Immunomodulation properties of multi-species fermented milks

Food Microbiology

Volumn 53, Issue , 2016, Pages 60-69

  Foligné, Benoît ^a   Parayre, Sandrine ^b   Cheddani, Redouane ^b   Famelart, Marie Hélène ^b   Madec, Marie Noëlle ^b   Plé, Coline ^a   Breton, Jérôme ^a   Dewulf, Joëlle ^a   Jan, Gwénaël ^b   Deutsch, Stéphanie Marie ^b  

^a INSERM U1019   (France)

^b UMR1253   (France)

Author keywords

Anti inflammatory; Dairy; Immunomodulation; Lactic acid bacteria; Propionibacteria; Propionibacterium freudenreichii

Indexed keywords

IL10 PROTEIN, HUMAN; INTERLEUKIN 10; INTERLEUKIN 12; PROBIOTIC AGENT;

ANIMAL; BIOSYNTHESIS; FERMENTED MILK PRODUCT; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASES; LACTOBACILLACEAE; METABOLISM; MICROBIOLOGY; MONONUCLEAR CELL; MOUSE; PHYSIOLOGY; PROPIONIBACTERIUM;

ANIMALS; CULTURED MILK PRODUCTS; HUMANS; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; INTERLEUKIN-12; LACTOBACILLACEAE; LEUKOCYTES, MONONUCLEAR; MICE; PROBIOTICS; PROPIONIBACTERIUM;

EID: 84928816143     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2015.04.002     Document Type: Article

References (74)

