Cell surface-associated aggregation-promoting factor from Lactobacillus gasseriSBT2055 facilitates host colonization and competitive exclusion of Campylobacter jejuni

Molecular Microbiology

Volumn 98, Issue 4, 2015, Pages 712-726

  Nishiyama, Keita ^a   Nakazato, Akiko ^a   Ueno, Shintaro ^a   Seto, Yasuyuki ^b   Kakuda, Tsutomu ^a   Takai, Shinji ^a   Yamamoto, Yuji ^a   Mukai, Takao ^a  

^a KITASATO UNIVERSITY   (Japan)

^b SNOW BRAND MILK PRODUCTS CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION PROMOTING FACTOR 1; AGGREGATION PROMOTING FACTOR 2; BACTERIAL PROTEIN; FIBRONECTIN; PROBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APF1 GENE; APF2 GENE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SELF AGGREGATION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BINDING AFFINITY; BINDING COMPETITION; CAMPYLOBACTER ENTERITIS; CAMPYLOBACTER JEJUNI; COMPETITIVE EXCLUSION; CONTROLLED STUDY; DRUG ACTIVITY; GENE INACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LACTOBACILLUS GASSERI; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SPECIES INVASION; ANIMAL; ANTIBIOSIS; CAMPYLOBACTER INFECTIONS; CHEMISTRY; CHICKEN; EPITHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTIBIOSIS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CHICKENS; EPITHELIAL CELLS; HUMANS; INTESTINES; LACTOBACILLUS; PROBIOTICS;

EID: 84947025032     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13153     Document Type: Article

References (73)

