22397361]
[34]
Hadass O, Tomlinson BN, Gooyit M, et al. Selective inhibition of matrix metalloproteinase-9 attenuates secondary damage resulting from severe traumatic brain injury. PLoS One 2013; 8(10): e76904.
[http://dx.doi.org/10.1371/journal.pone.0076904] [PMID: 24194849]
[35]
Abdul-Muneer PM, Pfister BJ, Haorah J, Chandra N. Role of matrix metalloproteinases in the pathogenesis of traumatic brain injury. Mol Neurobiol 2016; 53(9): 6106-23.
[http://dx.doi.org/10.1007/s12035-015-9520-8] [PMID: 26541883]
[36]
Dwivedi S, Nagarajan R, Hanif K, Siddiqui HH, Nath C, Shukla R. Standardized extract of Bacopa monniera attenuates okadaic acid induced memory dysfunction in rats: Effect on Nrf2 pathway. Evid Based Complement Alternat Med 2014; 2014: 262639.
[http://dx.doi.org/10.1155/2014/262639] [PMID: 24078822]
[37]
Kishore K, Singh M. Effect of bacosides, alcoholic extract of Bacopa monniera Linn. (brahmi), on experimental amnesia in mice. Indian J Exp Biol 2005; 43(7): 640-5.
[PMID: 16053272]
[38]
Srivastav S, Fatima M, Mondal AC. Important medicinal herbs in Parkinson’s disease pharmacotherapy. Biomed Pharmacother 2017; 92: 856-63.
[http://dx.doi.org/10.1016/j.biopha.2017.05.137] [PMID: 28599249]
[39]
Uabundit N, Wattanathorn J, Mucimapura S, Ingkaninan K. Cognitive enhancement and neuroprotective effects of Bacopa monnieri in Alzheimer’s disease model. J Ethnopharmacol 2010; 127(1): 26-31.
[http://dx.doi.org/10.1016/j.jep.2009.09.056] [PMID: 19808086]
[40]
Piyabhan P, Tingpej P, Duansak N. Effect of pre- and post-treatment with Bacopa monnieri (Brahmi) on phencyclidine-induced disruptions in object recognition memory and cerebral calbindin, parvalbumin, and calretinin immunoreactivity in rats. Neuropsychiatr Dis Treat 2019; 15: 1103-17.
[http://dx.doi.org/10.2147/NDT.S193222] [PMID: 31118643]
[41]
Channa S, Dar A, Anjum S, Yaqoob M, Atta-Ur-Rahman . Anti-inflammatory activity of Bacopa monniera in rodents. J Ethnopharmacol 2006; 104(1-2): 286-9.
[http://dx.doi.org/10.1016/j.jep.2005.10.009] [PMID: 16343831]
[42]
Farooqui AA, Farooqui T, Madan A, Ong JH, Ong WY. Ayurvedic medicine for the treatment of dementia: Mechanistic aspects. Evid Based Complement Alternat Med 2018; 2018: 2481076.
[http://dx.doi.org/10.1155/2018/2481076] [PMID: 29861767]
[43]
Brimson JM, Brimson S, Prasanth MI, Thitilertdecha P, Malar DS, Tencomnao T. The effectiveness of Bacopa monnieri (Linn.) Wettst. as a nootropic, neuroprotective, or antidepressant supplement: Analysis of the available clinical data. Sci Rep 2021; 11(1): 596.
[http://dx.doi.org/10.1038/s41598-020-80045-2] [PMID: 33436817]
[44]
Khan AV, Ahmed QU, Shukla I, Khan AA. Antibacterial efficacy of Bacopa monnieri leaf extracts against pathogenic bacteria. Asian Biomed 2011; 4(4): 651-5.
[http://dx.doi.org/10.2478/abm-2010-0084]
[45]
Bhandari P, Sendri N, Devidas SB. Dammarane triterpenoid glycosides in Bacopa monnieri: A review on chemical diversity and bioactivity. Phytochemistry 2020; 172: 112276.
[http://dx.doi.org/10.1016/j.phytochem.2020.112276] [PMID: 32058865]
[46]
Rai D, Bhatia G, Palit G, Pal R, Singh S, Singh HK. Adaptogenic effect of Bacopa monniera (Brahmi). Pharmacol Biochem Behav 2003; 75(4): 823-30.
