Mulberry leaf alleviates streptozotocin-induced diabetic rats by attenuating NEFA signaling and modulating intestinal microflora

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Sheng, Yao ^a   Zheng, Shujuan ^a   Ma, Tianshi ^a   Zhang, Chuanhai ^a   Ou, Xiaoqun ^a   He, Xiaoyun ^a,b   Xu, Wentao ^a,b   Huang, Kunlun ^a,b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; PLANT EXTRACT;

ANIMAL; CHEMISTRY; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; MORUS; PATHOLOGY; PLANT LEAF; RAT; SIGNAL TRANSDUCTION;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; FATTY ACIDS, NONESTERIFIED; MORUS; PLANT EXTRACTS; PLANT LEAVES; RATS; SIGNAL TRANSDUCTION;

EID: 85029846767     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-12245-2     Document Type: Article

References (73)

1. IDF. International Diabetes Federation Diabetes Atlas Seventh Edition 2015. International Diabetes Federation. Seventh Edition, 9-12 (2016).
2. Mckimmie, R. L. et al. Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for type 2 diabetes: The Diabetes Heart Study. Am J Gastroenterol. 103, 3029-3035 (2008).
3. Kitabchi, A. E., Umpierrez, G. E., Miles, J. M. & Fisher, J. N. Hyperglycemic crises in adult patients with diabetes. Diabetes care. 32, 1335-1343 (2009).
4. Wang, C. et al. Increased serum microRNAs are closely associated with the presence of microvascular complications in type 2 diabetes mellitus. Sci Rep. 6, 20032 (2016).
5. Carlson, R. W. Manual of Intensive Care Medicine. Jama J Am Med Assoc. 253, 84-84 (2001).
6. De Smet, P. A. G. M. Drug therapy: Herbal remedies. New Engl J Med 347, 2046-2056 (2002).
7. Jouad, H., Haloui, M., Rhiouani, H., Hilaly, J. E. & Eddouks, M. Ethnobotanical survey of medicinal plants used for the treatment of diabetes, cardiac and renal diseases in the North centre region of Morocco (Fez-Boulemane). J Ethnopharmacol. 77, 175-182 (2001).
8. Asano, N. et al. Polyhydroxylated alkaloids isolated from mulberry trees (Morus alba L.) and silkworms (Bombyx mori L.). J Agr Food Chem. 49, 4208-4213 (2001).
9. Venkatesh Kumar, R. & Chauhan, S. Mulberry: life enhancer. J Med Plants Res. 2, 271-278 (2008).
10. Kimura, T. et al. Determination of 1-deoxynojirimycin in mulberry leaves using hydrophilic interaction chromatography with evaporative light scattering detection. J Agr Food Chem. 52, 1415-1418 (2004).
11. Reaven, G. M., Hollenbeck, C., Jeng, C.-Y., Wu, M. S. & Chen, Y.-D. I. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes. 37, 1020-1024 (1988).
12. Boden, G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes. 46, 3-10 (1997).
13. Roden, M. et al. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest. 97, 2859-2865 (1996).
14. Santomauro, A. et al. Overnight lowering of free fatty acids with Acipimox improves insulin resistance and glucose tolerance in obese diabetic and nondiabetic subjects. Diabetes. 48, 1836-1841 (1999).
15. Dobbins, R. L. et al. A fatty acid-dependent step is critically important for both glucose-and non-glucose-stimulated insulin secretion. J Clin Invest. 101, 2370-2376 (1998).
16. Prentki, M., Joly, E., El-Assaad, W. & Roduit, R. Malonyl-CoA Signaling, Lipid Partitioning, and Glucolipotoxicity Role in-Cell Adaptation and Failure in the Etiology of Diabetes. Diabetes. 51, S405-S413 (2002).
17. Guo, Z. et al. Intestinal Microbiota Distinguish Gout Patients from Healthy Humans. Sci Rep. 6, 20602 (2016).
18. Matsumoto, M. et al. Impact of Intestinal Microbiota on Intestinal Luminal Metabolome. Sci Rep. 2, 233 (2011).
19. Karlsson, F. H. et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 498, 99-103 (2013).
20. Sepp, E., Kolk, H., Lõivukene, K. & Mikelsaar, M. Higher blood glucose level associated with body mass index and gut microbiota in elderly people. Microb Ecol Health Dis. 25, 22857 (2014).
21. Arimatsu, K. et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci Rep. 4, 4828 (2013).
