Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zhang, Zhen ^a   Zhou, Zhigang ^a   Li, Yu ^a   Zhou, Linkang ^b   Ding, Qianwen ^a   Xu, Li ^a,b  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; CHOLESTEROL; PROBIOTIC AGENT; TLR2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2; TRIACYLGLYCEROL;

ADIPOGENESIS; ANIMAL; BLOOD; CELL CULTURE; CHEMISTRY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; FIBROBLAST; GENE KNOCKDOWN; INFLAMMATION; ISOLATION AND PURIFICATION; LACTOBACILLUS RHAMNOSUS; LIPID DIET; LIVER; METABOLISM; MOUSE; OBESITY; PATHOLOGY;

ADIPOGENESIS; ANIMALS; CELLS, CULTURED; CHOLESTEROL; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; INFLAMMATION; LACTOBACILLUS RHAMNOSUS; LIVER; MICE; OBESITY; POLYSACCHARIDES, BACTERIAL; PROBIOTICS; TOLL-LIKE RECEPTOR 2; TRIGLYCERIDES;

EID: 84994049570     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36083     Document Type: Article

References (59)

1. Locke, A. E. et al. Genetic studies of body mass index yield new insights for obesity biology. Nature 518, 197-206 (2015).
2. Friedman, J. M.Obesity: Causes and control of excess body fat. Nature 459, 340-342 (2009).
3. Dhurandhar, N. V. A framework for identification of infections that contribute to human obesity. Lancet Infect. Dis. 11, 963-969 (2011).
4. Turnbaugh, P. J., Bäckhed, F., Fulton, L. & Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213-223 (2008).
5. Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013).
6. Schwiertz, A. et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18, 190-195 (2010).
7. Million, M. et al. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes. (Lond.) 36, 817-825 (2012).
8. Neyrinck, A. M. et al. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS One 6, e20944 (2011).
9. Kalliomäki, M., Collado, M. C., Salminen, S. & Isolauri, E. Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 87, 534-538 (2008).
10. Soderborg, T. K., Borengasser, S. J., Barbour, L. A. & Friedman, J. E. Microbial transmission from mothers with obesity or diabetes to infants: an innovative opportunity to interrupt a vicious cycle. Diabetologia 2016, 1-12 (2016).
11. Agus, A. et al. Western diet induces a shift in microbiota composition enhancing susceptibility to Adherent-Invasive E. coli infection and intestinal inflammation. Sci. Rep. 6 (2016).
12. Hill, C. et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506-514 (2014).
13. Tuomola, E. M. & Salminen, S. J. Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int. J. Food Microbiol. 41, 45-51 (1998).
14. Ouwehand, A. C., Kirjavainen, P. V., Grönlund, M. M., Isolauri, E. & Salminen, S. J. Adhesion of probiotic micro-organisms to intestinal mucus. Int. Dairy J. 9, 623-630 (1999).
15. Donato, K. A., Gareau, M. G., Wang, Y. J. J. & Sherman, P. M. Lactobacillus rhamnosus GG attenuates interferon-γ and tumour necrosis factor-a-induced barrier dysfunction and pro-inflammatory signalling. Microbiology 156, 3288-3297 (2010).
16. Lee, S. K., Yang, K. M., Cheon, J. H., Kim, T. I. & Kim, W. H. Anti-inflammatory mechanism of Lactobacillus rhamnosus GG in lipopolysaccharide-stimulated HT-29 cell. Korean J. Gastroenterol. 60, 86-93 (2012).
17. Ganguli, K. et al. Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatr. Res (2015).
18. Wang, Y. et al. Lactobacillus rhamnosus GG reduces hepatic TNFa production and inflammation in chronic alcohol-induced liver injury. J. Nutr. Biochem. 24, 1609 (2013).
