Animal models and natural products to investigate in vivo and in vitro antidiabetic activity

Biomedicine and Pharmacotherapy

Volumn 101, Issue , 2018, Pages 833-841

  Hasan, Md Mahmudul ^a   Ahmed, Qamar Uddin ^a   Mat Soad, Siti Zaiton ^a   Tunna, Tasnuva Sarwar ^a  

^a INTERNATIONAL ISLAMIC UNIVERSITY MALAYSIA   (Malaysia)

Author keywords

Animal model; Diabetes; Diabetes mechanisms; Flavonoids; Medicinal plants

Indexed keywords

ANTIDIABETIC AGENT; FLAVONOID; HERBACEOUS AGENT; INSULIN SENSITIZING AGENT; BIOLOGICAL PRODUCT; INSULIN;

ANIMAL MODEL; ANTIDIABETIC ACTIVITY; CHEMICALLY INDUCED DISORDER; DRUG EFFICACY; DRUG MECHANISM; ETHNOPHARMACOLOGY; EVALUATION STUDY; EXPERIMENTAL ANIMAL; EXPERIMENTAL DIABETES MELLITUS; IN VITRO STUDY; IN VIVO STUDY; INSULIN LIKE ACTIVITY; INSULIN SENSITIVITY; MEDICINAL PLANT; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSGENIC ANIMAL; ANIMAL; CHEMISTRY; DISEASE MODEL; METABOLISM;

ANIMALS; BIOLOGICAL PRODUCTS; DISEASE MODELS, ANIMAL; FLAVONOIDS; HYPOGLYCEMIC AGENTS; INSULIN;

EID: 85043367013     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2018.02.137     Document Type: Review

References (133)

1. Eddouks, M., Lemhadri, A., Michel, J.B., Hypolipidemic activity of aqueous extract of Capparis spinosa L. in normal and diabetic rats. J. Ethnopharmacol. 98:3 (2005), 345–350.
2. Bnouham, M., Ziyyat, A., Mekhfi, H., Tahri, A., Legssyer, A., Medicinal plants with potential antidiabetic activity—a review of ten years of herbal medicine research (1990–2000). Int. J. Diabetes Metab., 14(1), 2006, 1.
3. Srinivasan, K., Ramarao, P., Animal models in type 2 diabetes research: an overview. Indian J. Med. Res., 125(3), 2007, 451.
4. Vedtofte, L., Bodvarsdottir, T.B., Gotfredsen, C.F., Karlsen, A.E., Knudsen, L.B., Heller, R.S., Liraglutide, but not vildagliptin, restores normoglycaemia and insulin content in the animal model of type 2 diabetes, Psammomys obesus. Regul. Pept. 160:1 (2010), 106–114.
5. Xiao, J., Lv, Y., Lin, S., Jin, L., Zhang, Y., Wang, X., Ma, J., Hu, K., Feng, W., Cai, L., Cardiac protection by basic fibroblast growth factor from ischemia/reperfusion-induced injury in diabetic rats. Biol. Pharm. Bull. 33:3 (2010), 444–449.
6. Hotamisligil, G.S., Peraldi, P., Budavari, A., Ellis, R., IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science, 271(5249), 1996, 665.
7. Wu, G.Z., Hong, G., Zhang, W.P., Zhang, H.B., Effect of 1-[4-[2-(4-bromobenzenesulfonamino) ethyl] phenylsulfonyl]-3-(trans-4-methylcyclohexyl) urea (i4), a new synthetic sulfonylurea compound, on glucose metabolism in vivo and in vitro. Arzneimittelforschung. 59:11 (2009), 550–556.
8. Ro, S., Park, C., Jin, J., Zheng, H., Blair, P.J., Redelman, D., Ward, S.M., Yan, W., Sanders, K.M., A model to study the phenotypic changes of interstitial cells of Cajal in gastrointestinal diseases. Gastroenterology 138:3 (2010), 1068–1078 e2.
9. Wei, D., Li, J., Shen, M., Jia, W., Chen, N., Chen, T., Su, D., Tian, H., Zheng, S., Dai, Y., Cellular production of n-3 PUFAs and reduction of n-6-to-n-3 ratios in the pancreatic ß-cells and islets enhance insulin secretion and confer protection against cytokine-induced cell death. Diabetes 59:2 (2010), 471–478.
10. Seo, E., Park, E.-J., Joe, Y., Kang, S., Kim, M.-S., Hong, S.-H., Park, M.-K., Kim, D.K., Koh, H., Lee, H.-J., Overexpression of AMPK α1 ameliorates fatty liver in hyperlipidemic diabetic rats. Korean J. Physiol. Pharmacol. 13:6 (2009), 449–454.
