Parquetina nigrescens and Spondias mombin protects against neurochemical alterations in the scopolamine model of cognitive dysfunction
Corresponding Author
Ayokunle O. Ademosun
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Correspondence
Ayokunle O. Ademosun, Department of Biochemistry, School of Sciences, Federal University of Technology, P.M.B. 704, Akure, Nigeria.
Email: [email protected]
Search for more papers by this authorTemitope V. Popoola
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Search for more papers by this authorGaniyu Oboh
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Contribution: Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Software, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorOlamide W. Fasakin
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Contribution: Investigation, Methodology, Resources, Software, Writing - review & editing
Search for more papers by this authorCorresponding Author
Ayokunle O. Ademosun
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Correspondence
Ayokunle O. Ademosun, Department of Biochemistry, School of Sciences, Federal University of Technology, P.M.B. 704, Akure, Nigeria.
Email: [email protected]
Search for more papers by this authorTemitope V. Popoola
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Search for more papers by this authorGaniyu Oboh
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Contribution: Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Software, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorOlamide W. Fasakin
Department of Biochemistry, School of Sciences, Federal University of Technology, Akure, Nigeria
Contribution: Investigation, Methodology, Resources, Software, Writing - review & editing
Search for more papers by this authorAbstract
Natural plants which are effective in Alzheimer's disease (AD) management are of pharmacological importance, though there is little or no scientific proof for most of their claims. This study sought to evaluate the effect of Hog plum (Spondias mombin) and Ogbo (Parquetina nigrescens) leaves extracts on antioxidant levels and activities of key enzymes linked to cognitive function in scopolamine-induced cognitive dysfunctioned rats. Rats were pretreated with S. mombin (SM) and P. nigrescens (PN) leaves extracts (50 and 100 mg/kg), donepezil (5 mg/kg) for 2 weeks via oral administration before induction of memory impairment via single i.p. administration of scopolamine (3 mg/kg body weight). Experimental rats were subjected to behavioral tests to check for cognitive performance before experiment termination. The activities of hippocampal key enzymes linked to cognitive function were determined. Results showed that pretreatment with SM and PN prevented the cognitive impairment induced by scopolamine. Furthermore, increased cholinesterases, adenosine deaminase (ADA), ATP hydrolysis, monoamine oxidase (MAO), and arginase activities induced by scopolamine were significantly reduced in rats treated with SM and PN leaves extract. Additionally, elevated malondialdehyde (MDA) and reactive oxygen species (ROS) levels observed in scopolamine-induced rats were reduced significantly in SM- and PN- pretreated rats. Decreased AMP hydrolysis, and nitric oxide and antioxidant level induced by scopolamine were prevented in pretreated rats. This study concluded that SM and PN leave extract effectiveness in cognitive management may be due to their high antioxidant activities and neuromodulatory effects on key enzymes linked to AD.
Practical applications
The use of natural products in the treatment and management of neurodegenerative diseases in Africa is becoming pertinent as the continent is blessed with medicinal plants while the price of synthetic drugs has been observed to be an economic burden on the continent. Parquetina nigrescens and Spondias mombin are examples of such medicinal plants that have been explored in folklore for the management of neurodegenerative diseases but there is a dearth of scientific validation for their use while there is no present data to evaluate possible mechanisms of action employed by these medicinal plants to mediate the therapeutic potential observed in folklore. Therefore, the present study seeks to validate the therapeutic use of P. nigrescens and S. mombin as observed in folklore as well as explore the possible mechanism of actions the plants may employ in mediating the proposed therapeutic potentials in neurodegenerative disease conditions while considering its toxicological effects in experimental animals.
CONFLICT OF INTEREST
The authors of the present study currently have no conflict of interest to declare.
Open Research
DATA AVAILABILITY STATEMENT
None.
