Alpha-glucosidase inhibition and antihyperglycemic activity of flavonoids rich fractions of Rosmarinus officinalis in normal and streptozotocin diabetic mice

  • Messaoud Belmouhoub
  • Noureddine Bribi
  • Mokrane Iguer-ouada
Research Article
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Abstract

The aim of the present study was to evaluate the antihyperglycemic effect of flavonoids rich fractions of Rosmarinus officinalis L. namely n-butanol fraction (BUT) and diethyl ether fraction (D.E). Antihyperglycemic action was studied in vitro through the inhibitory tests on α-glucosidase of Saccharomyces cerevisiae. In vivo, the antidiabetic effects were tested in both normal and streptozotocin (STZ) induced diabetic mice using various tests including: the decrease of post prandial hyperglycemia, oral glucose tolerance test (OGTT), hypoglycemic effect and inhibition of glucose intestinal transporters. The in vitro α-glucosidase inhibition activity showed that both fractions (BUT and D.E) presented a potent effect. The maximum inhibition with D.E and BUT fractions was, 77 and 72% at 250 μg/ml, respectively. In vivo, BUT fraction at 800 mg/kg, showed a significant impact on post prandial hyperglycemia with 40.77% and 28.2% as a maximum glucose level reduction using sucrose and maltose, respectively. In OGTT, the maximum antihyperglycemic effect (51.65%) was also obtained with BUT fraction at 800 mg/kg. When testing the impact on glucose intestinal transport, a dose of 800 mg/kg of D.E fraction exhibited a significant inhibition with 24.12% as a maximum reduction. The present results clearly demonstrated the complementary effect of Rosmarinus officinalis flavonoids rich fractions, resulting to α-glucosidase inhibition and to antihyperglycemic action through glucose transport inhibition and blood glucose level reduction.

Keywords

Rosmarinus officinalis OGTT Intestinal glucose transport Streptozotocin Diabetic mice Postprandial hyperglycemia 
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Notes

Acknowledgements

Special thanks to Professor Mohammed Sahnoune for his help in plant identification, Dr. Rachid Ladjouzi for his assistance in oral glucose tolerance test, Mr. Mustapha Lazazen for his help in preparing the manuscript.

Compliance with ethical standards

Ethical statements

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.”