11. Serreze, D.V., Niens, M., Kulik, J., DiLorenzo, T.P., Bridging mice to men: using HLA transgenic mice to enhance the future prediction and prevention of autoimmune type 1 diabetes in humans. Mouse Models Drug Discov.: Methods Protoc., 2010, 119–134.
12. Sordi, V., Melzi, R., Mercalli, A., Formicola, R., Doglioni, C., Tiboni, F., Ferrari, G., Nano, R., Chwalek, K., Lammert, E., Mesenchymal cells appearing in pancreatic tissue culture are bone marrow-derived stem cells with the capacity to improve transplanted islet function. Stem Cells 28:1 (2010), 140–151.
13. Sugii, S., Olson, P., Sears, D.D., Saberi, M., Atkins, A.R., Barish, G.D., Hong, S.-H., Castro, G.L., Yin, Y.-Q., Nelson, M.C., PPARγ activation in adipocytes is sufficient for systemic insulin sensitization. Proc. Natl. Acad. Sci. 106:52 (2009), 22504–22509.
14. Stranahan, A.M., Arumugam, T.V., Lee, K., Mattson, M.P., Mineralocorticoid receptor activation restores medial perforant path LTP in diabetic rats. Synapse 64:7 (2010), 528–532.
15. Sugrue, M.L., Vella, K.R., Morales, C., Lopez, M.E., Hollenberg, A.N., The thyrotropin-releasing hormone gene is regulated by thyroid hormone at the level of transcription in vivo. Endocrinology 151:2 (2010), 793–801.
16. Fernández-Millán, E., Gangnerau, M.N., De Miguel-Santos, L., Calderari, S., Serradas, P., Escrivá F., Portha, B., Álvarez, C., Undernutrition of the GK rat during gestation improves pancreatic IGF-2 and beta-cell mass in the fetuses. Growth Factors 27:6 (2009), 409–418.
17. Matsui-Inohara, H., Uematsu, H., Narita, T., Satoh, K., Yonezawa, H., Kuroda, K., Ito, T., Yoneda, S., Kawarai, T., Sugiya, H., E2F-1-deficient NOD/SCID mice developed showing decreased saliva production. Exp. Biol. Med. 234:12 (2009), 1525–1536.
18. Matsumoto, Y., Torimoto, K., Matsuyoshi, H., Hirayama, A., Fujimoto, K., Yoshimura, N., Hirao, Y., Long-term effects of diabetes mellitus on voiding function in a new model of type 2 diabetes mellitus, the Spontaneously Diabetic Torii (SDT) rat. Biomed. Res. 30:6 (2009), 331–335.
19. Kretschmer, G., Sutherland, D., Matas, A., Cain, T., Najarian, J., Autotransplantation of pancreatic islets without separation of exocrine and endocrine tissue in totally pancreatectomized dogs. Surgery 82:1 (1977), 74–81.
20. Stewart, T., Hultgren, B., Huang, X., Pitts-Meek, S., Hully, J., MacLachlan, N., Induction of type I diabetes by interferon – in transgenic mice. Science-New York Then Washington, 260, 1993, 1942.
21. Hutchinson, I.V., An endothelin-transforming growth factor beta pathway in the nephrotoxicity of immunosuppressive drugs. Curr. Opin. Nephrol. Hypertens. 7:6 (1998), 665–672.
22. Szkudelski, T., The mechanism of alloxan and streptozotocin action in b cells of the rat pancreas. Physiol. Res. 50:6 (2001), 537–546.
23. Lenzen, S., The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 51:2 (2008), 216–226.
24. Islam, M.S., Loots, d.T., Experimental rodent models of type 2 diabetes: a review. Methods Find. Exp. Clin. Pharmacol. 31:4 (2009), 249–261.
25. Han, J., Liu, Y., Reduction of islet pyruvate carboxylase activity might be related to the development of type 2 diabetes mellitus in agouti-K mice. J. Endocrinol. 204:2 (2010), 143–152.
26. Higuchi, A., Ohashi, K., Shibata, R., Sono-Romanelli, S., Walsh, K., Ouchi, N., Thiazolidinediones reduce pathological neovascularization in ischemic retina via an adiponectin-dependent mechanism. Arterioscler. Thromb. Vasc. Biol. 30:1 (2010), 46–53.
27. Hotta, H., Miura, T., Miki, T., Togashi, N., Maeda, T., Kim, S.J., Tanno, M., Yano, T., Kuno, A., Itoh, T., Short communication: Angiotensin ii type 1 receptor-mediated upregulation of calcineurin activity underlies impairment of cardioprotective signaling in diabetic hearts. Circ. Res. 106:1 (2010), 129–132.
