Intracellular Recognition of Lipopolysaccharide by Toll-like Receptor 4 in Intestinal Epithelial Cells

Journal of Experimental Medicine

Volumn 198, Issue 8, 2003, Pages 1225-1235

  Hornef, Mathias W ^a,c   Normark, Birgitta Henriques ^a   Vandewalle, Alain ^b   Normark, Staffan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSERM   (France)

^c SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

Endotoxin; Golgi apparatus; Innate immunity; Mucosal immunology

Indexed keywords

ADAPTOR PROTEIN; CHAPERONE; CLATHRIN; GLYCOPROTEIN GP 96; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN SERINE THREONINE KINASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GOLGI COMPLEX; INTERNALIZATION; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; MOLECULAR RECOGNITION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL LINE; ENZYME ACTIVATION; EPITHELIAL CELLS; GOLGI APPARATUS; HSP70 HEAT-SHOCK PROTEINS; INTESTINES; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; NF-KAPPA B; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 0142157000     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20022194     Document Type: Article

References (50)

1. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135-145.
2. Poltorak, A., X. He, I. Smirnova, M.Y. Liu, C.V. 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. 282:2085-2088.
3. Underhill, D.M., A. Ozinsky, A.M. Hajjar, A. Stevens, C.B. Wilson, M. Bassetti, and A. Aderem. 1999. The toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature. 401:811-815.
4. Akashi, S., R. Shimazu, H. Ogata, Y. Nagai, K. Takeda, M. Kimoto, and K. Miyake. 2000. Cutting edge: cell surface expression and lipopolysaccharide signaling via the toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J. Immunol. 164:3471-3475.
5. Hacker, H., H. Mischak, T. Miethke, S. Liptay, R. Schmid, T. Sparwasser, K. Heeg, G.B. Lipford, and H. Wagner. 1998. CpG-DNA specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 17:6230-6240.
6. Gewirtz, A.T., T.A. Navas, S. Lyons, P.J. Godowski, and J.L. Madara. 2001. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167:1882-1885.
7. Gewirtz, A.T., P.O. Simon, Jr., C.K. Schmitt, L.J. Taylor, C.H. Hagedorn, A.D. O'Brien, A.S. Neish, and L.J. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107:99-109.
8. Abreu, M.T., P. Vora, E. Faure, L.S. Thomas, E.T. Arnold, and M. Arditi. 2001. Decreased expression of toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccaride. J. Immunol. 167:1609-1616.
9. Smith, P.D., L.E. Smythies, M. Mosteller-Barnum, D.A. Sibley, M.W. Russell, M. Merger, M.T. Sellers, J.M. Orenstein, T. Shimada, M.F. Graham, et al. 2001. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS and IgA-mediated activities. J. Immunol. 167:2651-2656.
10. cl2) that maintain a crypt phenotype. Am. J. Physiol. 270: C1666-C1674.
11. Hornef, M.W., T. Frisan, A. Vandewalle, S. Normark, and A. Richter-Dahlfors. 2002. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J. Exp. Med. 195:559-570.
12. Thieblemont, N., and S.D. Wright. 1999. Transport of bacterial lipopolysaccaride to the Golgi apparatus. J. Exp. Med. 190:523-534.
13. Poltorak, A., P. Ricciardi-Castagnoli, S. Citterio, and B. Beutler. 2000. Physical contact between lipopolysaccharide and toll-like receptor 4 revealed by genetic complementation. Proc. Natl. Acad. Sci. USA. 97:2163-2167.