REFERENCES
- Ademiluyi, A. O., Ogunsuyi, O. B., Oboh, G., & Agbebi, O. J. (2016). Jimson weed (Datura stramonium). Comparative Clinical Pathology, 25(4), 733–741.
10.1007/s00580-016-2257-6 Google Scholar
- Ademosun, A. O., Adebayo, A. A., Popoola, T. V., & Oboh, G. (2020). Shaddock (Citrus maxima) peels extract restores cognitive function, cholinergic and purinergic enzyme systems in scopolamine-induced amnesic rats. Drug and Chemical Toxicology, 45(3), 1073–1080.
- Adeniyi, P. A., Omatsuli, E. P., Akinyemi, A. J., & Ishola, A. O. (2016). Caffeine plus nicotine improves motor function, spatial and non-spatial working memory and functional indices in BALB/c male mice. Pathophysiology, 23(4), 251–258.
- Ajayi, L. O., Ayeleso, A. O., & Oyedepo, T. A. (2021). Protective effect of hydroethanolic leaf extract of Parquetina nigrescens against d-galactose-induced neurotoxicity in male Wistar rats. Chemical Biology Letters, 8(2), 79–87.
- Akinmoladun, A. C., Adelabu, A. A., Saliu, I. O., Adetuyi, A. R., & Olaleye, M. T. (2021). Protective properties of Spondias mombin Linn leaves on redox status, cholinergic dysfunction and electrolyte disturbance in cyanide-intoxicated rats. Science Progress, 104, 1–17.
10.1177/00368504211011866 Google Scholar
- Akinyemi, A. J., Oboh, G., Oyeleye, S. I., & Ogunsuyi, O. (2017). Antiamnestic effect of curcumin in combination with donepezil, an anticholinesterase drug: Involvement of cholinergic system. Neurotoxicity Research, 31, 560–569.
- Akinyemi, A. J., Okonkwo, P. K., Faboya, O. A., Onikanni, S. A., Fadaka, A., Olayide, I., Akinyemi, E. O., & Oboh, G. (2017). Curcumin improves episodic memory in cadmium induced memory impairment through inhibition of acetylcholinesterase and adenosine deaminase activities in a rat model. Metabolic Brain Disease, 32(1), 87–95.
- Akinyemi, A. J., Throme, G. R., Morsch, V. M., Stefanello, N., da Costa, P., Cardos, A., & Schetinger, M. R. C. (2016). Effect of dietary supplementation of ginger and turmeric rhizomes on ectonucleosidase, adenosine deminase and acetylcholineesterase in synaptosomes from the cerebral cortex of hypertensive rats. Journal of Applied Biomedicine, 14, 59–70.
- Alison, Y., Lynn, R., & David, J. B. (2011). The interplay of cholinergic function, attention, and falls in Parkinson's disease. Movement Disorders, 26, 2496–2503.
- Asuquo, O. R., Udonwa, U. N., Eluwa, M. A., & Ekanem, T. B. (2013). Effects of Spondias mombin leaf extract on the cytoarchitecture of the cerebal cortex and on learning and memory in Wistar rats. International Journal of Science and Research, 2, 5–8.
- Barai, P., Raval, N., Acharya, S., & Acharya, N. (2018). Bergenia ciliata ameliorates streptozotocin- induced spatial memory deficits through dual cholinesterase inhibition and attenuation of oxidative stress in rats. Biomedicine & Pharmacotherapy, 102, 966–980.
- Bono, M. R., Fernández, D., Flores-Santibáñez, F., Rosemblatt, M., & Sauma, D. (2015). CD73 and CD39 ectonucleotidases in T cell differentiation: Beyond immunosuppression. FEBS Letters, 589(22), 3454–3460.
- Broadbent, N. J., Squire, L. R., & Clark, R. E. (2004). Spatial memory, recognition memory, and the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 101, 14515–14520.
- Burnstock, G. (2017). Purinergic signalling and neurological diseases: An update. CNS & Neurological Disorders - Drug Targets, 16, 257–265.