1. 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.
2. Araujo R., Rodrigues A.G., Pina-Vaz C. A fast, practical and reproducible procedure for the standardization of the cell density of an Aspergillus suspension. J. Med. Microbiol. 2004, 53:783-786.
3. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., Taniguchi T., Takeda K., Hori S., Ivanov I.I., Umesaki Y., Itoh K., Honda K. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341. 10.1126/science.1198469.
4. Beermann C., Hartung J. Physiological properties of milk ingredients released by fermentation. Food Funct. 2013, 4:185-199. 10.1039/c2fo30153a.
5. Bradley P.P., Priebat D.A., Christensen R.D., Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol 1982, 78:206-209.
6. Burns P., Cuffia F., Milesi M., Vinderola G., Meinardi C., Sabbag N., Hynes E. Technological and probiotic role of adjunct cultures of non-starter lactobacilli in soft cheeses. Food Microbiol. 2012, 30:45-50. 10.1016/j.fm.2011.09.015.
7. Chapman C.M.C., Gibson G.R., Rowland I. In vitro evaluation of single- and multi-strain probiotics: Inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe 2012, 18:405-413. 10.1016/j.anaerobe.2012.05.004.
8. Chapman C.M.C., Gibson G.R., Rowland I. Health benefits of probiotics: are mixtures more effective than single strains?. Eur. J. Nutr. 2011, 50:1-17. 10.1007/s00394-010-0166-z.
9. Chatterton D.E.W., Nguyen D.N., Bering S.B., Sangild P.T. Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns. Int. J. Biochem.. Cell. Biol. 2013, 45:1730-1747. 10.1016/j.biocel.2013.04.028.
10. Claes I.J.J., De Keersmaecker S.C.J., Vanderleyden J., Lebeer S. Lessons from probiotic-host interaction studies in murine models of experimental colitis. Mol. Nutr. Food Res. 2011, 55:1441-1453. 10.1002/mnfr.201100139.
11. Cousin F.J., Foligné 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. J. Agric. Food Chem. 2012, 60:7917-7927. 10.1021/jf302245m.
12. Cousin F.J., Louesdon S., Maillard M.-B., Parayre S., Falentin H., Deutsch S.-M., Boudry G., Jan G. The first dairy product exclusively fermented by Propionibacterium freudenreichii: a new vector to study probiotic potentialities in vivo. Food Microbiol. 2012, 32:135-146. 10.1016/j.fm.2012.05.003.
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. 10.1038/nature12820.
14. Deepika G., Karunakaran E., Hurley C.R., Biggs C.A., Charalampopoulos D. Influence of fermentation conditions on the surface properties and adhesion of Lactobacillus rhamnosus GG. Microb. Cell. Factories 2012, 11:116. 10.1186/1475-2859-11-116.
15. De Moreno de Leblanc A., Del Carmen S., Zurita-Turk M., Santos Rocha C., van de Guchte M., Azevedo V., Miyoshi A., Leblanc J.G. Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases. ISRN Gastroenterol. 2011, 2011:892971. 10.5402/2011/892971.
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 β-Glucan polysaccharide to physicochemical and immunomodulatory properties of Propionibacterium freudenreichii. Appl. Environ. Microbiol. 2012, 78:1765-1775. 10.1128/AEM.07027-11.
17. Drouault-Holowacz S., Foligné B., Dennin V., Goudercourt D., Terpend K., Burckel A., Pot B. Anti-inflammatory potential of the probiotic dietary supplement Lactibiane Tolérance: in vitro and in vivo considerations. Clin. Nutr. Edinb. Scotl. 2006, 25:994-1003. 10.1016/j.clnu.2006.03.006.
18. Duboc H., Rajca S., Rainteau D., Benarous D., Maubert M.-A., Quervain E., Thomas G., Barbu V., Humbert L., Despras G., Bridonneau C., Dumetz F., Grill J.-P., Masliah J., Beaugerie L., Cosnes J., Chazouillères O., Poupon R., Wolf C., Mallet J.-M., Langella P., Trugnan G., Sokol H., Seksik P. Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 2013, 62:531-539. 10.1136/gutjnl-2012-302578.
19. Eeckhaut V., Machiels K., Perrier C., Romero C., Maes S., Flahou B., Steppe M., Haesebrouck F., Sas B., Ducatelle R., Vermeire S., Van Immerseel F. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 2013, 62:1745-1752. 10.1136/gutjnl-2012-303611.
