Immune modulating capability of two exopolysaccharide-producing bifidobacterium strains in a wistar rat model

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Salazar, Nuria ^a   López, Patricia ^b   Garrido, Pablo ^b   Moran, Javier ^b   Cabello, Estefanía ^b   Gueimonde, Miguel ^a   Suárez, Ana ^b   González, Celestino ^b   De Los Reyes Gavilán, Clara G ^a   Ruas Madiedo, Patricia ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b UNIVERSITY OF OVIEDO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; GAMMA INTERFERON; GLUCOSE; GLUCOSE TRANSPORTER 4; IMMUNOGLOBULIN; INSULIN; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 4; INTERLEUKIN 6; PROBIOTIC AGENT; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA; BACTERIAL POLYSACCHARIDE; CYTOKINE; IMMUNOLOGIC FACTOR;

ADIPOSE TISSUE CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM LONGUM; CONTROLLED STUDY; EXPERIMENTAL DESIGN; GASTROCNEMIUS MUSCLE; GLUCOSE HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOMODULATION; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; MACROPHAGE; NONHUMAN; RANK SUM TEST; RAT; ANIMAL; FERMENTATION; HUMAN; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; MILK; ORAL DRUG ADMINISTRATION; WISTAR RAT;

ADMINISTRATION, ORAL; ANIMALS; BIFIDOBACTERIUM; CYTOKINES; FERMENTATION; HUMANS; IMMUNOLOGIC FACTORS; INTERLEUKIN-6; MALE; MILK; MODELS, ANIMAL; POLYSACCHARIDES, BACTERIAL; PROBIOTICS; RATS; RATS, WISTAR;

EID: 84902154532     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/106290     Document Type: Article

References (44)