- Burnstock, G., Fredholm, B. B., & Verkhratsky, A. (2011). Adenosine and ATP receptors in the brain. Current Topics in Medicinal Chemistry, 11, 973–1011.
- Caldwell, R. W., Rodriguez, P. C., Toque, H. A., Narayanan, S. P., & Caldwell, R. B. (2018). Arginase: A multifaceted enzyme important in health and disease. Physiological Reviews, 98, 641–656.
- Cieślak, M., & Komoszyński, M. (2011). The role of ecto-purines in inflammation leading to demyelination—New means for therapies against multiple sclerosis. Neurologia i Neurochirurgia Polska, 45(5), 489–499.
- Clairborne, A. (1995). Catalase activity. In A. R. Greewald (Ed.), Handbook of methods for oxygen radical research (pp. 237–242). CRC Press.
- da Silva, T. S., Soares, A. A., Rocha, T. M., Pimenta, A. T., Miron, D., Silva, R. J., Viana, G. S. B., & Leal, L. K. K. (2020). Spondias mombin: Quality control and anti-inflammatory activity in human neutrophils. Journal of Herbal Medicine, 24(100), 393.
- Davey, M. W., Stals, E., Panis, B., Keulemans, J., & Swennen, R. L. (2005). High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry, 347, 201–207.
- Ellman, G. L., Courtney, K. D., Andres, V., Jr., & Featherstone, R. M. (1961). A new and rapid cholimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7, 88–95.
- Ellman, G. L. (1959). Tissue sulfhydryl groups. Arch Biochem Biophys, 82, 70–77.
- Elufioye, T. O., Obuotor, E. M., Agbedahunsi, J. M., & Adesanya, S. A. (2017). Anticholinesterase constituents from the leaves of Spondias mombin L. (Anacardiaceae). Dovepress Biologics, Targets and Therapy, 11, 107–114.
- Femi-olabisi, F. J., Faokunla, O., Agboola, A. O., & Olorunyolemi, I. M. (2020). Biochemical and toxicological evaluations of aqueous extract of Parquetina nigrescens (Afzel.) leaves on mifepristone-induced polycystic ovarian syndrome in rats. Journal of Drug Delivery and Therapeutics, 10, 94–10.
10.22270/jddt.v10i2-s.3956 Google Scholar
- Gautam, A., Wadhwa, R., & Thakur, M. K. (2016). Assessment of cholinergic properties of ashwagandha leaf-extract in the amnesic mouse brain. Annals of Neurosciences, 23, 68–75.
- Green, A. L., & Haughton, T. M. (1961). Colorimetric method for the estimation of monoamine oxidase. Biochemical Journal, 78, 172–175.
- Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S., & Tannenbaum, S. R. (1982). Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Analytical Biochemistry, 126, 131–138.
- Guisti, G., & Galanti, B. (1984). Colorimetric method. In H. U. Bergmeyer (Ed.), Methods of enzymatic analysis (pp. 315–323). Chemie Weinheim: Verlag.
- Hashimoto, T., Hatayama, Y., Nakamichi, K., & Yoshida, N. (2014). Procognitive effect of AC-3933 in aged mice, and synergistic effect of combination with donepezil in scopolamine-treated mice. European Journal of Pharmacology, 745, 123–128.
- Hayashi-Park, E., Ozment, B. N., Griffith, C. M., Zhang, H., Patrylo, P. R., & Rose, G. M. (2017). Experimentally induced diabetes worsens neuropathology, but not learning and memory, in middle aged 3xTg mice. Behavioural Brain Research, 322, 280–287.
- Hayashi, I., Morishita, Y., Imai, K., Nakamura, M., Nakachi, K., & Hayashi, T. (2007). High-throughput spectrophotometric assay of reactive oxygen species in serum. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 631, 55–61.
