Adhesion to the host intestinal mucosa is considered relevant for orally delivered probiotics as it prolongs their persistence in the gut and their health promoting effects. Classical propionibacteria are microorganisms of interest due to their role as dairy starters as well as for their functions as probiotics. Propionibacterium acidipropionici Q4, is a dairy strain isolated from a Swiss-type cheese made in Argentina that displays probiotic potential. In the present work we assessed the ability of this strain to adhere to the human enterocyte-like HT-29 cell line and to counteract the adhesion of two common human enteropathogens, such as Escherichia coli C3 and Salmonella Enteritidis 90/390. The results were compared with those obtained with the well-known probiotic Lactobacillus rhamnosus GG. P. acidipropionici Q4 showed a high adhesion capacity, even higher than the reference strain L. rhamnosus GG (42.3±4.4% and 36.2±2.3%, respectively), whereas adhesion of enteropathogens was significantly lower (25.2±2.2% for E. coli and 21.0±3.4% for S. Enteritidis). Propionibacteria as well as lactobacilli were able to inhibit by exclusion and competition the adherence of E. coli C3 and S. Enteritidis 90/390 whereas only L. rhamnosus GG displaced S. Enteritidis from HT-29 intestinal cells. Inhibition of pathogens by propionibacteria was not exerted by antimicrobials or coaggregation but was mainly due to exclusion by cell surface components, such as proteins and carbohydrates. The relevance of cell surface proteins (CSP) for preventing pathogens infection was confirmed by their concentration dependent effect observed for both pathogens: 100 µg/ml of CSP inhibited E. coli attachment almost as untreated propionibacteria, whereas it partially inhibited the attachment of S. Enteritidis. Results suggest that P. acidipropionici Q4 could be considered for the development of propionibacteria containing functional foods helpful in counteracting enteropathogen infection.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Azcarate-Peril, M.A. and Klaenhammer, T.R., 2010. Genomics of lactic acid bacteria: the post-genomics challenge – from sequence to function. In: Mozzi, F., Raya, R.R. and Vignolo, G.M. (eds.) Biotechnology of lactic acid bacteria: novel applications. Wiley-Blackwell, Oxford, UK, pp. 35-56.
'Genomics of lactic acid bacteria: the post-genomics challenge – from sequence to function ', in Biotechnology of lactic acid bacteria: novel applications , () 35 -56.
Chen, X., Xu, J., Shuai, J., Chen, J., Zhang, Z. and Fang, W., 2007. The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157: H7 and Salmonella typhimurium. International Journal of Food Microbiology 115: 307-312.
The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157: H7 and Salmonella typhimurium International Journal of Food Microbiology 115 307 312
Collado, M.C., Gueimonde, M. and Salminen, S., 2010. Probiotics in adhesion of pathogens: mechanisms of action. In: Watson, R.R. and Preedy, V.R. (eds.) Bioactive foods in promoting health. Probiotics and Prebiotics. Academic Press, London, UK, pp. 353-370.
'Probiotics in adhesion of pathogens: mechanisms of action ', in Bioactive foods in promoting health. Probiotics and Prebiotics , () 353 -370.
Collado, M.C., Meriluoto, J. and Salminen, S., 2007. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Letters in Applied Microbiology 45: 454-460.
'Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus ' () 45 Letters in Applied Microbiology : 454 -460.
Cousin, F., Mater, D.D.G., Foligné, B. and Jan, G., 2011. Dairy propionibacteria as human probiotics: a review of recent evidence. Dairy Science and Technology 91: 1-26.
'Dairy propionibacteria as human probiotics: a review of recent evidence ' () 91 Dairy Science and Technology : 1 -26.
Dhanani, A.S. and Bagchi, T., 2013. Lactobacillus plantarum CS24.2 prevents E. coli adhesion to HT-29 cells and also down-regulates enteropathogen induced TNFalpha and IL-8 expression. Microbiology and Immunology 57: 309-315.
'Lactobacillus plantarum CS24.2 prevents E. coli adhesion to HT-29 cells and also down-regulates enteropathogen induced TNFalpha and IL-8 expression ' () 57 Microbiology and Immunology : 309 -315.
Falentin, H., Deutsch, S.M., Jan, G., Loux, V., Thierry, A. and Parayre, S., 2010. The complete genome of Propionibacterium freudenreichii CIRM-BIA1, a hardy actinobacterium with food and probiotic applications. PloS One 5: e11748.
'The complete genome of Propionibacterium freudenreichii CIRM-BIA1, a hardy actinobacterium with food and probiotic applications ' () 5 PloS One : e11748.
Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO), 2002. Guidelines for the evaluation of probiotics in food. Report of a Joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Available at: http://tinyurl.com/ou88oa2.
