Interaction of endotoxins with toll-like receptor 4 correlates with their endotoxic potential and may explain the proinflammatory effect of Brucella spp. LPS

International Immunology

Volumn 16, Issue 10, 2004, Pages 1467-1475

  Dueñas, Ana I ^a   Orduña, Antonio ^a,b   Sánchez Crespo, Mariano ^c   García Rodríguez, Carmen ^c  

^a HOSPITAL CLÍNICO UNIVERSITARIO DE VALLADOLID   (Spain)

^b UNIVERSITY OF VALLADOLID   (Spain)

^c UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

Bacterial infection; Chemokines; Endotoxin shock; Lipopolysaccharide; Transcription factors

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BIOLOGICAL MARKER; CD14 ANTIGEN; CHEMOKINE; ENDOTOXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN KAPPA CHAIN; INTERLEUKIN 8; LIPID A; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MOLECULAR MARKER; MONOCYTE CHEMOTACTIC PROTEIN 1; TOLL LIKE RECEPTOR;

ARTICLE; BRUCELLA; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; INFLAMMATORY DISEASE; MONOCYTE; NONHUMAN; OCHROBACTRUM ANTHROPI; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; STATISTICAL SIGNIFICANCE; YERSINIA ENTEROCOLITICA;

ANIMALS; ANTIGENS, CD14; ANTIGENS, SURFACE; BRUCELLA; CARRIER PROTEINS; CELL LINE; CHEMOKINES; ENDOTOXINS; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; LIPID A; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; MEMBRANE GLYCOPROTEINS; MONOCYTES; OCHROBACTRUM; RECEPTORS, CELL SURFACE; RNA, MESSENGER; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; TRANS-ACTIVATION (GENETICS); TRANSFECTION;

EID: 5044249204     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/dxh148     Document Type: Article

References (53)

