Beneficial Propionibacteria within a Probiotic Emmental Cheese: Impact on Dextran Sodium Sulphate-Induced Colitis in Mice

Microorganisms - Tập 8 Số 3 - Trang 380
Hassan Rabah1,2, Fillipe Luiz Rosa Do Carmo3, Rodrigo Dias de Oliveira Carvalho4, Bárbara Fernandes Cordeiro3, Sara Heloísa da Silva3, Emiliano Rosa Oliveira3, Álvaro Cantini Nunes3, Denise Carmona Cara3, Ana Maria Caetano Faria3, Gilles Garric2, Marielle Harel-Oger2, Yves Le Loir2, Vasco Azevedo3, Guillaume Bouguen5,6, Gwénaël Jan2
1Pôle Agronomique Ouest, Régions Bretagne et Pays de la Loire (France)
2STLO - Science et Technologie du Lait et de l'Oeuf (65, rue de Saint Brieuc 35042 Rennes - France)
3UFMG - Universidade Federal de Minas Gerais = Federal University of Minas Gerais [Belo Horizonte, Brazil] (Av. Antônio Carlos, 6627, Pampulha - Belo Horizonte - MG - CEP 31270-901 BRAZIL - Brésil)
4Sechenov First Moscow State Medical University (8-2 Trubetskaya st., Moscow 119991, Russia - Russie)
5CIC - Centre d'Investigation Clinique [Rennes] (Rue Henri Le Guilloux - Pavillon Clémenceau 35033 Rennes Cedex 9 - France)
6NuMeCan - Nutrition, Métabolismes et Cancer (Campus Villejean (Bât 8) - CHU Rennes (Bât 15) - Université de Rennes 1, 2 Avenue du Professeur Léon Bernard, 35043 Rennes, France - France)

Tóm tắt

Backgrounds and Aims. Inflammatory Bowel Diseases (IBD), including Ulcerative Colitis (UC), coincide with alterations in the gut microbiota. Consumption of immunomodulatory strains of probiotic bacteria may induce or prolong remission in UC patients. Fermented foods, including cheeses, constitute major vectors for bacteria consumption. New evidences revealed anti-inflammatory effects in selected strains of Propionibacterium freudenreichii. We thus hypothesized that consumption of a functional cheese, fermented by such a strain, may exert a positive effect on IBD. Methods. We investigated the impact of cheese fermented by P. freudenreichii on gut inflammation. We developed an experimental single-strain cheese solely fermented by a selected immunomodulatory strain of P. freudenreichii, CIRM-BIA 129. We moreover produced, in industrial conditions, an Emmental cheese using the same strain, in combination with Lactobacillus delbrueckii CNRZ327 and Streptococcus thermophilus LMD-9, as starters. Consumption of both cheeses was investigated with respect to prevention of Dextran Sodium Sulphate (DSS)-induced colitis in mice. Results. Consumption of the single-strain experimental cheese, or of the industrial Emmental, both fermented by P. freudenreichii CIRM-BIA 129, reduced severity of subsequent DSS-induced colitis, weight loss, disease activity index and histological score. Both treatments, in a preventive way, reduced small bowel Immunoglobulin A (IgA) secretion, restored occludin gene expression and prevented induction of Tumor Necrosis Factor α (TNFα), Interferon γ (IFNγ) and Interleukin-17 (IL-17). Conclusions. A combination of immunomodulatory strains of starter bacteria can be used to manufacture an anti-inflammatory cheese, as revealed in an animal model of colitis. This opens new perspectives for personalised nutrition in the context of IBD.

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Tài liệu tham khảo

Diplock, 1999, Scientific concepts of functional foods in europe: Consensus document, Br. J. Nutr., 81, S1, 10.1017/S0007114599000471

Saris, 1998, Functional food science and substrate metabolism, Br. J. Nutr., 80, S47, 10.1079/BJN19980105

Rabah, H., Do Carmo, F.L.R., and Jan, G. (2017). Dairy propionibacteria: Versatile probiotics. Microorganisms, 5.