[http://dx.doi.org/10.1016/S0091-3057(03)00156-4] [PMID: 12957224]
[47]
Nuydens R, de Jong M, Van Den Kieboom G, et al. Okadaic acid-induced apoptosis in neuronal cells: Evidence for an abortive mitotic attempt. J Neurochem 1998; 70(3): 1124-33.
[http://dx.doi.org/10.1046/j.1471-4159.1998.70031124.x] [PMID: 9489733]
[48]
Del Barrio L, Martín-de-Saavedra MD, Romero A, et al. Neurotoxicity induced by okadaic acid in the human neuroblastoma SH-SY5Y line can be differentially prevented by α7 and β2* nicotinic stimulation. Toxicol Sci 2011; 123(1): 193-205.
[http://dx.doi.org/10.1093/toxsci/kfr163] [PMID: 21715663]
[49]
Abdul-Muneer PM, Schuetz H, Wang F, et al. Induction of oxidative and nitrosative damage leads to cerebrovascular inflammation in an animal model of mild traumatic brain injury induced by primary blast. Free Radic Biol Med 2013; 60: 282-91.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.02.029] [PMID: 23466554]
[50]
Abdul-Muneer PM, Chandra N, Haorah J. Interactions of oxidative stress and neurovascular inflammation in the pathogenesis of traumatic brain injury. Mol Neurobiol 2015; 51(3): 966-79.
[http://dx.doi.org/10.1007/s12035-014-8752-3] [PMID: 24865512]
[51]
Kumaria A. In vitro models as a platform to investigate traumatic brain injury. ATLA 45 2017; 45(4): 201-11.
[http://dx.doi.org/10.1177/026119291704500405]
[52]
Frugier T, Morganti-Kossmann MC, O’Reilly D, McLean CA. In situ detection of inflammatory mediators in post mortem human brain tissue after traumatic injury. J Neurotrauma 2010; 27(3): 497-507.
[http://dx.doi.org/10.1089/neu.2009.1120] [PMID: 20030565]
[53]
Ellis EF, McKinney JS, Willoughby KA, Liang S, Povlishock JT. A new model for rapid stretch-induced injury of cells in culture: Characterization of the model using astrocytes. J Neurotrauma 1995; 12(3): 325-39.
[http://dx.doi.org/10.1089/neu.1995.12.325] [PMID: 7473807]
[54]
Ishida Y, Kondo T, Takayasu T, Iwakura Y, Mukaida N. The essential involvement of cross-talk between IFN-γ and TGF-β in the skin wound-healing process. J Immunol 2004; 172(3): 1848-55.
[http://dx.doi.org/10.4049/jimmunol.172.3.1848] [PMID: 14734769]
[55]
Ashcroft GS, Jeong MJ, Ashworth JJ, et al. TNFα is a therapeutic target for impaired utaneous wound healing. Wound Repair Regen 2012; 20(1): 38-49.
[http://dx.doi.org/10.1111/j.1524-475X.2011.00748.x] [PMID: 22151742]
[56]
Shelke GV, Jagtap JC, Kim DK, et al. TNF-α and IFN-γ together up-regulates Par-4 expression and induce apoptosis in human neuroblastomas. Biomedicines 2017; 6(1): 4.
[http://dx.doi.org/10.3390/biomedicines6010004] [PMID: 29278364]
[57]
Nemetchek MD, Stierle AA, Stierle DB, Lurie DI. The Ayurvedic plant Bacopa monnieri inhibits inflammatory pathways in the brain. J Ethnopharmacol 2017; 197: 92-100.
[http://dx.doi.org/10.1016/j.jep.2016.07.073] [PMID: 27473605]
[58]
Kongkeaw C, Dilokthornsakul P, Thanarangsarit P, Limpeanchob N, Norman Scholfield C. Meta-analysis of randomized controlled trials on cognitive effects of Bacopa monnieri extract. J Ethnopharmacol 2014; 151(1): 528-35.
[http://dx.doi.org/10.1016/j.jep.2013.11.008] [PMID: 24252493]

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