Single-strain starter experimental cheese reveals anti-inflammatory effect of Propionibacterium freudenreichii CIRM BIA 129 in TNBS-colitis model

Journal of Functional Foods

Volumn 18, Issue , 2015, Pages 575-585

  Plé, Coline ^a   Richoux, Romain ^b   Jardin, Julien ^c   Nurdin, Marine ^b   Briard Bion, Valérie ^c   Parayre, Sandrine ^c   Ferreira, Stéphanie ^d   Pot, Bruno ^a   Bouguen, Guillaume ^e,f   Deutsch, Stéphanie Marie ^c   Falentin, Hélène ^c   Foligné, Benoit ^a   Jan, Gwénaël ^c  

^a UNIV LILLE   (France)

^b Actalia Produits Laitiers   (France)

^c UMR1253   (France)

^d Genoscreen   (France)

^e University Hospital of Rennes   (France)

^f UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Colitis; Probiotic cheese; Proteome, inflammation, dairy propionibacteria; Surfaceome

Indexed keywords

EID: 84942520899     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2015.08.015     Document Type: Article

References (49)

1. Albenberg L.G., Wu G.D. Diet and the intestinal microbiome: Associations, functions, and implications for health and disease. Gastroenterology 2014, 146:1564-1572.
2. Ameho C.K., Adjei A.A., Harrison E.K., Takeshita K., Morioka T., Arakaki Y., Ito E., Suzuki I., Kulkarni A.D., Kawajiri A., Yamamoto S. Prophylactic effect of dietary glutamine supplementation on interleukin 8 and tumour necrosis factor alpha production in trinitrobenzene sulphonic acid induced colitis. Gut 1997, 41:487-493.
3. Baumgart D.C., Carding S.R. Inflammatory bowel disease: Cause and immunobiology. Lancet 2007, 369:1627-1640.
4. Baumgart D.C., Sandborn W.J. Inflammatory bowel disease: Clinical aspects and established and evolving therapies. Lancet 2007, 369:1641-1657.
5. Bibiloni R., Fedorak R.N., Tannock G.W., Madsen K.L., Gionchetti P., Campieri M., De Simone C., Sartor R.B. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. The American Journal of Gastroenterology 2005, 100:1539-1546.
6. Bouglé D., Roland N., Lebeurrier F., Arhan P. Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects. Scandinavian Journal of Gastroenterology 1999, 34:144-148.
7. Bradley P.P., Priebat D.A., Christensen R.D., Rothstein G. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. The Journal of Investigative Dermatology 1982, 78:206-209.
8. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., McDonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 2010, 7:335-336.
9. Cotillard A., Kennedy S.P., Kong L.C., Prifti E., Pons N., Le C.E., Le Chatelier E., Almeida M., Quinquis B., Levenez F., Galleron N., Gougis S., Rizkalla S., Batto J.M., Renault P., Doré J., Zucker J.D., Clément K., Ehrlich S.D. Dietary intervention impact on gut microbial gene richness. Nature 2013, 500:585-588. ANR MicroObes Consortium.
10. Cousin F.J., Foligne B., Deutsch S.M., Massart S., Parayre S., Le Loir Y., Boudry G., Jan G. Assessment of the probiotic potential of a dairy product fermented by Propionibacterium freudenreichii in piglets. Journal of Agricultural and Food Chemistry 2012, 60:7917-7927.
11. Cousin F.J., Mater D., Foligné B., Jan G. Dairy propionibacteria as human probiotics: A review of recent evidence. Dairy Science & Technology 2011, 91:1-26.
12. Danese S., Fiocchi C. Ulcerative colitis. New England Journal of Medicine 2011, 365:1713-1725.
13. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A., Biddinger S.B., Dutton R.J., Turnbaugh P.J. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505:559-563.
14. DeSantis T.Z., Hugenholtz P., Larsen N., Rojas M., Brodie E.L., Keller K., Huber T., Dalevi D., Hu P., Andersen G.L. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 2006, 72:5069-5072.
15. Deutsch S.M., Le Bivic P., Hervé C., Madec M.N., Lapointe G., Jan G., Le Loir Y., Falentin H. Correlation of the capsular phenotype in Propionibacterium freudenreichii with the level of expression of gtf, a unique polysaccharide synthase-encoding gene. Applied and Environmental Microbiology 2010, 76:2740-2746.
16. Deutsch S.M., Parayre S., Bouchoux A., Guyomarc'h F., Dewulf J., Dols-Lafargue M., Baglinière F., Cousin F.J., Falentin H., Jan G., Foligné B. Contribution of surface beta-glucan polysaccharide to physicochemical and immunomodulatory properties of Propionibacterium freudenreichii. Applied and Environmental Microbiology 2012, 78:1765-1775.
