The Expression of GroEL Protein Amplified from Bifidobacterium animalis subsp. lactis KLDS 2.0603 and its Role in Competitive Adhesion to Caco-2

References

• Barrangou, R., Briczinski, E.P., Traeger, L.L., Loquasto, J.R., Richards, M., Horvath, P., Coûté-Monvoisin, A.C., Leyer, G., Rendulic, S., Steele, J.L., Broadbent, J.R., Oberg, T., Dudley, E.G., Schuster, S., Romero, D.A., Roberts, R.F. (2009). Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J. Bacteriol. 191:4144–4151.
   PubMed Web of Science ®Google Scholar
• Bergonzelli, G.E., Granato, D., Pridmore, R.D., Marvin-Guy, L.F., Dominique, D., Corthésy-Theulaz, I.E. (2006). GroEL of Lactobacillus johnsonii la1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect. Immun. 74:425–434.
   PubMed Web of Science ®Google Scholar
• Bezkorovainy, A. (2001). Probiotics: determinants of survival and growth in the gut. Am. J. Clin. Nutr. 73:399S–405S.
   PubMed Web of Science ®Google Scholar
• Bianchi, M.A., Del Rio, D., Pellegrini, N., Sansebastiano, G., Neviani, E., Brighenti, F. (2004). A fluorescence-based method for the detection of adhesive properties of lactic acid bacteria to Caco-2 cells. Lett. Appl. Microbiol. 39:301–305.
   PubMed Web of Science ®Google Scholar
• Bulut, Y., Faure, E., Thomas, L., Karahashi, H., Michelsen, K.S., Equils, O., Morrison, S.G., Morrison, R.P., Arditi, M. (2002). Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J. Immunol. 168:1435–1440.
   PubMed Web of Science ®Google Scholar
• Candela, M., Bergmann, S., Vici, M., Vitali, B., Turroni, S., Eikmanns, B.J., Hammerschmidt, S., Brigidi, P. (2007). Binding of human plasminogen to Bifidobacterium. J. Bacteriol. 189:5929–5936.
   PubMed Web of Science ®Google Scholar
• Candela, M., Centanni, M., Fiori, J., Biagi, E., Turroni, E., Orrico, C., Bergmann, S., Hammerschmidt, S., Brigidi, P. (2010). DnaK from Bifidobacterium animalis subsp. lactis is a surface-exposed human plasminogen receptor upregulated in response to bile salts. Microbiology. 156: 1609–1618.
   Google Scholar
• Candela, M., Perna, F., Carnevali, P., Vitali, B., Ciati, R., Gionchetti, P., Rizzello, F., Campieri, M., Briqidi, P. (2008). Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int. J. Food Microbiol. 125:286–292.
   PubMed Web of Science ®Google Scholar
• Candela, M., Seibold, G., Vitali, B., Lachenmaier, S., Eikmanns, B.J., Brigidi, P. (2005). Real-time PCR quantification of bacterial adhesion to Caco-2 cells: competition between bifidobacteria and enteropathogens. Res. Microbiol. 156:887–895.
   PubMed Web of Science ®Google Scholar
• Candela, M., Biagi, E., Centanni, M., Turroni, S., Vici, M., Musiani, F., Vitali, B., Bergmann, S., Hammerschmidt, S., Brigidi, P. (2009). Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology. 155:3294–3303.
   PubMed Web of Science ®Google Scholar
• Chow, W.L., Lee, Y.K. (2008). Free fucose is a danger signal to human intestinal epithelial cells. Br. J. Nutr. 99:449–454.
   PubMed Web of Science ®Google Scholar
• Collado, M.C., Gueimonde, M., Hernandez, M., Sanz, Y., Salminen, S. (2005). Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J. Food Prot. 68:2672–2678.
   PubMed Web of Science ®Google Scholar
• Doyle, M.P., Schoeni, J.L. (1984). Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Appl. Environ. Microbiol. 48:855–856.
   PubMed Web of Science ®Google Scholar
• Dunn, B.E., Vakil, N.B., Schneider, B.G., Miller, M.M., Zitzer, J.B., Peutz, T., Phadnis, S.H. (1997). Localization of Helicobacter pylori urease and heat shock protein in human gastric biopsies. Infect. Immun. 65:1181–1188.
