Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice

ISME Journal

Volumn 9, Issue 1, 2015, Pages 1-15

  Wang, Jingjing ^a,b   Tang, Huang ^b   Zhang, Chenhong ^b   Zhao, Yufeng ^a   Derrien, Muriel ^c   Rocher, Emilie ^c   Van Hylckama Vlieg, Johan Et ^c   Strissel, Katherine ^d   Zhao, Liping ^a,b   Obin, Martin ^d   Shen, Jian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Shanghai Jiao Tong University   (China)

^c DANONE RESEARCH   (France)

^d TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS; LACTOBACILLUS; LACTOBACILLUS PARACASEI; LACTOBACILLUS RHAMNOSUS; MUS; OTUS;

PROBIOTIC AGENT;

ADVERSE EFFECTS; ANIMAL; BACTERIUM; BIFIDOBACTERIUM; C57BL MOUSE; CLASSIFICATION; FECES; GASTROINTESTINAL TRACT; INFLAMMATION; INTESTINE; ISOLATION AND PURIFICATION; LACTOBACILLUS; LIPID DIET; MALE; METABOLIC SYNDROME X; MICROBIOLOGY; MICROFLORA; MOUSE;

ANIMALS; BACTERIA; BIFIDOBACTERIUM; DIET, HIGH-FAT; FECES; GASTROINTESTINAL TRACT; INFLAMMATION; INTESTINES; LACTOBACILLUS; MALE; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; MICROBIOTA; PROBIOTICS;

EID: 84927694747     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.99     Document Type: Article

References (60)

1. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF. (2002). Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277: 1531-1537.
2. Amar J, Chabo C, Waget A, Klopp P, Vachoux C, Bermudez-Humaran LG et al. (2011). Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med 3: 559-572.
3. An HM, Park SY, Lee do K, Kim JR, Cha MK, Lee SW et al. (2011). Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10 116.
4. Araya MML, Reid G, Sanders ME, Stanton C. (2002). Guidelines for the Evaluation of Probiotics in Food. Jt. FAO/WHOWork. Group: London, UK; Ontario, Canada.
5. Aronsson L, Huang Y, Parini P, Korach-Andre M, Hakansson J, Gustafsson JA et al. (2010). Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS One 5: e13087.
6. Caesar R, Reigstad CS, Backhed HK, Reinhardt C, Ketonen M, Lunden GO et al. (2012). Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 61: 1701-1707.
7. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C et al. (2005). Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54: 2277-2286.
8. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. (2008). Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481.
9. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM et al. (2007). Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50: 2374-2383.
10. Carvalho BM, Guadagnini D, Tsukumo DM, Schenka AA, Latuf-Filho P, Vassallo J et al. (2012). Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 55: 2823-2834.
11. Chen J, Wang R, Li XF, Wang RL. (2012). Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. Br J Nutr 107: 1429-1434.
12. Chen JJ, Wang R, Li XF, Wang RL. (2011). Bifidobacterium longum supplementation improved high-fat-fed-induced metabolic syndrome and promoted intestinal Reg I gene expression. Exp Biol Med (Maywood) 236: 823-831.
13. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. (2005). Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46: 2347-2355.
14. Clarke SF, Murphy EF, O'Sullivan O, Ross RP, O'Toole PW, Shanahan F et al. (2013). Targeting the microbiota to address diet-induced obesity: a time dependent challenge. PLoS One 8: e65790.
15. Collins JW, Chervaux C, Raymond B, Derrien M, Brazeilles R, Kosta A et al. (2014). Fermented dairy products modulate C. rodentium induced colonic hyperplasia. J Infect Dis; e-pub ahead of print 4 April 2014; doi:10.1093/infdis/jiu205.
16. Delzenne NM, Neyrinck AM, Backhed F, Cani PD. (2011). Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7: 639-646.
17. Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM et al. (2013). Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62: 1112-1121.
18. Eckel RH, Grundy SM, Zimmet PZ. (2005). The metabolic syndrome. Lancet 365: 1415-1428.
19. Engeli S, Feldpausch M, Gorzelniak K, Hartwig F, Heintze U, Janke J et al. (2003). Association between adiponectin and mediators of inflammation in obese women. Diabetes 52: 942-947.
20. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB et al. (2013). Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110: 9066-9071.
21. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM et al. (2011). Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60: 2775-2786.
22. Fak F, Backhed F. (2012). Lactobacillus reuteri prevents dietinduced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/- mice. PLoS One 7: e46837.
23. Fei N, Zhao L. (2013). An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J 7: 880-884.
24. Gauffin Cano P, Santacruz A, Moya A, Sanz Y. (2012). Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One 7: e41079.
25. Grompone G, Martorell P, Llopis S, Gonzalez N, Genoves S, Mulet AP et al. (2012). Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS One 7: e52493.
26. Kanety H, Feinstein R, Papa MZ, Hemi R, Karasik A. (1995). Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1). Possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of IRS-1. J Biol Chem 270: 23780-23784.
27. Kim SW, Park KY, Kim B, Kim E, Hyun CK. (2013). Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431: 258-263.
28. Kondo T, Kishi M, Fushimi T, Kaga T. (2009). Acetic acid upregulates the expression of genes for fatty acid oxidation enzymes in liver to suppress body fat accumulation. J Agric Food Chem 57: 5982-5986.
29. Lam YY, Ha CW, Campbell CR, Mitchell AJ, Dinudom A, Oscarsson J et al. (2012). Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in dietinduced obese mice. PLoS One 7: e34233.
30. Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C et al. (2012). Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62: 1787-1794.
31. Lee HY, Park JH, Seok SH, Baek MW, Kim DJ, Lee KE et al. (2006). Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim Biophys Acta 1761: 736-744.
32. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. (2006). Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023.
33. Ma X, Hua J, Li Z. (2008). Probiotics improve high fat dietinduced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol 49: 821-830.
34. Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. (2012). Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog 53: 100-108.
35. Ohkawara S, Furuya H, Nagashima K, Asanuma N, Hino T. (2006). Effect of oral administration of Butyrivibrio fibrisolvens MDT-1 on experimental enterocolitis in mice. Clin Vaccine Immunol 13: 1231-1236.
36. Park DY, Ahn YT, Huh CS, McGregor RA, Choi MS. (2013a). Dual probiotic strains suppress high fructoseinduced metabolic syndrome. World J Gastroenterol 19: 274-283.
37. Park DY, Ahn YT, Park SH, Huh CS, Yoo SR, Yu R et al. (2013b). Supplementation of Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032 in dietinduced obese mice is associated with gut microbial changes and reduction in obesity. PLoS One 8: e59470.
38. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F et al. (2012). A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60.
39. Robinson CJ, Bohannan BJ, Young VB. (2010). From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74: 453-476.
40. Roselli M, Finamore A, Britti MS, Mengheri E. (2006). Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 95: 1177-1184.
41. Sakakibara S, Yamauchi T, Oshima Y, Tsukamoto Y, Kadowaki T. (2006). Acetic acid activates hepatic AMPK and reduces hyperglycemia in diabetic KK-A(y) mice. Biochem Biophys Res Commun 344: 597-604.
42. Sakamoto M, Lan PT, Benno Y. (2007). Barnesiella viscericola gen. nov., sp. nov., a novel member of the family Porphyromonadaceae isolated from chicken caecum. Int J Syst Evol Microbiol 57: 342-346.
43. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. (2010). Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice. Diabetes 59: 1171-1181.
44. Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS et al. (2014). An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63: 727-735.
45. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW 2nd, DeFuria J, Jick Z et al. (2007). Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56: 2910-2918.
46. Sun L, Yu Z, Ye X, Zou S, Li H, Yu D et al. (2010). A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care 33: 1925-1932.
47. Tuovinen E, Keto J, Nikkila J, Matto J, Lahteenmaki K. (2013). Cytokine response of human mononuclear cells induced by intestinal Clostridium species. Anaerobe 19: 70-76.
48. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031.
49. Veiga P, Gallini CA, Beal C, Michaud M, Delaney ML, DuBois A et al. (2010). Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc Natl Acad Sci USA 107: 18132-18137.
50. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF et al. (2012). Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143: 913-916. e917.
51. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. (2003). Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
52. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ et al. (2003). Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830.
53. Xu RY, Wan YP, Fang QY, Lu W, Cai W. (2012). Supplementation with probiotics modifies gut flora and attenuates liver fat accumulation in rat nonalcoholic fatty liver disease model. J Clin Biochem Nutr 50: 72-77.
54. Yamashita H, Fujisawa K, Ito E, Idei S, Kawaguchi N, Kimoto M et al. (2007). Improvement of obesity and glucose tolerance by acetate in Type 2 diabetic Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Biosci Biotechnol Biochem 71: 1236-1243.
55. Yin YN, Yu QF, Fu N, Liu XW, Lu FG. (2010). Effects of four Bifidobacteria on obesity in high-fat diet induced rats. World J Gastroenterol 16: 3394-3401.
56. Yoo SR, Kim YJ, Park DY, Jung UJ, Jeon SM, Ahn YT et al. (2013). Probiotics L. plantarum and L. curvatus in combination alter hepatic lipid metabolism and suppress diet-induced obesity. Obesity (Silver Spring) 21: 2571-2578.
57. Zhang C, Zhang M, Pang X, Zhao Y, Wang L, Zhao L. (2012a). Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J 6: 1848-1857.
58. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W et al. (2010). Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4: 232-241.
59. Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C et al. (2012b). Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One 7: e42529.
60. Zhao X, Higashikawa F, Noda M, Kawamura Y, Matoba Y, Kumagai T et al. (2012). The obesity and fatty liver are reduced by plant-derived Pediococcus pentosaceus LP28 in high fat diet-induced obese mice. PLoS One 7: e30696.