Santaolalla, 2012, Innate immunity in the small intestine, Curr. Opin. Gastroenterol., 28, 124, 10.1097/MOG.0b013e3283506559

Ko, 2014, Inflammatory bowel disease: Etiology, pathogenesis and current therapy, Curr. Pharm. Des., 20, 1082, 10.2174/13816128113199990416

Vindigni, 2016, The intestinal microbiome, barrier function, and immune system in inflammatory bowel disease: A tripartite pathophysiological circuit with implications for new therapeutic directions, Therap. Adv. Gastroenterol., 9, 606, 10.1177/1756283X16644242

Zhang, 2014, Inflammatory bowel disease: Pathogenesis, World J. Gastroenterol., 20, 91, 10.3748/wjg.v20.i1.91

Derwa, 2017, Systematic review with meta-analysis: The efficacy of probiotics in inflammatory bowel disease, Aliment. Pharmacol. Ther., 46, 389, 10.1111/apt.14203

Ghouri, 2014, Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease, Clin. Exp. Gastroenterol., 7, 473

Sniffen, J.C., McFarland, L.V., Evans, C.T., and Goldstein, E.J.C. (2018). Choosing an appropriate probiotic product for your patient: An evidence-based practical guide. PLoS ONE, 13.

Colliou, 2017, Commensal Propionibacterium strain UF1 mitigates intestinal inflammation via Th17 cell regulation, J. Clin. Investig., 127, 3970, 10.1172/JCI95376

Breton, 2013, Tracking the microbiome functionality: Focus on Propionibacterium species, Gut, 62, 1227, 10.1136/gutjnl-2012-304393

Fuquay, J.W., Fox, P.F., and Mc Sweeney, P.L.H. (2011). Propionibacterium spp.. Encyclopedia of Dairy Sciences, Academic Press.

Deutsch, 2010, Promising immunomodulatory effects of selected strains of dairy propionibacteria as evidenced in vitro and in vivo, Appl. Environ. Microbiol., 76, 8259, 10.1128/AEM.01976-10

Peton, 2015, Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties, J. Proteom., 113C, 447

Deutsch, 2017, Identification of proteins involved in the anti-inflammatory properties of Propionibacterium freudenreichii by means of a multi-strain study, Sci. Rep., 7, 46409, 10.1038/srep46409

Rabah, 2018, Cheese matrix protects the immunomodulatory surface protein SlpB of Propionibacterium freudenreichii during in vitro digestion, Food Res. Int., 106, 712, 10.1016/j.foodres.2018.01.035

Rabah, 2018, The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets, Front. Microbiol., 9, 2584, 10.3389/fmicb.2018.02584

Breton, 2016, Combining selected immunomodulatory Propionibacterium freudenreichii and Lactobacillus delbrueckii strains: Reverse engineering development of an anti-inflammatory cheese, Mol. Nutr. Food Res., 60, 935, 10.1002/mnfr.201500580

Richoux, 2015, Single-strain starter experimental cheese reveals anti-inflammatory effect of Propionibacterium freudenreichii CIRM BIA 129 in TNBS-colitis model, J. Funct. Foods, 18, 575, 10.1016/j.jff.2015.08.015

Ge, 2019, Neonatal intestinal immune regulation by the commensal bacterium, P. UF1, Mucosal Immunol., 12, 434, 10.1038/s41385-018-0125-1

George, 2018, Occurrence and Dynamism of Lactic Acid Bacteria in Distinct Ecological Niches: A Multifaceted Functional Health Perspective, Front. Microbiol., 9, 2899, 10.3389/fmicb.2018.02899

Santos Rocha, C., Gomes-Santos, A.C., Garcias Moreira, T., de Azevedo, M., Diniz Luerce, T., Mariadassou, M., Longaray Delamare, A.P., Langella, P., Maguin, E., and Azevedo, V. (2014). Local and systemic immune mechanisms underlying the anti-colitis effects of the dairy bacterium Lactobacillus delbrueckii. PLoS ONE, 9.

Lakhdari, 2012, Anti-inflammatory properties of dairy lactobacilli, Inflamm. Bowel. Dis., 18, 657, 10.1002/ibd.21834

Junjua, 2016, A large scale in vitro screening of Streptococcus thermophilus strains revealed strains with a high anti-inflammatory potential, LWT—Food Sci. Technol., 70, 78, 10.1016/j.lwt.2016.02.006

Rogosa, 1960, A medium for the cultivation of lactobacilli, J. Appl. Bacteriol., 23, 130, 10.1111/j.1365-2672.1960.tb00188.x

Terzaghi, 1975, Improved medium for lactic streptococci and their bacteriophages, Appl. Microbiol., 29, 807, 10.1128/am.29.6.807-813.1975

Malik, 1968, An evaluation of the taxonomy of Propionibacterium, Can. J. Microbiol., 14, 1185, 10.1139/m68-199