1. Alemka, A., Clyne, M., Shanahan, F., Tompkins, T., Corcionivoschi, N., and Bourke, B. (2010) Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect Immun 78: 2812-2822.
2. Allos, B.M. (2001) Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32: 1201-1206.
3. Antikainen, J., Anton, L., Sillanpää, J., and Korhonen, T.K. (2002) Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly. Mol Microbiol 46: 381-394.
4. Bergonzelli, G.E., Granato, D., Pridmore, R.D., Marvin-Guy, L.F., Donnicola, D., and 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.
5. Biswas, I., Gruss, A., Ehrlich, S.D., and Maguin, E. (1993) High-efficiency gene inactivation and replacement system for gram-positive bacteria. J Bacteriol 175: 3628-3635.
6. Blikslager, A.T., Moeser, A.J., Gookin, J.L., Jones, S.L., and Odle, J. (2007) Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87: 545-564.
7. Boehm, M., Krause-Gruszczynska, M., Rohde, M., Tegtmeyer, N., Takahashi, S., Oyarzabal, O.A., and Backert, S. (2011) Major host factors involved in epithelial cell invasion of Campylobacter jejuni: role of fibronectin, integrin beta1, FAK, Tiam-1, and DOCK180 in activating Rho GTPase Rac1. Front Cell Infect Microbiol 1: 17.
8. Bonnans, C., Chou, J., and Werb, Z. (2014) Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 15: 786-801.
9. Boonaert, C.J., and Rouxhet, P.G. (2000) Surface of lactic acid bacteria: relationships between chemical composition and physicochemical properties. Appl Environ Microbiol 66: 2548-2554.
10. Breitwieser, A., Gruber, K., and Sleytr, U.B. (1992) Evidence for an S-layer protein pool in the peptidoglycan of Bacillus stearothermophilus. J Bacteriol 174: 8008-8015.
11. Callaway, T.R., Edrington, T.S., Anderson, R.C., Harvey, R.B., Genovese, K.J., Kennedy, C.N., etal. (2008) Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim Health Res Rev 9: 217-225.
12. Cesena, C., Morelli, L., Alander, M., Siljander, T., Tuomola, E., Salminen, S., etal. (2001) Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J Dairy Sci 84: 1001-1010.
13. Chagnot, C., Listrat, A., Astruc, T., and Desvaux, M. (2012) Bacterial adhesion to animal tissues: protein determinants for recognition of extracellular matrix components. Cell Microbiol 14: 1687-1696.
14. 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. Int J Food Microbiol 115: 307-312.
15. Collado, M.C., Meriluoto, J., and Salminen, S. (2007a) In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus. Food Res Int 40: 629-636.
16. Collado, M.C., Meriluoto, J., and Salminen, S. (2007b) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226: 1065-1073.
17. Dasti, J.I., Tareen, A.M., Lugert, R., Zautner, A.E., and Gross, U. (2010) Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 300: 205-211.
18. Day, C.J., Semchenko, E.A., and Korolik, V. (2012) Glycoconjugates play a key role in Campylobacter jejuni Infection: interactions between host and pathogen. Front Cell Infect Microbiol 2: 9.
19. Eucker, T.P., and Konkel, M.E. (2012) The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling. Cell Microbiol 14: 226-238.
20. European Food Safety Authority (EFSA) (2014) Committed to ensuring that Europe's food is safe. [WWW document]. URL http://www.efsa.europa.eu
21. Frese, S.A., Mackenzie, D.A., Peterson, D.A., Schmaltz, R., Fangman, T., Zhou, Y., etal. (2013) Molecular characterization of host-specific biofilm formation in a vertebrate gut symbiont. PLoS Genet 9: e1004057.
22. Friedman, C.R., Hoekstra, R.M., Samuel, M., Marcus, R., Bender, J., Shiferaw, B., etal. (2004) Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin Infect Dis 38: S285-S296.
23. Fujiwara, S., Seto, Y., Kimura, A., and Hashiba, H. (2001) Establishment of orally-administered Lactobacillus gasseri SBT2055SR in the gastrointestinal tract of humans and its influence on intestinal microflora and metabolism. J Appl Microbiol 90: 343-352.
24. Fuller, R. (1989) Probiotics in man and animals. J Appl Bacteriol 66: 365-378.
25. Goh, Y.J., and Klaenhammer, T.R. (2010) Functional roles of aggregation-promoting-like factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 76: 5005-5012.
26. Hamad, E.M., Sato, M., Uzu, K., Yoshida, T., Higashi, S., Kawakami, H., etal. (2009) Milk fermented by Lactobacillus gasseri SBT2055 influences adipocyte size via inhibition of dietary fat absorption in Zucker rats. Br J Nutr 101: 716-724.
