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Shotgun Phage Display of Lactobacillus casei BL23 Against Collagen and Fibronectin

  • Munoz-Provencio, Diego (Laboratorio de Bacterias Lacticas y Probioticos, Instituto de Agroquimica y Tecnologia de Alimentos-CSIC) ;
  • Monedero, Vicente (Laboratorio de Bacterias Lacticas y Probioticos, Instituto de Agroquimica y Tecnologia de Alimentos-CSIC)
  • Received : 2010.09.09
  • Accepted : 2010.11.17
  • Published : 2011.02.28

Abstract

Lactobacilli are normal constituents of the intestinal microbiota, and some strains show the capacity to bind to extracellular matrix proteins and components of the mucosal layer, which represents an adaptation to persist in this niche. A shotgun phage-display library of Lactobacillus casei BL23 was constructed and screened for peptides able to bind to fibronectin and collagen. Clones showing binding to these proteins were isolated, which encoded overlapping fragments of a putative transcriptional regulator (LCABL_29260), a hypothetical protein exclusively found in the L. casei/rhamnosus group (LCABL_01820), and a putative phage-related endolysin (LCABL_13470). The construction of different glutathione S-transferase (GST) fusions confirmed the binding activity and demonstrated that the three identified proteins could interact with fibronectin, fibrinogen, and collagen. The results illustrate the utility of phage display for the isolation of putative adhesins in lactobacilli. However, it remains to be determined whether the primary function of these proteins actually is adhesion to mucosal surfaces.

