Lactobacillus S-layer protein inhibition of Salmonella-induced reorganization of the cytoskeleton and activation of MAPK signalling pathways in Caco-2 cells

Microbiology

Volumn 157, Issue 9, 2011, Pages 2639-2646

  Li, Pengcheng ^a   Yu, Qinghua ^a   Ye, Xiaolan ^a   Wang, Zhisheng ^a   Yang, Qian ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL PROTEIN; F ACTIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; SURFACE LAYER PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; CELL STRAIN CACO 2; CYTOKINE RELEASE; CYTOSKELETON; DIARRHEA; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HOST CELL; HUMAN; HUMAN CELL; LACTOBACILLUS; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTIN CYTOSKELETON; ACTINS; BACTERIAL ADHESION; CACO-2 CELLS; ENZYME ACTIVATION; HUMANS; INTERLEUKIN-8; LACTOBACILLUS; MAP KINASE SIGNALING SYSTEM; MEMBRANE GLYCOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; SALMONELLA;

LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 80052389705     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.049148-0     Document Type: Article

References (42)

1. Antikainen, J., Anton, L., Sillanpää, J. & 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.
2. Åvall-Jääskeläinen, S. & Palva, A. (2005). Lactobacillus surface layers and their applications. FEMS Microbiol Rev 29, 511-529.
3. Banan, A., Zhang, Y., Losurdo, J. & Keshavarzian, A. (2000). Carbonylation and disassembly of the F-actin cytoskeleton in oxidant induced barrier dysfunction and its prevention by epidermal growth factor and transforming growth factor a in a human colonic cell line. Gut 46, 830-837.
4. Banan, A., Keshavarzian, A., Zhang, L., Shaikh, M., Forsyth, C. B., Tang, Y. & Fields, J. Z. (2007). NF-kB activation as a key mechanism in ethanol-induced disruption of the F-actin cytoskeleton and monolayer barrier integrity in intestinal epithelium. Alcohol 41, 447-460.
5. Bhavsar, A. P., Guttman, J. A. & Finlay, B. B. (2007). Manipulation of host-cell pathways by bacterial pathogens. Nature 449, 827-834.
6. Boot, H. J., Kolen, C. P., van Noort, J. M. & Pouwels, P. H. (1993). S-layer protein of Lactobacillus acidophilus ATCC 4356: purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene. J Bacteriol 175, 6089-6096.
7. Cario, E., Rosenberg, I. M., Brandwein, S. L., Beck, P. L., Reinecker, H. C. & Podolsky, D. K. (2000). Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Tolllike receptors. J Immunol 164, 966-972.
8. Chen, Z., Gibson, T. B., Robinson, F., Silvestro, L., Pearson, G., Xu, B., Wright, A., Vanderbilt, C. & Cobb, M. H. (2001). MAP kinases. Chem Rev 101, 2449-2476.
9. Chen, X., Xu, J., Shuai, J., Chen, J., Zhang, Z. & 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.
10. Coconnier, M. H., Liévin, V., Lorrot, M. & Servin, A. L. (2000). Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar Typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl Environ Microbiol 66, 1152-1157.
11. Eckmann, L., Kagnoff, M. F. & Fierer, J. (1993). Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61, 4569-4574.
12. Galán, J. E. (1996). Molecular and cellular bases of Salmonella entry into host cells. Curr Top Microbiol Immunol 209, 43-60.
13. Galán, J. E. & Bliska, J. B. (1996). Cross-talk between bacterial pathogens and their host cells. Annu Rev Cell Dev Biol 12, 221-255.
14. Golowczyc, M. A., Mobili, P., Garrote, G. L., Abraham, A. G. & De Antoni, G. L. (2007). Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. Int J Food Microbiol 118, 264-273.
15. Gordon, M. A., Graham, S. M., Walsh, A. L., Wilson, L., Phiri, A., Molyneux, E., Zijlstra, E. E., Heyderman, R. S., Hart, C. A. & Molyneux, M. E. (2008). Epidemics of invasive Salmonella enterica serovar Enteritidis and S. enterica serovar Typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46, 963-969.
16. Helms, M., Ethelberg, S., Mølbak, K. & DT104 Study Group (2005). International Salmonella Typhimurium DT104 infections, 1992-2001. Emerg Infect Dis 11, 859-867.
17. Hobbie, S., Chen, L. M., Davis, R. J. & Galán, J. E. (1997). Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 159, 5550-5559.
18. Huang, F. C., Werne, A., Li, Q., Galyov, E. E., Walker, W. A. & Cherayil, B. J. (2004). Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar Typhimurium infection. Infect Immun 72, 5052-5062.