17. Drouault-Holowacz S., Foligne B., Dennin V., Goudercourt D., Terpend K., Burckel A., Pot B. Anti-inflammatory potential of the probiotic dietary supplement Lactibiane Tolerance: In vitro and in vivo considerations. Clinical Nutrition (Edinburgh, Scotland) 2006, 25:994-1003.
18. Eloe-Fadrosh E.A., Brady A., Crabtree J., Drabek E.F., Ma B., Mahurkar A., Ravel J., Haverkamp M., Fiorino A.M., Botelho C., Andreyeva I., Hibberd P.L., Fraser C.M. Functional dynamics of the gut microbiome in elderly people during probiotic consumption. MBio 2015, 6.
19. Falentin H., Henaff N., Le Bivic P., Deutsch S.M., Parayre S., Richoux R., Sohier D., Thierry A., Lortal S., Postollec F. Reverse transcription quantitative PCR revealed persistency of thermophilic lactic acid bacteria metabolic activity until the end of the ripening of Emmental cheese. Food Microbiology 2012, 29:132-140.
20. Falentin H., Postollec F., Parayre S., Henaff N., Le B.P., Richoux R., Thierry A., Sohier D. Specific metabolic activity of ripening bacteria quantified by real-time reverse transcription PCR throughout Emmental cheese manufacture. International Journal of Food Microbiology 2010, 144:10-19.
21. Foligné B., Breton J., Mater D., Jan G. Tracking the microbiome functionality: Focus on Propionibacterium species. Gut 2013, 62:1227-1228.
22. Foligné B., Deutsch S.M., Breton J., Cousin F.J., Dewulf J., Samson M., Pot B., Jan G. Promising immunomodulatory effects of selected strains of dairy propionibacteria as evidenced in vitro and in vivo. Applied and Environmental Microbiology 2010, 76:8259-8264.
23. Foligné B., Nutten S., Grangette C., Dennin V., Goudercourt D., Poiret S., Dewulf J., Brassart D., Mercenier A., Pot B. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World Journal of Gastroenterology 2007, 13:236-243.
24. Furrie E., Macfarlane S., Kennedy A., Cummings J.H., Walsh S.V., O'neil D.A., Macfarlane G.T. Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: A randomised controlled pilot trial. Gut 2005, 54:242-249.
25. Hartley M.G., Hudson M.J., Swarbrick E.T., Hill M.J., Gent A.E., Hellier M.D., Grace R.H. The rectal mucosa-associated microflora in patients with ulcerative colitis. Journal of Medical Microbiology 1992, 36:96-103.
26. Hesketh J. Personalised nutrition: How far has nutrigenomics progressed?. European Journal of Clinical Nutrition 2013, 67:430-435.
27. Hojo K., Yoda N., Tsuchita H., Ohtsu T., Seki K., Taketomo N., Murayama T., Lino H. Effect of ingested culture of Propionibacterium freudenreichii ET-3 on fecal microflora and stool frequency in healthy females. Bioscience and Microflora 2002, 21:115-120.
28. Hosoya T., Sakai F., Yamashita M., Shiozaki T., Endo T., Ukibe K., Uenishi H., Kadooka Y., Moriya T., Nakagawa H., Nakayama Y., Miyazaki T. Lactobacillus helveticus SBT2171 inhibits lymphocyte proliferation by regulation of the JNK signaling pathway. PLoS ONE 2014, 9. e108360.
29. Huang H., Vangay P., McKinlay C.E., Knights D. Multi-omics analysis of inflammatory bowel disease. Immunology Letters 2014, 162:62-68.
30. Kaneko T. A novel bifidogenic growth stimulator produced by Propionibacterium freudenreichii. Bioscience and Microflora 1999, 18:73-80.
31. Kekkonen R.A., Kajasto E., Miettinen M., Veckman V., Korpela R., Julkunen I. Probiotic Leuconostoc mesenteroides ssp. cremoris and Streptococcus thermophilus induce IL-12 and IFN-gamma production. World Journal of Gastroenterology 2008, 14:1192-1203.
32. Le Marechal C., Peton V., Ple C., Vroland C., Jardin J., Briard-Bion V., Durant G., Chuat V., Loux V., Foligné B., Deutsch S.M., Falentin H., Jan G. Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties. Journal of Proteomics 2015, 113C:447-461.
33. Malik A.C., Reinbold G.W., Vedamuthu E.R. An evaluation of the taxonomy of Propionibacterium. Canadian Journal of Microbiology 1968, 14:1185-1191.
34. Mitsuyama K., Masuda J., Yamasaki H., Kuwaki K., Kitazaki S., Koga H., Uchida M., Sata M. Treatment of ulcerative colitis with milk whey culture with Propionibacterium freudenreichii. Journal of Intestinal Microbiology 2007, 21:143-147.