22. Poroyko, V. A. et al. Chronic Sleep Disruption Alters Gut Microbiota, Induces Systemic and Adipose Tissue Inflammation and Insulin Resistance in Mice. Sci Rep. 6, 35405 (2016).
23. Khosravi, Y. et al. Helicobacter pylori infection can affect energy modulating hormones and body weight in germ free mice. Sci Rep. 5, 8731 (2015).
24. Zhang, X. et al. Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PloS one. 7, e42529 (2012).
25. Paulson, J. N., Stine, O. C., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat Methods. 10, 1200-1202 (2013).
26. Rosen, E. D. & Spiegelman, B. M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 444, 847-853 (2006).
27. Roden, M. et al. Effects of free fatty acid elevation on postabsorptive endogenous glucose production and gluconeogenesis in humans. Diabetes 49, 701-707 (2000).
28. Simha, V. & Garg, A. Lipodystrophy: lessons in lipid and energy metabolism. Curr Opin Lipidol. 17, 162-169 (2006).
29. Gil-Campos, M., Ramírez Tortosa, M. C., Aguilera, C. M., Cañete, R. & Gil, A. Fasting and postprandial adiponectin alterations anticipate NEFA and TNF-changes in prepubertal obese children. Nutr Metab Cardiovasc Dis. 21, 62-68 (2011).
30. Reddy, N. L. et al. Enhanced thermic effect of food, postprandial NEFA suppression and raised adiponectin in obese women who eat slowly. Clin Endocrinol. 82, 831-837 (2014).
31. Reed, M. J. et al. A new rat model of type 2 diabetes: The fat-fed, streptozotocin-treated rat. Metab Clin Exp. 49, 1390-1392 (2000).
32. Serrano-Martín, X., Payares, G. & Mendoza-León, A. Glibenclamide, a blocker of K + (ATP) channels, shows antileishmanial activity in experimental murine cutaneous leishmaniasis. Antimicrob Agents Ch. 50, 4214-4216 (2006).
33. Beck-Nielsen, H., Pedersen, O. & Lindskov, H. O. Increased insulin sensitivity and cellular insulin binding in obese diabetics following treatment with glibenclamide. Acta Endocrinol. 90, 451-462 (1979).
34. Carvalho-Martini, M., de Oliveira, D. S., Suzuki-Kemmelmeier, F. & Bracht, A. The action of glibenclamide on glycogen catabolism and related parameters in the isolated perfused rat liver. Res Commun Mol Path. 119, 115-126 (2006).
35. Okamoto, R. M. et al. Comparison with Glimepiride and Glibenclamide on Gycogen Accumulation in Liver. Diabetes. 56, pA677 (2007).
36. Kirpichnikov, D., McFarlane, S. I. & Sowers, J. R. Metformin: An update. Ann Intern Med. 137, 25-33 (2002).
37. Zhou, G. et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 108, 1167-1174 (2001).
38. Collier, C. A., Bruce, C. R., Smith, A. C., Lopaschuk, G. & Dyck, D. J. Metformin counters the insulin-induced suppression of fatty acid oxidation and stimulation of triacylglycerol storage in rodent skeletal muscle. Am J Physiol-Endoc M. 291, E182-E189 (2006).
39. Rena, G., Pearson, E. R. & Sakamoto, K. Molecular mechanism of action of metformin: old or new insights Diabetologia. 56, 1898-1906 (2013).
40. González-Ortiz, M. et al. Efficacy of glimepiride/metformin combination versus glibenclamide/metformin in patients with uncontrolled type 2 diabetes mellitus. J Diabetes Complica. 23, 376-379 (2009).
41. Tosi, F. et al. Combination treatment with metformin and glibenclamide versus single-drug therapies in type 2 diabetes mellitus: A randomized, double-blind, comparative study. Metabolism 52, 862-867 (2003).
42. Barelli, G. & De Regis, M. Glibenclamide-metformin combination for the treatment of diabetes mellitus of type II. U. S. Patent No. 5, 922, 769. (1999).
43. Katsube, T. et al. Antioxidant flavonol glycosides in mulberry (Morus alba L.) leaves isolated based on LDL antioxidant activity. Food Chem. 97, 25-31 (2006).
44. Katsube, T., Tsurunaga, Y., Sugiyama, M., Furuno, T. & Yamasaki, Y. Effect of air-drying temperature on antioxidant capacity and stability of polyphenolic compounds in mulberry (Morus alba L.) leaves. Food Chem. 113, 964-969 (2009).
45. Wu, C.-H. et al. Improvement in high-fat diet-induced obesity and body fat accumulation by a Nelumbo nucifera leaf flavonoid-rich extract in mice. J Agr Food Chem. 58, 7075-7081 (2010).