28. Karunanayake, E., Baker, J.R., Christian, R., Hearse, D., Mellows, G., Autoradiographic study of the distribution and cellular uptake of (14C)-streptozotocin in the rat. Diabetologia 12:2 (1976), 123–128.
29. Tjälve, H., Wilander, E., Johansson, E.-B., Distribution of labelled streptozotocin in mice: uptake and retention in pancreatic islets. J. Endocrinol. 69:3 (1976), 455–NP.
30. Ledoux, S.P., Wilson, G.L., Effects of streptozotocin on a clonal isolate of rat insulinoma cells. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 804:4 (1984), 387–392.
31. Schnedl, W.J., Ferber, S., Johnson, J.H., Newgard, C.B., STZ transport and cytotoxicity: specific enhancement in GLUT2-expressing cells. Diabetes 43:11 (1994), 1326–1333.
32. Elsner, M., Guldbakke, B., Tiedge, M., Munday, R., Lenzen, S., Relative importance of transport and alkylation for pancreatic beta-cell toxicity of streptozotocin. Diabetologia 43:12 (2000), 1528–1533.
33. Yamamoto, H., Uchigata, Y., Okamoto, H., Streptozotocin and alloxan induce DNA strand breaks and poly (ADP-ribose) synthetase in pancreatic islets. Nature, 1981.
34. Uchigata, Y., Yamamoto, H., Kawamura, A., Okamoto, H., Protection by superoxide dismutase, catalase, and poly (ADP-ribose) synthetase inhibitors against alloxan- and streptozotocin-induced islet DNA strand breaks and against the inhibition of proinsulin synthesis. J. Biol. Chem. 257:11 (1982), 6084–6088.
35. Murata, M., Takahashi, A., Saito, I., Kawanishi, S., Site-specific DNA methylation and apoptosis: induction by diabetogenic streptozotocin. Biochem. Pharmacol. 57:8 (1999), 881–887.
36. Pieper, A.A., Verma, A., Zhang, J., Snyder, S.H., Poly(ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol. Sci. 20:4 (1999), 171–181.
37. Turk, J., Corbett, J.A., Ramanadham, S., Bohrer, A., McDaniel, M.L., Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochem. Biophys. Res. Commun. 197:3 (1993), 1458–1464.
38. Delaney, C.A., Dunger, A., Di Matteo, M., Cunningham, J.M., Green, M.H., Green, I.C., Comparison of inhibition of glucose-stimulated insulin secretion in rat islets of langerhans by streptozotocin and methyl and ethyl nitrosoureas and methanesulphonates: lack of correlation with nitric oxide-releasing or o6-alkylating ability. Biochem. Pharmacol. 50:12 (1995), 2015–2020.
39. Nukatsuka, M., Yoshimura, Y., Nishida, M., Kawada, J., Allopurinol protects pancreatic ß cells from the cytotoxic effect of streptozotocin: in vitro study. J. Pharmacobiodyn. 13:4 (1990), 259–262.
40. Munday, R., Dialuric acid autoxidation: effects of transition metals on the reaction rate and on the generation of “active oxygen” species. Biochem. Pharmacol. 37:3 (1988), 409–413.
41. Winterbourn, C.C., Munday, R., Glutathione-mediated redox cycling of alloxan: mechanisms of superoxide dismutase inhibition and of metal-catalyzed oh formation. Biochem. Pharmacol. 38:2 (1989), 271–277.
42. Winterbourn, C.C., Cowden, W.B., Sutton, H.C., Auto-oxidation of dialuric acid, divicine and isouramil: superoxide dependent and independent mechanisms. Biochem. Pharmacol. 38:4 (1989), 611–618.
43. Liang, C., DeCourcy, K., Prater, M.R., High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metabolism 59:7 (2010), 943–950.
44. Wang, Y., Fu, G., Chen, F., Wang, H., The effect of valsartan and fluvastatin on the connective tissue growth factor expression in experimental diabetic cardiomyopathy. Zhonghua Nei Ke Za Zhi 48:8 (2009), 660–665.
45. Bonner-Weir, S., Trent, D., Weir, G., Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J. Clin. Invest., 71(6), 1983, 1544.
46. Vogel, H.G., Antidiabetic Activity. 2008, Springer, 1323–1607.
47. Müller, G., Methods to Induce Experimental Diabetes Mellitus. Hock, F., (eds.) Drug Discovery and Evaluation: Pharmacological Assays, 2016, Springer, Cham, 2569–2581.
