Saccharomyces boulardii administration changes gut microbiota and reduces hepatic steatosis, low-grade inflammation, and fat mass in obese and type 2 diabetic db/db mice

mBio

Volumn 5, Issue 3, 2014, Pages

  Everard, Amandine ^a   Matamoros, Sébastien ^a   Geurts, Lucie ^a   Delzenne, Nathalie M ^a   Cani, Patrice D ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PROBIOTIC AGENT; FAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CECUM; CONTROLLED STUDY; FAT MASS; FATTY LIVER; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; ORGAN WEIGHT; PRIORITY JOURNAL; SACCHAROMYCES BOULARDII; WEIGHT REDUCTION; ANIMAL; BODY WEIGHT; COMPLICATION; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; FEMALE; GASTROINTESTINAL TRACT; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE MUTANT; PHYSIOLOGY; SACCHAROMYCES;

ANIMALS; BODY WEIGHT; DIABETES MELLITUS, TYPE 2; FATS; FATTY LIVER; FEMALE; GASTROINTESTINAL TRACT; HUMANS; MALE; MICE; MICE, OBESE; MICROBIOTA; OBESITY; PROBIOTICS; SACCHAROMYCES;

EID: 84903975395     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01011-14     Document Type: Article

References (65)

1. Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O, Richards SE, Wang Y, Dumas ME, Ross A, Rezzi S, Kochhar S, van BP, Lindon JC, Holmes E, Nicholson JK. 2011. Colonization-induced host-gut microbial metabolic interaction. mBio 2: e00271-10. http://dx. doi. org/10. 1128/mBio. 00271-10.
2. Cani PD. 2014. Metabolism in 2013: the gut microbiota manages host metabolism. Nat. Rev. Endocrinol. 10: 74-76. http://dx. doi. org/10. 1038/nrendo. 2013. 240.
3. Petschow B, Doré J, Hibberd P, Dinan T, Reid G, Blaser M, Cani PD, Degnan FH, Foster J, Gibson G, Hutton J, Klaenhammer TR, Ley R, Nieuwdorp M, Pot B, Relman D, Serazin A, Sanders ME. 2013. Probiotics, prebiotics, and the host microbiome: the science of translation. Ann. N. Y. Acad. Sci. 1306: 1-17. http://dx. doi. org/10. 1111/nyas. 12303.
4. Cox LM, Blaser MJ. 2013. Pathways in microbe-induced obesity. Cell. Metab. 17: 883-894. http://dx. doi. org/10. 1016/j. cmet. 2013. 05. 004.
5. Everard A, Cani PD. 2013. Diabetes, obesity and gut microbiota. Best Pract. Res. Clin. Gastroenterol. 27: 73-83. http://dx. doi. org/10. 1016/j. bpg. 2013. 03. 007.
6. Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489: 242-249. http://dx. doi. org/10. 1038/nature11552.
7. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck AM, Lambert DM, Muccioli GG, Delzenne NM. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103. http://dx. doi. org/10. 1136/gut. 2008. 165886.
8. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GM, Neyrinck AM, Possemiers S, Van HA, Francois P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD. 2011. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptinresistant mice. Diabetes 60: 2775-2786. http://dx. doi. org/10. 2337/db11-0227.
9. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 110: 9066-9071. http://dx. doi. org/10. 1073/pnas. 1219451110.
10. Neyrinck AM, Van Hée VF, Piront N, De Backer F, Toussaint O, Cani PD, Delzenne NM. 2012. Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice. Nutr. Diabetes 2: e28. http://dx. doi. org/10. 1038/nutd. 2011. 24.
11. Aziz AA, Kenney LS, Goulet B, Abdel-Aal E-S. 2009. Dietary starch type affects body weight and glycemic control in freely fed but not energyrestricted obese rats. J. Nutr. 139: 1881-1889. http://dx. doi. org/10. 3945/jn. 109. 110650.
12. Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, Danna SC, Tripathy S, Hegsted M, Keenan MJ. 2008. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am. J. Physiol. Endocrinol. Metab. 295: E1160-E1166. http://dx. doi. org/10. 1152/ajpendo. 90637. 2008.
13. Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD. 2011. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat. Rev. Endocrinol. 7: 639-646. http://dx. doi. org/10. 1038/nrendo. 2011. 126.