Garriga, M., Rubio, R., Aymerich, T. and Ruas-Madiedo, P., 2014. Potentially probiotic and bioprotective lactic acid bacteria starter cultures antagonise the Listeria monocytogenes adhesion to HT29 colonocyte-like cells. Beneficial Microbes 6: 337-343.
'Potentially probiotic and bioprotective lactic acid bacteria starter cultures antagonise the Listeria monocytogenes adhesion to HT29 colonocyte-like cells ' () 6 Beneficial Microbes : 337 -343.
Gueimonde, M., Jalonen, L., He, F., Hiramatsu, M. and Salminen, S., 2006. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Research International 39: 467-471.
'Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli ' () 39 Food Research International : 467 -471.
Huang, Y. and Adams, M.C., 2003. An in vitro model for investigating intestinal adhesion of potential dairy propionibacteria probiotic strains using cell line C2BBe1. Letters in Applied Microbiology 36: 213-216.
'An in vitro model for investigating intestinal adhesion of potential dairy propionibacteria probiotic strains using cell line C2BBe1 ' () 36 Letters in Applied Microbiology : 213 -216.
Johnson-Henry, K.C., Hagen, K.E., Gordonpour, M., Tompkins, T.A. and Sherman, P.M., 2007. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cellular Microbiology 9: 356-367.
'Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells ' () 9 Cellular Microbiology : 356 -367.
Laparra, J.M. and Sanz, Y., 2009. Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Letters in Applied Microbiology 49: 695-701.
'Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium ' () 49 Letters in Applied Microbiology : 695 -701.
Le Maréchal, C., Peton, V., Plé, C., Vroland, C., Jardin, J. and Briard-Bion, V., 2015. Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties. Journal of Proteomics 112: 447-461.
Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties Journal of Proteomics 112 447 461
Lebeer, S., Vanderleyden, J. and De Keersmaecker, S.C., 2010. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nature Reviews Microbiology 8: 171-184.
'Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens ' () 8 Nature Reviews Microbiology : 171 -184.
Lee, Y.K., Puong, K.Y., Ouwehand, A.C. and Salminen, S., 2003. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. Journal of Medical Microbiology 52: 925-930.
Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli Journal of Medical Microbiology 52 925 930
Lehto, E.M. and Salminen, S., 1997. Adhesion of two Lactobacillus strains, one Lactococcus and one Propionibacterium strain to cultured human intestinal Caco-2 cell line. Bioscience and Microflora 16: 13-17.
'Adhesion of two Lactobacillus strains, one Lactococcus and one Propionibacterium strain to cultured human intestinal Caco-2 cell line ' () 16 Bioscience and Microflora : 13 -17.
Leuschner, R.G.K., Robinson, T.P., Hugas, M., Cocconcelli, P.S., Richard-Forget, F. and Klein, G., 2010. Qualified presumption of safety (QPS): a generic risk assessment approach for biological agents notified to the European Food Safety Authority (EFSA). Trends in Food Science and Technology 21: 425-435.
'Qualified presumption of safety (QPS): a generic risk assessment approach for biological agents notified to the European Food Safety Authority (EFSA) ' () 21 Trends in Food Science and Technology : 425 -435.
Li, X.J., Yue, L.Y., Guan, X.F. and Qiao, S.Y., 2008. The adhesion of putative probiotic lactobacilli to cultured cells and porcine intestinal mucus. Journal of Applied Microbiology 104: 1082-1091.
The adhesion of putative probiotic lactobacilli to cultured cells and porcine intestinal mucus Journal of Applied Microbiology 104 1082 1091
Livins’ka, O.P., Garmasheva, I.L. and Kovalenko, N.K., 2013. The influence of teichoic acids from probiotic lactobacilli on microbial adhesion to epithelial cells. Mikrobiolohichnyĭ Zhurnal 74: 16-22.
'The influence of teichoic acids from probiotic lactobacilli on microbial adhesion to epithelial cells ' () 74 Mikrobiolohichnyĭ Zhurnal : 16 -22.
Lorenzo-Pisarello, M.J., Gultemirian, M.L., Nieto-Peñalver, C. and Pérez Chaia, A., 2010. Propionibacterium acidipropionici CRL 1198 influences the production of acids and the growth of bacterial genera stimulated by inulin in a murine model of cecal slurries. Anaerobe 16: 345-354.
'Propionibacterium acidipropionici CRL 1198 influences the production of acids and the growth of bacterial genera stimulated by inulin in a murine model of cecal slurries ' () 16 Anaerobe : 345 -354.
Myllyluoma, E., Ahonen, A.M., Korpela, R., Vapaatalo, H. and Kankuri, E., 2008. Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clinical and Vaccine Immunology 15: 1472-1482.
'Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro ' () 15 Clinical and Vaccine Immunology : 1472 -1482.
