Isothiocyanate-rich Moringa oleifera extract reduces weight gain, insulin resistance, and hepatic gluconeogenesis in mice

Molecular Nutrition and Food Research

Volumn 59, Issue 6, 2015, Pages 1013-1024

  Rojas Silva, Patricio ^a   Tumer, Tugba Boyunegmez ^a,b   Kuhn, Peter ^a   Richard, Allison J ^c   Wicks, Shawna ^c   Stephens, Jacqueline M ^c   Wang, Zhong ^c   Mynatt, Randy ^c   Cefalu, William ^c   Raskin, Ilya ^a  

^a RUTGERS UNIVERSITY   (United States)

^b ÇANAKKALE ONSEKIZ MART UNIVERSITY   (Turkey)

^c PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Diabetes; Insulin resistance; Isothiocyanates; Moringa oleifera; Obesity

Indexed keywords

MORINGA; MORINGA OLEIFERA; MUS;

ANTIDIABETIC AGENT; ANTIOBESITY AGENT; CHOLESTEROL; GLUCOSE 6 PHOSPHATASE; INSULIN; INTERLEUKIN 1BETA; ISOTHIOCYANIC ACID; ISOTHIOCYANIC ACID DERIVATIVE; LEPTIN; PLANT EXTRACT; RESISTIN; RETN PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ADIPOSE TISSUE; ANIMAL; BLOOD; BODY COMPOSITION; C57BL MOUSE; CHEMISTRY; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; FATTY LIVER; GLUCONEOGENESIS; INSULIN RESISTANCE; LIPID DIET; LIVER; MALE; METABOLISM; MORINGA OLEIFERA; MOUSE; OBESITY; WEIGHT GAIN;

ADIPOSE TISSUE; ANIMALS; ANTI-OBESITY AGENTS; BODY COMPOSITION; CHOLESTEROL; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; FATTY LIVER; GLUCONEOGENESIS; GLUCOSE-6-PHOSPHATASE; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-1BETA; ISOTHIOCYANATES; LEPTIN; LIVER; MALE; MICE; MICE, INBRED C57BL; MORINGA OLEIFERA; OBESITY; PLANT EXTRACTS; RESISTIN; TUMOR NECROSIS FACTOR-ALPHA; WEIGHT GAIN;

EID: 84930179436     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400679     Document Type: Article

References (48)