Richoux, 2009, Impact of the proteolysis due to lactobacilli on the stretchability of Swiss-type cheese, Dairy Sci. Technol., 89, 31, 10.1051/dst:2008030

Li, 2017, Somatic cell recovery by microfiltration technologies: A novel strategy to study the actual impact of somatic cells on cheese matrix, Int. Dairy J., 65, 5, 10.1016/j.idairyj.2016.09.003

Chuat, 2015, Biodiversity of dairy Propionibacterium isolated from dairy farms in Minas Gerais, Brazil, Int. J. Food Microbiol., 203, 70, 10.1016/j.ijfoodmicro.2015.03.006

Gautier, 1996, DNA fingerprinting of dairy propionibacteria strains by pulsed-field gel electrophoresis, Curr. Microbiol., 32, 17, 10.1007/s002849900004

Jan, 2000, Acid stress susceptibility and acid adaptation of Propionibacterium freudenreichii subsp., shermanii. Lait, 80, 325, 10.1051/lait:2000128

Rossi, F., Amadoro, C., and Colavita, G. (2019). Members of the Lactobacillus Genus Complex (LGC) as Opportunistic Pathogens: A Review. Microorganisms, 7.

Jenkins, 2002, Genetic diversity in Swiss cheese starter cultures assessed by pulsed field gel electrophoresis and arbitrarily primed PCR, Lett. Appl. Microbiol., 35, 423, 10.1046/j.1472-765X.2002.01212.x

Diehl, 2001, European Federation of Pharmaceutical Industries Association and European Centre for the Validation of Alternative Methods A good practice guide to the administration of substances and removal of blood, including routes and volumes, J. Appl. Toxicol., 21, 15, 10.1002/jat.727

Cooper, 1993, Clinicopathologic study of dextran sulfate sodium experimental murine colitis, Lab. Investig., 69, 238

McCafferty, 2000, Spontaneously developing chronic colitis in IL-10/iNOS double-deficient mice, Am. J. Physiol. Gastrointest. Liver Physiol., 279, G90, 10.1152/ajpgi.2000.279.1.G90

Carvalho, 2017, Secretion of biologically active pancreatitis-associated protein I (PAP) by genetically modified dairy Lactococcus lactis NZ9000 in the prevention of intestinal mucositis, Microb. Cell Fact., 16, 27, 10.1186/s12934-017-0624-x

Oliveira, 2018, In vitro and in vivo evaluation of two potential probiotic lactobacilli isolated from cocoa fermentation (Theobroma cacao L.), J. Funct. Foods, 47, 184, 10.1016/j.jff.2018.05.055

Thierry, 1998, Swiss cheese ripening: Dynamics of bacterial populations and evolution of the aqueous phase composition for three industrial cheeses, Lait, 78, 521, 10.1051/lait:1998549

Langsrud, 1973, Flavor development and microbiology of Swiss cheese. A. Review. II Starters, manufacturing process and procedures, J. Milk Food Technol., 36, 531, 10.4315/0022-2747-36.11.531

Gagnaire, 2001, Peptides identified during Emmental cheese ripening: Origin and proteolytic systems involved, J. Agric. Food Chem., 49, 4402, 10.1021/jf000895z

Parayre, 2016, Immunomodulation properties of multi-species fermented milks, Food Microbiol., 53, 60, 10.1016/j.fm.2015.04.002

Ohtsuka, 2003, Dextran sulfate sodium-induced inflammation is enhanced by intestinal epithelial cell chemokine expression in mice, Pediatr. Res., 53, 143

Cerar, 2012, Dextran sodium sulphate colitis mouse model: Traps and tricks, J. Biomed. Biotechnol., 2012, 718617

Rabah, 2019, Probiotic Propionibacterium freudenreichii requires SlpB protein to mitigate mucositis induced by chemotherapy, Oncotarget, 10, 7198, 10.18632/oncotarget.27319

Vancamelbeke, 2017, The intestinal barrier: A fundamental role in health and disease, Expert Rev. Gastroenterol. Hepatol., 11, 821, 10.1080/17474124.2017.1343143

Landy, 2016, Tight junctions in inflammatory bowel diseases and inflammatory bowel disease associated colorectal cancer, World J. Gastroenterol., 22, 3117, 10.3748/wjg.v22.i11.3117

Roda, G., Marocchi, M., Sartini, A., and Roda, E. (2019, January 01). Cytokine Networks in Ulcerative Colitis. Available online: https://www.hindawi.com/journals/ulcers/2011/391787/.

