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Research Article

Neuroprotective Effect of Boswellia serrata against 3-NP Induced Experimental Huntington’s Disease

Author(s): Vinay Kumar, Chanchal Sharma, Mohamad Taleuzzaman*, Kandasamy Nagarajan, Anzarul Haque, Mamta Bhatia, Sumayya Khan, Mohamad Ayman Salkini and Pankaj Bhatt

Volume 20, Issue 6, 2024

Published on: 18 January, 2024

Article ID: e180124225809 Pages: 14

DOI: 10.2174/0115734072272233231119161319

Price: $65

Abstract

Objectives: The study aimed to assess the neuroprotective effect of Boswellia serrata against 3-NP-induced experimental Huntington’s disease.

Background: Previous studies have shown Boswellia to have sedative, analgesic, and anti-tumour effects. Boswellia serrata yields four pentacyclic triterpene acids and boswellic acid, a bioactive substance that prevents leukotriene biogenesis.

Methods: The potential neuroprotective effect of Boswellia serrata against 3-nitro propionic acid (3-NP)-induced Huntington's disease (HD) was examined at oral doses of 45 mg/kg, 90 mg/kg, and 180 mg/kg. In this study, HD was induced by 3-NP at a dose of 10 mg/kg in Wistar rats. The study used 56 Wistar rats (8 per group) for biochemical (inflammatory markers, acetylcholinesterase activity) and behavioural (elevated plus maze, Y-maze, open-field, tail suspension tests, etc.) assessments. Additionally, a histological examination of the brain was carried out. In addition, the analysis of Boswellia serrata extract was performed by different analytical techniques, like UV spectrophotometer, FTIR, and HPLC methods.

Results: In the brain, succinate dehydrogenase is a mitochondrial enzyme irreversibly inhibited by 3-NP. Administration of 3-NP resulted in HD with altered behavioural and motor changes in rats. Treatment with Boswellia serrata resulted in remarkable protection of rats against 3-NP-induced behaviour and motor deficits in a dose-dependent manner. Moreover, in rats administered with 3-NP, Boswellia serrata improved memory performance and lowered levels of inflammatory biomarkers. These results have also been supported by histopathological analysis. Acetyl-11-keto-p-boswellic acid was found to be the main active component of Boswellia serrata extract.

Conclusion: Boswellia serrata at a dose of 180 mg/kg exhibited better protection compared to the other doses against HD induced by 3-NP. More detailed studies based on molecular targets are needed for the Boswellia serrata to transition from the bench to the bedside for use as an adjuvant in HD patients.

Keywords: Analytical characterization, behavioural parameters, Boswellia serrata, 3-nitropropionic acid, Huntington’s disease, inflammatory markers.