35. Okada Y., Tsuzuki Y., Miyazaki J., Matsuzaki K., Hokari R., Komoto S., Kato S., Kawaguchi A., Nagao S., Itoh K., Watanabe T., Miura S. Propionibacterium freudenreichii component 1.4-dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing. Gut 2006, 55:681-688.
36. Ouwehand A.C., Lagstrom H., Suomalainen T., Salminen S. Effect of probiotics on constipation, fecal azoreductase activity and fecal mucin content in the elderly. Annals of Nutrition and Metabolism 2002, 46:159-162.
37. Ple C., Adouard N., Breton J., Dewulf J., Pot B., Bonnarme P., Foligné B. Designing specific cheese-ripening ecosystems to shape the immune effects of dairy products?. Journal of Functional Foods 2015, 12:219-229.
38. Rodriguez C., Medici M., Mozzi F., Font de Valdez G. Therapeutic effect of Streptococcus thermophilus CRL 1190-fermented milk on chronic gastritis. World Journal of Gastroenterology 2010, 16:1622-1630.
39. Roland N., Bougle D., Lebeurrier F., Arhan P., Maubois J.L. Propionibacterium freudenreichii stimulates the growth of Bifidobacterium bifidum in vitro and increases fecal bifidobacteria in healthy human volunteers. International Dairy Journal 1998, 8:587-588.
40. Rubin D.T., Dubinsky M.C., Panaccione R., Siegel C.A., Binion D.G., Kane S.V., Hopper J. The impact of ulcerative colitis on patients' lives compared to other chronic diseases: A patient survey. Digestive Diseases and Sciences 2010, 55:1044-1052.
41. Santos-Rocha C., Lakhdari O., Blottiere H.M., Blugeon S., Sokol H., Bermudez-Humaran L.G., Azevedo V., Miyoshi A., Doré J., Langella P., Maguin E., van de Guchte M. Anti-inflammatory properties of dairy lactobacilli. Inflammatory Bowel Diseases 2012, 18:657-666.
42. Seki K., Nakao H., Umino H., Isshiki H., Yoda N., Tachihara R., Ohuchi T., Saruta H., Suzuki K., Mitsuoka T. Effects of fermented milk whey containing novel bifidogenic growth stimulator produced by Propionibacterium on fecal bacteria, putrefactive metabolite, defecation frequency and fecal properties in senile volunteers needed serious nursing-care taking enteral nutrition by tube feeding. Journal of Intestinal Microbiology 2004, 18:107-115.
43. Siragusa S., De A.M., Calasso M., Campanella D., Minervini F., Di Cagno R., Gobbetti M. Fermentation and proteome profiles of Lactobacillus plantarum strains during growth under food-like conditions. Journal of Proteomics 2014, 96:366-380.
44. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L.G., Gratadoux J.J., Blugeon S., Bridonneau C., Furet J.P., Corthier G., Grangette C., Vasquez N., Pochart P., Trugnan G., Thomas G., Blottière H.M., Doré J., Marteau P., Seksik P., Langella P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:16731-16736.
45. Sood A., Midha V., Makharia G.K., Ahuja V., Singal D., Goswami P., Tandon R.K. The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clinical Gastroenterology and Hepatology 2009, 7:1202-1209. 1209.e1.
46. Tursi A., Brandimarte G., Papa A., Giglio A., Elisei W., Giorgetti G.M., Forti G., Morini S., Hassan C., Pistoia M.A., Modeo M.E., Rodino' S., D'Amico T., Sebkova L., Sacca' N., Di Giulio E., Luzza F., Imeneo M., Larussa T., Di Rosa S., Annese V., Danese S., Gasbarrini A. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: A double-blind, randomized, placebo-controlled study. The American Journal of Gastroenterology 2010, 105:2218-2227.
47. Uchida M., Mogami O. Milk whey culture with Propionibacterium freudenreichii ET-3 is effective on the colitis induced by 2,4,6-trinitrobenzene sulfonic acid in rats. Journal of Pharmacological Sciences 2005, 99:329-334.
48. Wallace J.L., MacNaughton W.K., Morris G.P., Beck P.L. Inhibition of leukotriene synthesis markedly accelerates healing in a rat model of inflammatory bowel disease. Gastroenterology 1989, 96:29-36.
49. Wu G.D., Chen J., Hoffmann C., Bittinger K., Chen Y.Y., Keilbaugh S.A., Bewtra M., Knights D., Walters W.A., Knight R., Sinha R., Gilroy E., Gupta K., Baldassano R., Nessel L., Li H., Bushman F.D., Lewis J.D. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011, 334:105-108.