The Adhesion of Lactobacillus salivarius REN to a Human Intestinal Epithelial Cell Line Requires S-layer Proteins

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Wang, Ran ^a   Jiang, Lun ^a   Zhang, Ming ^b   Zhao, Liang ^a   Hao, Yanling ^a   Guo, Huiyuan ^a   Sang, Yue ^c   Zhang, Hao ^a   Ren, Fazheng ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b BEIJING TECHNOLOGY AND BUSINESS UNIVERSITY   (China)

^c Research Center of Animal Product   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; MEMBRANE PROTEIN; S-LAYER PROTEINS;

BACTERIUM ADHERENCE; CHEMISTRY; EPITHELIUM CELL; HT-29 CELL LINE; HUMAN; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; LACTOBACILLUS SALIVARIUS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; EPITHELIAL CELLS; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; LACTOBACILLUS SALIVARIUS; MEMBRANE GLYCOPROTEINS;

EID: 85014955543     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44029     Document Type: Article

References (61)

1. Hynonen, U. & Palva, A. Lactobacillus surface layer proteins: structure, function and applications. Appl Microbiol Biot 97, 5225-5243 (2013).
2. Zhang, W. et al. Adhesive ability means inhibition activities for lactobacillus against pathogens and S-layer protein plays an important role in adhesion. Anaerobe 22, 97-103 (2013).
3. Servin, A. L. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS microbiol rev 28, 405-440 (2004).
4. Johnson, B., Selle, K., O'Flaherty, S., Goh, Y. J. & Klaenhammer, T. Identification of extracellular surface-layer associated proteins in Lactobacillus acidophilus NCFM. Microbiol-Sgm 159, 2269-2282 (2013).
5. Ventura, M., Jankovic, I., Walker, D. C., Pridmore, R. D. & Zink, R. Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl environ microbiol 68, 6172-6181 (2002).
6. Morata de Ambrosini, V. I., Gonzalez, S. N. & Oliver, G. Study of adhesion of Lactobacillus casei CRL 431 to ileal intestinal cells of mice. J food prot 62, 1430-1434 (1999).
7. Gusils, C., Cuozzo, S., Sesma, F. & Gonzalez, S. Examination of adhesive determinants in three species of Lactobacillus isolated from chicken. Can J microbiol 48, 34-42 (2002).
8. Greene, J. D. & Klaenhammer, T. R. Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl environ microbiol 60, 4487-4494 (1994).
9. Granato, D. et al. Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl environ microbiol 65, 1071-1077 (1999).
10. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. J. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol R 72, 728-764 (2008).
11. Reunanen, J., von Ossowski, I., Hendrickx, A. P. A., Palva, A. & de Vos, W. M. Characterization of the spaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl environ microbiol 78, 2337-2344 (2012).
12. von Ossowski, I. et al. Functional characterization of a mucus-specific LPXTG surface adhesin from probiotic Lactobacillus rhamnosus GG. Appl environ microbiol 77, 4465-4472 (2011).
13. Adlerberth, I. et al. A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29. Appl environ microbiol 62, 2244-2251 (1996).
14. Mukai, T., Arihara, K. & Itoh, H. Lectin-like activity of Lactobacillus acidophilus strain JCM 1026. Fems Microbiol Lett 98, 71-74 (1992).
15. Yamamoto, K. et al. Binding specificity of Lactobacillus to glycolipids. Biochem Bioph Res Co 228 (1996).
16. Garrote, G. L. et al. Lactobacilli isolated from kefir grains: evidence of the presence of S-layer proteins. J Dairy Res 71, 222-230 (2004).
17. Frece, J. et al. Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98, 285-292 (2005).
18. Chen, X. Y. et al. 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 (2007).