46. Naowaboot, J. et al. Mulberry leaf extract restores arterial pressure in streptozotocin-induced chronic diabetic rats. Nutr Res. 29, 602-608 (2009).
47. Kimura, T. et al. Food-grade mulberry powder enriched with 1-deoxynojirimycin suppresses the elevation of postprandial blood glucose in humans. J Agr Food Chem. 55, 5869-5874 (2007).
48. Dugo, P. et al. Characterization of the polyphenolic fraction of Morus alba leaves extracts by HPLC coupled to a hybrid ITTOF MS system. J Sep Sci. 32, 3627-3634 (2009).
49. Li, Y.-G. et al. Hybrid of 1-deoxynojirimycin and polysaccharide from mulberry leaves treat diabetes mellitus by activating PDX-1/ insulin-1 signaling pathway and regulating the expression of glucokinase, phosphoenolpyruvate carboxykinase and glucose-6-phosphatase in alloxan-induced diabetic mice. J Ethnopharmacol. 134, 961-970 (2011).
50. Naowaboot, J., Pannangpetch, P., Kukongviriyapan, V. & Kongyingyoes, B. Antihyperglycemic, antioxidant and antiglycation activities of mulberry leaf extract in streptozotocin-induced chronic diabetic rats. Plant Food Hum Nutr. 64, 116-121 (2009).
51. Wang, G. Singularity analysis of the AKT signaling pathway reveals connections between cancer and metabolic diseases. Phys Biol. 7, 046015 (2010).
52. Leung, N. et al. Prolonged increase of plasma non-esterified fatty acids fully abolishes the stimulatory effect of 24 hours of moderate hyperglycaemia on insulin sensitivity and pancreatic beta-cell function in obese men. Diabetologia. 47, 204-213 (2004).
53. Shulman, G. I. Cellular mechanisms of insulin resistance. J Clin Invest. 106, 171-176 (2000).
54. Shi, Y. et al. Resveratrol enhances HBV replication through activating Sirt1-PGC-1-PPAR pathway. Sci Rep. 6, 24744 (2016).
55. Patti, M. E. et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. PNAS. 100, 8466-8471 (2003).
56. Köhler, C. et al. Release of adenylate kinase 2 from the mitochondrial intermembrane space during apoptosis. Febs Lett. 447, 10-12 (1999).
57. Marini, C. et al. Divergent targets of glycolysis and oxidative phosphorylation result in additive effects of metformin and starvation in colon and breast cancer. Sci Rep. 6, 19569 (2016).
58. Mori, T. et al. Ultrastructural Localization of Adiponectin protein in Vasculature of Normal and Atherosclerotic mice. Sci Rep. 4, 4895 (2014).
59. Ukkola, O. & Santaniemi, M. Adiponectin: A link between excess adiposity and associated comorbidities J Mol Med. 80, 696-702 (2002).
60. Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature. 457, 480-484 (2009).
61. Ley, R. E. et al. Obesity alters gut microbial ecology. PNAS. 102, 11070-11075 (2005).
62. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 444, 1027-1131 (2006).
63. Larsen, N. et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PloS one. 5, e9085 (2010).
64. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature. 444, 1022-1023 (2006).
65. Wu, X. et al. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr Microbiol. 61, 69-78 (2010).
66. Cani, P. D. et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 58, 1091-1103 (2009).
67. Cani, P. D. et al. Changes in gut microbiota control intestinal permeability-induced inflammation in obese and diabetic mice through unexpected dependent mechanisms. Diabetologia. 51, S34-S35 (2008).
68. Greetham, H. L. et al. Allobaculum stercoricanis gen. nov., sp. nov., isolated from canine feces. Anaerobe. 10, 301-307 (2004).
69. Reeves, P. G., Nielsen, F. H. & Fahey Jr, G. C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J nutr. 123, 1939-1951 (1993).
70. Guo, M. et al. Combination of metagenomics and culture-based methods to study the interaction between ochratoxin a and gut microbiota. Toxicol Sci. 141, 314-323 (2014).
71. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 10, 996-998 (2013).
72. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb. 73, 5261-5267 (2007).
73. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).