20. Ekinci F.Y., Gurel M. Effect of using propionic acid bacteria as an adjunct culture in yogurt production. J. Dairy Sci. 2008, 91:892-899. 10.3168/jds.2007-0244.
21. Falentin H., Deutsch S.-M., Jan G., Loux V., Thierry A., Parayre S., Maillard M.-B., Dherbécourt J., Cousin F.J., Jardin J., Siguier P., Couloux A., Barbe V., Vacherie B., Wincker P., Gibrat J.-F., Gaillardin C., Lortal S. The complete genome of Propionibacterium freudenreichii CIRM-BIA1, a hardy actinobacterium with food and probiotic applications. PloS One 2010, 5:e11748. 10.1371/journal.pone.0011748.
22. Foligné B., Breton J., Mater D., Jan G. Tracking the microbiome functionality: focus on Propionibacterium species. Gut 2013, 62:1227-1228. 10.1136/gutjnl-2012-304393.
23. Foligné B., Daniel C., Pot B. Probiotics from research to market: the possibilities, risks and challenges. Curr. Opin. Microbiol. 2013, 16:284-292. 10.1016/j.mib.2013.06.008.
24. Foligne B., Dessein R., Marceau M., Poiret S., Chamaillard M., Pot B., Simonet M., Daniel C. Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein. Gastroenterology 2007, 133:862-874. 10.1053/j.gastro.2007.06.018.
25. 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. Appl. Environ. Microbiol. 2010, 76:8259-8264. 10.1128/AEM.01976-10.
26. 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 J. Gastroenterol. WJG 2007, 13:236-243.
27. Georgalaki M., Papadelli M., Chassioti E., Anastasiou R., Aktypis A., De Vuyst L., Van Driessche G., Devreese B., Tsakalidou E. Milk protein fragments induce the biosynthesis of macedocin, the lantibiotic produced by Streptococcus macedonicus ACA-DC 198. Appl. Environ. Microbiol. 2010, 76:1143-1151. 10.1128/AEM.00151-09.
28. Hartmann G., Bidlingmaier C., Siegmund B., Albrich S., Schulze J., Tschoep K., Eigler A., Lehr H.A., Endres S. Specific type IV phosphodiesterase inhibitor rolipram mitigates experimental colitis in mice. J. Pharmacol. Exp. Ther. 2000, 292:22-30.
29. Håversen L., Ohlsson B.G., Hahn-Zoric M., Hanson L.A., Mattsby-Baltzer I. Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappa B. Cell. Immunol. 2002, 220:83-95.
30. Hervé C., Fondrevez M., Chéron A., Barloy-Hubler F., Jan G. Transcarboxylase mRNA: a marker which evidences P. freudenreichii survival and metabolic activity during its transit in the human gut. Int. J. Food Microbiol. 2007, 113:303-314. 10.1016/j.ijfoodmicro.2006.08.013.
31. 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. Biosci. Microflora 2002, 21:115-120.
32. Jan G., Leverrier P., Pichereau V., Boyaval P. Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii. Appl. Environ. Microbiol. 2001, 67:2029-2036. 10.1128/AEM.67.5.2029-2036.2001.
33. Kamada N., Chen G.Y., Inohara N., Núñez G. Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 2013, 14:685-690. 10.1038/ni.2608.
34. Kang S., Denman S.E., Morrison M., Yu Z., Dore J., Leclerc M., McSweeney C.S. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm. Bowel Dis. 2010, 16:2034-2042. 10.1002/ibd.21319.
35. Kekkonen R.-A., Lummela N., Karjalainen H., Latvala S., Tynkkynen S., Jarvenpaa S., Kautiainen H., Julkunen I., Vapaatalo H., Korpela R. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J. Gastroenterol. WJG 2008, 14:2029-2036.
36. Konstantinov S.R., Smidt H., de Vos W.M., Bruijns S.C.M., Singh S.K., Valence F., Molle D., Lortal S., Altermann E., Klaenhammer T.R., van Kooyk Y. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19474-19479. 10.1073/pnas.0810305105.
37. Koskenniemi K., Koponen J., Kankainen M., Savijoki K., Tynkkynen S., de Vos W.M., Kalkkinen N., Varmanen P. Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media. J. Proteome Res. 2009, 8:4993-5007. 10.1021/pr9003823.
