Host–parasite relationship modulates the effect of African mistletoe leaves on the cholinergic, monoaminergic and carbohydrate hydrolyzing enzymes in fruit fly
Abstract
Objectives
Mistletoe infests common plant trees of great medicinal values such as Moringa and Almond. According to folklore, mistletoe leaves have been found to have application as food and medicine in the alleviation of various degenerative diseases. Host–parasite relationship may possibly influence the phytochemical and biological activities of mistletoe leaves. Hence, we examined the polyphenol contents, antioxidant properties, α-amylase, α-glucosidase, acetylcholinesterase (AChE) and monoamine oxidase (MAO) inhibitory activities of African mistletoe leaves obtained from Moringa and Almond host plants in fruit fly in vitro.
Methods
The phenolic constituents of the leaves were evaluated using HPLC system. The antioxidant activities were determined through the ABTS, DPPH and OH free radicals scavenging properties, ferric (Fe3+) and malondialdehyde (MDA) reducing abilities and Fe2+ chelation. The inhibitory effects of the leaves aqueous extracts on α-amylase, α-glucosidase, AChE and MAO activities were also assessed.
Results
The HPLC characterization of the leaves revealed that host plants caused marked variation in their phenolic composition, however, Almond mistletoe leaves had significantly (p<0.05) greater amounts of phenolic constituents. Both Moringa and Almond mistletoe leaves reduced Fe3+ and MDA levels, scavenged free radicals, chelated Fe2+ and inhibited α-amylase, α-glucosidase, AChE and MAO activities with the Almond mistletoe leaves having significantly (p<0.05) higher antioxidant properties and enzyme inhibitory activities.
Conclusions
This present study indicated that host plants could positively modulate the phenolic profile of mistletoe leaves and this probably brought about the vivid noticeable changes in their antioxidant abilities, cholinergic, monoaminergic and carbohydrate hydrolyzing enzymes inhibitory activities.
Acknowledgments
Not applicable.
-
Research funding: None declared.
-
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Competing interests: Authors state no conflict of interest.
-
Informed consent: Not applicable.
-
Ethical approval: The local Institutional Review Board deemed the study exempt from review. The use of fruit fly as a model for research is exempted from regulations pertaining to ethical approvals and/or animal protection laws. However, the use of the fruit fly as a model organism is in compliance with the 3Rs protocol of the European Centre for the Validation of Alternative Methods on 3Rs – refinement, replacement and reduction.
References
1. Oyeniran, OH, Ademiluyi, AO, Oboh, G. Modulatory effects of moringa (Moringa oleifera L.) leaves infested with African mistletoe (Tapinanthus bangwensis L.) on the antioxidant, antidiabetic, and neurochemical indices in high sucrose diet-induced diabetic-like phenotype in fruit flies (Drosophila melanogaster M.). J Food Biochem 2021;45:e13318.10.1111/jfbc.13318Suche in Google Scholar
2. Ademiluyi, AO, Oboh, G. Antioxidant properties of methanolic extracts of mistletoes (Viscum album) from cocoa and cashew trees in Nigeria. Afr J Biotechnol 2008;7:3138–42.Suche in Google Scholar
3. Obatomi, DK, Bikomo, EO, Temple, VJ. Effect of African mistletoe extract on blood pressure in spontaneously hypertensive rat. J Pharm Biol 1996;34:124–7. https://doi.org/10.1076/phbi.34.2.124.13197.Suche in Google Scholar