Graphical Abstract

[1]
Malik, J.; Choudhary, S.; Kumar, P. Plants and phytochemicals for Huntington's disease. Pharmacogn. Rev., 2013, 7(14), 81-91.
[http://dx.doi.org/10.4103/0973-7847.120505] [PMID: 24347915]
[2]
Roos, R.A.C. Huntington’s disease: A clinical review. Orphanet J. Rare Dis., 2010, 5(1), 40.
[http://dx.doi.org/10.1186/1750-1172-5-40] [PMID: 21171977]
[3]
Ajitkumar, A.; De Jesus, O. Huntington Disease. In: In: StatPearls; Stat Pearls Publishing: Treasure Island, 2022.
[4]
Mukherjee, A.; Hussain, Z.; Ganguly, G.; Joardar, A.; Roy, S.; Guin, D.; Sinharoy, U.; Biswas, A.; Das, S. Clinical profile of genetically proven huntington’s disease patients from Eastern India. Ann. Indian Acad. Neurol., 2020, 23(2), 195-200.
[http://dx.doi.org/10.4103/aian.AIAN_505_19] [PMID: 32189861]
[5]
Hong, J.C.; Liu, Y.; Liu, Y.; Zhao, L. High school students’ online learning ineffectiveness in experimental courses during the COVID-19 Pandemic. Front. Psychol., 2021, 12, 738695.
[http://dx.doi.org/10.3389/fpsyg.2021.738695]
[6]
Finkbeiner, S. Huntington’s Disease. Cold Spring Harb. Perspect. Biol., 2011, 3(6), a007476.
[http://dx.doi.org/10.1101/cshperspect.a007476] [PMID: 21441583]
[7]
Agrawal, M.; Biswas, A. Molecular diagnostics of neurodegenerative disorders. Front. Mol. Biosci., 2015, 54.
[http://dx.doi.org/10.3389/fmolb.2015.00054]
[8]
Shacham, T.; Sharma, N.; Lederkremer, G.Z. Protein Misfolding and ER Stress in Huntington’s Disease. Front. Mol. Biosci., 2019, 6, 20.
[http://dx.doi.org/10.3389/fmolb.2019.00020] [PMID: 31001537]
[9]
Guo, C.; Sun, L.; Chen, X.; Zhang, D. Oxidative stress, mitochondrial damage and neurodegenerative diseases. Neural Regen. Res., 2013, 8(21), 2003-2014.
[http://dx.doi.org/10.3969/j.issn.1673-5374.2013.21.009] [PMID: 25206509]
[10]
Brouillet, E.; Jenkins, B.G.; Hyman, B.T.; Ferrante, R.J.; Kowall, N.W.; Srivastava, R.; Roy, D.S.; Rosen, B.R.; Beal, M.F. Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J. Neurochem., 1993, 60(1), 356-359.
[http://dx.doi.org/10.1111/j.1471-4159.1993.tb05859.x] [PMID: 8417157]
[11]
Kumar, P.; Kumar, A. Prolonged pretreatment with carvedilol prevents 3-nitropropionic acid-induced behavioral alterations and oxidative stress in rats. Pharmacol. Rep., 2008, 60(5), 706-715.
[PMID: 19066418]
[12]
Gupta, S.; Sharma, B. Protective effects of phosphodiesterase-1 (PDE1) and ATP sensitive potassium (KATP) channel modulators against 3-nitropropionic acid induced behavioral and biochemical toxicities in experimental Huntington's disease. Eur. J. Pharmacol., 2014, 732, 111-122.
[http://dx.doi.org/10.1016/j.ejphar.2014.03.032] [PMID: 24690258]
[13]
Jurcau, A.; Jurcau, M.C. Therapeutic strategies in huntington’s disease: From genetic defect to gene therapy. Biomedicines, 2022, 10(8), 1895.
[http://dx.doi.org/10.3390/biomedicines10081895] [PMID: 36009443]
[14]
Kenney, C.; Jankovic, J. Tetrabenazine in the treatment of hyperkinetic movement disorders. Expert Rev. Neurother., 2006, 6(1), 7-17.
[http://dx.doi.org/10.1586/14737175.6.1.7] [PMID: 16466307]
[15]
Yero, T.; Rey, J.A. Tetrabenazine (Xenazine), An FDA-approved treatment option for huntington’s disease-related chorea. P&T, 2008, 33(12), 690-694.
[PMID: 19750050]
[16]
Kumar, G.P.; Khanum, F. Neuroprotective potential of phytochemicals. Pharmacogn. Rev., 2012, 6(12), 81-90.
[http://dx.doi.org/10.4103/0973-7847.99898] [PMID: 23055633]
[17]
Hassan, S.S.U.; Samanta, S.; Dash, R.; Karpinski, T.M.; Habibi, E.; Sadiq, A.; Ahmadi, A.; Bunagu, S. The neuroprotective effects of fisetin, a natural flavonoid in neurodegenerative diseases: Focus on the role of oxidative stress. Front. Pharmacol., 2022, 13, 1015835.
[http://dx.doi.org/10.3389/fphar.2022.1015835]
[18]
Yu, G.; Xiang, W.; Zhang, T.; Zeng, L.; Yang, K.; Li, J. Effectiveness of Boswellia and Boswellia extract for osteoarthritis patients: A systematic review and meta-analysis. BMC Complement Med Ther, 2020, 20(1), 255.
[http://dx.doi.org/10.1186/s12906-020-02985-6]
[19]