27. Harper, S., and Speicher, D.W. (2011) Purification of proteins fused to glutathione S-transferase. Methods Mol Biol 681: 259-280.
28. Hevia, A., Martínez, N., Ladero, V., Alvarez, M.A., Margolles, A., and Sánchez, B. (2013) An extracellular Serine/Threonine-rich protein from Lactobacillus plantarum NCIMB 8826 is a novel aggregation-promoting factor with affinity to mucin. Appl Environ Microbiol 79: 6059-6066.
29. Holo, H., and Nes, I.F. (1989) High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 55: 3119-3123.
30. Jankovic, I., Ventura, M., Meylan, V., Rouvet, M., Elli, M., and Zink, R. (2003) Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. J Bacteriol 185: 3288-3296.
31. 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. Cell Microbiol 9: 356-367.
32. Kadooka, Y., Sato, M., Imaizumi, K., Ogawa, A., Ikuyama, K., Akai, Y., etal. (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64: 636-643.
33. Kainulainen, V., Loimaranta, V., Pekkala, A., Edelman, S., Antikainen, J., Kylväjä, R., etal. (2012) Glutamine synthetase and glucose-6-phosphate isomerase are adhesive moonlighting proteins of Lactobacillus crispatus released by epithelial cathelicidin LL-37. J Bacteriol 194: 2509-2519.
34. Kmet, V., Callegari, M.L., Bottazzi, V., and Morelli, L. (1995) Aggregation-promoting factor in pig intestinal Lactobacillus strains. Lett Appl Microbiol 21: 351-353.
35. Konkel, M.E., Larson, C.L., and Flanagan, R.C. (2010) Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J Bacteriol 192: 68-76.
36. Krause-Gruszczynska, M., Boehm, M., Rohde, M., Tegtmeyer, N., Takahashi, S., Buday, L., etal. (2011) The signaling pathway of Campylobacter jejuni-induced Cdc42 activation: role of fibronectin, integrin beta1, tyrosine kinases and guanine exchange factor Vav2. Cell Commun Signal 9: 32.
37. Kuusela, P., Moran, A.P., Vartio, T., and Kosunen, T.U. (1989) Interaction of Campylobacter jejuni with extracellular matrix components. Biochim Biophys Acta 993: 297-300.
38. de Leeuw, E., Li, X., and Lu, W. (2006) Binding characteristics of the Lactobacillus brevis ATCC 8287 surface layer to extracellular matrix proteins. FEMS Microbiol Lett 260: 210-215.
39. McGuckin, M.A., Lindén, S.K., Sutton, P., and Florin, T.H. (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265-278.
40. Marcotte, H., Ferrari, S., Cesena, C., Hammarström, L., Morelli, L., Pozzi, G., and Oggioni, M.R. (2004) The aggregation-promoting factor of Lactobacillus crispatus M247 and its genetic locus. J Appl Microbiol 97: 749-756.
41. Matsui, H., Takahashi, T., Øverby, A., Murayama, S.Y., Yoshida, H., Yamamoto, Y., etal. (2015) Mouse models for assessing the protective efficacy of Lactobacillus gasseri SBT2055 against Helicobacter suis infection associated with the development of gastric mucosa-associated lymphoid tissue lymphoma. Helicobacter 20: 291-298.
42. Miljkovic, M., Strahinic, I., Tolinacki, M., Zivkovic, M., Kojic, S., Golic, N., and Kojic, M. (2015) AggLb is the largest cell-aggregation factor from Lactobacillus paracasei subsp. paracasei BGNJ1-64, functions in collagen adhesion, and pathogen exclusion in vitro. PLoS ONE 10: e0126387.
43. Miyoshi, M., Ogawa, A., Higurashi, S., and Kadooka, Y. (2014) Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice. Eur J Nutr 53: 599-606.
44. Monteville, M.R., Yoon, J.E., and Konkel, M.E. (2003) Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149: 153-165.
45. Morishita, T.Y., Aye, P.P., Harr, B.S., Cobb, C.W., and Clifford, J.R. (1997) Evaluation of an avian-specific probiotic to reduce the colonization and shedding of Campylobacter jejuni in broilers. Avian Dis 41: 850-855.
46. Nakayama, Y., Moriya, T., Sakai, F., Ikeda, N., Shiozaki, T., Hosoya, T., etal. (2014) Oral administration of Lactobacillus gasseri SBT2055 is effective for preventing influenza in mice. Sci Rep 4: 4638.
47. Neal-McKinney, J.M., Lu, X., Duong, T., Larson, C.L., Call, D.R., Shah, D.H., and Konkel, M.E. (2012) Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS ONE 7: e43928.
48. Nishiyama, K., Seto, Y., Yoshioka, K., Kakuda, T., Takai, S., Yamamoto, Y., and Mukai, T. (2014a) Lactobacillus gasseri SBT2055 reduces infection by and colonization of Campylobacter jejuni. PLoS ONE 9: e108827.