19. Jakava-Vijanen, M. & Palva, A. Isolation of surface (S) layer protein carrying Lactobacillus species from porcine intestine and faeces and characterization of their adhesion properties to different host tissues. Vet Microbiol 124, 264-273 (2007).
20. Sillanpaa, J. et al. Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 182, 6440-6450 (2000).
21. Sun, Z. L. et al. Characterization of a S-layer protein from Lactobacillus crispatus K313 and the domains responsible for binding to cell wall and adherence to collagen. Appl Microbiol Biot 97 (2013).
22. Konstantinov, S. R. et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. P Natl Acad Sci USA 105, 19474-19479 (2008).
23. Hymes, J. P., Johnson, B. R., Barrangou, R. & Klaenhammer, T. R. Functional analysis of an S-layer-associated fibronectin-binding protein in Lactobacillus acidophilus NCFM. Appl environ microbiol 82, 2676-2685 (2016).
24. de Leeuw, E., Li, X. Q. & Lu, W. Y. Binding characteristics of the Lactobacillus brevis ATCC 8287 surface layer to extracellular matrix proteins. Fems Microbiol Lett 260, 210-215 (2006).
25. Buck, B. L., Altermann, E., Svingerud, T. & Klaenhammer, T. R. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl environ microbiol 71, 8344-8351 (2005).
26. Hynonen, U., Westerlund-Wikstrom, B., Palva, A. & Korhonen, T. K. Identification by flagellum display of an epithelial cell-and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis. J Bacteriol 184, 3360-3367 (2002).
27. Antikainen, J., Anton, L., Sillanpaa, J. & Korhonen, T. K. 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 (2002).
28. Avall-Jaaskelainen, S. et al. Identification and characterization of domains responsible for self-assembly and cell wall binding of the surface layer protein of Lactobacillus brevis ATCC 8287. Bmc Microbiol 8 (2008).
29. Sun, E., R. F., Liu, S. et al. Complete genome sequence of Lactobacillus salivarius Ren, a probiotic strain with anti-tumor activity. J Biotechnol 210, 57-58 (2015).
30. Wang, F., Jiang, L., Liu, A. P., Guo, X. H. & Ren, F. Z. Analysis of antigenotoxicity of Lactobacillus salivarius by high performance liquid chromatography. Chinese J Anal Chem 36, 740-744 (2008).
31. Zhang, M. et al. Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide. Cancer Prev Res 6, 686-694 (2013).
32. Zhu, J. et al. Lactobacillus salivarius Ren prevent the early colorectal carcinogenesis in 1, 2-dimethylhydrazine-induced rat model. J Appl Microbiol 117, 208-216 (2014).
33. Zhang, M., Qiao, X. W., Zhao, L., Jiang, L. & Ren, F. Z. Lactobacillus salivarius REN counteracted unfavorable 4-nitroquinoline-1-oxide-induced changes in colonic microflora of rats. J Microbiol 49, 877-883 (2011).
34. Lortal, S., H. J. V., Gruber, K. et al. S-layer of Lactobacillus helveticus ATCC 12046: Isolation, chemical characterization and reformation after extraction with lithium chloride. J Gen Microbiol 138, 611-618 (1992).
35. Garau, G., Lemaire, D., Vernet, T., Dideberg, O. & Di Guilmi, A. M. Crystal structure of phosphorylcholine esterase domain of the virulence factor choline-binding protein E from Streptococcus pneumoniae-New structural features among the metallo-betalactamase superfamily. J Biol Chem 280, 28591-28600 (2005).
36. Fernandez-Tornero, C., Lopez, R., Garcia, E., Gimenez-Gallego, G. & Romero, A. A novel solenoid fold in the cell wall anchoring domain of the pneumococcal virulence factor LytA. Nat Struct Biol 8 (2001).
37. Smit, E., Oling, F., Demel, R., Martinez, B. & Pouwels, P. H. The S-layer protein of Lactobacillus acidophilus ATCC 4356, Identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J Mol Biol 305, 245-257 (2001).
38. Smit, E. & Pouwels, P. H. One repeat of the cell wall binding domain is sufficient for anchoring the Lactobacillus acidophilus surface layer protein. J Bacteriol 184, 4617-4619 (2002).
