Glucoraphanin ameliorates obesity and insulin resistance through adipose tissue browning and reduction of metabolic endotoxemia in mice

Diabetes

Volumn 66, Issue 5, 2017, Pages 1222-1236

  Nagata, Naoto ^a   Xu, Liang ^a   Kohno, Susumu ^a   Ushida, Yusuke ^b   Aoki, Yudai ^b   Umeda, Ryohei ^b   Fuke, Nobuo ^b   Zhuge, Fen ^a   Ni, Yinhua ^a   Nagashimada, Mayumi ^a   Takahashi, Chiaki ^a   Suganuma, Hiroyuki ^b   Kaneko, Shuichi ^a   Ota, Tsuguhito ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b KAGOME CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; LIPOPOLYSACCHARIDE; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2; UNCOUPLING PROTEIN 1; GLUCORAPHANIN; GLUCOSINOLATE; IMIDOESTER; NFE2L2 PROTEIN, MOUSE; UCP1 PROTEIN, MOUSE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DESULFOVIBRIONACEAE; DIET INDUCED OBESITY; ENDOTOXEMIA; ENERGY BALANCE; GLUCOSE TOLERANCE; INDIRECT CALORIMETRY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTESTINE FLORA; LIPID DIET; LIPID PEROXIDATION; MACROPHAGE; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDOX STRESS; WEIGHT GAIN; ANIMAL; BLOOD; BROWN ADIPOSE TISSUE; DESULFOVIBRIO; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; INFLAMMATION; KNOCKOUT MOUSE; LIVER; METABOLISM; OBESITY; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; DESULFOVIBRIO; DIET, HIGH-FAT; ENDOTOXEMIA; ENERGY METABOLISM; GASTROINTESTINAL MICROBIOME; GLUCOSINOLATES; IMIDOESTERS; INFLAMMATION; INSULIN RESISTANCE; LIPID PEROXIDATION; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; UNCOUPLING PROTEIN 1;

EID: 85019363454     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db16-0662     Document Type: Article

References (49)

1. Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-1772
2. Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008;57:1470-1481
3. Dietrich MO, Horvath TL. Limitations in anti-obesity drug development: the critical role of hunger-promoting neurons. Nat Rev Drug Discov 2012;11:675-691
4. Sanyal AJ, Chalasani N, Kowdley KV, et al.; NASH CRN. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med 2010;362:1675-1685
5. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 2004;10:549-557
6. Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 1997;236:313-322
7. Uruno A, Furusawa Y, Yagishita Y, et al. The Keap1-Nrf2 system prevents onset of diabetes mellitus. Mol Cell Biol 2013;33:2996-3010
8. Yates MS, Tran QT, Dolan PM, et al. Genetic versus chemoprotective activation of Nrf2 signaling: overlapping yet distinct gene expression profiles between Keap1 knockout and triterpenoid-treated mice. Carcinogenesis 2009;30:1024-1031
9. Shin S, Wakabayashi J, Yates MS, et al. Role of Nrf2 in prevention of highfat diet-induced obesity by synthetic triterpenoid CDDO-imidazolide. Eur J Pharmacol 2009;620:138-144
10. Saha PK, Reddy VT, Konopleva M, Andreeff M, Chan L. The triterpenoid 2-cyano-3, 12-dioxooleana-1, 9-dien-28-oic-acid methyl ester has potent antidiabetic effects in diet-induced diabetic mice and Lepr (db/db) mice. J Biol Chem 2010;285:40581-40592
11. Yu Z, Shao W, Chiang Y, et al. Oltipraz upregulates the nuclear factor (erythroid-derived 2)-like 2 [corrected] (NRF2) antioxidant system and prevents insulin resistance and obesity induced by a high-fat diet in C57BL/6J mice. Diabetologia 2011;54:922-934
12. de Zeeuw D, Akizawa T, Audhya P, et al.; BEACON Trial Investigators. Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease. N Engl J Med 2013;369:2492-2503
13. Kelley MJ, Glaser EM, Herndon JE 2nd, et al. Safety and efficacy of weekly oral oltipraz in chronic smokers. Cancer Epidemiol Biomarkers Prev 2005;14:892-899
14. Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci U S A 1997;94:10367-10372
15. Zhang Y, Talalay P, Cho CG, Posner GH. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci U S A 1992;89:2399-2403
16. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev 1998;7:1091-1100
17. Kensler TW, Ng D, Carmella SG, et al. Modulation of the metabolism of airborne pollutants by glucoraphanin-rich and sulforaphane-rich broccoli sprout beverages in Qidong, China. Carcinogenesis 2012;33:101-107
18. Kikuchi M, Ushida Y, Shiozawa H, et al. Sulforaphane-rich broccoli sprout extract improves hepatic abnormalities in male subjects. World J Gastroenterol 2015;21:12457-12467
19. Wade KL, Garrard IJ, Fahey JW. Improved hydrophilic interaction chromatography method for the identification and quantification of glucosinolates. J Chromatogr A 2007;1154:469-472
20. Nagata N, Matsuo K, Bettaieb A, et al. Hepatic Src homology phosphatase 2 regulates energy balance in mice. Endocrinology 2012;153:3158-3169
21. Aune UL, Ruiz L, Kajimura S. Isolation and differentiation of stromal vascular cells to beige/brite cells. J Vis Exp 2013; (73): e50191
22. Kitade H, Sawamoto K, Nagashimada M, et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 2012;61:1680-1690
23. Kim SW, Suda W, Kim S, et al. Robustness of gut microbiota of healthy adults in response to probiotic intervention revealed by high-throughput pyrosequencing. DNA Res 2013;20:241-253
24. Greaney AJ, Maier NK, Leppla SH, Moayeri M. Sulforaphane inhibits multiple inflammasomes through an Nrf2-independent mechanism. J Leukoc Biol 2016;99:189-199
25. Myzak MC, Karplus PA, Chung FL, Dashwood RH. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 2004;64:5767-5774
26. Cohen P, Levy JD, Zhang Y, et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 2014;156:304-316
27. Huang W, Metlakunta A, Dedousis N, et al. Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 2010;59:347-357
28. Obstfeld AE, Sugaru E, Thearle M, et al. C-C chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis. Diabetes 2010;59:916-925
29. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004;25:677-686
30. Zhang C, Zhang M, Wang S, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 2010;4:232-241
31. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009;137:1716-24.e1, 2
32. Conaway CC, Wang CX, Pittman B, et al. Phenethyl isothiocyanate and sulforaphane and their N-acetylcysteine conjugates inhibit malignant progression of lung adenomas induced by tobacco carcinogens in A/J mice. Cancer Res 2005;65:8548-8557
33. Shen G, Khor TO, Hu R, et al. Chemoprevention of familial adenomatous polyposis by natural dietary compounds sulforaphane and dibenzoylmethane alone and in combination in ApcMin/+ mouse. Cancer Res 2007;67:9937-9944
34. Pi J, Leung L, Xue P, et al. Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against dietinduced obesity. J Biol Chem 2010;285:9292-9300
35. Schneider K, Valdez J, Nguyen J, et al. Increased energy expenditure, Ucp1 expression, and resistance to diet-induced obesity in mice lacking nuclear factorerythroid-2-related transcription factor-2 (Nrf2). J Biol Chem 2016;291:7754-7766
36. Hou Y, Xue P, Bai Y, et al. Nuclear factor erythroid-derived factor 2-related factor 2 regulates transcription of CCAAT/enhancer-binding protein β during adipogenesis. Free Radic Biol Med 2012;52:462-472
37. Rim JS, Kozak LP. Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene. J Biol Chem 2002;277:34589-34600
38. Kajimura S, Spiegelman BM, Seale P. Brown and beige fat: physiological roles beyond heat generation. Cell Metab 2015;22:546-559
39. Chouchani ET, Kazak L, Jedrychowski MP, et al. Mitochondrial ROS regulate thermogenic energy expenditure and sulfenylation of UCP1. Nature 2016;532:112-116
40. Ma KL, Ruan XZ, Powis SH, Chen Y, Moorhead JF, Varghese Z. Inflammatory stress exacerbates lipid accumulation in hepatic cells and fatty livers of apolipoprotein E knockout mice. Hepatology 2008;48:770-781
41. Lawler JF Jr, Yin M, Diehl AM, Roberts E, Chatterjee S. Tumor necrosis factor-alpha stimulates the maturation of sterol regulatory element binding protein-1 in human hepatocytes through the action of neutral sphingomyelinase. J Biol Chem 1998;273:5053-5059
42. Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006;116:1494-1505
43. Weisberg SP, Hunter D, Huber R, et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006;116:115-124
44. Patsouris D, Li PP, Thapar D, Chapman J, Olefsky JM, Neels JG. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab 2008;8:301-309
45. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 2008;7:496-507
46. Xiao S, Fei N, Pang X, et al. A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome. FEMS Microbiol Ecol 2014;87:357-367
47. Aires A, Mota VR, Saavedra MJ, Rosa EA, Bennett RN. The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J Appl Microbiol 2009;106:2086-2095
48. Sofrata A, Santangelo EM, Azeem M, Borg-Karlson A-K, Gustafsson A, Pütsep K. Benzyl isothiocyanate, a major component from the roots of Salvadora persica is highly active against gram-negative bacteria. PLoS One 2011;6:e23045
49. Fahey JW, Haristoy X, Dolan PM, et al. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci U S A 2002;99:7610-7615