4. Oboh, G, Omojokun, OS, Ademiluyi, AO. Drying methods alter angiotensin-I converting enzyme inhibitory activity, antioxidant properties, and phenolic constituents of African mistletoe (Loranthus bengwensis L) leaves. J Evid Based Complement Alternat Med 2016;21:260–70.10.1177/2156587215600560Suche in Google Scholar
5. Malami, MS, Mainasara, MM, Aliero, AA, Aliero, BL, Maishanu, HM. Phytochemical screening of African mistletoes Tapinanthus globiferus (A.Rich) Tieghem (loranthaceae) on some host species in Birnin-Kebbi, Nigeria. Elixir Biosci 2017;107:47019–23.Suche in Google Scholar
6. Ekhaise, FO, Ofoezie, VG, Enobakhare, DA. Antibacterial properties and preliminary phytochemical analysis of methanolic extract of mistletoe (Tapinanthus bangwensis). Bayero J Pure Appl Sci 2010;3:65–8.10.4314/bajopas.v3i2.63223Suche in Google Scholar
7. Oboh, G, Ademosun, AO, Ademiluyi, AO, Omojokun, OS, Nwanna, EE, Longe, KO. In vitro studies on the antioxidant property and inhibition of α-amylase, α-glucosidase and angiotensin I-converting enzyme by polyphenol-rich extracts from cocoa (Theobroma cacao) bean. Pathol Res Int 2014;2014:549287.10.1155/2014/549287Suche in Google Scholar
8. Ademiluyi, AO, Aladeselu, OH, Oboh, G, Boligon, AA. Drying alters the phenolic constituents, antioxidant properties, α-amylase and α-glucosidase inhibitory properties of Moringa (Moringa oleifera) leaf. Food Sci Nutr 2018;6:2123–33. https://doi.org/10.1002/fsn3.770.Suche in Google Scholar PubMed PubMed Central
9. Oyeniran, OH, Ademiluyi, AO, Oboh, G. Comparative study of the phenolic profile, antioxidant properties and inhibitory effects of Moringa (Moringa oleifera L.) and Almond (Terminalia catappa L.) leaves on acetylcholinesterase and monoamine oxidase activities in the head region of Fruit fly (Drosophila melanogaster Meigen) in vitro. J Food Biochem 2021;45:e13401.10.1111/jfbc.13401Suche in Google Scholar
10. Maher, PA, Schubert, DR. Metabolic links between diabetes and Alzheimer’s disease. Expert Rev Neurother 2009;9:617–30. https://doi.org/10.1586/ern.09.18.Suche in Google Scholar PubMed
11. Sabu, MC, Kuttan, R. Antidiabetic and antioxidant activity of Terminalia bellerica Roxb. Indian J Exp Biol 2009;47:270–5.Suche in Google Scholar
12. Palanuvej, C, Hokputsa, S, Tunsaringkarn, T, Ruangrungsi, N. In vitro glucose entrapment and alpha-glucosidase inhibition of mucilaginous substances from selected Thai medicinal plants. Sci Pharm 2009;77:837–49. https://doi.org/10.3797/scipharm.0907-17.Suche in Google Scholar
13. Rathmann, W, Giani, G, Wild, SH. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:2568–9. https://doi.org/10.2337/diacare.27.10.2568.Suche in Google Scholar PubMed
14. Gispen, WH, Biessels, G. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 2000;23:542–9. https://doi.org/10.1016/s0166-2236(00)01656-8.Suche in Google Scholar PubMed
15. Biessels, GJ, Heide, LP, Kamal, A, Bleys, RL, Gispen, WH. Ageing and diabetes: implications for brain function. Eur J Pharmacol 2002;441:1–14. https://doi.org/10.1016/s0014-2999(02)01486-3.Suche in Google Scholar PubMed
16. Racchi, M, Mazzucchelli, M, Porello, E, Lanni, C, Govoni, S. Acetylcholinesterase inhibitors: novel activities of old molecules. Pharmacol Res 2004;50:441–51. https://doi.org/10.1016/j.phrs.2003.12.027.Suche in Google Scholar PubMed
