Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing toll-like receptors

Journal of Immunology

Volumn 164, Issue 2, 2000, Pages 966-972

  Cario, Elke ^a   Rosenberg, Ian M ^a   Brandwein, Steven L ^a   Beck, Paul L ^a   Reinecker, Hans Christian ^a   Podolsky, Daniel K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CELL RECEPTOR; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 0034650930     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.2.966     Document Type: Article

References (53)

1. Yang, S. K., L. Eckmann, A. Panja, and M. F. Kagnoff. 1997. Differential and regulated expression of CXC, CC and C-chemokines by human colon epithelial cells. Gastroenterology 113:1214.
2. Jung, H. C., L. Eckmann, S. K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95:55.
3. DeWitt, R. C., and K. A. Kudsk. 1999. The gut's role in metabolism, mucosal barrier function and gut immunology. Infect. Dis. Clin. North Am. 13:465.
4. Beatty, W. L., and P. J. Sansonetti. 1997. Role of lipopolysaccharide in signaling to subepithelial polymorphonuclear leukocytes. Infect. Immun. 65:4395.
5. Beatty, W. L., S. Méresse, P. Gounon, J. Davoust, J. Mounier, P. J. Sansonetti, and J. P. Gorvel. 1999. Trafficking of shigella lipopolysaccharide in polarized intestinal epithelial cells. J. Cell Biol. 145:689.
6. Morrison, D. C., and R. J. Ulevitch. 1978. The effects of bacterial endotoxins on host mediation systems. Am. J. Pathol. 93:525.
7. Wright, S. D. 1995. CD14 and innate recognition of bacteria. J. Immunol. 155:6.
8. Ulevitch, R. J., and P. S. Tobias. 1999. Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11:19.
9. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431.
10. Schutt, C., T. Schilling, U. Grunwald, W. Schoenfeld, and C. Kruger. 1992. Endotoxin-neutralizing capacity of soluble CD14. Res. Immunol. 143:71.
11. Schumann, R. R., D. Pfeil, N. Lamping, C. Kirschning, G. Scherzinger, P. Schlag, L. Karawajew, and F. Herrmann. 1996. Lipopolysaccharide induces rapid tyrosine phosphorylation of the mitogen-activated protein kinases erk-1 and p38 in cultured human vascular endothelial cells requiring the presence of soluble CD14. Blood 87:2805.
12. Pugin, J., C. C. Schürer-Maly, D. Leturcq, A. Moriarty, R. J. Ulevitch, and P. S. Tobias. 1993. Lipopolysaccharide activation of human endothelial and epithelial' cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA 90:2744.
13. Matsushita, K., R. Motani, T. Sakuta, S. Nagaoka, T. Matsuyama, K. Abeyama, I. Maruyama, H. Takada, and M. Torii. 1999. Lipopolysaccharide enhances the production of vascular endothelial growth factor by human pulp cells in culture. Infect. Immun. 67:1633.
14. Ingalls, R. R., B. G. Monks, R. Savedra, W. J. Christ, R. L. Delude, A. E. Medvedev, T. Espevik, and D. T. Golenbock. 1998. CD11/CD18 and CD14 share a common lipid A signaling pathway. J. Immunol. 161:5413.
15. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394.
16. Rock, F. L., G. Hardiman, J. C. Timans, R. A. Kastelein, and J. F. Bazan. 1998. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. USA 95:588.
17. Wright, S. D. 1999. Toll, a new piece in the puzzle of innate immunity. J. Exp. Med. 189:605.
18. Kopp, E. B., and R. Medzhitov. 1999. The Toll-receptor family and control of innate immunity. Curr. Opin. Immunol. 11:13.
19. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085.
20. Heine, H., C. J. Kirschning, E. Lien, B. G. Monks, M. Rothe, and D. T. Golenbock. 1999. Cells that carry a null allele for Toll-like receptor 2 are capable of responding to endotoxin. J. Immunol. 162:6971.
21. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162:3749.
22. Yang, R. B., M. R. Mark, A. Gray, A. Huang, M. H. Xie, M. Zhang, A. Goddard, W. I. Wood, A. L. Gurney, and P. J. Godowski. 1998. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signaling. Nature 395:284.
23. Qureshi, S. T., L. Larivière, G. Leveque, S. Clermont, K. J. Moore, P. Gros, and D. Malo. 1999. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med. 189:615.
24. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689.
25. Reimann, T., D. Büscher, R. A. Hipskind, S. Krautwald, M. L. Lohmann-Matthes, and M. Baccarini. 1994. Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. J. Immunol 153:5740.
26. Hambleton, J., S. L. Weinstein, L. Lem, and A. L. DeFranco. 1996. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA 93:2774.
27. Baldassare, J. J., Y. Bi, and C. J. Bellone. 1999. The role of p38 mitogen-activated protein kinase in IL-1β transcription. J. Immunol. 162:5367.
28. Hall, A. J., H. L. Vos, and R. M. Bertina. 1999. Lipopolysaccharide induction of tissue factor in THP-1 cells involves Jun protein phosphorylation and nuclear factor κB nuclear translocation. J. Biol. Chem. 274:376.