Ofek, I., Hasty, D.L. and Sharon, N., 2003. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunology and Medical Microbiology 38: 181-191.
'Anti-adhesion therapy of bacterial diseases: prospects and problems ' () 38 FEMS Immunology and Medical Microbiology : 181 -191.
Osset, J., Bartolome, R.M., García, E. and Andreu, A., 2001. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. Journal of Infection Disease 183: 485-491.
Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells Journal of Infection Disease 183 485 491
Ouwehand, A.C. and Salminen, S., 2003. In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microbial Ecology in Health and Disease 15: 175-184.
'In vitro adhesion assays for probiotics and their in vivo relevance: a review ' () 15 Microbial Ecology in Health and Disease : 175 -184.
Ouwehand, A., Tölkko, S., Kulmala, J., Salminen, S. and Salminen, E., 2000. Adhesion of inactivated probiotic strains to intestinal mucus. Letters in Applied Microbiology 31: 82-86.
'Adhesion of inactivated probiotic strains to intestinal mucus ' () 31 Letters in Applied Microbiology : 82 -86.
Pérez Chaia, A. and Zárate, G., 2005. Dairy propionibacteria from milk or cheese diets remain viable and enhance propionic acid production in the mouse caecum. Lait 85: 85-98.
'Dairy propionibacteria from milk or cheese diets remain viable and enhance propionic acid production in the mouse caecum ' () 85 Lait : 85 -98.
Pérez Chaia, A., Zárate, G. and Oliver, G., 1999. The probiotic properties of propionibacteria. Lait 79: 175-185.
'The probiotic properties of propionibacteria ' () 79 Lait : 175 -185.
Ranadheera, C.S., Evans, C.A., Adams, M.C. and Baines, S.K., 2012. In vitro analysis of gastrointestinal tolerance and intestinal cell adhesion of probiotics in goat’s milk ice cream and yogurt. Food Research International 49: 619-625.
'In vitro analysis of gastrointestinal tolerance and intestinal cell adhesion of probiotics in goat’s milk ice cream and yogurt ' () 49 Food Research International : 619 -625.
Ren, D., Li, C., Qin, Y., Yin, R., Li, X. and Tian, M., 2012. Inhibition of Staphylococcus aureus adherence to Caco-2 cells by lactobacilli and cell surface properties that influence attachment. Anaerobe 18: 508-515.
'Inhibition of Staphylococcus aureus adherence to Caco-2 cells by lactobacilli and cell surface properties that influence attachment ' () 18 Anaerobe : 508 -515.
Ribet, D. and Cossart, P., 2015. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes and Infection 17: 173-183.
'How bacterial pathogens colonize their hosts and invade deeper tissues ' () 17 Microbes and Infection : 173 -183.
Sengupta, R., Altermann, E., Anderson, R.C., McNabb, W.C., Moughan, P.J. and Roy, N.C., 2013. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators of Inflammation 2013: 237921.
'The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract ' () 2013 Mediators of Inflammation : 237921.
Tareb, R., Bernardeau, M., Gueguen, M. and Vernoux, J.-P., 2013. In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. Journal of Medical Microbiology 62: 637-649.
In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni Journal of Medical Microbiology 62 637 649
Thiel, A., Eikmanns, B., Salminen, S. and Ouwehand, A.C., 2004. In vitro adhesion of propionibacteria to human intestinal mucus. Journal of Food Science 16: 245-254.
In vitro adhesion of propionibacteria to human intestinal mucus Journal of Food Science 16 245 254
Tripathi, M.K. and Giri, S.K., 2014. Probiotic functional foods: survival of probiotics during processing and storage. Journal of Functional Foods 9: 225-241.
Probiotic functional foods: survival of probiotics during processing and storage Journal of Functional Foods 9 225 241
Zárate, G. and Nader-Macías, M.E., 2006. Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells. Letters in Applied Microbiology 43: 174-180.
'Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells ' () 43 Letters in Applied Microbiology : 174 -180.
Zárate, G. and Pérez Chaia, A., 2012a. Influence of lactose and lactate on growth and β-galactosidase activity of potential probiotic Propionibacterium acidipropionici. Anaerobe 18: 25-30.
'Influence of lactose and lactate on growth and β-galactosidase activity of potential probiotic Propionibacterium acidipropionici ' () 18 Anaerobe : 25 -30.
Zárate, G. and Pérez Chaia, A., 2012b. Feeding with dairy Propionibacterium acidipropionici CRL 1198 reduces the incidence of concanavalin-A induced alterations in mouse small intestinal epithelium. Food Research International 47: 13-22.
'Feeding with dairy Propionibacterium acidipropionici CRL 1198 reduces the incidence of concanavalin-A induced alterations in mouse small intestinal epithelium ' () 47 Food Research International : 13 -22.