   PubMed Web of Science ®Google Scholar
• Engle, M.J., Goetz, G.S., Alpers, D.H. (1998). Caco-2 cells express a combination of colonocyte and enterocyte phenotypes. J. Cell Physiol. 174:362–369.
   PubMed Web of Science ®Google Scholar
• Estrada, A., Wilkie, D.C., Drew, M. (2001). Administration of Bifidobacterium bifidum to chicken broilers reduces the number of carcass condemnations for cellulitis at the abattoir. J. Appl. Poult. Res. 10:329–334.
   Web of Science ®Google Scholar
• Frisk, A., Ison, C.A., Lagergård, T. (1998). GroEL heat shock protein of Haemophilus ducreyi: association with cell surface and capacity to bind to eukaryotic cells. Infect. Immun. 66:1252–1257.
   PubMed Web of Science ®Google Scholar
• Garduño, R.A., Faulkner, G., Trevors, M.A., Vats, N., Hoffman, P.S. (1998). Immunolocalization of Hsp60 in Legionella pneumophila. J. Bacteriol. 180:505–513.
   PubMed Web of Science ®Google Scholar
• Genovese, F., Coïsson, J.D., Majumder, A., Pessione, A., Svensson, B., Jacobsen, S., Pessione, E. (2013). An exoproteome approach to monitor safety of a cheese-isolated Lactococcus lactis. Food Res. Int. 54:1072–1079.
   Google Scholar
• Gillis, T.P., Miller, R.A., Young, D.B., Khanolkar, S.R., Buchanan, T.M. (1985). Immunochemical characterization of a protein associated with Mycobacterium leprae cell wall. Infect. Immun. 49:371–377.
   PubMed Web of Science ®Google Scholar
• Gleinser, M., Grimm, V., Zhurina, D., Yuan, J., Riedel, C.U. (2012). Improved adhesive properties of recombinant bifidobacteria expressing the Bifidobacterium bifidum-specific lipoprotein BopA. Microb. Cell Fact. 11:80.
   PubMed Web of Science ®Google Scholar
• González-Rodríguez, I., Sánchez, B., Ruiz, L., Turroni, F., Ventura, M., Ruas-Madiedo, P., Gueimonde, M., Margolles, A. (2012). Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl. Environ. Microbiol. 78:3992–3998.
   PubMed Web of Science ®Google Scholar
• Guglielmetti, S., Tamagnini, I., Mora, D., Minuzzo, M., Scarafoni, A., Arioli, S., Hellman, J., Karp, M., Parini, C. (2008). Implication of an outer surface lipoprotein in adhesion of Bifidobacterium bifidum to Caco-2 cells. Appl. Environ. Microbiol. 74:4695–4702.
   PubMed Web of Science ®Google Scholar
• Gupta, R.S. (1995). Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15:1–11.
   PubMed Web of Science ®Google Scholar
• Guy, C.L. (1990). Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:187–223.
   Web of Science ®Google Scholar
• Hennequin, C., Porcheray, F., Waligora-Dupriet, A., Collignon, A., Barc, M., Bourlioux, P., Karjalainen, T. (2001a). GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology. 147:87–96.
   PubMed Web of Science ®Google Scholar
• Hennequin, C., Collignon, A., Karjalainen, T. (2001b). Analysis of expression of GroEL (Hsp60) of Clostridium difficile in response to stress. Microb. Pathog. 31:255–260.
   PubMed Web of Science ®Google Scholar
• Junick, J., Blaut, M. (2012). Quantification of human fecal Bifidobacterium species by use of quantitative real-time PCR analysis targeting the groEL Gene. Appl. Environ. Microbiol. 78:2613–2622.
   PubMed Web of Science ®Google Scholar
• Klijn, A., Mercenier, A., Arigoni, F. (2005). Lessons from the genomes of bifidobacteria. FEMS Microbiol. Rev. 29:491–509.
   PubMed Web of Science ®Google Scholar
• Le Blay, G., Fliss, I., Lacroix, C. (2004). Comparative detection of bacterial adhesion to Caco-2 cells with ELISA, radioactivity and plate count methods. J. Microbiol. Meth. 59:211–221.
   PubMed Web of Science ®Google Scholar
• Morita, H., He, F., Fuse, T., Ouwehand, A.C., Hashimoto, H., Hosoda, M., Mizumachi, K., Kurisaki J (2002). Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol. Immunol. 46:293–297.