29. 2terminal kinase mitogen-activated protein kinases by bacterial peptidoglycan. J. Infect. Dis. 174: 777.
30. Kirschning, C. J., H. Wesche, T. M. Ayres, and M. Rothe. Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. 1998. J. Exp. Med. 188:2091.
31. Zhang, F. X., C. J. Kirschning, R. Mancinelli, X. P. Xu, Y. Jin, E. Faure, A. Mantovani, M. Rothe, M. Muzio, and M. Arditi. 1999. Bacterial lipopolysaccharide activates nuclear factor-κB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol Chem. 274:7611.
32. Muzio, M., G. Natoli, S. Saccani, M. Levrero, and A. Mantovani. 1998. The human toll signaling pathway: divergence of nuclear factor κB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med. 187:2097.
33. Mayer, L., D. Eisenhardt, P. Salomon, W. Bauer, R. Plous, and L. Piccini. 1991. Expression of class II molecules on intestinal epithelial cells in humans: differences between normal and inflammatory bowel disease. Gastroenterology 100:3.
34. Eckmann, L., H. C. Jung, C. Schürer-Maly, A. Panja, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1993. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology 105: 1689.
35. Lévy, P., H. Robin, M. Kornprobst, J. Capeau, and G. Cherqui. 1998. Enterocytic differentiation of the human Caco-2 cell line correlates with alterations in integrin signaling. J. Cell. Physiol. 177:618.
36. Setoguchi, M., N. Nasu, S. Yoshida, Y. Higuchi, S. Akizuki, and S. Yamamoto. 1989. Mouse and human CD14 (myeloid cell-specific leucine-rich glycoprotein) primary structure deduced from cDNA clones. Biochim. Biophys. Acta 1008:213.
37. Lee, J. D., K. Kato, P. S. Tobias, T. N. Kirkland, and R. J. Ulevitch. 1992. Translection of CD14 into 70Z/3 cells dramatically enhances the sensitivity to complexes of lipopolysaccharide (LPS) and LPS binding protein. J. Exp. Med. 175:1697.
38. Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17:6419.
39. Göke, M., and D. K. Podolsky. 1996. Regulation of the mucosal epithelial barrier. Baillière's Clin. Gastroenterol. 10:393.
40. Fearns, C., V. V. Kravchenko, R. J. Ulevitch, and D. J. Loskutoff. 1995. Murine CD14 gene expression in vivo: extramyeloid synthesis and regulation by lipopolysaccharide. J. Exp. Med. 181:857.
41. Meijssen, M. A., S. L. Brandwein, H. C. Reinecker, A. K. Bhan, and D. K. Podolsky. 1998. Alteration of gene expression by intestinal epithelial cells precedes colitis in interleukin-2-deficient mice. Am. J. Physiol. 274:G472.
42. Perdomo, J. J., P. Gounon, and P. J. Sansonetti. 1994. Polymorphonuclear leukocyte transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J. Clin. Invest. 93:631.
43. Bazil, V., and J. L. Strominger. 1991. Shedding as a mechanism of down-modulation of CD14 on stimulated human monocytes. J. Immunol. 147:1567.
44. Haziot, A., E. Ferrero, F. Kontgen, N. Hijiyen, S. Yamamoto, J. Silver, C. L. Stewart, and S. M. Goyert. 1996. Resistance to endotoxin shock and reduced dissemination of Gram-negative bacteria in CD14-deficient mice. Immunity 4:407.
45. Rogler, G., K. Brand, D. Vogl, S. Page, R. Hofmeister, T. Andus, R. Knuechel, P.A. Baeuerle, J. Schölmerich, and V. Gross. 1998. Nuclear factor κB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115:357.
46. Hausmann, M., D. Vogl, W. Falk, J. Schölmerich, T. Andus, and G. Rogler. 1999. Toll-like Receptor mRNA is absent in macrophages from normal mucosa but expressed in inflamed mucosa. Gastroenterology 116:A271 (G1516).
47. Nick, J. A., N. J. Avdi, P. Gerwins, G. L. Johnson, and G. S. Worthen. 1996. Activation of a p38 mitogen-activated protein kinase in human neutrophils by lipopolysaccharide. J. Immunol. 156.4867.
48. Epstein, F. H. 1997. Nuclear factor-κB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336:1066.
49. Awane, M., P. G. Andres, D. J. Li, and H. C. Reinecker. 1999. NF-κB-inducing kinase is a common mediator of IL-17-, TNFα-, and IL-1-β-induced chemokine promoter activation in intestinal epithelial cells. J. Immunol. 162:5337.
50. O'Connell, M. A., B. L. Bennett, F. Mercurio, A. M. Manning, and N. Mackman. 1998. Role of IKK1 and IKK2 in lipopolysaccharide signaling in human monocytic cells. J. Biol. Chem. 273:30410.
51. Savkovic, S. D., A. Koutsouris, and G. Hecht. 1997. Activation of NF-κB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am. J. Physiol. 273:C1160.
52. Naumann, M., S. Weßler, C. Bartsch, B. Wieland, and T. F. Meyer. 1997. Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor κB and activator protein 1 and the induction of inflammatory cytokines. J. Exp. Med. 186:247.
53. Held, T. K., X. Weihua, L. Yuan, D. V. Kalvakolanu, and A. S. Cross. 1999. Gamma interferon augments macrophage activation by lipopolysaccharide by two distinct mechanisms, at the signal transduction level and via an autocrine mechanism involving tumor necrosis factor α and interleukin-1. Infect. Immun. 67:206.