39. Bochtler, M., Odintsov, S. G., Marcyjaniak, M. & Sabala, I. Similar active sites in lysostaphins and D-Ala-D-Ala metallopeptidases. Prot sci 13, 854-861 (2004).
40. Holm, L. & Sander, C. Dali: a network tool for protein structure comparison. Trends biochem sci 20, 478-480 (1995).
41. Sabala, I. et al. Crystal structure of the antimicrobial peptidase lysostaphin from Staphylococcus simulans. FEBS J 281, 4112-4122 (2014).
42. Bamford, C. V., Francescutti, T., Cameron, C. E., Jenkinson, H. F. & Dymock, D. Characterization of a novel family of fibronectinbinding proteins with M23 peptidase domains from Treponema denticola. Mol Oral Microbiol 25, 369-383 (2010).
43. Moll, A. et al. Cell separation in Vibrio cholerae is mediated by a single amidase whose action is modulated by two nonredundant activators. J Bacteriol 196, 3937-3948 (2014).
44. Bonis, M., Ecobichon, C., Guadagnini, S., Prevost, M. C. & Boneca, I. G. A M23B family metallopeptidase of Helicobacter pylori required for cell shape, pole formation and virulence. Mol Microbiol 78, 809-819 (2010).
45. Heilmann, C., Hussain, M., Peters, G. & Gotz, F. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24, 1013-1024 (1997).
46. Hirschhausen, N., Schlesier, T., Peters, G. & Heilmann, C. Characterization of the modular design of the autolysin/adhesin Aaa from Staphylococcus aureus. Plos One 7 (2012).
47. Sleytr, U. B. & Beveridge, T. J. Bacterial S-layers. Trends Microbiol 7, 253-260 (1999).
48. Mann, B. et al. Multifunctional role of choline binding protein G in pneumococcal pathogenesis. Infect Immun 74, 821-829 (2006).
49. Pancholi, V. Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58, 902-920 (2001).
50. Bergmann, S., Schoenen, H. & Hammerschmidt, S. The interaction between bacterial enolase and plasminogen promotes adherence of Streptococcus pneumoniae to epithelial and endothelial cells. Int J Med Microbiol 303, 452-462 (2013).
51. Redlitz, A., Fowler, B. J., Plow, E. F. & Miles, L. A. The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 227, 407-415 (1995).
52. Rios-Steiner, J. L., Schenone, M., Mochalkin, I., Tulinsky, A. & Castellino, F. J. Structure and binding determinants of the recombinant kringle-2 domain of human plasminogen to an internal peptide from a group A Streptococcal surface protein. J Mol Biol 308, 705-719 (2001).
53. Mathews, I. I., VanderhoffHanaver, P., Castellino, F. J. & Tulinsky, A. Crystal structures of the recombinant kringle 1 domain of human plasminogen in complexes with the ligands epsilon-aminocaproic acid and trans-4-(aminomethyl)cyclohexane-1-carboxylic acid. Biochemistry-Us 35, 2567-2576 (1996).
54. Marti, D. N., Schaller, J. & Llinas, M. Solution structure and dynamics of the plasminogen kringle 2-AMCHA complex: 3(1)-helix in homologous domains. Biochemistry-Us 38, 15741-15755 (1999).
55. Rejante, M. R. & Llinas, M. Solution structure of the epsilon-aminohexanoic acid complex of human plasminogen kringle-1. Eur J Biochem 221, 939-949 (1994).
56. Chauviere, G., Coconnier, M. H., Kerneis, S., Fourniat, J. & Servin, A. L. Adhesion of human Lactobacillus acidophilus strain Lb to human enterocyte-like Caco-2 cells. J Gen Microbiol 138, 1689-1696 (1992).
57. van Pijkeren, J. P. et al. Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl environ microbiol 72, 4143-4153 (2006).
58. Russell, W. M. & Klaenhammer, T. R. Efficient system for directed integration into the Lactobacillus acidophilus and Lactobacillus gasseri chromosomes via homologous recombination. Appl environ microbiol 67, 4361-4364 (2001).
59. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D 67, 235-242 (2011).
60. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr D 60, 2126-2132 (2004).
61. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D 67, 355-367 (2011).