48. Spasov, A., Kucheriavenko, A., Salaznikova, O., Effect of hypoglycemic drugs on hemorheological parameters. Eksp. Klin. Farmakol. 72:5 (2008), 31–34.
49. Pravenec, M., Use of rat genomics for investigating the metabolic syndrome. Rat Genomics: Methods Protoc., 2010, 415–426.
50. Renner, S., Fehlings, C., Herbach, N., Hofmann, A., von Waldthausen, D.C., Kessler, B., Ulrichs, K., Chodnevskaja, I., Moskalenko, V., Amselgruber, W., Glucose intolerance and reduced proliferation of pancreatic ß-cells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function. Diabetes 59:5 (2010), 1228–1238.
51. Craighead, J.E., Current views on the etiology of insulin-dependent diabetes mellitus. N. Engl. J. Med. 299:26 (1978), 1439–1445.
52. Giron, D.J., Cohen, S., Lyons, S., Trombley, M., Gould, C., Virus-induced diabetes mellitus in ICR Swiss mice is age dependent. Infect. Immun. 41:2 (1983), 834–836.
53. Yoon, J., McClintock, P., Onodera, T., Notkins, A., Virus-induced diabetes mellitus. XVIII. Inhibition by a nondiabetogenic variant of encephalomyocarditis virus. J. Exp. Med. 152:4 (1980), 878–892.
54. Gould, C.L., McMannama, K.G., Bigley, N.J., Giron, D.J., Virus-induced murine diabetes: enhancement by immunosuppression. Diabetes 34:12 (1985), 1217–1221.
55. Björntorp, P., The effect of insulin in vitro on human adipose tissue from normal and diabetic subjects. J. Intern. Med. 181:4 (1967), 389–402.
56. Kobayashi, M., Olefsky, J.M., Effects of streptozotocin-induced diabetes on insulin binding, glucose transport, and intracellular glucose metabolism in isolated rat adipocytes. Diabetes 28:2 (1979), 87–95.
57. Ball, E.G., Merrill, M.A., A manometric assay of insulin and some results of the application of the method to sera and islet containing tissues. Endocrinology 69:3 (1961), 596–607.
58. Morse, W.I., Soeldner, J.S., The measurement of human adipose tissue mass. Compr. Physiol, 2011.
59. Liu, F., Kim, J.-k., Li, Y., Liu, X.-q., Li, J., Chen, X., An extract of Lagerstroemia speciosa L. has insulin-like glucose uptake-stimulatory and adipocyte differentiation-inhibitory activities in 3T3-L1 cells. J. Nutr. 131:9 (2001), 2242–2247.
60. Groot, H.d., Rauen, U., Tissue injury by reactive oxygen species and the protective effects of flavonoids. Fundam. Clin. Pharmacol. 12:3 (1998), 249–255.
61. Cook, N., Samman, S., Flavonoids-chemistry, metabolism, cardioprotective effects, and dietary sources. J. Nutr. Biochem. 7:2 (1996), 66–76.
62. Hollman, P.H., Katan, M., Dietary flavonoids: intake, health effects and bioavailability. Food Chem. Toxicol. 37:9 (1999), 937–942.
63. Heim, K.E., Tagliaferro, A.R., Bobilya, D.J., Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J. Nutr. Biochem. 13:10 (2002), 572–584.
64. Cushnie, T.T., Lamb, A.J., Antimicrobial activity of flavonoids. Int. J. Antimicrob. Agents 26:5 (2005), 343–356.
65. Fernández, S.P., Wasowski, C., Loscalzo, L.M., Granger, R.E., Johnston, G.A., Paladini, A.C., Marder, M., Central nervous system depressant action of flavonoid glycosides. Eur. J. Pharmacol. 539:3 (2006), 168–176.
66. Patra, J.C., Chua, B.H., Artificial neural network-based drug design for diabetes mellitus using flavonoids. J. Comput. Chem. 32:4 (2011), 555–567.
67. Alberti, K., Zimmet, P., New diagnostic criteria and classification of diabetes-again?. Diabet. Med. 15:7 (1998), 535–536.
68. Aslan, M., Orhan, D.D., Orhan, N., Sezik, E., Yesilada, E., In vivo antidiabetic and antioxidant potential of Helichrysum plicatum ssp. plicatum capitulums in streptozotocin-induced-diabetic rats. J. Ethnopharmacol. 109:1 (2007), 54–59.
69. Mohan, S., Nandhakumar, L., Role of various flavonoids: hypotheses on novel approach to treat diabetes. J. Med. Hypotheses Ideas 8:1 (2014), 1–6.