19. Ishii, K. J., Koyama, S., Nakagawa, A., Coban, C. & Akira, S. (2008). Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3, 352-363.
20. Jakava-Viljanen, M. & Palva, A. (2007). 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.
21. Johnson-Henry, K. C., Hagen, K. E., Gordonpour, M., Tompkins, T. A. & 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.
22. Jones, R. M., Wu, H., Wentworth, C., Luo, L., Collier-Hyams, L. & Neish, A. S. (2008). Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 3, 233-244.
23. Kucharzik, T. & Williams, I. R. (2002). Neutrophil migration across the intestinal epithelial barrier-summary of in vitro data and description of a new transgenic mouse model with doxycyclineinducible interleukin-8 expression in intestinal epithelial cells. Pathobiology 70, 143-149.
24. Kyriakis, J. M. & Avruch, J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81, 807-869.
25. Li, P., Ye, X., Wang, Z., Yu, Q. & Yang, Q. (2010). [Effects of S-layer proteins from Lactobacillus against Salmonella typhimurium adhesion and invasion on Caco-2 cells]. Wei Sheng Wu Xue Bao 50, 1226-1231 (in Chinese).
26. Li, P., Yin, Y., Yu, Q. & Yang, Q. (2011). Lactobacillus acidophilus S-layer protein-mediated inhibition of Salmonella-induced apoptosis in Caco-2 cells. Biochem Biophys Res Commun 409, 142-147.
27. Ly, K. T. & Casanova, J. E. (2007). Mechanisms of Salmonella entry into host cells. Cell Microbiol 9, 2103-2111.
28. Mumy, K. L. & McCormick, B. A. (2009). The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol 9, 697-701.
29. Mynott, T. L., Crossett, B. & Prathalingam, S. R. (2002). Proteolytic inhibition of Salmonella enterica serovar Typhimurium-induced activation of the mitogen-activated protein kinases ERK and JNK in cultured human intestinal cells. Infect Immun 70, 86-95.
30. Patel, J. C. & Galán, J. E. (2005). Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr Opin Microbiol 8, 10-15.
31. Patel, J. C., Rossanese, O. W. & Galán, J. E. (2005). The functional interface between Salmonella and its host cell: opportunities for therapeutic intervention. Trends Pharmacol Sci 26, 564-570.
32. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. & Medzhitov, R. (2004). Recognition of commensal microflora by Tolllike receptors is required for intestinal homeostasis. Cell 118, 229-241.
33. Roux, P. P. & Blenis, J. (2004). ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68, 320-344.
34. Rugbjerg, H., Wingstrand, A., Hald, T., Andersen, J. S., Lo Fo Wong, D. M. & Korsgaard, H. (2004). Estimating the number of undetected multiresistant Salmonella Typhimurium DT104 infected pig herds in Denmark. Prev Vet Med 65, 147-171.
35. Sánchez, B., Urdaci, M. C. & Margolles, A. (2010). Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology 156, 3232-3242.
36. Tafazoli, F., Magnusson, K. E. & Zheng, L. (2003). Disruption of epithelial barrier integrity by Salmonella enterica serovar Typhimurium requires geranylgeranylated proteins. Infect Immun 71, 872-881.
37. Thomas, C. M. & Versalovic, J. (2010). Probiotics-host communication: modulation of signaling pathways in the intestine. Gut Microbes 1, 148-163.
38. Vadillo-Rodríguez, V., Busscher, H. J., van der Mei, H. C., de Vries, J. & Norde, W. (2005). Role of lactobacillus cell surface hydrophobicity as probed by AFM in adhesion to surfaces at low and high ionic strength. Colloids Surf B Biointerfaces 41, 33-41.
39. Veiga, E., Guttman, J. A., Bonazzi, M., Boucrot, E., Toledo-Arana, A., Lin, A. E., Enninga, J., Pizarro-Cerdá, J., Finlay, B. B. & other authors (2007). Invasive and adherent bacterial pathogens co-opt host clathrin for infection. Cell Host Microbe 2, 340-351.
40. Vizoso Pinto, M. G., Rodriguez Gómez, M., Seifert, S., Watzl, B., Holzapfel, W. H. & Franz, C. M. (2009). Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 133, 86-93.
41. Wang, B., Wei, H., Yuan, J., Li, Q., Li, Y., Li, N. & Li, J. (2008). Identification of a surface protein from Lactobacillus reuteri JCM1081 that adheres to porcine gastric mucin and human enterocyte-like HT-29 cells. Curr Microbiol 57, 33-38.
42. Weston, C. R. & Davis, R. J. (2007). The JNK signal transduction pathway. Curr Opin Cell Biol 19, 142-149.