The all procedures used in the present study were carried out in accordance with the care of laboratory animals and the ethical guidelines for investigations of experimental and pain in conscious animals, following the directive number 2010/63/EU of 22 September 2010.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Ahmed QU, Dogarai BBS, Amiroudine MZAM, Taher M, Latip J, Umar A, Muhammad BY (2012) Antidiabetic activity of the leaves of Tetracera indica Merr. (Dilleniaceae) in vivo and in vitro. Journal of Medicinal Plant Research 6(49):5912–5922Google Scholar
  2. Al-Attar AM, Zari TA (2010) Influences of crude extract of tea leaves, Camellia sinensis, on streptozotocin diabetic male albino mice. Saudi Journal of Biological Sciences 17:295–301Google Scholar
  3. Ali H, Houghton PJ, Soumyanath A (2006) Alpha-amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus. Journal of Ethnopharmacology 107:449–455Google Scholar
  4. Ali KM, Chatterjee K, De D, Jana K, Bera TK, Ghosh D (2011) Inhibitory effect of hydro-methanolic extract of seed of Holarrhena antidysenterica on alpha-glucosidase activity and postprandial blood glucose level in normoglycemic rat. Journal of Ethnopharmacology 135:194–196Google Scholar
  5. Ali RB, Atangwho IJ, Kuar N, Ahmad M, Mahmud R, Asmawi MZ (2013) In vitro and in vivo effects of standardized extract and fractions of Phaleria macrocarpa fruits pericarp on lead carbohydrate digesting enzymes. BMC Complement Alternative Medecine 13(39):1–11Google Scholar
  6. Anderson OM, Markham KR (2006). Flavonoids - chemistry, biochemistry and applications. CRC Press Taylor and Francis Group. 1-1197Google Scholar
  7. Arya A, Looi CY, Cheah SC, Mustafa MR, Mohd MA (2012) Anti-diabetic effects of Centratherum anthelminticum seeds methanolic fraction on pancreatic cells, b-TC6 and its alleviating role in type2 diabetic rats. Journal of Ethnopharmacology 144:22–32Google Scholar
  8. Atti-Santos AC, Rossato M, Pauletti GF, Rota LD, Rech JC, Pansera MR, Agostini F, Serafini LA, Moyna P (2005) Physico-chemical Evaluation of Rosmarinus officinalis L. Essential Oils. Brazil Archiv Biol Technol 48(6):1035–1039CrossRefGoogle Scholar
  9. Bakırel T, Bakırel U, Keles OS, Ulgen SG, Yardibi H (2008) In vivo assessment of antidiabetic and antioxidant activities of rosemary (Rosmarinus officinalis) in alloxan-diabetic rabbits. J Ethnopharmacol 116:64–73CrossRefPubMedGoogle Scholar
  10. Ceriello A (2005) Postprandial hyperglycemia and diabetes complications: is it time to treat? Diabetes 54:1–7CrossRefPubMedGoogle Scholar
  11. Cheung S, Tai J (2007) Anti-proliferative and antioxidant properties of rosemary Rosmarinus officinalis. Oncol Rep 17:1525–1531PubMedGoogle Scholar
  12. Eddouks M, Jouad H, Maghrani M, Lemhadri A, Burcelin R (2003) Inhibition of endogenous glucose production accounts for hypoglycemic effect of Spergularia purpurea in streptozotocin mice. Phytomedicine 10:594–599CrossRefPubMedGoogle Scholar
  13. Gholamhoseinian H, Fallah H, Sharifi-Far F, Mirtajaddini M (2008) The inhibitory effect of some Iranian plants extracts on the alpha glucosidase. Iran J Basic Med Sci 11(1):1–9Google Scholar
  14. Gholamhoseinian A, Fallah H, Sharifi-Far F (2009) Inhibitory effect of methanol extract of Rosa damascena Mill. Flowers on a-glucosidase activity and postprandial hyperglycemia in normal and diabetic rats. Phytomedicine 16:935–941CrossRefPubMedGoogle Scholar
  15. Gupta RK, Kumar D, Chaudhary AK, Maithani M, Singh R (2012) Antidiabetic activity of Passiflora incarnata Linn. in streptozotocin-induced diabetes in mice. J Ethnopharmacol 139:801–806CrossRefPubMedGoogle Scholar
  16. Hogan S, Zhang L, Li J, Sun S, Canning C, Zhou K (2010) Antioxidant rich grape pomace extract suppresses postprandial hyperglycemia in diabetic mice by specifically inhibiting alpha-glucosidase. Nutr Metab 7(71):1–9Google Scholar
  17. International Diabetes Federation (2009) web page: http://www.idf.org/latestdiabetes-figures-paint-grim-global-picture (accessed: 2009)
  18. Koga K, Nomoto K, Yoshino K, Shibata H (2006) Effects of 50% ethanol extract from rosemary (Rosmarinus officinalis) on α-glucosidase inhibitory activity and the elevation of plasma glucose level in rats, and its active compound. J Food Sci 71(7):579–512CrossRefGoogle Scholar
  19. Kumar TS, Shanmugam S, Palvannan T, Kumar VMB (2008) Evaluation of antioxidant properties of Elaeocarpus ganitrus Roxb. leaves. Iran J Pharmaceut Res 7(3):211–215Google Scholar
  20. Kwon O, Eck P, Chen S, Corpe CP, Lee JH, Kruhlak M, Levine M (2007) Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J 21(2):366–377CrossRefPubMedGoogle Scholar
  21. Marles RJ, Farnsworth NR (1995) Antidiabetic plants and their active constituents. Phytomedicine 2:137–189CrossRefPubMedGoogle Scholar
  22. Martin HJ, Kornmann F, Fuhrmann GF (2003) The inhibitory effects of flavonoids and antiestrogens on the Glut1 glucose transporter in human erythrocytes. Chem Biol Interact 146:225–235CrossRefPubMedGoogle Scholar