14. Molinaro F, Paschetta E, Cassader M, Gambino R, Musso G. 2012. Probiotics, prebiotics, energy balance, and obesity: mechanistic insights and therapeutic implications. Gastroenterol. Clin. North Am. 41: 843-854. http://dx. doi. org/10. 1016/j. gtc. 2012. 08. 009.
15. Aronsson L, Huang Y, Parini P, Korach-André M, Håkansson J, Gustafsson JÅ, Pettersson S, Arulampalam V, Rafter J. 2010. Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS One 5: e13087. http://dx. doi. org/10. 1371/journal. pone. 0013087.
16. Arora T, Anastasovska J, Gibson G, Tuohy K, Sharma RK, Bell J, Frost G. 2012. Effect of lactobacillus acidophilus NCDC 13 supplementation on the progression of obesity in diet-induced obese mice. Br. J. Nutr. 108: 1-8. http://dx. doi. org/10. 1017/S0007114511006957.
17. Fåk F, Bäckhed F. 2012. Lactobacillus reuteri prevents diet-induced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/-m i c e. PLoS One 7: e 4 6 8 3 7. h t t p://d x. d o i. o r g/1 0. 1 3 7 1/journal. pone. 0046837.
18. 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. (Maywood) 236: 823-831. http://dx. doi. org/10. 1258/ebm. 2011. 0. 010339.
19. Gauffin Cano P, Santacruz A, Moya Á, Sanz Y. 2012. Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One 7: e41079. http://dx. doi. org/10. 1371/journal. pone. 0041079.
20. McFarland LV. 2010. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 16: 2202-2222. http://dx. doi. org/10. 3748/wjg. v16. i18. 2202.
21. Graff S, Chaumeil JC, Boy P, Lai-Kuen R, Charrueau C. 2008. Influence of pH conditions on the viability of Saccharomyces boulardii yeast. J. Gen. Appl. Microbiol. 54: 221-227. http://dx. doi. org/10. 2323/jgam. 54. 221.
22. Edwards-Ingram L, Gitsham P, Burton N, Warhurst G, Clarke I, Hoyle D, Oliver SG, Stateva L. 2007. Genotypic and physiological characterization of Saccharomyces boulardii, the probiotic strain of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 73: 2458-2467. http://dx. doi. org/10. 1128/AEM. 02201-06.
23. Schneider SM, Girard-Pipau F, Filippi J, Hebuterne X, Moyse D, Hinojosa GC, Pompei A, Rampal P. 2005. Effects of Saccharomyces boulardii on fecal short-chain fatty acids and microflora in patients on long-term total enteral nutrition. World J. Gastroenterol. 11: 6165-6169. http://www. wjgnet. com/1007-9327/11/6165. asp.
24. Leonel AJ, Alvarez-Leite JI. 2012. Butyrate: implications for intestinal function. Curr. Opin. Clin. Nutr. Metab. Care 15: 474-479. http://dx. doi. org/10. 1097/MCO. 0b013e32835665fa.
25. Geurts L, Lazarevic V, Derrien M, Everard A, Van Roye M, Knauf C, Valet P, Girard M, Muccioli GG, Francois P, de Vos WM, Schrenzel J, Delzenne NM, Cani PD. 2011. Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front. Microbiol. 2: 149. http://dx. doi. org/10. 3389/fmicb. 2011. 00149.
26. Lanthier N, Molendi-Coste O, Cani PD, van Rooijen N, Horsmans Y, Leclercq IA. 2011. Kupffer cell depletion prevents but has no therapeutic effect on metabolic and inflammatory changes induced by a high-fat diet. FASEB J. 25: 4301-4311. http://dx. doi. org/10. 1096/fj. 11-189472.
27. Lanthier N, Molendi-Coste O, Horsmans Y, van Rooijen N, Cani PD, Leclercq IA. 2010. Kupffer cell activation is a causal factor for hepatic insulin resistance. Am. J. Physiol. Gastrointest. Liver Physiol. 298: G107-G116. http://dx. doi. org/10. 1152/ajpgi. 00391. 2009.
28. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772. http://dx. doi. org/10. 2337/db06-1491.
29. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481. http://dx. doi. org/10. 2337/db07-1403.
30. Vereecke L, Beyaert R, van Loo G. 2011. Enterocyte death and intestinal barrier maintenance in homeostasis and disease. Trends Mol. Med. 17: 584-593. http://dx. doi. org/10. 1016/j. molmed. 2011. 05. 011.
31. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. 2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308: 1463-1465. http://dx. doi. org/10. 1126/science. 1108661.
32. Jahn HU, Ullrich R, Schneider T, Liehr RM, Schieferdecker HL, Holst H, Zeitz M. 1996. Immunological and trophical effects of Saccharomyces boulardii on the small intestine in healthy human volunteers. Digestion 57: 95-104. http://dx. doi. org/10. 1159/000201320.
33. Buts JP, De Keyser N, Marandi S, Hermans D, Sokal EM, Chae YH, Lambotte L, Chanteux H, Tulkens PM. 1999. Saccharomyces boulardii upgrades cellular adaptation after proximal enterectomy in rats. Gut 45: 89-96. http://dx. doi. org/10. 1136/gut. 45. 1. 89.
34. Duman DG, Kumral ZN, Ercan F, Deniz M, Can G, Caǧlayan Yeǧen B. 2013. Saccharomyces boulardii ameliorates clarithromycin-and methotrexate-induced intestinal and hepatic injury in rats. Br. J. Nutr. 110: 493-499. http://dx. doi. org/10. 1017/S000711451200517X.
35. Martins FS, Vieira AT, Elian SD, Arantes RM, Tiago FC, Sousa LP, Araújo HR, Pimenta PF, Bonjardim CA, Nicoli JR, Teixeira MM. 2013. Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect. 15: 270-279. http://dx. doi. org/10. 1016/j. micinf. 2012. 12. 007.
36. Justino PF, Melo LF, Nogueira AF, Costa JV, Silva LM, Santos CM, Mendes WO, Costa MR, Franco AX, Lima AA, Ribeiro RA, Souza MH, Soares PM. 2014. Treatment with Saccharomyces boulardii reduces the inflammation and dysfunction of the gastrointestinal tract in 5-fluorouracil-induced intestinal mucositis in mice. Br. J. Nutr. 111: 1-11. http://dx. doi. org/10. 1017/S0007114513004248.
37. Buts JP, De Keyser N. 2010. Transduction pathways regulating the trophic effects of Saccharomyces boulardii in rat intestinal mucosa. Scand. J. Gastroenterol. 45: 175-185. http://dx. doi. org/10. 3109/00365520903453141.
38. Fooks LJ, Gibson GR. 2003. Mixed culture fermentation studies on the effects of Synbiotics on the human intestinal pathogens Campylobacter jejuni and Escherichia coli. Anaerobe 9: 231-242. http://dx. doi. org/10. 1016/S1075-9964(03)00043-X.
39. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM. 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. http://dx. doi. org/10. 1007/s00125-007-0791-0.
40. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101: 15718-15723. http://dx. doi. org/10. 1073/pnas. 0407076101.
41. Axling U, Olsson C, Xu J, Fernandez C, Larsson S, Ström K, Ahrné S, Holm C, Molin G, Berger K. 2012. Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6J mice. Nutr. Metab. (Lond) 9: 105. http://dx. doi. org/10. 1186/1743-7075-9-105.
42. Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, Perlemuter G, Cassard-Doulcier AM, Gérard P. 2013. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62: 1787-1794. http://dx. doi. org/10. 1136/gutjnl-2012-303816.
43. Pachikian BD, Essaghir A, Demoulin JB, Catry E, Neyrinck AM, Dewulf EM, Sohet FM, Portois L, Clerbaux LA, Carpentier YA, Possemiers S, Bommer GT, Cani PD, Delzenne NM. 2013. Prebiotic approach alleviates hepatic steatosis: implication of fatty acid oxidative and cholesterol synthesis pathways. Mol. Nutr. Food Res. 57: 347-359. http://dx. doi. org/10. 1002/mnfr. 201200364.
44. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A. 102: 11070-11075. http://dx. doi. org/10. 1073/pnas. 0504978102.
45. 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. http://dx. doi. org/10. 1038/nature05414.
46. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213-223. http://dx. doi. org/10. 1016/j. chom. 2008. 02. 015.
47. Brahe LK, Astrup A, Larsen LH. 2013. Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes. Rev. 14:-950-959.