Cardoso, 2018, The Dynamics of Interleukin-10-Afforded Protection during Dextran Sulfate Sodium-Induced Colitis, Front. Immunol., 9, 400, 10.3389/fimmu.2018.00400

Letterio, 1998, Regulation of immune responses by TGF-beta, Annu. Rev. Immunol., 16, 137, 10.1146/annurev.immunol.16.1.137

Wen, 2015, The role of Th17/Treg balance and Th22 cell in the pathogenesis of DSS-induced colitis in mice, Eur. J. Inflamm., 13, 101, 10.1177/1721727X15580902

Lazzi, 2016, Can the development and autolysis of lactic acid bacteria influence the cheese volatile fraction? The case of Grana Padano, Int. J. Food Microbiol., 233, 20, 10.1016/j.ijfoodmicro.2016.06.009

Pang, 2017, Identification and Functional Validation of Autolysis-Associated Genes in Lactobacillus bulgaricus ATCC BAA-365, Front. Microbiol., 8, 1367, 10.3389/fmicb.2017.01367

Valence, 2000, Autolysis and related proteolysis in Swiss cheese for two Lactobacillus helveticus strains, J. Dairy Res., 67, 261, 10.1017/S0022029900004118

Nutten, 2006, Recommendations for improved use of the murine TNBS-induced colitis model in evaluating anti-inflammatory properties of lactic acid bacteria: Technical and microbiological aspects, Dig. Dis. Sci., 51, 390, 10.1007/s10620-006-3143-x

Sang, 2015, Live and heat-killed probiotic: Effects on chronic experimental colitis induced by dextran sulfate sodium (DSS) in rats, Int. J. Clin. Exp. Med., 8, 20072

Thakur, 2016, Live and heat-killed probiotic Lactobacillus casei Lbs2 protects from experimental colitis through Toll-like receptor 2-dependent induction of T-regulatory response, Int. Immunopharmacol., 36, 39, 10.1016/j.intimp.2016.03.033

Ueno, 2011, Heat-killed body of lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function, Inflamm. Bowel Dis., 17, 2235, 10.1002/ibd.21597

Baer, 1995, Influence of casein proteolysis by starter bacteria, rennet and plasmin on the growth of propionibacteria in Swiss-type cheese, Lait, 75, 391, 10.1051/lait:19954-529

Brown, 2017, Lactic Acid Bacteria as Cell Factories for the Generation of Bioactive Peptides, Protein Pept. Lett., 24, 146, 10.2174/0929866524666161123111333

Bösze, Z. (2008). Milk Peptides and Immune Response in the Neonate. Bioactive Components of Milk, Springer New York. Advances in Experimental Medicine and Biology.

Kaneko, 1999, A novel bifidogenic growth stimulator produced by Propionibacterium freudenreichii, Biosci. Microfl., 18, 73, 10.12938/bifidus1996.18.73

Seki, 2004, 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, J. Intest. Microbiol., 18, 107

Figliuolo, 2017, Sulfate-reducing bacteria stimulate gut immune responses and contribute to inflammation in experimental colitis, Life Sci., 189, 29, 10.1016/j.lfs.2017.09.014

Figliuolo, 2018, Contribution of sulfate-reducing bacteria to homeostasis disruption during intestinal inflammation, Life Sci., 215, 145, 10.1016/j.lfs.2018.11.009

Kushkevych, I., Leščanová, O., Dordević, D., Jančíková, S., Hošek, J., Vítězová, M., Buňková, L., and Drago, L. (2019). The Sulfate-Reducing Microbial Communities and Meta-Analysis of Their Occurrence during Diseases of Small-Large Intestine Axis. J. Clin. Med., 8.

Wallace, 2018, Hydrogen sulfide: An agent of stability at the microbiome-mucosa interface, Am. J. Physiol. Gastrointest. Liver Physiol., 314, G143, 10.1152/ajpgi.00249.2017

Kushkevych, I., Kotrsová, V., Dordević, D., Buňková, L., Vítězová, M., and Amedei, A. (2019). Hydrogen Sulfide Effects on the Survival of Lactobacilli with Emphasis on the Development of Inflammatory Bowel Diseases. Biomolecules, 9.

Kushkevych, I., Dordević, D., Kollar, P., Vítězová, M., and Drago, L. (2019). Hydrogen Sulfide as a Toxic Product in the Small-Large Intestine Axis and its Role in IBD Development. J. Clin. Med., 8.