19. Harb, H. et al. Neonatal supplementation of processed supernatant from Lactobacillus rhamnosus GG improves allergic airway inflammation in mice later in life. Clin. Exp. Allergy 43, 353-364 (2013).
20. Kim, S. W., Park, K. Y., Kim, B., Kim, E. & Hyun, C. K. Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biophys. Res. Commun. 431, 258-263 (2013).
21. Ji, Y. et al. Modulation of the murine microbiome with a concomitant anti-obesity effect by Lactobacillus rhamnosus GG and Lactobacillus sakei NR28. Benef. Microbes 3, 13-22 (2012).
22. Park, K. Y., Kim, B. & Hyun, C. K. Lactobacillus rhamnosus GG reverses insulin resistance but does not block its onset in dietinduced obese mice. J. Microbiol. Biotechnol. 25, 753-757 (2015).
23. Park, D. Y. et al. Supplementation of Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032 in diet-induced obese mice is associated with gut microbial changes and reduction in obesity. PLoS One 8, e59470 (2013).
24. Yadav, H., Lee, J. H., Lloyd, J., Walter, P. & Rane, S. G. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J. Biol. Chem. 288, 25088-25097 (2013).
25. Kimura, I. et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4, 1829 (2013).
26. Lee, H. Y. et al. 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 (2006).
27. Kleerebezem, M. et al. The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34, 199-230 (2010).
28. Ryan, P. M., Ross, R. P., Fitzgerald, G. F., Caplice, N. M. & Stanton, C., Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications. Food Funct. 6, 679-693 (2015).
29. Patten, D. A. & Laws, A. P., Lactobacillus-produced exopolysaccharides and their potential health benefits: a review. Benef. Microbes. 6(4), 457-471 (2015).
30. Park, J. E., Oh, S. H. & Cha, Y. S. Lactobacillus plantarum LG42 isolated from gajami sik-hae inhibits adipogenesis in 3T3-L1 adipocyte. Biomed. Res. Int. 2013 (2013).
31. Park, D. Y., Ahn, Y. T., Huh, C. S., Jeon, S. M. & Choi, M. S. The inhibitory effect of Lactobacillus plantarum KY1032 cell extract on the adipogenesis of 3T3-L1 Cells. J. Med. Food 14, 670-675 (2011).
32. Miao, M. et al. Physicochemical characteristics of a high molecular weight bioengineered a-D-glucan from Leuconostoc citreum SK24. 002. Food Hydrocoll. 50, 37-43 (2015).
33. Lundqvist, J. et al. Isolation and characterization of galactoglucomannan from spruce (Picea abies). Carbohydr. Polym. 48, 29-39 (2002).
34. Zhang, H., Nie, S. P., Yin, J. Y., Wang, Y. X. & Xie, M. Y. Structural characterization of a heterogalactan purified from fruiting bodies of Ganoderma atrum. Food Hydrocoll. 36, 339-347 (2014).
35. Landersjö, C., Yang, Z., Huttunen, E. & Widmalm, G. Structural Studies of the Exopolysaccharide Produced by Lactobacillus rhamnosus strain GG (ATCC 53103). Biomacromolecules 3, 880-884 (2002).
36. Wachi, S. et al. Lactobacillus delbrueckii TUA4408L and its extracellular polysaccharides attenuate enterotoxigenic Escherichia coliinduced inflammatory response in porcine intestinal epitheliocytes via Toll-like receptor-2 and 4. Mol. Nutr. Food Res. 58, 2080-2093 (2014).
37. Round, J. L. et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974-977 (2011).
38. Fedorak, R. N. Understanding why probiotic therapies can be effective in treating IBD.J. Clin. Gastroenterol. 42, S111-S115 (2008).
39. van Baarlen, P., Wells, J. M. & Kleerebezem, M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol. 34, 208-215 (2013).