70. Bailey, C.J., Day, C., Traditional plant medicines as treatments for diabetes. Diabetes Care 12:8 (1989), 553–564.
71. Goossen, K., Graber, S., Longer term safety of dipeptidyl peptidase-4 inhibitors in patients with type 2 diabetes mellitus: systematic review and meta-analysis. Diabetes Obes. Metab. 14:12 (2012), 1061–1072.
72. Cobble, M.E., Peters, A.L., Clinical practice in type 2 diabetes: after metformin and lifestyle, then what?. J. Fam. Pract., 58(11), 2009 S7–S7.
73. Gabrielsen, J.S., Gao, Y., Simcox, J.A., Huang, J.Y., Thorup, D., Jones, D., Cooksey, R.C., Gabrielsen, D., Adams, T.D., Hunt, S.C., Hopkins, P.N., Cefalu, W.T., McClain, D.A., Adipocyte iron regulates adiponectin and insulin sensitivity. J. Clin. Invest. 122:10 (2012), 3529–3540.
74. Q.U. Ahmed, A. Umar, M. Taher, D. Susanti, M.Z.A.M. Amiroudine, J. Latip., Phytochemical investigation of the leaves of Tetracera scandens Linn and in vitro antidiabetic activity of hypoletin Proceedings of the International Conference on Science, Technology and Social Sciences (ICSTSS) Springer (2012) 591-608.
75. Jung, M., Park, M., Lee, H.C., Kang, Y.H., Kang, E.S., Kim, S.K., Antidiabetic agents from medicinal plants. Curr. Med. Chem. 13:10 (2006), 1203–1218.
76. Sun, S., Liang, N., Piao, H., Yamamoto, H., Kawashima, Y., Cui, F., Insulin-so (sodium oleate) complex-loaded PLGA nanoparticles: formulation, characterization and in vivo evaluation. J. Microencapsulation 27:6 (2010), 471–478.
77. Beigelman, P.M., Onoprienko, I.S., Insulin-like effects of serum albumin and globulin fractions on glucose uptake by rat epididymal adipose tissue. Diabetes 8:6 (1959), 438–441.
78. Rodbell, M., Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis. J. Biol. Chem. 239 (1964), 375–380.
79. Santos, J.C., Gotardo, R.M., Brianti, M.T., Piraee, M., Gambero, A., Ribeiro, M.L., Effects of yerba maté a plant extract formulation (“YGD”) and resveratrol in 3T3-L1 adipogenesis. Molecules 19:10 (2014), 16909–16924.
80. Gautam, S., Ishrat, N., Singh, R., Narender, T., Srivastava, A.K., Aegeline from Aegle marmelos stimulates glucose transport via AKT and rac1 signaling, and contributes to a cytoskeletal rearrangement through PI3K/Rac1. Eur. J. Pharmacol. 762 (2015), 419–429.
81. Tracy, S., Drescher, K., Jackson, J., Kim, K., Kono, K., Enteroviruses, type 1 diabetes and hygiene: a complex relationship. Rev. Med. Virol. 20:2 (2010), 106–116.
82. o.D.D. Tufts Center for the Study, T.C. for the Study, Cost to develop and win marketing approval for a new drug is $ 2.6 billion. http://csdd.tufts.edu/news/complete_story/pr_tufts_csdd_2014_cost_study, 2018 (accessed 26.02.18).
83. Henkel, A., Ross, J., The effect of acquisitions on pharmaceutical drug prices. 2017 https://economics.yale.edu/sites/default/files/files/Undergraduate/Nominated%20Senior%20Essays/2016-17/Alexis%20Henkel_Senior%20Essay.pdf (accessed 28.02.18).
84. Kumar, R., Patel, D.K., Prasad, S.K., Laloo, D., Krishnamurthy, S., Hemalatha, S., Type 2 antidiabetic activity of bergenin from the roots of Caesalpinia digyna Rottler. Fitoterapia 83:2 (2012), 395–401.
85. Kumar, S., Kumar, V., Prakash, O., Antidiabetic, hypolipidemic and histopathological analysis of Dillenia indica (L.) leaves extract on alloxan induced diabetic rats. Asian Pac. J. Trop. Med. 4:5 (2011), 347–352.
86. Ibeh, B.O., Ezeaja, M.I., Preliminary study of antidiabetic activity of the methanolic leaf extract of Axonopus compressus (P. Beauv) in alloxan-induced diabetic rats. J. Ethnopharmacol. 138:3 (2011), 713–716.
87. Meliani, N., Dib, M.E.A., Allali, H., Tabti, B., Hypoglycaemic effect of Berberis vulgaris L. in normal and streptozotocin-induced diabetic rats. Asian Pac. J. Trop. Biomed. 1:6 (2011), 468–471.