17. Mukherjee, P, Venkatesan, K, Mainak, M, Peter, JH. Acetylcholinesterase inhibitors from plants. Phytomedicine 2007;14:289–300. https://doi.org/10.1016/j.phymed.2007.02.002.Suche in Google Scholar PubMed
18. Ademiluyi, OA, Oyeniran, OH, Oboh, G. Dietary monosodium glutamate altered redox status and dopamine metabolism in lobster cockroach (Nauphoeta cinerea). J Food Biochem 2020;44:e13451.10.1111/jfbc.13451Suche in Google Scholar
19. Bharucha, KN. The epicurean fly: using Drosophila melanogaster to study metabolism. Pediatr Res 2009;65:132–7. https://doi.org/10.1203/PDR.0b013e318191fc68.Suche in Google Scholar PubMed
20. Morris, SNS, Coogan, C, Chamseddin, K, Fernandez-Kim, SO, Kolli, S, Keller, JN, et al.. Development of diet-induced insulin resistance in adult Drosophila melanogaster. Biochim Biophys Acta 2012;1822:1230–7. https://doi.org/10.1016/j.bbadis.2012.04.012.Suche in Google Scholar PubMed PubMed Central
21. Garelli, A, Gontijo, AM, Miguela, V, Caparros, E, Dominguez, M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 2012;336:579–82. https://doi.org/10.1126/science.1216735.Suche in Google Scholar PubMed
22. Lenz, S, Karsten, P, Schulz, JB, Voigt, A. Drosophila as a screening tool to study human neurodegenerative diseases. J Neurochem 2013;127:453–60. https://doi.org/10.1111/jnc.12446.Suche in Google Scholar PubMed
23. Ademiluyi, AO, Oyeniran, OH, Jimoh, TO, Oboh, G, Boligon, AA. Fluted Pumpkin (Telfairia occidentalis) seed modulate markers of erectile function in isolated rat’s corpus cavernosum: influence of polyphenol and amino acid constituents. J Food Biochem 2019;43:1–11. https://doi.org/10.1111/jfbc.13037.Suche in Google Scholar PubMed
24. Oboh, G, Ogunsuyi, OB, Ojelade, MT, Akomolafe, SF. Effect of dietary inclusions of bitter kola seed on geotactic behavior and oxidative stress markers in Drosophila melanogaster. Food Sci Nutr 2018;6:2177–87. https://doi.org/10.1002/fsn3.782.Suche in Google Scholar PubMed PubMed Central
25. Singleton, VL, Orthofer, R, Lamuela-Raventos, RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods Enzymol 1999;299:152–78. https://doi.org/10.1016/S0076-6879(99)99017-1.Suche in Google Scholar
26. Meda, A, Lamien, CE, Romito, M, Millogo, J, Nacoulma, OG. Determination of the total phenol, flavonoid and proline contents in Burkina Faso honey, as well as their radical scavenging activity. Food Chem 2005;91:571–7. https://doi.org/10.1016/j.foodchem.2004.10.006.Suche in Google Scholar
27. Kelley, WTD, Coffey, DL, Mueller, TC. Lipid chromatographic determination of phenolic acids in soil. J Assoc Anal Commun Int 1994;77:805–9. https://doi.org/10.1093/jaoac/77.4.805.Suche in Google Scholar
28. Provan, GL, Scobbie, L, Chesson, A. Determination of phenolic acids in plant cell walls by microwave digestion. J Sci Food Agric 1994;64:63–5. https://doi.org/10.1002/jsfa.2740640110.Suche in Google Scholar
29. Whitehead, D, Dibb, D, Hartley, R. Bound phenolic compounds in water extracts of soils, plant roots and leaf litter. J Soil Biol Biochem 1983;15:133–6. https://doi.org/10.1016/0038-0717(83)90092-5.Suche in Google Scholar
30. Re, R, Pellegrini, N, Proteggente, A, Pannala, A, Yang, M, Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorisation assay. Free Radic Biol Med 1999;26:1231–7. https://doi.org/10.1016/s0891-5849(98)00315-3.Suche in Google Scholar PubMed
31. Oyaizu, M. Studies on products of browning reaction: antioxidative activity of products of browning reaction prepared from glucosamine. Jpn J Nutr 1986;44:307–15. https://doi.org/10.5264/eiyogakuzashi.44.307.Suche in Google Scholar