40. Panwar, H., Rashmi, H. M., Batish, V. K. & Grover, S. Probiotics as potential biotherapeutics in the management of type 2 diabetes-prospects and perspectives. Diabetes Metab. Res. Rev. 29, 103-112 (2013).
41. Yadav, H., Lee, J. H., Lloyd, J., Walter, P. & Rane, S. G., Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J. Biol. Chem. 288, 25088-25097 (2013).
42. Stenman, L. K. et al. Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in dietinduced obese mice. Benef. Microbes 5, 437-445 (2014).
43. Shimizu, K. et al. Probiotic/synbiotic therapy for treating critically ill patients from a gut microbiota perspective. Dig. Dis. Sci. 58, 23-32 (2013).
44. Overduin, J., Schoterman, M. H., Calame, W., Schonewille, A. J. & Ten Bruggencate, S. J., Dietary galacto-oligosaccharides and calcium: effects on energy intake, fat-pad weight and satiety-related, gastrointestinal hormones in rats. Br. J. Nutr. 109, 1338-1348 (2013).
45. Eagle, A. R. & Chawla, A. In obesity and weight loss, all roads lead to the mighty macrophage. J Clin Invest. 120(10), 3437-3440 (2010).
46. Lumeng, C. N., Bodzin, J. L. & Saltiel, A. R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 117(1), 175-184 (2007).
47. Jeong, H. J., Yoon, S. J. & Pyun, Y. R. Polysaccharides from edible mushroom hinmogi (Tremella fuciformis) inhibit differentiation of 3T3-L1 adipocytes by reducing mRNA expression of PPARγ, C/EBPa, and leptin. Food Sci. Biotechnol. 17, 267-273 (2008).
48. Xu, Y. et al. The anti-obesity effect of green tea polysaccharides, polyphenols and caffeine in rats fed with a high-fat diet. Food Funct. 6, 296-303 (2015).
49. Wang, Y., Zhu, Y., Ruan, K., Wei, H. & Feng, Y. MDG-1, a polysaccharide from Ophiopogon japonicus, prevents high fat diet-induced obesity and increases energy expenditure in mice. Carbohydr. Polym. 114, 183-189 (2015).
50. Zhu, X., Pan, Y., Zheng, L., Cui, L. & Cao, Y. Polysaccharides from the Chinese medicinal herb Achyranthes bidentata enhance antimalarial immunity during Plasmodium yoelii 17XL infection in mice. Malar. J. 11, 49 (2012).
51. Skurk, T., Alberti-Huber, C., Herder, C. & Hauner, H., Relationship between adipocyte size and adipokine expression and secretion. J. Clin. Endocrinol. Metab. 92, 1023-1033 (2007).
52. Mirza, M. S. Obesity, visceral fat, and NAFLD: querying the role of adipokines in the progression of nonalcoholic fatty liver disease. ISRN Gastroenterol. 2011 (2011).
53. Jin, L. Q. et al. Opposite effects on tumor growth depending on dose of Achyranthes bidentata polysaccharides in C57BL/6 mice. Int. Immunopharmacol. 7, 568-577 (2007).
54. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. & Smith, F., Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356 (1956).
55. Tanaka, T. et al. A unique chitinase with dual active sites and triple substrate binding sites from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. Appl. Environ. Microbiol. 65, 5338-5344 (1999).
56. Cui, J., Gu, X., Wang, F., Ouyang, J. & Wang, J. Purification and structural characterization of an a-glucosidase inhibitory polysaccharide from apricot (Armeniaca sibirica L. Lam.) pulp. Carbohydr. Polym. 121, 309-314 (2015).
57. Sun, Z. et al. Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat. Commun. 4, 1594 (2013).
58. Zhou, L. et al. Insulin resistance and white adipose tissue inflammation are uncoupled in energetically challenged Fsp27-deficient mice. Nat Commun. 6 (2015).
59. Liu, S. et al. TLR2 is a primary receptor for Alzheimer's amyloid β peptide to trigger neuroinflammatory activation. J Immunol. 188, 1098-1107 (2012).