48. Puertollano E, Kolida S, Yaqoob P. 2014. Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Curr. Opin. Clin. Nutr. Metab. Care 17: 139-144. http://dx. doi. org/10. 1097/MCO. 0000000000000025.
49. Vidrine K, Ye J, Martin RJ, McCutcheon KL, Raggio AM, Pelkman C, Durham HA, Zhou J, Senevirathne RN, Williams C, Greenway F, Finley J, Gao Z, Goldsmith F, Keenan MJ. 2014. Resistant starch from high amylose maize (HAM-RS2) and Dietary butyrate reduce abdominal fat by a different apparent mechanism. Obesity (Silver Spring) 22: 344-348. http://dx. doi. org/10. 1002/oby. 20501.
50. Mattace Raso G, Simeoli R, Russo R, Iacono A, Santoro A, Paciello O, Ferrante MC, Canani RB, Calignano A, Meli R. 2013. Effects of sodium butyrate and its synthetic amide derivative on liver inflammation and glucose tolerance in an animal model of steatosis induced by high fat diet. PLoS One 8: e68626. http://dx. doi. org/10. 1371/journal. pone. 0068626.
51. Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, Gill SR. 2013. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57: 601-609. http://dx. doi. org/10. 1002/hep. 26093.
52. Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, Delzenne NM, Schrenzel J, Francois P, Cani PD. 2014. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J., in press. http://dx. doi. org/10. 1038/ismej. 2014. 45.
53. Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C, Li M, Zhang C, Zhang Z, Zhang Y, Li X, Ning G, Zhao L. 2012. Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One 7: e42529. http://dx. doi. org/10. 1371/journal. pone. 0042529.
54. Manners DJ, Masson AJ, Patterson JC. 1973. The structure of a beta-(1 leads to 3)-D-glucan from yeast cell walls. Biochem. J. 135:-19-30.
55. Hughes SA, Shewry PR, Gibson GR, McCleary BV, Rastall RA. 2008. In vitro fermentation of oat and barley derived beta-glucans by human faecal microbiota. FEMS Microbiol. Ecol. 64: 482-493. http://dx. doi. org/10. 1111/j. 1574-6941. 2008. 00478. x.
56. Salyers AA, Palmer JK, Wilkins TD. 1977. Laminarinase (betaglucanase) activity in Bacteroides from the human colon. Appl. Environ. Microbiol. 33: 1118-1124.
57. Matsushita O, Russell JB, Wilson DB. 1990. Cloning and sequencing of a Bacteroides ruminicola B(1)4 endoglucanase gene. J. Bacteriol. 172: 3620-3630.
58. Larsbrink J, Rogers TE, Hemsworth GR, McKee LS, Tauzin AS, Spadiut O, Klinter S, Pudlo NA, Urs K, Koropatkin NM, Creagh AL, Haynes CA, Kelly AG, Cederholm SN, Davies GJ, Martens EC, Brumer H. 2014. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506: 498-502. http://dx. doi. org/10. 1038/nature12907.
59. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
60. Geurts L, Everard A, le Ruyet P, Delzenne NM, Cani PD. 2012. Ripened dairy products differentially affect hepatic lipid content and adipose tissue oxidative stress markers in obese and type 2 diabetic mice. J. Agric. Food Chem. 60: 2063-2068. http://dx. doi. org/10. 1021/jf204916x.
61. Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM, Bindels LB, de Vos WM, Gibson GR, Thissen JP, Delzenne NM. 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. http://dx. doi. org/10. 1136/gutjnl-2012-303304.
62. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072. http://dx. doi. org/10. 1128/AEM. 03006-05.
63. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6: 610-618. http://dx. doi. org/10. 1038/ismej. 2011. 139.
64. Hierro N, Esteve-Zarzoso B, Gonzalez A, Mas A, Guillamon JM. 2006. Real-time quantitative PCR (QPCR) and reverse transcription-QPCR for detection and enumeration of total yeasts in wine. Appl. Environ. Microbiol. 72: 7148-7155. http://dx. doi. org/10. 1128/AEM. 00388-06.
65. Zott K, Claisse O, Lucas P, Coulon J, Lonvaud-Funel A, Masneuf-Pomarede I. 2010. Characterization of the yeast ecosystem in grape must and wine using real-time PCR. Food Microbiol. 27: 559-567. http://dx. doi. org/10. 1016/j. fm. 2010. 01. 006.