49. Nishiyama, K., Nakamata, K., Ueno, S., Terao, A., Aryantini, N.P., Sujaya, I.N., etal. (2014b) Adhesion properties of Lactobacillus rhamnosus mucus-binding factor to mucin and extracellular matrix proteins. Biosci Biotechnol Biochem 29: 1-9.
50. Nurmi, E., and Rantala, M. (1973) New aspects of Salmonella infection in broiler production. Nature 241: 210-211.
51. O'Cróinín, T., and Backert, S. (2012) Host epithelial cell invasion by Campylobacter jejuni: trigger or zipper mechanism? Front Cell Infect Microbiol 2: 25.
52. Preidis, G.A., Hill, C., Guerrant, R.L., Ramakrishna, B.S., Tannock, G.W., and Versalovic, J. (2011) Probiotics, enteric and diarrheal diseases, and global health. Gastroenterology 140: 8-14.
53. Reniero, R., Cocconcelli, P., Bottazzi, V., and Morelli, L. (1992) High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J Gen Microbiol 138: 763-768.
54. Robinson, C.J., Bohannan, B.J.M., and Young, V.B. (2010) From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74: 453-476.
55. Sato, M., Uzu, K., Yoshida, T., Hamad, E.M., Kawakami, H., Matsuyama, H., etal. (2008) Effects of milk fermented by Lactobacillus gasseri SBT2055 on adipocyte size in rats. Br J Nutr 99: 1013-1017.
56. Schachtsiek, M., Hammes, W.P., and Hertel, C. (2004) Characterization of Lactobacillus coryniformis DSM 20001T surface protein Cpf mediating coaggregation with and aggregation among pathogens. Appl Environ Microbiol 70: 7078-7085.
57. Schär-Zammaretti, P., Dillmann, M.-L., D'Amico, N., Affolter, M., and Ubbink, J. (2005) Influence of fermentation medium composition on physicochemical surface properties of Lactobacillus acidophilus. Appl Environ Microbiol 71: 8165-8173.
58. Schröder, W., and Moser, I. (2006) Primary structure analysis and adhesion studies on the major outer membrane protein of Campylobacter jejuni. FEMS Microbiol Lett 150: 141-147.
59. Schwarz-Linek, U., Höök, M., and Potts, J.R. (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 52: 631-641.
60. Schwarz-Linek, U., Höök, M., and Potts, J.R. (2006) Fibronectin-binding proteins of gram-positive cocci. Microbes Infect 8: 2291-2298.
61. Simon, D., and Chopin, A. (1988) Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie 70: 559-566.
62. Spurbeck, R.R., and Arvidson, C.G. (2010) Lactobacillus jensenii surface-associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect Immun 78: 3103-3111.
63. Stern, N.J., Svetoch, E.A., Eruslanov, B.V., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P., etal. (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 50: 3111-3116.
64. Svetoch, E.A., Eruslanov, B.V., Levchuk, V.P., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P., etal. (2011) Isolation of Lactobacillus salivarius 1077 (NRRL B-50053) and characterization of its bacteriocin, including the antimicrobial activity spectrum. Appl Environ Microbiol 77: 2749-2754.
65. Thorns, C.J. (2000) Bacterial food-borne zoonoses. Rev Sci Tech 19: 226-239.
66. Turner, M.S., Hafner, L.M., Walsh, T., and Giffard, P.M. (2004) Identification and characterization of the novel LysM domain-containing surface protein Sep from Lactobacillus fermentum BR11 and its use as a peptide fusion partner in Lactobacillus and Lactococcus. Appl Environ Microbiol 70: 3673-3680.
67. Ventura, M., Jankovic, I., Walker, D.C., Pridmore, R.D., and Zink, R. (2002) Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl Environ Microbiol 68: 6172-6181.
68. Wei, M.-Q., Rush, C.M., Norman, J.M., Hafner, L.M., Epping, R.J., and Timms, P. (1995) An improved method for the transformation of Lactobacillus strains using electroporation. J Microbiol Methods 21: 97-109.
69. Willis, W.L., and Reid, L. (2005) Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni presence. Poult Sci 87: 606-611.
70. Wine, E., Gareau, M.G., Johnson-Henry, K., and Sherman, P.M. (2009) Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. FEMS Microbiol Lett 300: 146-152.
71. Young, K.T., Davis, L.M., and Dirita, V.J. (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5: 665-679.
72. Zhang, G., Ma, L., and Doyle, M.P. (2007) Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and Salmonella. J Food Prot 70: 867-873.
73. Ziprin, R.L., Young, C.R., Stanker, L.H., Hume, M.E., and Konkel, M.E. (1999) The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein. Avian Dis 43: 586-589.