   PubMed Web of Science ®Google Scholar
• Noah, C.E., Malik, M., Bublitz, D.A.C., Camenares, D., Sellati, T.J., Benach, J.L., Furie1, M.B. (2010). GroEL and lipopolysaccharide from Francisella tularensis live vaccine strain synergistically activate human macrophages. Infect. Immun. 78:1797–1806.
   PubMed Web of Science ®Google Scholar
• O’Connell Motherway, M., Zomer, A., Leahy, S.C., Reunanen, J., Bottacini, F., Claesson, M.J., O’Brien, F., Flynn, K., Casey, P.G., Munoz, J.A., Kearney, B., Houston, A.M., O’Mahony, C., Hiqqins, D.G., Shanahan, F., Palva, A., De Vos, W.M., Fitzqerald, G.F., Ventura, M., O’Toole, P.W., Van Sinderen, D. (2011). Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc. Natl. Acad. Sci. USA. 108:11217–11222.
   PubMed Web of Science ®Google Scholar
• Pérez, P.F., Minnaard, Y., Disalvo, E.A., De Antoni, G.L. (1998). Surface properties of bifidobacterial strains of human origin. Appl. Environ. Microbiol. 64:21–26.
   PubMed Web of Science ®Google Scholar
• Phadnis, S.H., Parlow, M.H., Levy, M., Ilver, D., Caulkins, C.M., Connors, J.B., Dunn, B.E. (1996). Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 64:905–912.
   PubMed Web of Science ®Google Scholar
• Rabsch, W., Andrews, H.L., Kingsley, R.A., Prager, R., Tschäpe, H., Adams, L.G., Bäumle, A.J. (2002). Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect. Immun. 70:2249–2255.
   PubMed Web of Science ®Google Scholar
• Ranford, J.C., Henderson, B. (2002). Chaperonins in disease: mechanisms, models, and treatments. Mol. Pathol. 55:209–213.
   PubMedGoogle Scholar
• Servin, A.L., Coconnier, M.H. (2003). Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract. Res. Clin. Gastroenterol. 17:741–754.
   PubMed Web of Science ®Google Scholar
• Török, Z., Goloubinoff, P., Horváth, I., Tsvetkova, N.M., Glatz, A., Balogh, G., Varvasovszki, V., Los, D.A., Vierling, E., Crowe, J.H., Vigh, L. (2001). Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc. Natl. Acad. Sci. USA. 98:3098–3103.
   PubMed Web of Science ®Google Scholar
• Vanet, A., Labigne, A. (1998). Evidence for specific secretion rather than autolysis in the release of some Helicobacter pylori proteins. Infect. Immun. 66:1023–1027.
   PubMed Web of Science ®Google Scholar
• Wang, L.Q., Meng, X.C., Zhang, B.R., Wang, Y., Shang, Y.L. (2010). Influence of cell surface properties on adhesion ability of bifidobacteria. World J. Microbiol. Biotechnol. 26:1999–2007.
   Web of Science ®Google Scholar
• Wei, X., Yan, X., Chen, X., Yang, Z., Li, H., Zou, D., He, X., Wang, S., Cui, Q., Liu, W., Zhurina, D., Wang, X., Zhao, X., Huang, L., Zeng, M., Ye, Q., Riedel, C.U., Yuan, J. (2014). Proteomic analysis of the interaction of Bifidobacterium longum NCC2705 with the intestine cells Caco-2 and identification of plasminogen receptors. J. Proteomics. 108:89–98.
   PubMed Web of Science ®Google Scholar
• Yildirim, Z., Winters, D.K., Johnson, M.G. (1999). Purification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. J. Appl. Microbiol. 86:45–54.
   PubMed Web of Science ®Google Scholar
• Zhu, D., Sun, Y., Liu, F., Li, A., Yang, L., Meng, X.C. (2016). Identification of surface-associated proteins of Bifidobacterium animalis ssp. lactis KLDS 2.0603 by enzymatic shaving. J. Dairy. Sci. 99:1–18.
   PubMed Web of Science ®Google Scholar
• Zhu, H., Lee, C., Zhang, D., Wu, W., Wang, L., Fang, X., Xu, X., Song, D., Xie, J., Ren, S., Gu, J. (2013). Surface-associated GroEL facilitates the adhesion of Escherichia coli to macrophages through lectin-like oxidized low-density lipoprotein receptor-1. Microbes. and Infect. 15:172–180.
   PubMed Web of Science ®Google Scholar