Keywords

References

  1. Acedo-Felix, E. and G. Perez-Martinez. 2003. Significant differences between Lactobacillus casei subsp. casei ATCC 393T and a commonly used plasmid-cured derivative revealed by a polyphasic study. Int. J. Syst. Evol. Microbiol. 53: 67-75. https://doi.org/10.1099/ijs.0.02325-0
  2. Antikainen, J., V. Kuparinen, K. Lahteenmaki, and T. K. Korhonen. 2007. Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol. Med. Microbiol. 51: 526-534. https://doi.org/10.1111/j.1574-695X.2007.00330.x
  3. Beck, H. C., S. M. Madsen, J. Glenting, J. Petersen, H. Israelsen, M. R. Norrelykke, M. Antonsson, and A. M. Hansen. 2009. Proteomic analysis of cell surface-associated proteins from probiotic Lactobacillus plantarum. FEMS Microbiol. Lett. 297: 61-66. https://doi.org/10.1111/j.1574-6968.2009.01662.x
  4. Bjerketorp, J., M. Nilsson, A. Ljungh, J. I. Flock, K. Jacobsson, and L. Frykberg. 2002. A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 148: 2037-2044. https://doi.org/10.1099/00221287-148-7-2037
  5. Boekhorst, J., Q. Helmer, M. Kleerebezem, and R. J. Siezen. 2006. Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 152: 273-280. https://doi.org/10.1099/mic.0.28415-0
  6. Boekhorst, J., M. Wels, M. Kleerebezem, and R. J. Siezen. 2006. The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 152: 3175-3183. https://doi.org/10.1099/mic.0.29217-0
  7. Castaldo, C., V. Vastano, R. A. Siciliano, M. Candela, M. Vici, L. Muscariello, R. Marasco, and M. Sacco. 2009. Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb. Cell Fact. 8: 14. https://doi.org/10.1186/1475-2859-8-14
  8. de Leeuw, E., X. Li, and W. Lu. 2006. Binding characteristics of the Lactobacillus brevis ATCC 8287 surface layer to extracellular matrix proteins. FEMS Microbiol. Lett. 260: 210-215. https://doi.org/10.1111/j.1574-6968.2006.00313.x
  9. Foligne, B., S. Nutten, C. Grangette, V. Dennin, D. Goudercourt, S. Poiret, J. Dewulf, D. Brassart, A. Mercenier, and B. Pot. 2007. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 13: 236-243. https://doi.org/10.3748/wjg.v13.i2.236
  10. Hansmeier, N., T. C. Chao, J. Kalinowski, A. Puhler, and A. Tauch. 2006. Mapping and comprehensive analysis of the extracellular and cell surface proteome of the human pathogen Corynebacterium diphtheriae. Proteomics 6: 2465-2476. https://doi.org/10.1002/pmic.200500360
  11. Heilmann, C., J. Hartleib, M. S. Hussain, and G. Peters. 2005. The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect. Immun. 73: 4793-4802. https://doi.org/10.1128/IAI.73.8.4793-4802.2005
  12. Heilmann, C., S. Niemann, B. Sinha, M. Herrmann, B. E. Kehrel, and G. Peters. 2004. Staphylococcus aureus fibronectinbinding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB. J. Infect. Dis. 190: 321-329. https://doi.org/10.1086/421914
  13. Jacobsson, K. 2003. A novel family of fibrinogen-binding proteins in Streptococcus agalactiae. Vet. Microbiol. 96: 103-113. https://doi.org/10.1016/S0378-1135(03)00206-2
  14. Jacobsson, K., A. Rosander, J. Bjerketorp, and L. Frykberg. 2003. Shotgun phage display - selection for bacterial receptins or other exported proteins. Biol. Proced. Online 5: 123-135. https://doi.org/10.1251/bpo54
  15. Kleerebezem, M., P. Hols, E. Bernard, T. Rolain, M. Zhou, R. J. Siezen, and P. A. Bron. 2010. The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34: 199-230. https://doi.org/10.1111/j.1574-6976.2009.00208.x
  16. Lorca, G., M. I. Torino, G. Font de Valdez, and A. A. Ljungh. 2002. Lactobacilli express cell surface proteins which mediate binding of immobilized collagen and fibronectin. FEMS Microbiol. Lett. 206: 31-37. https://doi.org/10.1111/j.1574-6968.2002.tb10982.x
  17. Maze, A., G. Boel, M. Zuniga, A. Bourand, V. Loux, M. J. Yebra, et al. 2010. Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J. Bacteriol. 192: 2647-2648. https://doi.org/10.1128/JB.00076-10
  18. Miyoshi, Y., S. Okada, T. Uchimura, and E. Satoh. 2006. A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci. Biotechnol. Biochem. 70: 1622-1628. https://doi.org/10.1271/bbb.50688
  19. Munoz-Provencio, D., M. Llopis, M. Antolin, I. de Torres, F. Guarner, G. Perez-Martinez, and V. Monedero. 2009. Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix. Arch. Microbiol. 191: 153-161. https://doi.org/10.1007/s00203-008-0436-9
  20. Munoz-Provencio, D., G. Perez-Martinez, and V. Monedero. 2010. Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J. Appl. Microbiol. 108: 1050-1059. https://doi.org/10.1111/j.1365-2672.2009.04508.x
  21. Rochat, T., L. Bermudez-Humaran, J. J. Gratadoux, C. Fourage, C. Hoebler, G. Corthier, and P. Langella. 2007. Anti-inflammatory effects of Lactobacillus casei Bl23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb. Cell Fact. 6: 22. https://doi.org/10.1186/1475-2859-6-22
  22. Sanchez, B., P. Bressollier, and M. C. Urdaci. 2008. Exported proteins in probiotic bacteria: Adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol. Med. Microbiol. 54: 1-17. https://doi.org/10.1111/j.1574-695X.2008.00454.x
  23. Sanchez, B., J. M. Schmitter, and M. C. Urdaci. 2009. Identification of novel proteins secreted by Lactobacillus plantarum that bind to mucin and fibronectin. J. Mol. Microbiol. Biotechnol. 17: 158-162. https://doi.org/10.1159/000233579
  24. Schaumburg, J., O. Diekmann, P. Hagendorff, S. Bergmann, M. Rohde, S. Hammerschmidt, L. Jansch, J. Wehland, and U. Karst. 2004. The cell wall subproteome of Listeria monocytogenes. Proteomics 4: 2991-3006. https://doi.org/10.1002/pmic.200400928
  25. Shkoporov, A. N., E. V. Khokhlova, L. I. Kafarskaia, K. A. Pavlov, V. V. Smeianov, J. L. Steele, and B. A. Efimov. 2008. Search for protein adhesin gene in Bifidobacterium longum genome using surface phage display technology. Bull. Exp. Biol. Med. 146: 782-785. https://doi.org/10.1007/s10517-009-0423-4
  26. Styriak, I., R. Nemcova, Y. H. Chang, and A. Ljungh. 2003. Binding of extracellular matrix molecules by probiotic bacteria. Lett. Appl. Microbiol. 37: 329-333. https://doi.org/10.1046/j.1472-765X.2003.01402.x
  27. Teng, F., M. Kawalec, G. M. Weinstock, W. Hryniewicz, and B. E. Murray. 2003. An Enterococcus faecium secreted antigen, SagA, exhibits broad-spectrum binding to extracellular matrix proteins and appears essential for E. faecium growth. Infect. Immun. 71: 5033-5041. https://doi.org/10.1128/IAI.71.9.5033-5041.2003
  28. Velez, M. P., S. C. De Keersmaecker, and J. Vanderleyden. 2007. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276: 140-148. https://doi.org/10.1111/j.1574-6968.2007.00908.x
  29. von Ossowski, I., J. Reunanen, R. Satokari, S. Vesterlund, M. Kankainen, H. Huhtinen, et al. 2010. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG spaCBA and spaFED pilin subunits. Appl. Environ. Microbiol. 76: 2049-2057. https://doi.org/10.1128/AEM.01958-09
  30. Watanabe, M., H. Kinoshita, M. Nitta, R. Yukishita, Y. Kawai, K. Kimura, et al. 2010. Identification of a new adhesin-like protein from Lactobacillus mucosae ME-340 with specific affinity to the human blood group A and B antigens. J. Appl. Microbiol. 109: 927-935. https://doi.org/10.1111/j.1365-2672.2010.04719.x
  31. Watterlot, L., T. Rochat, H. Sokol, C. Cherbuy, I. Bouloufa, F. Lefevre, et al. 2010. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int. J. Food. Microbiol. 144: 35-41. https://doi.org/10.1016/j.ijfoodmicro.2010.03.037
  32. Wegmann, U., M. O'Connell-Motherway, A. Zomer, G. Buist, C. Shearman, C. Canchaya, et al. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189: 3256-3270. https://doi.org/10.1128/JB.01768-06
  33. Yevenes, A. and P. A. Frey. 2008. Cloning, expression, purification, cofactor requirements, and steady state kinetics of phosphoketolase-2 from Lactobacillus plantarum. Bioorg. Chem. 36: 121-127. https://doi.org/10.1016/j.bioorg.2008.03.002

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