- Heymann, D., Reddington, M., & Kreutzberg, G. W. (1984). Subcellular localization of 5′-nucleotidase in rat brain. Journal of Neurochemistry, 43, 971–978.
- Ishola, I. O., Ikuomola, B. O., & Adeyemi, O. O. (2018). Protective role of Spondias mombin leaf and Cola acuminata seed extracts against scopolamine-induced cognitive dysfunction. Alexandria Journal of Medicine, 54, 27–39.
- Kamat, P. K. (2011). Mitochondrial dysfunction: A crucial event in okadaic acid (ICV) induced memory impairment and apoptotic cell death in rat brain. Pharmacology, Biochemistry, and Behavior, 100, 311–319.
- Kayode, O. T., & Yakubu, M. T. (2017). Parquetina nigrescens leaves: Chemical profile and influence on the physical and biochemical indices of sexual activity of male Wistar rats. Journal of Integrative Medicine, 15, 64–76.
- Kaysen, G. A., & Strecker, H. J. (1973). Increased arginase activity levels caused by nitric oxide synthase dysfunction. The New England Journal of Medicine, 323, 1234–1238.
- Khakh, B. S., & North, R. A. (2012). Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron, 76, 51–69.
- Kutryb-Zajac, B., Mierzejewska, P., Slominska, E. M., & Smolenski, R. T. (2020). Therapeutic perspectives of adenosine deaminase inhibition in cardiovascular diseases. Molecules, 25(20), 4652.
- Liu, W., Rabinovich, A., Nash, Y., Frenkel, D., Wang, Y., Youdim, M. B., & Weinreb, O. (2017). Anti-inflammatory and protective effects of MT-031, a novel multitarget MAO-A and AChE/BuChE inhibitor in scopolamine mouse model and inflammatory cells. Neuropharmacology, 113, 445–456.
- Liu, Z., Zhou, T., Ziegler, A. C., Dimitrion, P., & Zuo, L. (2017). Oxidative stress in neurodegenerative diseases: From molecular mechanisms to clinical applications. Oxidative Medicine and Cellular Longevity, 2017, 1–11.
- Lobo, V., Patil, A., Phatak, A., & Chandra, N. (2010). Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy Reviews, 4, 118–126.
- Mahmud, B., Shehu, A., & Magaji, M. G. (2020). Ameliorative effect of methanol stem extract of Parquetina nigrescens (Afzel) bullock on scopolamine-induced sub-chronic cognitive deficit in mice. Journal of Basic and Clinical Physiology and Pharmacology, 31, 1–9.
10.1515/jbcpp-2019-0201 Google Scholar
- Marucci, G., Buccioni, M., Dal Ben, D., Lambertucci, C., Volpini, R., & Amenta, F. (2021). Efficacy of acetylcholinesterase inhibitors in Alzheimer's disease. Neuropharmacology, 190, 1–15.
- Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry, 247, 3170–3175.
- Nworu, C. S., Akah, P. A., Okoye, F. B. C., Toukam, D. K., Udeh, J., & Esimone, C. O. (2011). The leaf extract of Spondias mombin L. displays an anti-inflammatory effect and suppresses inducible formation of tumor necrosis factor-α and nitric oxide (NO). Journal of Immunotoxicology, 8, 10–16.
- Oboh, G., Adebayo, A. A., Ademosun, A. O., & Olowookere, O. G. (2019). Rutin alleviates cadmium-induced neurotoxicity in Wistar rats: Involvement of modulation of nucleotide-degrading enzymes and monoamine oxidase. Metabolic Brain Disease, 34(4), 1181–1190.
- Oboh, G., Adebayo, A. A., Ademosun, A. O., & Olowookere, O. G. (2020). Rutin restores neurobehavioral deficits via alterations in cadmium bioavailability in the brain of rats exposed to cadmium. Neurotoxicology, 77, 12–19.