88. Thirumalai, T., Therasa, S.V., Elumalai, E., David, E., Hypoglycemic effect of Brassica juncea (seeds) on streptozotocin induced diabetic male albino rat. Asian Pac. J. Trop. Biomed. 1:4 (2011), 323–325.
89. Kumar, R., Pate, D.K., Prasad, S.K., Sairam, K., Hemalatha, S., Antidiabetic activity of alcoholic leaves extract of Alangium lamarckii Thwaites on streptozotocin-nicotinamide induced type 2 diabetic rats. Asian Pac. J. Trop. Med. 4:11 (2011), 904–909.
90. Ohadoma, S., Michael, H., Effects of co-administration of methanol leaf extract of Catharanthus roseus on the hypoglycemic activity of metformin and glibenclamide in rats. Asian Pac. J. Trop. Med. 4:6 (2011), 475–477.
91. Sefi, M., Fetoui, H., Lachkar, N., Tahraoui, A., Lyoussi, B., Boudawara, T., Zeghal, N., Centaurium erythrea (gentianaceae) leaf extract alleviates streptozotocin-induced oxidative stress and ß-cell damage in rat pancreas. J. Ethnopharmacol. 135:2 (2011), 243–250.
92. Sancheti, S., Sancheti, S., Seo, S.-Y., Antidiabetic and antiacetylcholinesterase effects of ethyl acetate fraction of Chaenomeles sinensis (Thouin) Koehne fruits in streptozotocin-induced diabetic rats. Exp. Toxicol. Pathol. 65:1 (2013), 55–60.
93. Naskar, S., Mazumder, U.K., Pramanik, G., Gupta, M., Kumar, R.S., Bala, A., Islam, A., Evaluation of antihyperglycemic activity of Cocos nucifera Linn. on streptozotocin induced type 2 diabetic rats. J. Ethnopharmacol. 138:3 (2011), 769–773.
94. Eliza, J., Daisy, P., Ignacimuthu, S., Duraipandiyan, V., Antidiabetic and antilipidemic effect of eremanthin from Costus speciosus (Koen.) Sm., in STZ-induced diabetic rats. Chem. Biol. Interact. 182:1 (2009), 67–72.
95. Li, S., Li, J., Guan, X.-L., Li, J., Deng, S.-P., Li, L.-Q., Tang, M.-T., Huang, J.-G., Chen, Z.-Z., Yang, R.-Y., Hypoglycemic effects and constituents of the barks of Cyclocarya paliurus and their inhibiting activities to glucosidase and glycogen phosphorylase. Fitoterapia 82:7 (2011), 1081–1085.
96. Kumar, D., Kumar, S., Kohli, S., Arya, R., Gupta, J., Antidiabetic activity of methanolic bark extract of Albizia odoratissima Benth. in alloxan induced diabetic albino mice. Asian Pac. J. Trop. Med. 4:11 (2011), 900–903.
97. Mahendran, S., Badami, S., Maithili, V., Evaluation of antidiabetic effect of embelin from Embelia ribes in alloxan induced diabetes in rats. Biomed. Prev. Nutr. 1:1 (2011), 25–31.
98. Patel, D., Kumar, R., Prasad, S., Sairam, K., Hemalatha, S., Antidiabetic and in vitro antioxidant potential of Hybanthus enneaspermus (Linn) F. Muell in streptozotocin-induced diabetic rats. Asian Pac. J. Trop. Biomed. 1:4 (2011), 316–322.
99. Balamurugan, R., Ignacimuthu, S., Antidiabetic and hypolipidemic effect of methanol extract of Lippia nodiflora L. in streptozotocin induced diabetic rats. Asian Pac. J. Trop. Biomed. 1:1 (2011), S30–S36.
100. Hou, S.-z., Chen, S.-x., Huang, S., Jiang, D.-x., Zhou, C.-J., Chen, C.-q., Liang, Y.-m., Lai, X.-p., The hypoglycemic activity of Lithocarpus polystachyus Rehd. leaves in the experimental hyperglycemic rats. J. Ethnopharmacol. 138:1 (2011), 142–149.
101. Elberry, A.A., Harraz, F.M., Ghareib, S.A., Gabr, S.A., Nagy, A.A., Abdel-Sattar, E., Methanolic extract of Marrubium vulgare ameliorates hyperglycemia and dyslipidemia in streptozotocin-induced diabetic rats. Int. J. Diabetes Mellit. 3:1 (2015), 37–44.