1. Bigliardi B., Galati F., Innovation trends in the food industry: the case of functional foods. Trends in Food Science & Technology 2013 31 2 118 129 2-s2.0-84878352959 10.1016/j.tifs.2013.03.006
2. FAO-WHO, Probiotics in food. Health and nutritional properties and guidelines for evaluation. FAO Food and Nutritional Paper 2006 85
3. EFSA, Introduction of a Qualified Presumption of Safety (QPS) approach for assessment of selected microorganisms referred to EFSA. The EFSA Journal 2007 587 1 16 10.2903/j.efsa.2007.587
4. Hooper L. V., Littman D. R., Macpherson A. J., Interactions between the microbiota and the immune system. Science 2012 336 6086 1268 1273 2-s2.0-84861980130 10.1126/science.1223490
5. Reid G., Younes J. A., van der Mei H. C., Gloor G. B., Knight R., Busscher H. J., Microbiota restoration: natural and supplemented recovery of human microbial communities. Nature Reviews Microbiology 2011 9 1 27 38 2-s2.0-78650291202 10.1038/nrmicro2473
6. Dupont A. W., Dupont H. L., The intestinal microbiota and chronic disorders of the gut. Nature Reviews Gastroenterology & Hepatology 2011 8 9 523 531 2-s2.0-80052473669 10.1038/nrgastro.2011.133
7. Delzenne N. M., Neyrinck A. M., Bäckhed F., Cani P. D., Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nature Reviews Endocrinology 2011 7 11 639 646 2-s2.0-80054913827 10.1038/nrendo.2011.126
8. Cani P. D., Osto M., Geurts L., Everard A., Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012 3 4 279 288 2-s2.0-84863870958 10.4161/gmic.19625
9. Delzenne N. M., Neyrinck A. M., Cani P. D., Gut microbiota and metabolic disorders: how prebiotic can work? British Journal of Nutrition 2013 109 2 S81 S85 2-s2.0-84873805162 10.1017/S0007114512004047
10. Sanz Y., Rastmanesh R., Agostoni C., Understanding the role of gut microbes and probiotics in obesity: how far are we? Pharmacological Research 2013 69 144 155 10.1016/j.phrs.2012.10.021
11. Arribas B., Garrido-Mesa N., Perán L., Camuesco D., Comalada M., Bailón E., Olivares M., Xaus J., Kruidenier L., Sanderson I. R., Zarzuelo A., Rodríguez-Cabezas M. E., Gálvez J., The immunomodulatory properties of viable Lactobacillus salivarius ssp. salivarius CECT5713 are not restricted to the large intestine. European Journal of Nutrition 2012 51 3 365 374 2-s2.0-84860667500 10.1007/s00394-011-0221-4
12. Harata G., He F., Kawase M., Hosono A., Takahashi K., Kaminogawa S., Differentiated implication of Lactobacillus GG and L. gasseri TMC0356 to immune responses of murine Peyer's patch. Microbiology and Immunology 2009 53 8 475 480 2-s2.0-70349319698 10.1111/j.1348-0421.2009.00146.x
13. Zakostelska Z., Kverka M., Klimesova K., Rossmann P., Mrazek J., Kopecny J., Hornova M., Srutkova D., Hudcovic T., Ridl J., Tlaskalova-Hogenova H., Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS ONE 2011 6 11 2-s2.0-81555205689 10.1371/journal.pone.0027961 e27961
14. Fanning S., Hall L. J., Cronin M., Zomer A., MacSharry J., Goulding D., Motherway M. O., Shanahan F., Nally K., Dougan G., van Sinderen D., Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences of the United States of America 2012 109 6 2108 2113 2-s2.0-84857128238 10.1073/pnas.1115621109
15. Salazar N., Binetti A., Gueimonde M., Alonso A., Garrido P., González del Rey C., González C., Ruas-Madiedo P., de los Reyes-Gavilán C. G., Safety and intestinal microbiota modulation by the exopolysaccharide-producing strains Bifidobacterium animalis IPLA R1 and Bifidobacterium longum IPLA E44 orally administered to Wistar rats. International Journal of Food Microbiology 2011 144 3 342 351 2-s2.0-78650029085 10.1016/j.ijfoodmicro.2010.10.016
16. Vinderola G., Perdigón G., Duarte J., Farnworth E., Matar C., Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine 2006 36 5-6 254 260 2-s2.0-34047107761 10.1016/j.cyto.2007.01.003 (Pubitemid 46529477)
17. Hidalgo-Cantabrana C., López P., Gueimonde M., de los Reyes-Gavilán C. G., Suárez A., Margolles A., Ruas-Madiedo P., Immune modulation capability of exopolysaccharides synthesised by lactic acid bacteria and bifidobacteria. Probiotics & Antimicrobial Proteins 2012 4 4 227 237 2-s2.0-84870655569 10.1007/s12602-012-9110-2
18. Maslowski K. M., MacKay C. R., Diet, gut microbiota and immune responses. Nature Immunology 2011 12 1 5 9 2-s2.0-78650408264 10.1038/ni0111-5
19. Maynard C. L., Elson C. O., Hatton R. D., Weaver C. T., Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012 489 7415 231 241 2-s2.0-84866167497 10.1038/nature11551
20. Cacho J., Sevillano J., De Castro J., Herrera E., Ramos M. P., Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. American Journal of Physiology: Endocrinology and Metabolism 2008 295 5 E1269 E1276 2-s2.0-57049134614 10.1152/ajpendo.90207.2008
21. Hirshman M. F., Goodyear L. J., Wardzala L. J., Horton E. D., Horton E. S., Identification of an intracellular pool of glucose transporters from basal and insulin-stimulated rat skeletal muscle. Journal of Biological Chemistry 1990 265 2 987 991 2-s2.0-0025176936
22. Towbin H., Staehelin T., Gordon J., Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 1979 76 9 4350 4354 2-s2.0-0009482260 (Pubitemid 9256559)
23. Heuvelin E., Lebreton C., Grangette C., Pot B., Cerf-Bensussan N., Heyman M., Mechanisms involved in alleviation of intestinal inflammation by Bifidobacterium breve soluble factors. PLoS ONE 2009 4 4 2-s2.0-65449117970 10.1371/journal.pone.0005184 e5184