32. Gyamfi, MA, Yonamine, M, Aniya, Y. Free-radical scavenging action of medicinal herbs from Ghana Thonningia sanguinea on experimentally-induced liver injuries. Gen Pharmacol 1999;32:661–7. https://doi.org/10.1016/s0306-3623(98)00238-9.Suche in Google Scholar PubMed
33. Halliwell, B, Gutteridge, JMC. Formation of thiobarbituric acid-reactive substance from deoxyribose in the presence of iron salts. FEBS Lett 1981;128:347–52. https://doi.org/10.1016/0014-5793(81)80114-7.Suche in Google Scholar PubMed
34. Minotti, G, Aust, SD. An investigation into the mechanism of citrate-Fe2+-dependent lipid peroxidation. Free Radic Biol Med 1987;3:379–87. https://doi.org/10.1016/0891-5849(87)90016-5.Suche in Google Scholar PubMed
35. Ohkawa, H, Ohishi, N, Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–8. https://doi.org/10.1016/0003-2697(79)90738-3.Suche in Google Scholar PubMed
36. Oboh, G, Ogunsuyi, OB, Adegbola, DO, Ademiluyi, AO, Oladun, FL. Influence of gallic and tannic acid on therapeutic properties of acarbose in vitro and in vivo in Drosophila melanogaster. Biomed J 2019;317–27.10.1016/j.bj.2019.01.005Suche in Google Scholar
37. Ellman, GE, Courtney, KD, Anderson, V. A new calorimetric determination of acetyl cholinesterase activity. Biochem Pharmacol 1961;7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9.Suche in Google Scholar PubMed
38. Abolaji, AO, Olaiya, CO, Oluwadahunsi, OJ, Farombi, EO. Dietary consumption of monosodium L-glutamate induces adaptive response and reduction in the life span of Drosophila melanogaster. Cell Biochem Funct 2017;35:164–70. https://doi.org/10.1002/cbf.3259.Suche in Google Scholar PubMed
39. McEwen, CM. Human plasma monoamine oxidase I. Purification and Identification. J Biol Chem 2003;240:10.10.1016/S0021-9258(18)97417-XSuche in Google Scholar
40. Obatomi, DK, Bikomo, EO, Temple, VJ. Anti-diabetic properties of the African mistletoe in streptozotocin-induced diabetic rats. J Ethnopharmacol 1994;43:13–7. https://doi.org/10.1016/0378-8741(94)90111-2.Suche in Google Scholar PubMed
41. Taram, F, Winter, AN, Linseman, DA. Neuroprotection comparison of chlorogenic acid and its metabolites against mechanistically distinct cell death-inducing agents in cultured cerebellar granule neurons. Brain Res 2016;1648:69–80. https://doi.org/10.1016/j.brainres.2016.07.028.Suche in Google Scholar PubMed
42. Dajas, F, Rivera, F, Blasina, F, Arredondo, F, Echeverry, C, Lafon, L, et al.. Cell culture protection and in vivo neuroprotective capacity of flavonoids. Neurotox Res 2003;5:377–84. https://doi.org/10.1007/bf03033172.Suche in Google Scholar PubMed
43. Abdel-Moneim, AA, Yousef, AI, Abd El-Twab, SM, Abdel Reheim, ES, Ashour, MB. Gallic acid and p-coumaric acid attenuate type 2 diabetes-induced neurodegeneration in rats. Metab Brain Dis 2017;32:1279–86. https://doi.org/10.1007/s11011-017-0039-8.Suche in Google Scholar PubMed
44. Adel, A, Eman, SA, Sanaa, MA, Mohamed, BA, Ahmed, IY. Assessment of the ameliorative effect of p-coumaric acid and gallic acid on oxidative stress and haematological abnormalities in experimental type 2 diabetes. Gen Med Open 2018;2:1–6. https://doi.org/10.15761/GMO.1000150.Suche in Google Scholar
45. Amic, D, Davidovic-Amic, D, Beslo, D, Trinasjstic, N. Structure-radical scavenging activity relationship of flavonoids. Croat Chem Acta 2003;76:55–61.Suche in Google Scholar