Chacko, K.M.; Bhat, B.; Khandal, R.K.; Sultana, S.; Kuruvilla, B.T.; Singh, P.; Aggarwal, M.L. A-90 day gavage safety assessment of Boswellia serrata in rats. Toxicol. Int., 2012, 19(3), 273-278.
[http://dx.doi.org/10.4103/0971-6580.103668] [PMID: 23293466]
[20]
Xu, C.; Wang, B.; Pu, Y.; Tao, J.; Zhang, T. Techniques for the analysis of pentacyclic triterpenoids in medicinal plants. J. Sep. Sci., 2018, 41(1), 6-19.
[http://dx.doi.org/10.1002/jssc.201700201] [PMID: 28862795]
[21]
Mannino, G.; Occhipinti, A.; Maffei, M. Quantitative Determination of 3-O-Acetyl-11-Keto-βBoswellic Acid (AKBA) and other boswellic acids in Boswellia sacra flueck (syn. B. carteri Birdw) and boswellia serrata roxb. Molecules, 2016, 21(10), 1329.
[http://dx.doi.org/10.3390/molecules21101329] [PMID: 27782055]
[22]
Kumar, R.; Kumar, R.; Singh, S.; Saksena, A.K.; Pal, R.; Jaiswal, R. Effect of Boswellia serrata extract on acute inflammatory parameters and tumor necrosis factor-α in complete Freund’s adjuvant-induced animal model of rheumatoid arthritis. Int. J. Appl. Basic Med. Res., 2019, 9(2), 100-106.
[http://dx.doi.org/10.4103/ijabmr.IJABMR_248_18] [PMID: 31041173]
[23]
Roy, N.K.; Parama, D.; Banik, K.; Bordoloi, D.; Devi, A.K.; Thakur, K.K.; Padmavathi, G.; Shakibaei, M.; Fan, L.; Sethi, G.; Kunnumakkara, A.B. An update on pharmacological potential of boswellic acids against chronic diseases. Int. J. Mol. Sci., 2019, 20(17), 4101.
[http://dx.doi.org/10.3390/ijms20174101] [PMID: 31443458]
[24]
Catanzaro, D.; Rancan, S.; Orso, G.; Acqua, S.D.; Brun, P.; Giron, M.C.; Carrara, M.; Castagliuolo, L.; Ragazzi, E.; Caparrotta, L.; Montopoli, M. Boswellia serrata preserves intestinal epithelial barrier from oxidative and inflammatory damage. PLoS One, 2015, 10(5), e0125375.
[http://dx.doi.org/10.1371/journal.pone.0125375]
[25]
Iram, F.; Khan, S.A.; Husain, A. Phytochemistry and potential therapeutic actions of Boswellic acids: A mini-review. Asian Pac. J. Trop. Biomed., 2017, 7(6), 513-523.
[http://dx.doi.org/10.1016/j.apjtb.2017.05.001]
[26]
Gomaa, A.A.; Farghaly, H.A.; Abdel-Wadood, Y.A.; Gomaa, G.A. Potential therapeutic effects of boswellic acids/Boswellia serrata extract in the prevention and therapy of type 2 diabetes and Alzheimer’s disease. Naunyn Schmiedebergs Arch. Pharmacol., 2021, 394(11), 2167-2185.
[http://dx.doi.org/10.1007/s00210-021-02154-7] [PMID: 34542667]
[27]
Mabasa, X.E.; Mathomu, L.M.; Madala, N.E.; Musie, E.M. Sigidi, MT Molecular spectroscopic (FTIR and UV-Vis) and hyphenated chromatographic (UHPLC-qTOF-MS) analysis and in vitro bioactivities of the Momordica balsamina leaf extract. Biochem. Res. Int., 2021, 2854217.
[http://dx.doi.org/10.1155/2021/2854217]
[28]
Boulekbache-Makhlouf, L.; Meudec, E.; Mazauric, J.P.; Madani, K.; Cheynier, V. Qualitative and semi-quantitative analysis of phenolics in Eucalyptus globulus leaves by high-performance liquid chromatography coupled with diode array detection and electrospray ionisation mass spectrometry. Phytochem. Anal., 2013, 24(2), 162-170.
[http://dx.doi.org/10.1002/pca.2396] [PMID: 22930658]
[29]
Tariq, M.; Khan, H.A.; Elfaki, I.; Deeb, S.A.; Moutaery, K.A. Neuroprotective effect of nicotine against 3-nitropropionic acid (3-NP)-induced experimental Huntington’s disease in rats. Brain Res. Bull., 2005, 67(1-2), 161-168.
[http://dx.doi.org/10.1016/j.brainresbull.2005.06.024] [PMID: 16140176]
[30]
El-Sahar, A.E.; Rastanawi, A.A.; El-Yamany, M.F.; Saad, M.A. Dapagliflozin improves behavioral dysfunction of Huntington’s disease in rats via inhibiting apoptosis-related glycolysis. Life Sci., 2020, 257, 118076.
[http://dx.doi.org/10.1016/j.lfs.2020.118076] [PMID: 32659371]
[31]
Bortolatto, C.F.; Jesse, C.R.; Wilhelm, E.A.; Chagas, P.M.; Nogueira, C.W. Organoselenium bis selenide attenuates 3-nitropropionic acid-induced neurotoxicity in rats. Neurotox. Res., 2013, 23(3), 214-224.
[http://dx.doi.org/10.1007/s12640-012-9336-5] [PMID: 22739838]
[32]
Wexler, P.; Anderson, B.D.; Gad, S.C.; Hakkinen, P.B.; Kamrin, M. Encyclopedia of toxicology; Shugart, A., Ed.; Academic Press, 2005, p. 1.
[33]