102. Patil, R., Patil, R., Ahirwar, B., Ahirwar, D., Isolation and characterization of anti-diabetic component (bioactivity-guided fractionation) from Ocimum sanctum L. (Lamiaceae) aerial part. Asian Pac. J. Trop. Med. 4:4 (2011), 278–282.
103. Andrade-Cetto, A., Wiedenfeld, H., Anti-hyperglycemic effect of Opuntia streptacantha Lem. J. Ethnopharmacol. 133:2 (2011), 940–943.
104. Huang, C.-S., Yin, M.-C., Chiu, L.-C., Antihyperglycemic and antioxidative potential of Psidium guajava fruit in streptozotocin-induced diabetic rats. Food Chem. Toxicol. 49:9 (2011), 2189–2195.
105. Khan, H.B.H., Vinayagam, K.S., Palanivelu, S., Panchanatham, S., Anti-diabetic effect of Semecarpus anacardium Linn nut milk extract in a high fat diet STZ-induced type 2 diabetic rat model. Comp. Clin. Pathol. 21:6 (2012), 1395–1400.
106. George, C., Lochner, A., Huisamen, B., The efficacy of Prosopis glandulosa as antidiabetic treatment in rat models of diabetes and insulin resistance. J. Ethnopharmacol. 137:1 (2011), 298–304.
107. Chen, X., Jin, J., Tang, J., Wang, Z., Wang, J., Jin, L., Lu, J., Extraction, purification, characterization and hypoglycemic activity of a polysaccharide isolated from the root of Ophiopogon japonicus. Carbohydr. Polym. 83:2 (2011), 749–754.
108. Sireesha, Y., Kasetti, R.B., Nabi, S.A., Swapna, S., Apparao, C., Antihyperglycemic and hypolipidemic activities of Setaria italica seeds in STZ diabetic rats. Pathophysiology 18:2 (2011), 159–164.
109. Gandhi, G.R., Ignacimuthu, S., Paulraj, M.G., Sasikumar, P., Antihyperglycemic activity and antidiabetic effect of methyl caffeate isolated from Solanum torvum Swartz. fruit in streptozotocin induced diabetic rats. Eur. J. Pharmacol. 670:2 (2011), 623–631.
110. Gupta, S., Sharma, S.B., Singh, U.R., Bansal, S.K., Salutary effect of Cassia auriculate L. leaves on hyperglycemia-induced atherosclerotic environment in streptozotocin rats. Cardiovasc. Toxicol. 11:4 (2011), 308–315.
111. El Ghoul, J., Ghanem-Boughanmi, N., Ben-Attia, M., Biochemical study on the protective effect of ethanolic extract of Zygophyllum album on streptozotocin-induced oxidative stress and toxicity in mice. Biomed. Prev. Nutr. 1:2 (2011), 79–83.
112. Sundaram, R., Naresh, R., Shanthi, P., Sachdanandam, P., Antihyperglycemic effect of iridoid glucoside, isolated from the leaves of Vitex negundo in streptozotocin-induced diabetic rats with special reference to glycoprotein components. Phytomedicine 19:3 (2012), 211–216.
113. Abdel-Sattar, E.A., Elberry, A.A., Harraz, F.M., Ghareib, S.A., Nagy, A.A., Gabr, S.A., Antihyperglycemic and hypolipidaemic effects of the methanolic extract of Saudi mistletoe (Viscum schimperi Engl.). J. Adv. Res. 2:2 (2011), 171–177.
114. Sunil, C., Ignacimuthu, S., Agastian, P., Antidiabetic effect of Symplocos cochinchinensis (Lour.) S. Moore. in type 2 diabetic rats. J. Ethnopharmacol. 134:2 (2011), 298–304.
115. Sonawane, R.D., Vishwakarma, S.L., Lakshmi, S., Rajani, M., Padh, H., Goyal, R.K., Amelioration of STZ-induced type 1 diabetic nephropathy by aqueous extract of Enicostemma littorale Blume and swertiamarin in rats. Mol. Cell. Biochem. 340:1–2 (2010), 1–6.
116. Feshani, A.M., Kouhsari, S.M., Mohammadi, S., Vaccinium arctostaphylos, a common herbal medicine in Iran: molecular and biochemical study of its antidiabetic effects on alloxan-diabetic wistar rats. J. Ethnopharmacol. 133:1 (2011), 67–74.
117. Poongothai, K., Ponmurugan, P., Ahmed, K.S.Z., Kumar, B.S., Sheriff, S., Antihyperglycemic and antioxidant effects of Solanum xanthocarpum leaves (field grown & in vitro raised) extracts on alloxan induced diabetic rats. Asian Pac. J. Trop. Med. 4:10 (2011), 778–785.