1. Corbel, M. J. and Brinley-Morgan, W. J. 1984. Genus Brucella. In Krieg, N. R. and Holt, J. G., eds, Bergey's manual of systematic bacteriology, vol 1, p. 377. Williams & Wilkins, Baltimore.
2. Salata, R. A. 2000. Brucellosis. In Bennett, C. and Goldman L., eds, Cecil Textbook of Medicine 21st edn, Saunders Company, Philadelphia, PA. p. 717.
3. Golding, B., Eller, N., Levy, L., Beining, P., Inman, J., Matthews, N., Scott, D. E. and Golding, H. 2002. Mucosal immunity in mice immunized with HIV-1 peptide conjugated to Brucella abortus. Vaccine 20:1445.
4. López-Urrutia, L., Alonso, A., Nieto, M. L., Bayón, Y., Orduña, A. and Sánchez Crespo, M. 2000. Lipopolysaccharides of Brucella abortus and Brucella melitensis induce nitric oxide synthesis in rat peritoneal macrophages. Infect. Immun. 68:1740.
5. López-Urrutia, L., Alonso, A., Bayon, Y., Nieto, M. L., Orduña, A. and Sánchez Crespo, M. 2001. Brucella lipopolysaccharides induce cyclooxygenase-2 expression in monocytic cells. Biochem. Biophys. Res. Commun. 289:372.
6. Baeuerle, P. A. 1998. IκB-NF-κB structures: at the interface of inflammation control. Cell 95:729.
7. Barnes P. J. and Karin, M. 1997. Nuclear factor-κB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336:1066.
8. Eskra, L., Mathison, A. and Splitter, G. 2003. Microarray analysis of mRNA levels from RAW264.7 macrophages infected with Brucella abortus. Infect. Immun. 71:1125.
9. Guilloteau, L. A., Dornand, J., Gross, A., Olivier, M., Cortade, F. Vern, Y. L. and Kerboeuf, D. 2003. Nramp1 is not a major determinant in the control of Brucella melitensis infection in mice. Infect. Immun. 71:621.
10. Ding, X. Z., Fernandez-Prada, C., Bhattacharjee, A. K. and Hoover, D. L. 2001. Over-expression of hsp-70 inhibits bacterial lipopolysaccharide-induced production of cytokines in human monocyte-derived macrophages. Cytokine 16:210.
11. Huang, L. Y., Aliberti, J., Leifer, C. A., Segal, D. M., Sher, A., Golenbock, D. T. and Golding, B. 2003. Heat-killed Brucella abortus induces TNF and IL-12p40 by distinct MyD88-dependent pathways: TNF, unlike IL-12p40 secretion, is Toll-like receptor 2 dependent. J. Immunol. 171:1441.
12. Zhan, Y. and Cheers, C. 1988. Control of IL-12 and IFN-γ production in response to live or dead bacteria by TNF and other factors. J. Immunol. 161:1447.
13. Zaitseva, M., King, L. R., Manischewitz, J., Dougan, M., Stevan, L., Golding, H. and Golding, B. 2001. Human peripheral blood Tcells, monocytes and macrophages secrete macrophage inflammatory proteins 1α and 1β following stimulation with heat-inactivated Brucella abortus. Infect. Immun. 69:3817.
14. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135.
15. Sabroe, I., Read, R. C., Whyte, M. K., Dockrell, D. H., Vogel, S. N. and Dower, S. K. 2003. Toll-like receptors in health and disease: complex questions remain. J. Immunol. 171:1630.
16. Takeda, K., Kaisho, T. and Akira, S. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335.
17. Underhill, D. M. and Ozinsky, A. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14:103.
18. Takeda, K. and Akira, S. 2004. TLR signaling pathways. Semin. Immunol. 16:3.
19. Rietschel, E. T., Schade, U., Jensen, M., Wollenweber, H. W., Luderitz, O. and Greisman, S. G. 1982. Bacterial endotoxins: chemical structure, biological activity and role in septicaemia. Scand. J. Infect. Dis. Suppl. 3:8.
20. Schromm, A. B., Brandenburg, K., Loppnow, H., Moran, A. P., Koch, M. H., Rietschel, E. T. and Seydel, U. 2000. Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur. J. Biochem. 267:2008.
21. Seydel, U., Oikawa, M., Fukase, K., Kusumoto, S. and Brandenburg, K. 2000. Intrinsic conformation of lipid A is responsible for agonistic and antagonistic activity. Eur. J. Biochem. 267:3032.
22. Netea, M. G., van Deuren, M., Kullberg, B. J., Cavaillon, J. M. and van der Meer, J. W. M. 2002. Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol. 23:135.
23. Velasco, J., Romero, C., Lopez-Goñi, I., Leiva, J., Diaz, R. and Moriyon, I. 1998. Evaluation of the relatedness of Brucella spp. and Ochrobactrum anthropi and description of Ochrobactrum intermedium sp. nov., a new species with a closer relationship to Brucella spp. Int. J. Syst. Bacteriol. 48:759.
24. Velasco, J., Bengoechea, J. A., Brandenburg, K., Lindner, B., Seydel, U., Gonzalez, D., Zahringer, U., Moreno, E. and Moriyon, I. 2000. Brucella abortus and its closest phylogenetic relative, Ochrobactrum spp., differ in outer membrane permeability and cationic peptide resistance. Infect. Immun. 68:3210.
25. Gill, M. V., Ly, H., Mueenuddin, M., Schoch, P. E. and Cunha, B. A. 1997. Intravenous line infection due to Ochrobactrum anthropi (CDC Group Vd) in a normal host. Heart Lung 26:335.
26. Zahringer, U., Knirel, Y. A., Lindner, B., Helbig, J. H., Sonesson, A., Marre, R. and Rietschel, E. T. 1995. The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog. Clin. Biol. Res. 392:113.