Zárate, G. and Pérez Chaia, A., 2015. Propionibacteria also have probiotic potential. In: Venema, K. and Do Carmo, A.P. (eds.) Probiotics and prebiotics: current research and future trends. Caister Academic Press, Norfolk, UK, pp. 69-91.
'Propionibacteria also have probiotic potential ', in Probiotics and prebiotics: current research and future trends , () 69 -91.
Zárate, G., Chaia, A.P., Gonzalez, S. and Oliver, G., 2000. Viability and beta-galactosidase activity of dairy propionibacteria subjected to digestion by artificial gastric and intestinal fluids. Journal of Food Protection 63: 1214-1221.
Viability and beta-galactosidase activity of dairy propionibacteria subjected to digestion by artificial gastric and intestinal fluids Journal of Food Protection 63 1214 1221
Zarate, G., Morata de Ambrosini, V.I., Pérez Chaia, A. and Gonzalez, S.N., 2002a. Adhesion of dairy propionibacteria to intestinal epithelial tissue in vitro and in vivo. Journal of Food Protection 65: 534-539.
Adhesion of dairy propionibacteria to intestinal epithelial tissue in vitro and in vivo Journal of Food Protection 65 534 539
Zárate, G., Morata de Ambrosini, V., Pérez Chaia, A. and González, S., 2002b. Some factors affecting the adherence Propionibacterium acidipropionici CRL1198 to intestinal epithelial cells. Canadian Journal of Microbiology 48: 449-457.
Some factors affecting the adherence Propionibacterium acidipropionici CRL1198 to intestinal epithelial cells Canadian Journal of Microbiology 48 449 457
Zarate, G., Pérez Chaia, A. and Oliver, G., 2003. Some characteristics of practical relevance of the b-Galactosidase from potential probiotic strains of Propionibacterium acidipropionici. Anaerobe 8: 259-267.
'Some characteristics of practical relevance of the b-Galactosidase from potential probiotic strains of Propionibacterium acidipropionici ' () 8 Anaerobe : 259 -267.
Zivkovic, M., Hidalgo-Cantabrana, C., Kojic, M., Gueimonde, M., Golic, N. and Ruas-Madiedo, P., 2015. Capability of exopolysaccharide-producing Lactobacillus paraplantarum BGCG11 and its non-producing isogenic strain NB1, to counteract the effect of enteropathogens upon the epithelial cell line HT29-MTX. Food Research International 74: 199-207.
'Capability of exopolysaccharide-producing Lactobacillus paraplantarum BGCG11 and its non-producing isogenic strain NB1, to counteract the effect of enteropathogens upon the epithelial cell line HT29-MTX ' () 74 Food Research International : 199 -207.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 362 | 220 | 24 |
| Full Text Views | 30 | 14 | 0 |
| PDF Views & Downloads | 6 | 0 | 0 |
Adhesion to the host intestinal mucosa is considered relevant for orally delivered probiotics as it prolongs their persistence in the gut and their health promoting effects. Classical propionibacteria are microorganisms of interest due to their role as dairy starters as well as for their functions as probiotics. Propionibacterium acidipropionici Q4, is a dairy strain isolated from a Swiss-type cheese made in Argentina that displays probiotic potential. In the present work we assessed the ability of this strain to adhere to the human enterocyte-like HT-29 cell line and to counteract the adhesion of two common human enteropathogens, such as Escherichia coli C3 and Salmonella Enteritidis 90/390. The results were compared with those obtained with the well-known probiotic Lactobacillus rhamnosus GG. P. acidipropionici Q4 showed a high adhesion capacity, even higher than the reference strain L. rhamnosus GG (42.3±4.4% and 36.2±2.3%, respectively), whereas adhesion of enteropathogens was significantly lower (25.2±2.2% for E. coli and 21.0±3.4% for S. Enteritidis). Propionibacteria as well as lactobacilli were able to inhibit by exclusion and competition the adherence of E. coli C3 and S. Enteritidis 90/390 whereas only L. rhamnosus GG displaced S. Enteritidis from HT-29 intestinal cells. Inhibition of pathogens by propionibacteria was not exerted by antimicrobials or coaggregation but was mainly due to exclusion by cell surface components, such as proteins and carbohydrates. The relevance of cell surface proteins (CSP) for preventing pathogens infection was confirmed by their concentration dependent effect observed for both pathogens: 100 µg/ml of CSP inhibited E. coli attachment almost as untreated propionibacteria, whereas it partially inhibited the attachment of S. Enteritidis. Results suggest that P. acidipropionici Q4 could be considered for the development of propionibacteria containing functional foods helpful in counteracting enteropathogen infection.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 362 | 220 | 24 |
| Full Text Views | 30 | 14 | 0 |
| PDF Views & Downloads | 6 | 0 | 0 |