38. Laakso K., Koskenniemi K., Koponen J., Kankainen M., Surakka A., Salusjärvi T., Auvinen P., Savijoki K., Nyman T.A., Kalkkinen N., Tynkkynen S., Varmanen P. Growth phase-associated changes in the proteome and transcriptome of Lactobacillus rhamnosus GG in industrial-type whey medium. Microb. Biotechnol. 2011, 4:746-766. 10.1111/j.1751-7915.2011.00275.x.
39. Le Maréchal C., Peton V., Plé 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. J. Proteomics 2015, 113:447-461. 10.1016/j.jprot.2014.07.018.
40. Leone V., Chang E.B., Devkota S. Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases. J. Gastroenterol. 2013, 48:315-321. 10.1007/s00535-013-0777-2.
41. Leverrier P., Dimova D., Pichereau V., Auffray Y., Boyaval P., Jan G. Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl. Environ. Microbiol. 2003, 69:3809-3818.
42. Leverrier P., Fremont Y., Rouault A., Boyaval P., Jan G. In vitro tolerance to digestive stresses of propionibacteria: influence of food matrices. Food Microbiol. 2005, 22:11-18. 10.1016/j.fm.2004.05.003.
43. Machiels K., Joossens M., Sabino J., De Preter V., Arijs I., Eeckhaut V., Ballet V., Claes K., Van Immerseel F., Verbeke K., Ferrante M., Verhaegen J., Rutgeerts P., Vermeire S. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 2014, 63:1275-1283. 10.1136/gutjnl-2013-304833.
44. Macho Fernandez E., Fernandez E.M., Valenti V., Rockel C., Hermann C., Pot B., Boneca I.G., Grangette C. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 2011, 60:1050-1059. 10.1136/gut.2010.232918.
45. Malik A.C., Reinbold G.W., Vedamuthu E.R. An evaluation of the taxonomy of Propionibacterium. Can. J. Microbiol. 1968, 14:1185-1191.
46. Martín R., Miquel S., Ulmer J., Kechaou N., Langella P., Bermúdez-Humarán L.G. Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb. Cell. Factories 2013, 12:71. 10.1186/1475-2859-12-71.
47. Minocha A. Probiotics for preventive health. Nutr. Clin. Pract. Off. Publ. Am. Soc. Parenter. Enter. Nutr. 2009, 24:227-241. 10.1177/0884533608331177.
48. Mohamadzadeh M., Pfeiler E.A., Brown J.B., Zadeh M., Gramarossa M., Managlia E., Bere P., Sarraj B., Khan M.W., Pakanati K.C., Ansari M.J., O'Flaherty S., Barrett T., Klaenhammer T.R. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4623-4630. 10.1073/pnas.1005066107.
49. Morgan X.C., Tickle T.L., Sokol H., Gevers D., Devaney K.L., Ward D.V., Reyes J.A., Shah S.A., LeLeiko N., Snapper S.B., Bousvaros A., Korzenik J., Sands B.E., Xavier R.J., Huttenhower C. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012, 13:R79. 10.1186/gb-2012-13-9-r79.
50. Nguyen H.T.T., Dalmasso G., Müller S., Carrière J., Seibold F., Darfeuille-Michaud A. Crohn's disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology 2014, 146:508-519. 10.1053/j.gastro.2013.10.021.
51. Papadimitriou K., Zoumpopoulou G., Foligné B., Alexandraki V., Kazou M., Pot B., Tsakalidou E. Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front. Microbiol. 2015, 6:58. 10.3389/fmicb.2015.00058.
52. Piveteau P., Condon S., Cogan T.M. Inability of dairy propionibacteria to grow in milk from low inocula. J. Dairy Res. 2000, 67:65-71.
53. Purchiaroni F., Tortora A., Gabrielli M., Bertucci F., Gigante G., Ianiro G., Ojetti V., Scarpellini E., Gasbarrini A. The role of intestinal microbiota and the immune system. Eur. Rev. Med. Pharmacol. Sci. 2013, 17:323-333.
54. Ranadheera R.D.C.S., Baines S.K., Adams M.C. Importance of food in probiotic efficacy. Food Res. Int. 2010, 43:1-7. 10.1016/j.foodres.2009.09.009.
55. Sanders M.E., Guarner F., Guerrant R., Holt P.R., Quigley E.M.M., Sartor R.B., Sherman P.M., Mayer E.A. An update on the use and investigation of probiotics in health and disease. Gut 2013, 62:787-796. 10.1136/gutjnl-2012-302504.
56. Santos Rocha C., Lakhdari O., Blottière H.M., Blugeon S., Sokol H., Bermúdez-Humarán L.G., Azevedo V., Miyoshi A., Doré J., Langella P., Maguin E., van de Guchte M. Anti-inflammatory properties of dairy lactobacilli. Inflamm. Bowel Dis. 2012, 18:657-666. 10.1002/ibd.21834.