46. Srinivasan, M, Sudheer, AR, Menon, VP. Ferulic acid: therapeutic potential through its antioxidant property. J Clin Biochem Nutr 2007;40:92–100. https://doi.org/10.3164/jcbn.40.92.Suche in Google Scholar PubMed PubMed Central
47. Antonella, S, Daniela, G, Marta, C. Review on ferulic acid: a hope for Alzheimer’s disease therapy from plants. Nutrients 2015;7:5764–82. https://doi.org/10.3390/nu7075246.Suche in Google Scholar PubMed PubMed Central
48. Liu, YW, Liu, XL, Kong, L, Zhang, MY, Chen, YJ, Zhu, X, et al.. Neuroprotection of quercetin on central neurons against chronic high glucose through enhancement of Nrf2/ARE/glyoxalase-1 pathway mediated by phosphorylation regulation. Biomed Pharmacother 2019;109:2145–54. https://doi.org/10.1016/j.biopha.2018.11.066.Suche in Google Scholar PubMed
49. Tokmak, M, Yuksel, Y, Sehitoglu, MH, Güven, M, Akman, T, Aras, AB, et al.. The neuroprotective effect of syringic acid on spinal cord ischemia/reperfusion injury in rats. Inflammation 2015;38:1969–78. https://doi.org/10.1007/s10753-015-0177-2.Suche in Google Scholar PubMed
50. Farbood, Y, Sarkaki, A, Dolatshahi, M, Mansouri, SMT, Khodadadi, A. Ellagic acid protects the brain against 6-hydroxydopamine induced neuroinflammation in a rat model of Parkinson’s disease. Basic Clin Neurosci 2015;6:15–22.Suche in Google Scholar
51. Ragavendran, P, Arul Raj, C, Sophia, D, Starlin, T, Gopalakrishnan, VK. Evaluation of enzymatic and non-enzymatic antioxidant properties of Aerva lanata (L) – an in vitro study. Int J Pharm Pharm Sci 2012;1:522–6.Suche in Google Scholar
52. Rice-Evans, C, Miller, NJ, Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 1996;20:933–56. https://doi.org/10.1016/0891-5849(95)02227-9.Suche in Google Scholar PubMed
53. Halliwell, B, Gutteridge, JMC. Free radicals in biology and medicine, 3rd ed. New York, USA: Oxford University Press; 1999.Suche in Google Scholar
54. Fraga, CG, Oteiza, PI. Iron toxicity and antioxidants nutrients. J Toxicol 2002;180:23–32. https://doi.org/10.1016/s0300-483x(02)00379-7.Suche in Google Scholar PubMed
55. Oboh, G, Rocha, JBT. Polyphenols in red pepper [Capsicum annuum var. aviculare (Tepin)] and their protective effect on some pro-oxidants induced lipid peroxidation in brain and liver- in vitro. European Food Res 2007;225:2. https://doi.org/10.1007/s00217-006-0410-1.Suche in Google Scholar
56. Maya, S, Prakash, T, Madhu, KD, Goli, D. Multifaceted effects of aluminum in neurodegenerative diseases: a review. Biomed Pharmacother 2016;83:746–54. https://doi.org/10.1016/j.biopha.2016.07.035.Suche in Google Scholar PubMed
57. Ecker, A, Gonzaga, TKS, Seeger, RL, dos Santos, MM, Loreto, JS, Boligon, AA, et al.. High-sucrose diet induces diabetic-like phenotypes and oxidative stress in Drosophila melanogaster: protective role of Syzygium cumini and Bauhinia forficata. Biomed Pharmacother 2017;89:605–16.10.1016/j.biopha.2017.02.076Suche in Google Scholar
58. Kume, K, Kume, S, Park, SK, Hirsh, J, Jackson, FR. Dopamine is a regulator of arousal in the fruit fly. J Neurosci 2005;25:7377–84. https://doi.org/10.1523/jneurosci.2048-05.2005.Suche in Google Scholar
© 2021 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Editorials
- Deiodination and tumor progression: the interplay between thyroid hormones intracellular activation and the androgen signal
- The intricate role of glutamine in pathophysiological contexts
- Reviews
- Zebrafish as a model organism – can a fish mimic human?