- Oboh, G., Nwanna, E. E., Oyeleye, S. I., Olasehinde, T. A., Ogunsuyi, O. B., & Boligon, A. A. (2016). In vitro neuroprotective potentials of aqueous and methanol extracts from Heinsia crinita leaves. Food Science and Human Wellness, 5, 95–102.
10.1016/j.fshw.2016.03.001 Google Scholar
- Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Analytical Biochemistry, 95, 351–358.
- Owoyele, B. V., Nafiu, A. B., Oyewole, I. A., Oyewole, L. A., & Soladoye, V. (2009). Studies on the analgesic, anti-inflammatory and antipyretic effects of Parquetina nigrescens leaf extract. Journal of Ethnopharmacology, 122, 86–90.
- Robson, S., Sevigny, J., & Zimmermann, H. (2006). The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signalling, 2, 409–430.
- Schetinger, M. R. C., Porto, N. M., Moretto, M. B., Morsch, V. M., da Rocha, J. B. T., Vieira, V., Moro, F., Neis, R. T., Bittencourt, S., Bonacorso, H. G., & Zanatta, N. (2000). New benzodiazepines alter acetylcholinesterase and ATPDase activities. Neurochemical Research, 25, 949–955.
- Schliebs, R., & Arendt, T. (2006). The significance of the cholinergic system in the brain during aging and in Alzheimer's disease. Journal of Neural Transmission, 113, 1625–1164.
- Sinan, K. I., Zengin, G., Zheleva-Dimitrova, D., Gevrenova, R., Picot-Allain, M. C. N., Dall'Acqua, S., Behl, T., Goh, B. H., Ying, P. T. S., & Mahomoodally, M. F. (2021). Exploring the chemical profiles and biological values of two Spondias species (S. dulcis and S. mombin): Valuable sources of bioactive natural products. Antioxidants, 10, 1771.
- Sies, H., & Jones, D. P. (2020). Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nature Reviews Molecular Cell Biology, 21(7), 363–383.
- Sperlágh, B., & Sylvester Vizi, E. (2011). The role of extracellular adenosine in chemical neurotransmission in the hippocampus and basal ganglia: Pharmacological and clinical aspects. Current Topics in Medicinal Chemistry, 11(8), 1034–1046.
- Suresh, K., Surender, P., Yogesh, K. W., Aditya, K., & Parul, S. (2015). Therapeutic potential of medicinal plants. Journal Biological Chemistry Chron, 1, 46–54.
- Tang, Y., & Zhong, Z. (2014). Obtusifolin treatment improves hyperlipidemia and hyperglycemia: Possible mechanism involving oxidative stress. Cell Biochemistry and Biophysics, 70(3), 1751–1757.
- Tolossa, K., Debela, E., Athanasiadou, S., Tolera, A., Ganga, G., & Houdijk, J. G. (2013). Ethno-medicinal study of plants used for treatment of human and livestock ailments by traditional healers in South Omo, Southern Ethiopia. Journal of Ethnobiology and Ethnomedicine, 9(1), 1–15.
- Tripathi, S., & Mazumder, P. M. (2021). Neuroprotective efficacy of apple cider vinegar on zinc-high fat diet-induced mono amine oxidase alteration in murine model of AD. Journal of the American College of Nutrition, 1–10. https://doi.org/10.1080/07315724.2021.1948933
- Van Spronsen, M., & Hoogenraad, C. C. (2010). Synapse pathology in psychiatric and neurologic disease. Current Neurology and Neuroscience Reports, 10(3), 207–214.
- Verkhratsky, A., & Burnstock, G. (2014). Biology of purinergic signalling: Its ancient evolutionary roots, its omnipresence and its multiple functional significance. Bioessays, 36(7), 697–705.
- Zhang, L., Plotkin, R. C., Wang, G., Sandel, M. E., & Lee, S. (2004). Cholinergic augmentation with donepezil enhances recovery in short-term memory and sustained attention after traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 7, 1050–1055.