Enzymes inhibitory and radical scavenging potentials of two selected tropical vegetable (Moringa oleifera and Telfairia occidentalis) leaves relevant to type 2 diabetes mellitus

Abstract

Moringa oleifera Lam., Moringaceae, and Telfairia occidentalis Hook. f., Curcubitaceae, leaves are two tropical vegetables of medicinal properties. In this study, the inhibitory activities and the radical scavenging potentials of these vegetables on relevant enzymes of type 2-diabetes (α-amylase and α-glucosidase) were evaluated in vitro. HPLC-DAD was used to characterize the phenolic constituents and Fe2+-induced lipid peroxidation in rat’s pancreas was investigated. Various radical scavenging properties coupled with metal chelating abilities were also determined. However, phenolic extracts from the vegetables inhibited α-amylase, α-glucosidase and chelated the tested metals (Cu2+ and Fe2+) in a concentration-dependent manner. More so, the inhibitory properties of phenolic rich extracts from these vegetables could be linked to their radical scavenging abilities. Therefore, this study may offer a promising prospect for M. oleifera and T. occidentalis leaves as a potential functional food sources in the management of type 2-diabetes mellitus.

References

  1. Adefegha, S. A., Oboh, G., 2012. Inhibition of key enzymes linked to type 2 diabetes and sodium nitroprusside-induced lipid peroxidation in rat pancreas by water extractable phytochemicals from some tropical spices. Pharm. Biol. 50, 857–865.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Afifi, A.F., Kamel, E.M., Khalil, A.A., Foaad, M.A., Fawziand, E.M., Houseny, M., 2008. Purification and characterization of alphα-amylase from Penicillium olsonii under the effect of some antioxidant vitamins. Glob. J. Biotechnol. Biochem. 3, 14–21.

    Google Scholar 

  3. Akindahunsi, A.A., Oboh, G., 1999. Effect of some post-harvest treatments on the bioavailability of zinc from some selected tropical vegetables. La Riv. Ital. Delle Sost. Grasse 76, 285–287.

    Google Scholar 

  4. Anokwuru, C.P., Ajibaye, O., Adesuyi, A., 2011. Comparative antioxidant activity of water extract of Azadiractha indica stem bark and Telfairia occidentalis leaf. Curr. Res. J. Biol. Sci. 3, 430–434.

    Google Scholar 

  5. Apostolidis, E., Kwon, Y.I., Shetty, K., 2007. Inhibitory potential of herb, fruit, and fungal enriched cheese against key enzymes linked to type 2 diabetes and hypertension. Inn. Food Sci. Emerg. Technol. 8, 46–54.

    CAS  Google Scholar 

  6. Atawodi, S.E., Atawodi, J.C., Idakwo, G.A., Pfundstein, B., Haubner, R., Wurtele, G., Bartsch, H., Owen, R.W., 2010. Evaluation of the polyphenol content and antioxidant properties of methanol extracts of the leaves, stem, and root barks of Moringa oleifera Lam. J. Med. Food 13, 710–716.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Belle, N.A.V., Dalmolin, G.D., Fonini, G., Rubim, M.A., Rocha, J.B.T., 2004. Polyamines reduce lipid peroxidation induced by different prooxidant agents. Brain Res. 1008, 245–251.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen, X., Zheng, Y., Shen, Y., 2006. Voglibose (Basen, AO-128), one of the most important glucosidase inhibitors. Curr. Med. Chem. 13, 109–116.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Cheplick, S., Kwon, Y., Bhowmik, P., Shetty, K., 2010. Phenolic-linked variation in strawberry cultivars for potential dietary management of hyperglycemia and related complications of hypertension. Bioresour. Technol. 101, 404–413.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Chiasson, J.L., 2006. Acarbose forthe prevention of diabetes, hypertension, and cardiovascular disease in subjects with impaired glucose tolerance: the study to prevent non-insulin-dependent diabetes mellitus (STOP-NIDDM) trial. Endocr. Pract. 1, 25–30.

    Google Scholar 

  11. Chu, Y., Sun, J., Wu, X., Liu, R.H., 2002. Antioxidant and antiproliferative activity of common vegetables. J. Agric. Food Chem. 50, 6910–6916.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Dieye, A.M., Sarr, A., Diop, S.N., Ndiaye, M., Sy, G.Y., Diarra, M., Rajraji Gaffary, I., Ndiaye Sy, A., Faye, B., 2008. Medicinal plants and the treatment of diabetes in Senegal: survey with patients. Fundam. Clin. Pharmacol. 22, 211–216.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Duckworth, W.C., 2001. Hyperglycemia and cardiovascular disease. Curr. Atheroscler. 3, 383–391.

    CAS  Google Scholar 

  14. Finefrock, A.E., Bush, A.I., Doraiswamy, P.M., 2003. Current status of metals as therapeutic targets in Alzheimer’s disease. J. Am. Ger. Soc. 51, 1143–1148.