14. Ahmad-Nejad, P., H. Häcker, M. Rutz, S. Bauer, R.M. Vabulas, and H. Wagner. 2002. Bacterial CpG-DNA and lipopolysaccharide activate toll-like receptors at distinct cellular compartments. Eur. J. Immunol. 32:1958-1968.
15. Zheng, H., J. Dai, D. Stoilova, and Z. Li. 2001. Cell surface targeting of heat shock protein gp96 induces dendritic cell maturation and antitumor immunity. J. Immunol. 167:6731-6735.
16. Blaeke, A., Y. Delneste, N. Herbault, P. Jeannin, J.-Y. Bonnefoy, A. Beck, and J.-P. Aubry. 2002. Measurement of nuclear factor-kappa B translocation on lipopolysaccharide-activated human dendritic cells by confocal microscopy and flow cytometry. Cytometry. 48:71-79.
17. Mundy, D.I., T. Machleidt, Y.S. Ying, R.G. Anderson, and G.S. Bloom. 2002. Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115:4327-4339.
18. Ding, A.H., E. Sanchez, M. Tancinco, and C.F. Nathan. 1992. Interactions of bacterial lipopolysaccharide with microtubule proteins. J. Immunol. 148:2853-2858.
19. Detmers, P.A., N. Thieblemont, T. Vasselon, R. Pironkova, D.S. Miller, and S.D. Wright. 1996. Potential role of membrane internalization and vesicle fusion in adhesion of neutrophils in response to lipopolysaccharide and TNF-α. J. Immunol. 157:5589-5596.
20. Sandvig, K., A. Sundan, and S. Olsnes. 1984. Evidence that diphteria toxin and modeccin enter the cytosol from different vesicular compartments. J. Cell Biol. 98:963-970.
21. Triantafilou, M., K. Miyake, D.T. Golenbock, and K. Triantafilou. 2002. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115:2603-2611.
22. Nichols, B.J., A.K. Kenworthy, R.S. Polishchuk, R. Lodge, T.H. Roberts, K. Hirschberg, R.D. Phair, and J. Lippincott-Schwarz. 2001. Rapid recycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:529-541.
23. Ward, T.H., R.S. Polishchuk, S. Caplan, K. Hirschberg, and J. Lippinkott-Schwartz. 2001. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155:557-570.
24. Randow, F., and B. Seed. 2001. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat. Cell Biol. 3:891-896.
25. Chavany, C., E. Mimnaugh, P. Miller, R. Bitton, P. Nguyen, J. Trepel, L. Whitesell, R. Schnur, J.D. Moyer, and L. Neckers. 1996. p185(erbB2) binds to GKP94 in vivo-dissociation of the p185(erbB2)/GKP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185(erbB2). J. Biol. Chem. 271:4974-4977.
26. Latz, E., A. Visintin, E. Lien, K. Fitzgerald, B.G. Monks, E. Kurt-Jones, D.T. Golenbock, and T. Espevik. 2002. LPS rapidly traffics to and from the Golgi apparatus with the TLR4/MD-2/CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277:47834-47843.
27. Poussin, C., M. Foti, J.-L. Carpentier, and J. Pugin. 1998. CD14-dependent endotoxin internalization via a macropinocytotic pathway. J. Biol. Chem. 273:20285-20291.
28. Hampton, R.Y., D.T. Golenbock, M. Penman, M. Krieger, and C.R. Raetz. 1991. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature. 352:343-344.
29. Kitchens, R.L., R.J. Ulevitch, and R.S. Munford. 1992. Lipopolysaccharide (LPS) partial structures inhibit responses to LPS in a human macrophage cell line without inhibiting LPS uptake by a CD14-mediated pathway. J. Exp. Med. 176:485-494.
30. Gegner, J., R.J. Ulevitch, and P.S. Tobias. 1995. Lipopolysaccharide (LPS) signal transduction and clearance. J. Biol. Chem. 270:5320-5325.
31. Thieblemont, N., and S.D. Wright. 1999. Transport of bacterial lipopolysaccharide to the Golgi apparatus. J. Exp. Med. 190:523-534.