Shadfar, S.; Khanal, S.; Bohara, G.; Kim, G.; Sadigh-Eteghad, S.; Ghavami, S.; Choi, H.; Choi, D.Y. Methanolic extract of boswellia serrata gum protects the nigral dopaminergic neurons from rotenone-induced neurotoxicity. Mol. Neurobiol., 2022, 59(9), 5874-5890.
[http://dx.doi.org/10.1007/s12035-022-02943-y] [PMID: 35804280]
[34]
Mason, L.H.; Harp, J.P.; Han, D.Y. Pb neurotoxicity: neuropsychological effects of lead toxicity. BioMed Res. Int., 2014, 2014, 1-8.
[http://dx.doi.org/10.1155/2014/840547] [PMID: 24516855]
[35]
Khafaga, A.F.; El-Kazaz, S.E.; Noreldin, A.E. Boswellia serrata suppress fipronil-induced neuronal necrosis and neurobehavioral alterations via promoted inhibition of oxidative/inflammatory/] apoptotic pathways. Sci. Total Environ., 2021, 785, 147384.
[http://dx.doi.org/10.1016/j.scitotenv.2021.147384] [PMID: 33933775]
[36]
Khalaj-Kondori, M.; Sadeghi, F. Published, 1578, 2016(Nov), 17.
[http://dx.doi.org/10.3906/sag-1503-43] [PMID: 27966331]
[37]
Frank-Cannon, T.C.; Alto, L.T.; McAlpine, F.E.; Tansey, M.G. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol. Neurodegener., 2009, 47.
[http://dx.doi.org/10.1186/1750-1326-4-47]
[38]
Khan, A.; Jamwal, S.; Bijjem, K.R.V.; Prakash, A.; Kumar, P. Neuroprotective effect of hemeoxygenase-1/glycogen synthase kinase-3β modulators in 3-nitropropionic acid-induced neurotoxicity in rats. Neuroscience, 2015, 287, 66-77.
[http://dx.doi.org/10.1016/j.neuroscience.2014.12.018] [PMID: 25536048]
[39]
Wang, W.Y.; Tan, M.S.; Yu, J.T.; Tan, L. Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann. Transl. Med., 2015, 3(10), 136.
[http://dx.doi.org/10.3978/j.issn.2305-5839.2015.03.49] [PMID: 26207229]
[40]
Shawki, S.M.; Saad, M.A.; Rahmo, R.M.; Wadie, W.; El-Abhar, H.S. Liraglutide improves cognitive and neuronal function in 3-NP rat model of huntington’s disease. Front. Pharmacol., 2021, 12, 731483.
[http://dx.doi.org/10.3389/fphar.2021.731483] [PMID: 35002691]
[41]
Gomaa, A.A.; Farghaly, H.S.M.; El-Sers, D.A.; Farrag, M.M.; Al-Zokeim, N.I. Inhibition of adiposity and related metabolic disturbances by polyphenol-rich extract of Boswellia serrata gum through alteration of adipo/cytokine profiles. Inflammopharmacology, 2019, 27(3), 549-559.
[http://dx.doi.org/10.1007/s10787-018-0519-4] [PMID: 30069718]
[42]
Umar, S.; Umar, K.; Sarwar, A.H.M.G.; Khan, A.; Ahmad, N.; Ahmad, S.; Katiyar, C.K.; Husain, S.A.; Khan, H.A. Boswellia serrata extract attenuates inflammatory mediators and oxidative stress in collagen induced arthritis. Phytomedicine, 2014, 21(6), 847-856.
[http://dx.doi.org/10.1016/j.phymed.2014.02.001] [PMID: 24667331]
[43]
Túnez, I.; Tasset, I.; Pérez-De La Cruz, V.; Santamaría, A. 3-Nitropropionic acid as a tool to study the mechanisms involved in Huntington’s disease: past, present and future. Molecules, 2010, 15(2), 878-916.
[http://dx.doi.org/10.3390/molecules15020878] [PMID: 20335954]
[44]
Kumar, P.; Kalonia, H.; Kumar, A. Expression of Concern: Role of LOX/COX pathways in 3-nitropropionic acid-induced Huntington’s Disease-like symptoms in rats: protective effect of licofelone. Br. J. Pharmacol., 2011, 164(2b), 644-654.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01418.x] [PMID: 21486276]
[45]
Solesio, M.E.; Saez-Atienzar, S.; Jordan, J.; Galindo, M.F. 3-Nitropropionic acid induces autophagy by forming mitochondrial permeability transition pores rather than activatiing the mitochondrial fission pathway. Br. J. Pharmacol., 2013, 168(1), 63-75.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01994.x] [PMID: 22509855]
[46]
Assimopoulou, A.; Zlatanos, S.; Papageorgiou, V. Antioxidant activity of natural resins and bioactive triterpenes in oil substrates. Food Chem., 2005, 92(4), 721-727.
[http://dx.doi.org/10.1016/j.foodchem.2004.08.033]
[47]
Sadeghnia, H.R.; Arjmand, F.; Ghorbani, A. Neuroprotective effect of Boswellia serrata and its active constituent acetyl 11-keto-β-boswellic acid against oxygen-glucose-serum deprivation-induced cell injury. Acta Pol. Pharm., 2017, 74(3), 911-920.
[PMID: 29513961]

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