    Google Scholar 

  15. Fraga, C.G., Oteiza, P.I., 2002. Iron toxicity and antioxidant nutrients. Toxicology 180, 23–32.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Ghimeray, A.K., Jin, C., Ghimine, B.K., Cho, D.H., 2009. Antioxidant activity and quantitative estimation of azadirachtin and nimbin in Azadirachtaindica A, Juss grown in foothills of Nepal. Afr. J. Biotechnol. 8, 3084–3091.

    CAS  Google Scholar 

  17. Giridhari, V.A., Malathi, D., Geetha, K., 2011. Anti-diabetic property of drumstick (Moringa oleifera) leaf tablets. Int. J. Health Nutr. 2, 1–5.

    Google Scholar 

  18. Guevara, A.P., Vargas, C., Sakural, H., Fujiwara, Y., Hashimoto, K., Maoka, T., Kuzuka, M., Ito, Y., Tokuda, H., Hishino, H., 1999. An antitumor promoter from Moringa oleifera Lam. Mutat. Res. 440, 181–188.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Gyamfi, M.A., Yonamine, M., Aniya, Y., 1999. Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. Gen. Pharmacol. 32, 661–667.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Hsu, B., Coupar, I.M., Ng, K., 2006. Antioxidant activity of hot water extract from the fruit of the Doum palm, Hyphaene thebaica. Food Chem. 98, 317–328.

    CAS  Google Scholar 

  21. Ikpeme, E.V., Ekaluo, U.B., Udensi, O.U., Ekerette, E.E., 2014. Screening fresh and dried fruits of avocado pear (Perseaamericana) for antioxidant activities: an alternative for synthetic antioxidant. J. Life Sci. Res. Discov. 1, 19–25.

    Google Scholar 

  22. Islam, M.M., 2013. Biochemistry, medicinal and food values of jute (Corchorus capsularis L. and C olitorius L.) leaf: a review. Int. J. Enhanc. Res. Sci.Technol. Eng. 2, 135–144.

    Google Scholar 

  23. Jaiswal, D., Kumar Rai, P., Kumar, A., Mehta, S., Watal, G., 2009. Effect of Moringa oleifera Lam. leaves aqueous extract therapy on hyperglycemic rats. J. Ethnopharmacol. 123, 392–396.

    PubMed  PubMed Central  Google Scholar 

  24. Kar, A., Choudhary, B.K., Bandyopadhyay, N.G., 2003. Comparative evaluation of hypoglycemic activity of some Indian medicinal plants in alloxan diabetic rats. J. Ethnopharmacol. 84, 105–108.

    PubMed  PubMed Central  Google Scholar 

  25. Kasolo, J.N., Bimenya, G.S., Ojok, L., Ochleng, J., Ogwal-Okeng, J.W., 2010. Phytochemicals and uses of Moringa oleifera leaves in Ugandan rural communities. J. Med. Plant Res. 4, 753–757.

    Google Scholar 

  26. Kumar, S.P., Debasis, M., Goutam, G., Panda, C.S., 2010. Medicinal uses and pharmacological properties of Moringa oleifera. Int. J. Phytomed 2, 210–216.

    Google Scholar 

  27. Kumari, D.J., 2010. Hypoglycemic effect of Moringa oleifera and Azadirachta indica in type-2 diabetes. Bioscan 5, 211–214.

    Google Scholar 

  28. Kurma, S.R., Mishra, S.H., 1998. Antiinflammatory and hepatoprotective activities of fruits of Moringa pterygosperma Gaerth. Ind. J. Nat. Prod. 14, 3–10.

    Google Scholar 

  29. Kwon, Y.I., Apostolidis, E., Kim, Y.C., Shetty, K., 2007. Health benefits of traditional corn, beans and pumpkin: in vitro studies for hyperglycemia and hypertension management. J. Med. Food 10, 266–275.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Meda, A., Lamien, C.E., Romito, M., Millogo, J., Nacoulma, O.G., 2005. Determination of the total phenolic, flavonoid and proline contents in Burkina Faso honey, as well as their radical scavenging activity. J. Food Chem. 91, 571–587.

    CAS  Google Scholar 

  31. Minnoti, G., Aust, S.D., 1987. An investigation into the mechanism of citrate Fe2+ dependent lipid peroxidation. Free Radic. Biol. Med. 3, 379–387.

    Google Scholar 

  32. Monera, T.G., Maponga, C.C., 2010. Moringa oleifera supplementation by patients on antiretroviral therapy. J. Int. AIDS Soc. 13, 188.

    Google Scholar 

  33. Nwozo, S.O., Adaramoye, O.A., Ajaiyeoba, E.O., 2004. Anti-diabetic and hypolipidemic studies of Telifairia occidentalis on alloxan induced diabetic rabbits. Nigerian J. Natl. Prod. Med. 8, 37–39.