32. Cowan, D.B., S. Noria, C. Stmann, L.M. Garcia, D.N. Poutias, P.J. del Nido, and F.X. McGowan, Jr. 2001. Lipopolysaccharide internalization activates endotoxin-dependent signal transduction in cardiomyocytes. Circ. Res. 88:491-498.
33. Beatty, W.L., S. Meresse, 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. 145:689-698.
34. 2+ are required for endotoxin-stimulated TNF-α release by Kupffer cells. Am. J. Physiol. 271:G920-G928.
35. Thieblemont, N., R. Thieringer, and S.D. Wright. 1998. Innate immune recognition of bacterial lipopolysaccharide: dependence on interaction with membrane lipids and endocytic movement. Immunity. 8:771-777.
36. Thieblemont, N., and S.D. Wright. 1997. Mice genetically hyporesponsive to lipopolysaccharide (LPS) exhibit a defect in endocytic uptake of LPS and ceramide. J. Exp. Med. 185:2095-2100.
37. Kitchens, R.L., and R.S. Munford. 1998. CD14-dependent internalization of bacterial lipopolysaccharide (LPS) is strongly influenced by LPS aggregation but not by cellular responses to LPS. J. Immunol. 160:1920-1928.
38. Vasselon, T., E. Hailman, R. Thieringer, and P.A. Detmers. 1999. Internalization of monomeric lipopolysaccharide occurs after transfer out of cell surface CD14. J. Exp. Med. 190:509-521.
39. Luchi, M., and R.S. Munford. 1993. Binding, internalization, and deacylation of bacterial lipopolysaccharide by human neutrophils. J. Immunol. 151:959-969.
40. Rozelle, A.L., L.M. Machesky, M. Yamamoto, M.H. Driessens, K.H. Insall, M.G. Roth, K. Luby-Phelps, G. Marriott, A. Hall, and H.L. Yin. 2000. Phosphatidylinositol 4,5-bis-phosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10:311-320.
41. Kitchens, R.L., P. Wang, and R.S. Munford. 1998. Bacterial lipopolysaccharide can enter monocytes via two CD-14-dependent pathways. J. Immunol. 161:5534-5545.
42. Visintin, A., A. Mazzoni, J.A. Spitzer, and D.M. Segal. 2001. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to toll-like receptor 4. Proc. Natl. Acad. Sci. USA. 98:12156-12161.
43. Triantafilou, K., M. Triantafilou, and R.A. Dederick. 2001. A CD14-indendent LPS receptor cluster. Nat. Immunol. 2:338-345.
44. Nicchitta, C.V. 1998. Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96. Curr. Opin. Immunol. 10:103-109.
45. Srivastava, P.K. 1991. Protein tumor antigens. Curr. Opin. Immunol. 3:654-658.
46. Berwin, B., M.F. Rosser, K.G. Brinker, and C.V. Nicchitta. 2002. Transfer of GRP94(Go96)-associated peptides onto endosomal MHC class I molecules. Traffic. 3:358-366.
47. Vabulas, R.M., S. Braedel, N. Hilf, H. Singh-Jasaju, S. Herter, P. Ahmad-Nejad, C.J. Kirschning, C. da Costa, H.G. Rammensee, H. Wagner, et al. 2000. The ER-resident heat shock protein Gp96 activates dendritic cells via the TLR2/4 pathway. J. Biol. Chem. 277:20847-20853.
48. Miesenböck, G., and J.E. Rothman. 1995. The capacity to retrieve escaped ER proteins extends to the trans-most cisternae of the golgi stack. J. Biol. Chem. 129:309-319.
49. Da Silva Correia, J., and R.J. Ulevitch. 2001. MD-2 and TLR4 N-linked glycosylations are important for a functional lipopolysaccharide receptor. J. Biol. Chem. 227:1845-1854.
50. Mullen, G.E., M.N. Kennedy, A. Visintin, A. Mazzoni, C.A. Leifer, D.R. Davies, and D.M. Segal. 2003. The role of disulfide bonds in the assembly and function of MD-2. Proc. Natl. Acad. Sci. USA. 100:3919-3924.