57. Savaiano D.A. Lactose digestion from yogurt: mechanism and relevance. Am. J. Clin. Nutr. 2014, 99:1251S-1255S. 10.3945/ajcn.113.073023.
58. Shao L., Wu Z., Zhang H., Chen W., Ai L., Guo B. Partial characterization and immunostimulatory activity of exopolysaccharides from Lactobacillus rhamnosus KF5. Carbohydr. Polym. 2014, 107:51-56. 10.1016/j.carbpol.2014.02.037.
59. Shen J., Zuo Z.-X., Mao A.-P. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn's disease, and pouchitis: meta-analysis of randomized controlled trials. Inflamm. Bowel Dis. 2014, 20:21-35. 10.1097/01.MIB.0000437495.30052.be.
60. Sokol H., Lay C., Seksik P., Tannock G.W. Analysis of bacterial bowel communities of IBD patients: what has it revealed?. Inflamm. Bowel Dis. 2008, 14:858-867. 10.1002/ibd.20392.
61. Suzuki C., Kimoto-Nira H., Kobayashi M., Nomura M., Sasaki K., Mizumachi K. Immunomodulatory and cytotoxic effects of various Lactococcus strains on the murine macrophage cell line J774.1. Int. J. Food Microbiol. 2008, 123:159-165. 10.1016/j.ijfoodmicro.2007.12.022.
62. Taverniti V., Guglielmetti S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes. Nutr. 2011, 6:261-274. 10.1007/s12263-011-0218-x.
63. Taverniti V., Stuknyte M., Minuzzo M., Arioli S., De Noni I., Scabiosi C., Cordova Z.M., Junttila I., Hämäläinen S., Turpeinen H., Mora D., Karp M., Pesu M., Guglielmetti S. S-layer protein mediates the stimulatory effect of Lactobacillus helveticus MIMLh5 on innate immunity. Appl. Environ. Microbiol. 2013, 79:1221-1231. 10.1128/AEM.03056-12.
64. Terzaghi B.E., Sandine W.E. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 1975, 29:807-813.
65. Thierry A., Deutsch S.-M., Falentin H., Dalmasso M., Cousin F.J., Jan G. New insights into physiology and metabolism of Propionibacterium freudenreichii. Int. J. Food Microbiol. 2011, 149:19-27. 10.1016/j.ijfoodmicro.2011.04.026.
66. Thierry A., Madec M.N. Enumeration of propionibacteria in raw milk using a new selective medium. Le Lait. 1995, 75:315-323. 10.1051/lait:19954-523.
67. Timmerman H.M., Koning C.J.M., Mulder L., Rombouts F.M., Beynen A.C. Monostrain, multistrain and multispecies probiotics-A comparison of functionality and efficacy. Int. J. Food Microbiol. 2004, 96:219-233. 10.1016/j.ijfoodmicro.2004.05.012.
68. Van Hemert S., Meijerink M., Molenaar D., Bron P.A., de Vos P., Kleerebezem M., Wells J.M., Marco M.L. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 2010, 10:293. 10.1186/1471-2180-10-293.
69. Vinderola G., Binetti A., Burns P., Reinheimer J. Cell viability and functionality of probiotic bacteria in dairy products. Front. Microbiol. 2011, 2:70. 10.3389/fmicb.2011.00070.
70. Vinderola G., Zacarías M.F., Bockelmann W., Neve H., Reinheimer J., Heller K.J. Preservation of functionality of Bifidobacterium animalis subsp. lactis INL1 after incorporation of freeze-dried cells into different food matrices. Food Microbiol. 2012, 30:274-280. 10.1016/j.fm.2011.12.004.
71. 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.
72. Zheng B., van Bergenhenegouwen J., Overbeek S., van de Kant H.J.G., Garssen J., Folkerts G., Vos P., Morgan M.E., Kraneveld A.D. Bifidobacterium breve attenuates murine dextran sodium sulfate-induced colitis and increases regulatory t cell responses. PloS One 2014, 9:e95441. 10.1371/journal.pone.0095441.
73. Zhou F.-X., Chen L., Liu X.-W., Ouyang C.-H., Wu X.-P., Wang X.-H., Wang C.-L., Lu F.-G. Lactobacillus crispatus M206119 exacerbates murine DSS-colitis by interfering with inflammatory responses. World J. Gastroenterol. WJG 2012, 18:2344-2356. 10.3748/wjg.v18.i19.2344.
74. Zhou X.X., Pan Y.J., Wang Y.B., Li W.F. Optimization of medium composition for nisin fermentation with response surface methodology. J. Food Sci. 2008, 73:245-M249.