    Google Scholar 

  34. Oboh, G., Agunloye, O.M., Adefegha, S.A., Akinyemi, A.J., Ademiluyi, A.O., 2015. Caffeic and chlorogenic acids inhibit key enzymes linked to type-2 diabetes (in vitro): a comparative study. J. Basic Clin. Physiol. Pharmacol. 26, 165–170.

    CAS  PubMed  Google Scholar 

  35. Oboh, G., Rocha, J.B.T., 2007. Antioxidant in Foods: A New Challenge for Food Processors: Leading Edge Antioxidants Research. Nova Science Publishers Inc, New York, pp. 35–64.

    Google Scholar 

  36. Ohkawa, H., Ohishi, N., Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Ann. Biochem. 95, 351–358.

    CAS  Google Scholar 

  37. Oyaizu, M., 1986. Studies on products of browning reaction: antioxidative activity of products of browning reaction prepared from glucosamine. Jpn. J. Nutr. 44, 307–315.

    CAS  Google Scholar 

  38. Pereira, R.P., Boligon, A.A., Appel, A.S., Fachinetto, R., Ceron, C.S., Tanus-Santos, J.E., Athayde, M.L., 2014. Chemical composition, antioxidant and anticholinesterase activity of Melissa officinalis. Ind. Crop. Prod. 53, 34–45.

    CAS  Google Scholar 

  39. Puntel, R.L., Nogueira, C.W., Rocha, J.B.T., 2005. Krebs cycle intermediates modulate thiobarbituric reactive species (TBARS) production in Rat Brain In vitro. Neurochem. Res. 30, 225–235.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Sangeetha, R., Vedasree, N., 2012. In vitro α-amylase inhibitory activity of the leaves of Thespesia populnea. Int. Scholar. Res. Notices, https://doi.org/10.5402/2012/515634.

    Google Scholar 

  41. Shukla, S., Mehta, A., Bajpai, V.K., Shukla, S., 2009. In vitro antioxidant activity and total phenolic content of ethanolic leaf extract of Stevia rebaudiana Bert. Food Chem. Toxicol. 47, 2338–2343.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Siddaraju, M.N., Dharmesh, S.M., 2007. Inhibition of gastric H+, K+-ATPase and Helicobacter pylori growth by phenolic antioxidants of Curcuma amada. J. Agric. Food Chem. 55, 7377–7386.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Singleton, V.L., Orthofor, R., Lamuela-Raventos, R.M., 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteau reagent. Method Enzymol. 299, 152–178.

    CAS  Google Scholar 

  44. Talhiliani, P., Kar, A., 2000. Role of Moringa oleifera leaf extract in the regulation of thyroid hormone status in adult male and female rats. Pharmacol. Res. 41, 319–323.

    Google Scholar 

  45. Torres-Fuentes, W.P., Benson, G.S., McConnell, J., 2011. Role of copper and oxidative stress in cardiovascular diseases. Ann. Biol. Res. 1, 158–173.

    Google Scholar 

  46. Tripathy, S., Pradhan, D., Anjana, M., 2010. Antiinflammatory and antiarthritic potential of Ammania baccifera Linn. Int. J. Pharm. Biosci. 1, 1–7.

    Google Scholar 

  47. Udenigwe, C.C., Adebiyi, A.P., Doyen, A., Bazinet, L., Aluko, R.E., 2012. Low molecu-larweight flaxseed protein-derived arginine-containing peptides reduced blood pressure of spontaneously hypertensive rats faster than amino acid form of arginine and native flaxseed protein. Food Chem. 132, 468–475.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Uyoh, E.A., Chukwura, P.N., David, I.A., Bassey, A.C., 2013. Evaluation of antioxidant capacity of two Ocimum species consumed locally as spices in Nigeria as a justification for increased domestication. Am. J. Plant Sci. 4, 222–230.

    Google Scholar 

  49. Wadkar, K.A., Magdum, C.S., Patil, S.S., Naikwade, N.S., 2008. Anti-diabetic potential and Indian medicinal plants. J. Herbal Med. Toxicol. 2, 45–50.

    Google Scholar 

  50. Worthington, V., 1993. Alpha amylase. In: Worthington, V. (Ed.), Worthington Enzyme Manual. Worthington Biochemical Corp, Freehold, NJ, pp. 36–41.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tajudeen O. Jimoh.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jimoh, T.O. Enzymes inhibitory and radical scavenging potentials of two selected tropical vegetable (Moringa oleifera and Telfairia occidentalis) leaves relevant to type 2 diabetes mellitus. Rev. Bras. Farmacogn. 28, 73–79 (2018). https://doi.org/10.1016/j.bjp.2017.04.003

Download citation

Keywords

  • Type 2-diabetes
  • Tropical
  • Antioxidant
  • Lipid peroxidation
  • Medicinal
  • Phenolics