118. Cazarolli, L.H., Folador, P., Moresco, H.H., Brighente, I.M.C., Pizzolatti, M.G., Silva, F.R.M.B., Stimulatory effect of apigenin-6-c-ß-l-fucopyranoside on insulin secretion and glycogen synthesis. Eur. J. Med. Chem. 44:11 (2009), 4668–4673.
119. Sathya, A., Siddhuraju, P., Role of phenolics as antioxidants, biomolecule protectors and as anti-diabetic factors-evaluation on bark and empty pods of Acacia auriculiformis. Asian Pac. J. Trop. Med. 5:10 (2012), 757–765.
120. Silva, F.R.M.B., Szpoganicz, B., Pizzolatti, M.G., Willrich, M.A.V., de Sousa, E., Acute effect of Bauhinia forficata on serum glucose levels in normal and alloxan-induced diabetic rats. J. Ethnopharmacol. 83:1 (2002), 33–37.
121. Bao, H., Chen, L., Icariin reduces mitochondrial oxidative stress injury in diabetic rat hearts. Zhongguo Zhong yao za zhi 36:11 (2011), 1503–1507.
122. Cazarolli, L.H., Pereira, D.F., Kappel, V.D., Folador, P., Figueiredo, M.d.S.R.B., Pizzolatti, M.G., Silva, F.R.M.B., Insulin signaling: a potential signaling pathway for the stimulatory effect of kaempferitrin on glucose uptake in skeletal muscle. Eur. J. Pharmacol. 712:1 (2013), 1–7.
123. Fang, X.-K., Gao, J., Zhu, D.-N., Kaempferol and quercetin isolated from Euonymus alatus improve glucose uptake of 3T3-L1 cells without adipogenesis activity. Life Sci. 82:11 (2008), 615–622.
124. Zhang, Y., Liu, D., Flavonol kaempferol improves chronic hyperglycemia-impaired pancreatic beta-cell viability and insulin secretory function. Eur. J. Pharmacol. 670:1 (2011), 325–332.
125. Jorge, A.P., Horst, H., de Sousa, E., Pizzolatti, M.G., Silva, F.R.M.B., Insulinomimetic effects of kaempferitrin on glycaemia and on 14C-glucose uptake in rat soleus muscle. Chem. Biol. Interact. 149:2 (2004), 89–96.
126. Li, J.M., Che, C.T., Lau, C.B., Leung, P.S., Cheng, C.H., Inhibition of intestinal and renal Na+-glucose cotransporter by naringenin. Int. J. Biochem. Cell Biol. 38:5 (2006), 985–995.
127. Mahmoud, A.M., Ashour, M.B., Abdel-Moneim, A., Ahmed, O.M., Hesperidin and naringin attenuate hyperglycemia-mediated oxidative stress and proinflammatory cytokine production in high fat fed/streptozotocin-induced type 2 diabetic rats. J. Diabetes Complications 26:6 (2012), 483–490.
128. Ortiz-Andrade, R., Sánchez-Salgado, J., Navarrete-Vázquez, G., Webster, S., Binnie, M., García-Jiménez, S., León-Rivera, I., Cigarroa-Vázquez, P., Villalobos-Molina, R., Estrada-Soto, S., Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rat models and its implications on extra-pancreatic glucose regulation. Diabetes Obes. Metab. 10:11 (2008), 1097–1104.
129. Hasan, M.M., Ahmed, Q.U., Soad, S.Z.M., Latip, J., Taher, M., Syafiq, T.M.F., Sarian, M.N., Alhassan, A.M., Zakaria, Z.A., Flavonoids from Tetracera indica Merr. induce adipogenesis and exert glucose uptake activities in 3T3-L1 adipocyte cells. BMC Complement. Altern. Med., 17(1), 2017, 431.
130. Eneroth, G., Ahlund, K., Biological assay of insulin by blood sugar determination in mice. Acta Pharm. Suec. 5:6 (1968), 591–594.
131. Pharmacopoeia, E., European Pharmacopoeia. 2002, Council of Europe, Strasbourg.
132. Kohn, A.D., Summers, S.A., Birnbaum, M.J., Roth, R.A., Expression of a constitutively active AKT Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J. Biol. Chem. 271:49 (1996), 31372–31378.
133. Karlsson, M., Thorn, H., Danielsson, A., Stenkula, K.G., Ost, A., Gustavsson, J., Nystrom, F.H., Stralfors, P., Colocalization of insulin receptor and insulin receptor substrate-1 to caveolae in primary human adipocytes – cholesterol depletion blocks insulin signalling for metabolic and mitogenic control. Eur. J. Biochem. 271:12 (2004), 2471–2479.