1. Mbikay, M., Therapeutic potential of Moringa oleifera leaves in chronic hyperglycemia and dyslipidemia: a review. Front Pharmacol. 2012, 3, 1-12.
2. Waterman, C., Cheng, D. M., Rojas-Silva, P., Poulev, A. et al., Stable, water extractable isothiocyanates from Moringa oleifera leaves attenuate inflammation in vitro. Phytochemistry 2014, 103, 114-122.
3. Cheenpracha, S., Park, E.-J., Yoshida, W. Y., Barit, C. et al., Potential anti-inflammatory phenolic glycosides from the medicinal plant Moringa oleifera fruits. Bioorgan. Med. Chem. 2010, 18, 6598-6602.
4. Bae, J. Y., Lim, S. S., Kim, S. J., Choi, J. S., Park, J. et al., Bog blueberry anthocyanins alleviate photoaging in ultraviolet-B irradiation-induced human dermal fibroblasts. Mol. Nutr. Food Res. 2009, 53, 726-738.
5. Brunelli, D., Tavecchio, M., Falcioni, C., Frapolli, R. et al., The isothiocyanate produced from glucomoringin inhibits NF-kB and reduces myeloma growth in nude mice in vivo. Biochem. Pharmacol. 2010, 79, 1141-1148.
6. Faizi, S., Siddiqui, B. S., Saleem, R., Siddiqui, S. et al., Isolation and structure elucidation of new nitrile and mustard oil glycosides from Moringa oleifera and their effect on blood pressure. J. Nat. Prod. 1994, 57, 1256-1261.
7. Shapiro, T. A., Fahey, J. W., Wade, K. L., Stephenson, K. K., Talalay, P., Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts metabolism and excretion in humans. Cancer Epidem. Biomar. 2001, 10, 501-508.
8. Higdon, J. V., Delage, B., Williams, D. E., Dashwood, R. H., Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol. Res. 2007, 55, 224-236.
9. Verhoeven, D. T., Goldbohm, R.A., vanPoppel, G., Verhagen, H., vanden Brandt, P.A., Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidem. Biomar. 1996, 5, 733-748.
10. Traka, M., Mithen, R., Glucosinolates, isothiocyanates and human health. Phytochem. Rev. 2009, 8, 269-282.
11. Mirmiran, P., Bahadoran, Z., Hosseinpanah, F., Keyzad, A., Azizi, F., Effects of broccoli sprout with high sulforaphane concentration on inflammatory markers in type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial. J. Funct. Foods 2012, 4, 837-841.
12. Bahadoran, Z., Tohidi, M., Nazeri, P., Mehran, M. et al., Effect of broccoli sprouts on insulin resistance in type 2 diabetic patients: a randomized double-blind clinical trial. Int. J. Food Sci. Nutr. 2012, 63, 767-771.
13. Bahadoran, Z., Mirmiran, P., Azizi, F., Potential efficacy of broccoli sprouts as a unique supplement for management of type 2 diabetes and its complications. J. Med. Food 2013, 16, 375-382.
14. Wu, H., Liang, H., Yuan, Q., Wang, T., Yan, X., Preparation and stability investigation of the inclusion complex of sulforaphane with hydroxypropyl-β-cyclodextrin. Carbohyd. Polym. 2010, 82, 613-617.
15. Park, E.-J., Cheenpracha, S., Chang, L. C., Kondratyuk, T. P., Pezzuto, J. M., Inhibition of lipopolysaccharide-induced cyclooxygenase-2 and inducible nitric oxide synthase expression by 4-[(2′-O-acetyl-α-L-rhamnosyloxy)benzyl]isothiocyanate from Moringa oleifera. Nutr. Cancer 2011, 63, 971-982.
16. Shetty, P., Public health: India's diabetes time bomb. Nature 2012, 485, S14-S16.
17. Mbanya, J. C. N., Motala, A. A., Sobngwi, E., Assah, F. K., Enoru, S. T., Diabetes in Sub-Saharan Africa. Lancet 2010, 375, 2254-2266.
18. Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N. et al., Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014, 6736, 60460-60468.
19. Folch, J., Lees, M., Sloane-Stanley, G., A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226, 497-509.
20. Schmittgen, T. D., Livak, K. J., Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3, 1101-1108.
21. Wang, Z. Q., Zhang, X. H., Yu, Y., Poulev, A. et al., Bioactives from bitter melon enhance insulin signaling and modulate acyl carnitine content in skeletal muscle in high-fat diet-fed mice. J. Nutr. Biochem. 2011, 22, 1064-1073.
22. Cheng, D. M., Kuhn, P., Poulev, A., Rojo, L. E. et al., In vivo and in vitro antidiabetic effects of aqueous cinnamon extract and cinnamon polyphenol-enhanced food matrix. Food Chem. 2012, 135, 2994-3002.
23. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55-63.
24. Richard, A. J., Fuller, S., Fedorcenco, V., Beyl, R. et al., Artemisia scoparia enhances adipocyte development and endocrine function in vitro and enhances insulin action in vivo. Plos One 2014, 9, e98897.