24. O'Mahony D., Murphy S., Boileau T., Park J., O'Brien F., Groeger D., Konieczna P., Ziegler M., Scully P., Shanahan F., Kiely B., O'Mahony L., Bifidobacterium animalis AHC7 protects against pathogen-induced NF- B activation in vivo. BMC Immunology 2010 11, article 63 2-s2.0-78650350690 10.1186/1471-2172-11-63
25. Preising J., Philippe D., Gleinser M., Wei H., Blum S., Eikmanns B. J., Niess J.-H., Riedel C. U., Selection of bifidobacteria based on adhesion and anti-inflammatory capacity in vitro for amelioration of murine colitis. Applied and Environmental Microbiology 2010 76 9 3048 3051 2-s2.0-77951574475 10.1128/AEM.03127-09
26. López P., Monteserín D., Gueimonde M., Exopolysaccharide- producing Bifidobacterium strains elicit different in vitro responses upon interaction with human cells. Food Research International 2012 46 99 107 10.1016/j.foodres.2011.11.020
27. Bleau C., Monges A., Rashidan K., Laverdure J.-P., Lacroix M., van Calsteren M.-R., Millette M., Savard R., Lamontagne L., Intermediate chains of exopolysaccharides from Lactobacillus rhamnosus RW-9595M increase IL-10 production by macrophages. Journal of Applied Microbiology 2010 108 2 666 675 2-s2.0-74049130917 10.1111/j.1365-2672.2009.04450.x
28. Nikolic M., López P., Strahinic I., Suárez A., Kojic M., Fernández-García M., Topisirovic L., Golic N., Ruas-Madiedo P., Characterisation of the exopolysaccharide (EPS)-producing Lactobacillus paraplantarum BGCG11 and its non-EPS producing derivative strains as potential probiotics. International Journal of Food Microbiology 2012 158 2 155 162 2-s2.0-84865109744 10.1016/j.ijfoodmicro.2012.07.015
29. Chen J., Wang R., Li X.-F., Wang R.-L., Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. British Journal of Nutrition 2012 107 10 1429 1434 2-s2.0-84863562094 10.1017/S0007114511004491
30. Hsieh F.-C., Lee C.-L., Chai C.-Y., Chen W.-T., Lu Y.-C., Wu C.-S., Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutrition and Metabolism 2013 10 1, article 35 2-s2.0-84876087039 10.1186/1743-7075-10-35
31. Naito E., Yoshida Y., Makino K., Kounoshi Y., Kunihiro S., Takahashi R., Matsuzaki T., Miyazaki K., Ishikawa F., Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. Journal of Applied Microbiology 2011 110 3 650 657 2-s2.0-79551678401 10.1111/j.1365-2672.2010.04922.x
32. Tomaro-Duchesneau C., Saha S., Malhotra M., Effect of orally administered L. fermentum NCIMB 5221 on markers of metabolic syndrome: and in vivo analysis using ZDF rats. Applied Microbiology and Biotechnology 2014 98 1 115 126 10.1007/s00253-013-5252-8
33. Andreasen A. S., Larsen N., Pedersen-Skovsgaard T., Berg R. M. G., Mller K., Svendsen K. D., Jakobsen M., Pedersen B. K., Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. British Journal of Nutrition 2010 104 12 1831 1838 2-s2.0-78650011778 10.1017/S0007114510002874
34. Leto D., Saltiel A. R., Regulation of glucose transport by insulin: traffic control of GLUT4. Nature Reviews Molecular Cell Biology 2012 13 6 383 396 2-s2.0-84861444859 10.1038/nrm3351
35. Whiteman E. L., Cho H., Birnbaum M. J., Role of Akt/protein kinase B in metabolism. Trends in Endocrinology & Metabolism 2002 13 10 444 451 2-s2.0-0037600600 10.1016/S1043-2760(02)00662-8 (Pubitemid 36733939)
36. Febbraio M. A., Pedersen B. K., Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB Journal 2002 16 11 1335 1347 2-s2.0-0036720342 10.1096/fj.01-0876rev (Pubitemid 34913306)
37. Weigert C., Hennige A. M., Lehmann R., Brodbeck K., Baumgartner F., Schäuble M., Häring H. U., Schleicher E. D., Direct cross-talk of interleukin-6 and insulin signal transduction via insulin receptor substrate-1 in skeletal muscle cells. Journal of Biological Chemistry 2006 281 11 7060 7067 2-s2.0-33646350774 10.1074/jbc.M509782200 (Pubitemid 43847469)
38. Hoene M., Weigert C., The role of interleukin-6 in insulin resistance, body fat distribution and energy balance. Obesity Reviews 2008 9 1 20 29 2-s2.0-37249074063 10.1111/j.1467-789X.2007.00410.x (Pubitemid 350264626)
39. Ladygina N., Gottipati S., Ngo K., PI3Kg kinase activity is required for optimal T-cell activation and differentiation. European Journal of Immunology 2013 43 3183 3196 10.1002/eji.201343812
40. Nagai S., Kurebayashi Y., Koyasu S., Role of PI3K/Akt and mTOR complexes in Th17 cell differentiation. Annals of the New York Academy of Sciences 2013 1280 1 30 34 2-s2.0-84875661336 10.1111/nyas.12059
41. McGuire V. A., Gray A., Monk C. E., Cross talk between the Akt and p38 α pathways in macrophages downstream of toll-like receptor signaling. Molecular and Cellular Biology 2013 33 4152 4165
42. Zheng Y., Yang Y., Li Y., Xu L., Wang Y., Guo Z., Song H., Yang M., Luo B., Zheng A., Li P., Zhang Y., Ji G., Yu Y., Ephedrine hydrochloride inhibits PGN-induced inflammatory responses by promoting IL-10 production and decreasing proinflammatory cytokine secretion via the PI3K/Akt/GSK3 β pathway. Cellular and Molecular Immunology 2013 10 4 330 337 2-s2.0-84879958543 10.1038/cmi.2013.3
43. Raja S. B., Murali M. R., Devaraj H., Devaraj S. N., Differential expression of gastric MUC5AC in colonic epithelial cells: TFF3-wired IL1 β /Akt crosstalk-induced mucosal immune response against Shigella dysenteriae infection. Journal of Cell Science 2012 125 3 703 713 2-s2.0-84858121091 10.1242/jcs.092148
44. Hoarau C., Martin L., Faugaret D., Baron C., Dauba A., Aubert-Jacquin C., Velge-Roussel F., Lebranchu Y., Supernatant from Bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS ONE 2008 3 7 2-s2.0-50249109525 10.1371/journal.pone. 0002753 e2753