  23. Meddah B, Ducroc R, Faouzi ME, Eto B, Mahraoui L, Benhaddou-Andaloussi A, Martineau LC, Cherrah Y, Haddad PS (2009) Nigella sativa inhibits intestinal glucose absorption and improves glucose tolerance in rats. J Ethnopharmacol 121:419–424CrossRefPubMedGoogle Scholar
  24. Modak M, Dixit P, Londhe J, Ghaskadbi S, Devasagayam TPA (2007) Indian herbs and herbal drugs for the treatment of diabetes. J Clin Biochem Nutr 40(3):163–173CrossRefPubMedPubMedCentralGoogle Scholar
  25. Newey H, Parsons BJ, Smyth DH (1959) The Site of action of phlorizin in inhibiting intestinal absorption of glucose. J Physiol 148:83–92CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nistor Baldea LA, Martineau LC, Benhaddou-Andaloussi A, Arnason JT, Lévy E, Haddad PS (2010) Inhibition of intestinal glucose absorption by anti-diabetic medicinal plants derived from the James Bay Cree traditional pharmacopeia. J Ethnopharmacol 132:473–482CrossRefPubMedGoogle Scholar
  27. Oboh G, Ademiluyi AO, Akinyemi AJ, Henle T, Saliu JA, Schwarzenbolz U (2012) Inhibitory effect of polyphenol-rich extracts of jute leaf (Corchorus olitorius) on key enzyme linked to type 2 diabetes (α-amylase and α-glucosidase) and hypertension (angiotensin I converting) in vitro. J Funct Foods 4:450–458CrossRefGoogle Scholar
  28. OECD, Test guideline 425 (2008). Acute Oral Toxicity-Up-and-Down-Procedure (UDP). In: OECD Guideline for Testing of Chemical, Section 4-Health Effects, Organization of Economic Co-operation and Development, Paris, FranceGoogle Scholar
  29. Owen PL, Johns T (1999) Xanthine oxidase inhibitory activity of northeastern North American plant remedies used for gout. J Ethnopharmacol 64:149–160CrossRefPubMedGoogle Scholar
  30. Panunti B, Jawa AA, Fonseca VA (2004) Mechanisms and therapeutic targets in type 2 diabetes mellitus. Drug Discov Today Dis Mechanism 1:151–157CrossRefGoogle Scholar
  31. Petiwala SM, Puthenveetil AG, Johnson JJ (2013) Polyphenols from the Mediterranean herb rosemary (Rosmarinus officinalis) for prostate cancer. Front Pharmacol 4:1–4CrossRefGoogle Scholar
  32. Phan MAT, Wang J, Tang J, Lee YZ, Ng K (2013) Evaluation of α-glucosidase inhibition potential of some flavonoids from Epimedium brevicornum. LWT - Food Sci Technol 53:492–498CrossRefGoogle Scholar
  33. Ramadan KS, Khalil OA, Danial EN, Alnahdi HS, Ayaz NO (2013) Hypoglycemic and hepatoprotective activity of Rosmarinus officinalis extract in diabetic rats. Journal of Physiology and Biochemistry 69:779–783Google Scholar
  34. Ryu HW, Cho JK, Curtis-Long MJ, Yuk HJ, Kim YS, Jung S, Kim YS, Lee BW, Park KH (2011) α-Glucosidase inhibition and antihyperglycemic activity of prenylated xanthones from Garcinia mangostana. Phytochemistry (72):2148–2154Google Scholar
  35. Shim YJ, Doo HK, Ahn SY, Kim YS, Seong JK, Park IS, Min BH (2003) Inhibitory effect of aqueous extract from the gall of Rhus chinensis on alpha- glucosidase activity and postprandial blood glucose. Journal of Ethnopharmacology 85:283–287Google Scholar
  36. Therasa SV, Thirumalai T, Tamilselvan N, David E (2014) In-vivo and ex-vivo inhibition of intestinal glucose uptake: a scope for antihyperglycemia. Journal of Acute Disease 3(1):36–40Google Scholar
  37. Tian HL, Wei LS, Xu ZX, Zhao RT, Jin DL, Gao JS (2010) Correlations between blood glucose level and diabetes signs in streptozotocin-induced diabetic mice. Global Journal of Pharmacology 4(3):111–116Google Scholar
  38. Wang Y, Huang S, Shao S, Qian L, Xu P (2012) Studies on bioactivities of tea (Camellia sinensis L.) fruit peel extracts: antioxidant activity and inhibitory potential against α-glucosidase and α-amylase in vitro. Industrial Crops and Products 37:520–526Google Scholar
  39. Ye F, Shen Z, Xie M (2002) Alpha-glucosidase inhibition from a Chinese medical herb (Ramulus mori) in normal and diabetic rats and mice. Phytomedicine 9:161–166CrossRefPubMedGoogle Scholar
  40. Zheng J, He J, Ji B, Ye L, Zhang X (2007) Antihyperglycemic activity of Prunella vulgaris L. in streptozotocin-induced diabetic mice. Asia Pacific Journal of Clinical Nutrition 16(1):427–431Google Scholar
  41. Zheng X, Zhang L, Wang WW, Wu YY, Zhang QB, Fen WS (2011) Anti-diabetic activity and potential mechanism of total flavonoids of Selaginella tamariscina (Beauv.) Spring in rats induced by high fat diet and low dose STZ. Journal of Ethnopharmacology 137:662–668Google Scholar
  42. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16(2):109–110Google Scholar

Copyright information

© Institute of Korean Medicine, Kyung Hee University and Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Messaoud Belmouhoub
    • 1
  • Noureddine Bribi
    • 2
  • Mokrane Iguer-ouada
    • 1
  1. 1.Laboratoire Associé en Ecosystèmes Marins et Aquacoles, Faculté des Sciences de la Nature et de la VieUniversité de BejaiaBejaiaAlgeria
  2. 2.Laboratoire de biotechnologie végétale, Faculté des Sciences de la Nature et de la VieUniversité de BejaiaBejaiaAlgeria

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