25. Ndong, M., Uehara, M., Katsumata, S., Effects of oral administration of Moringa oleifera Lam on glucose tolerance in Goto-Kakizaki and Wistar rats. J. Clin. Biochem. Nutr. 2007, 40, 229-233.
26. Miller, R. S., Becker, K. G, Prabhu, V., Cooke, D. W., Adipocyte gene expression is altered in formerly obese mice and as a function of diet composition. J. Nutr. 2008, 138, 1033-1038.
27. Korda, M., Kubant, R., Patton, S., Malinski, T., Leptin-induced endothelial dysfunction in obesity. Am. J. Physiol-Heart C. 2008, 295, H1514-H1521.
28. Moller, D. E., Potential role of TNF-alpha in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrin. Met. 2000, 11, 212-217.
29. Uysal, K. T., Wiesbrock, S. M., Marino, M. W., Hotamisligil, G. S., Protection from obesity-induced insulin resistance in mice lacking TNFalpha function. Nature 1997, 389, 610-614.
30. Schreyer, S. A., Chua Jr, S. C., LeBoeuf, R. C., Obesity and diabetes in TNF-alpha receptor-deficient mice. J. Clinl. Invest. 1998, 102, 402-411.
31. Hotamisligil, G. S., Murray, D. L., Choy, L. N., Spiegelman, B. M., Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc. Natl. Acad. Sci. 1994, 91, 4854-4858.
32. Bose, M., Lambert, J. D., Ju, J., Reuhl, K. R. et al., The major green tea polyphenol, (-)-epigallocatechin-3-gallate, inhibits obesity, metabolic syndrome, and fatty liver disease in high-fat-fed mice. J. Nutr. 2008, 138, 1677-1683.
33. Hundal, R. S., Krssak, M., Dufour, S., Laurent, D. et al., Mechanism by which metformin reduces glucose production in type 2 diabetes. Diabetes 2000, 49, 2063-2069.
34. Knowler, W. C., Barrett-Connor, E., Fowler, S. E., Hamman, R. F. et al., Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 2002, 346, 393-403.
35. Rena, G., Pearson, E. R., Sakamoto, K., Molecular mechanism of action of metformin: old or new insights? Diabetologia 2013, 56, 1898-1906.
36. Geerling, J. J., Boon, M. R., vander Zon, G. C., vanden Berg, S. A. et al., Metformin lowers plasma triglycerides by promoting VLDL-triglyceride clearance by brown adipose tissue in mice. Diabetes 2014, 63, 880-891.
37. Madiraju, A. K., Erion, D. M., Rahimi, Y., Zhang, X.-M. et al., Metformin suppresses gluconeogenesis by inhibiting mitochondrial glycerophosphate dehydrogenase. Nature 2014, 510, 542-546.
38. Widjaja, A., Stratton, I. M., Horn, R., Holman, R. R. et al., UKPDS 20: plasma leptin, obesity, and plasma insulin in type 2 diabetic subjects. J. Clin. Endocrinol. Metab. 1997, 82, 654-657.
39. Steppan, C. M., Bailey, S. T., Bhat, S., Brown, E. J. et al., The hormone resistin links obesity to diabetes. Nature 2001, 409, 307-312.
40. Srinivasan, K., Viswanad, B., Asrat, L., Kaul, C. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol. Res. 2005, 52, 313-320.
41. El Messaoudi, S., Rongen, G. A., deBoer, R. A., Riksen, N. P., The cardioprotective effects of metformin. Curr. Opin. Lipidol. 2011, 22, 445-453.
42. Henry-Vitrac, C., Ibarra, A., Roller, M., Mérillon, J.-M., Vitrac, X., Contribution of chlorogenic acids to the inhibition of human hepatic glucose-6-phosphatase activity in vitro by Svetol, a standardized decaffeinated green coffee extract. J. Agric. Food Chem. 2010, 58, 4141-4144.
43. Tsukita, S., Yamada, T., Uno, K., Takahashi, K. et al., Hepatic glucokinase modulates obesity predisposition by regulating BAT thermogenesis via neural signals. Cell Metab. 2012, 16, 825-832.
44. Ferre, T., Riu, E., Franckhauser, S., Agudo, J., Bosch, F., Long-term overexpression of glucokinase in the liver of transgenic mice leads to insulin resistance. Diabetologia 2003, 46, 1662-1668.
45. Cousin, B., Cinti, S., Morroni, M., Raimbault, S. et al., Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J. Cell Sci. 1992, 103, 931-942.
46. Heilbronn, L. K., Gregersen, S., Shirkhedkar, D., Hu, D., Campbell, L. V., Impaired fat oxidation after a single high-fat meal in insulin-sensitive nondiabetic individuals with a family history of type 2 diabetes. Diabetes 2007, 56, 2046-2053.
47. Langin, D., Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome. Pharmacol. Res. 2006, 53, 482-491.
48. Ong, K. T., Mashek, M. T., Bu, S. Y., Greenberg, A. S., Mashek, D. G., Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 2011, 53, 116-126.