- Phytocompounds and their molecular targets in immunomodulation: a review
- Original Articles
- Host–parasite relationship modulates the effect of African mistletoe leaves on the cholinergic, monoaminergic and carbohydrate hydrolyzing enzymes in fruit fly
- Behavioral and biochemical investigations to explore the efficacy of quercetin and folacin in experimental diabetes induced vascular endothelium dysfunction and associated dementia in rats
- Chronic exposure of industrial grade calcium carbide and ethylene glycol exert genotoxic effect in Wistar albino rats
- A four-year review of uterine rupture at a secondary health facility in Okitipupa, Southwest Nigeria
- Increased nitric oxide availability worsens the cardiac performance during early re-perfusion period in adult rats
- Safety evaluation of an antimalarial herbal product from Andrographis paniculata (AS201-01) in healthy volunteers
- Tobacco use and clinical leukoplakia lesions among south Indian tribes
- Carcinogen sodium arsenite disrupts antioxidant and redox homeostasis in Drosophila melanogaster
- No association of the common Asian mitochondrial DNA haplogroups with lung cancer in East Indian population
- Cardioprotective effect of Justicia gendarussa on doxorubicin induced toxicity in mice
- Lung ultrasound-guided PEEP titration in COVID–19 patients treated with CPAP
- Short Communication
- Effects of the gaseous signalling molecule nitroxyl (HNO) on myenteric neurons governing intestinal motility
Artikel in diesem Heft
- Frontmatter
- Editorials
- Deiodination and tumor progression: the interplay between thyroid hormones intracellular activation and the androgen signal
- The intricate role of glutamine in pathophysiological contexts
- Reviews
- Zebrafish as a model organism – can a fish mimic human?
- Phytocompounds and their molecular targets in immunomodulation: a review
- Original Articles
- Host–parasite relationship modulates the effect of African mistletoe leaves on the cholinergic, monoaminergic and carbohydrate hydrolyzing enzymes in fruit fly
- Behavioral and biochemical investigations to explore the efficacy of quercetin and folacin in experimental diabetes induced vascular endothelium dysfunction and associated dementia in rats
- Chronic exposure of industrial grade calcium carbide and ethylene glycol exert genotoxic effect in Wistar albino rats
- A four-year review of uterine rupture at a secondary health facility in Okitipupa, Southwest Nigeria
- Increased nitric oxide availability worsens the cardiac performance during early re-perfusion period in adult rats
- Safety evaluation of an antimalarial herbal product from Andrographis paniculata (AS201-01) in healthy volunteers
- Tobacco use and clinical leukoplakia lesions among south Indian tribes
- Carcinogen sodium arsenite disrupts antioxidant and redox homeostasis in Drosophila melanogaster
- No association of the common Asian mitochondrial DNA haplogroups with lung cancer in East Indian population
- Cardioprotective effect of Justicia gendarussa on doxorubicin induced toxicity in mice
- Lung ultrasound-guided PEEP titration in COVID–19 patients treated with CPAP
- Short Communication
- Effects of the gaseous signalling molecule nitroxyl (HNO) on myenteric neurons governing intestinal motility