27. Lettinga, K. D., Florquin, S., Speelman, P., van Ketel, R., van der Poll, T. and Verbon, A. 2002. Toll-like receptor 4 is not involved in host defense against pulmonary Legionella pneumophila infection in a mouse model. J. Infect. Dis. 186:570.
28. Neumeister, B., Faigle, M., Sommer, M., Zahringer, U., Stelter, F., Menzel, R., Schutt, C. and Northoff, H. 1988. Low endotoxic potential of Legionella pneumophila lipopolysaccharide due to failure of interaction with the monocyte lipopolysaccharide receptor CD14. Infect. Immun. 66:4151.
29. Girard, R., Pedron, T., Uematsu, S., Balloy, V., Chignard, M., Akira, S. and Chaby, R. 2003. Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J. Cell Sci. 116:293.
30. Leong, D., Díaz, R., Milner, K., Rudbach, J. and Wilson, J. B. 1970. Some structural and biological properties of Brucella endotoxin. Infect. Immun. 1:174.
31. Moreno, E., Pitt, M. W., Jones, L. M., Schurig, G. G. and Berman, D. T. 1979. Purification and characterization of smooth and rough lipopolysaccharides from Brucella abortus. J. Bacteriol. 138:361.
32. Aragón, V., Díaz, R., Moreno, E. and Moriyón, I. 1996. Characterization of Brucella abortus and Brucella melitensis native haptens as outer membrane O-type polysaccharides independent from the smooth lipopolysaccharide. J. Bacteriol. 178:1070.
33. Muta, T. and Takeshige, K. 2001. Essential roles of CD14 and lipopolysaccharide-binding protein for activation of toll-like receptor (TLR)2 as well as TLR4. Reconstitution of TLR2 and TLR4-activation by distinguishable ligands in LPS preparations. Eur. J. Biochem. 268:4580.
34. Lee, J.-D., Kravchenko, V., Kirkland, T. N., Han, J., Mackman, N., Moriarty, A., Leturcq, D., Tobias, P. S. and Ulevitch, R. J. 1993. Glycosyl-phosphatidylinositol-anchored or integral membrane forms of CD14 mediate identical cellular responses to endotoxin. Proc. Natl Acad. Sci. USA 90:9930.
35. da Silva Correia, J., Soldau, K., Christen, U., Tobias, P. S. and Ulevitch, R. J. 2001. Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex. Transfer from CD14 to TLR4 and MD-2. J. Biol. Chem. 276:21129.
36. Takeuchi, O., Kawai, T., Muhlradt, P. F., Morr, M., Radolf, J. D., Zychlinsky, A., Takeda, K. and Akira, S. 2001. Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int. Immunol. 7:933.
37. García-Rodríguez, C. and Rao, A. 1998. Nuclear factor of activated T cells (NFAT)-dependent transactivation regulated by the coactivators p300/CREB-binding protein (CBP). J. Exp. Med. 187:2031.
38. Tamai, R., Sugawara, S., Takeuchi, O., Akira, S. and Takada, H. 2003. Synergistic effects of lipopolysaccharide and interferon-gamma in inducing interleukin-8 production in human monocytic THP-1 cells is accompanied by up-regulation of CD14, Toll-like receptor 4, MD-2 and MyD88 expression. J. Endotoxin Res. 9:145.
39. Fernández, N., Renedo, M., García-Rodríguez, C. and Sánchez Crespo, M. 2002. Activation of monocytic cells through Fcγ receptors induces the expression of macrophage-inflammatory protein (MIP)-1α, MIP-1β and RANTES. J. Immunol. 169:33221.
40. Read, M. A., Cordle, S. R., Veach, R. A., Carlisle, C. D. and Hawiger, J. 1994. Cell-free pool of CD14 mediates activation of transcription factor NF-κB by lipopolysaccharide in human endothelial cells. Proc. Natl Acad. Sci. USA 90:9887.
41. Schromm, A. B., Lien, E., Henneke, P. et al. 2001. Molecular genetic analysis of an endotoxin nonresponder mutant cell line: a point mutation in a conserved region of MD-2 abolishes endotoxin-induced signaling. J. Exp. Med. 194:79.
42. Nagai, Y., Akashi, S., Nagafuku, M. et al. 2002. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3:667.
43. Goldstein, J., Hoffman, T., Frasch, C. et al. 1992. Lipopolysaccharide (LPS) from Brucella abortus is less toxic than that from Escherichia coli, suggesting the possible use of B. abortus or LPS from B. abortus as a carrier in vaccines. Infect. Immun. 60:1385.
44. Finkelman, F. D., Katona, I. M., Mosmann, T. R. and Coffman, R. L. 1998. IFN-γ regulates the isotypes of Ig secreted during in vivo humoral immune responses. J. Immunol. 140:1022.
45. Golding, B., Eller, N., Levy, L., Beining, P., Inman, J., Matthews, N., Scott, D. E. and Golding, H. 2002. Mucosal immunity in mice immunized with HIV-1 peptide conjugated to Brucella abortus. Vaccine 20:1445.
46. Perera, V. Y., Winter, A. J. and Ganem, B. 1984. Evidence for covalent bonding of native hapten-protein complexes to smooth and rough lipopolysaccharide from Brucella abortus. FEMS Microbiol. Lett. 21:263.
47. Campos, M. A., Rosinha, G. M., Almeida, I. C. et al. 2004. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 72:176.
48. Ruckdeschel, K., Harb, S., Roggenkamp, A., Hornef, M., Zumbihl, R., Kohler, S., Heesemann, J. and Rouot, B. 1998. Yersinia enterocolitica impairs activation of transcription factor NF-κB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor-α production. J. Exp. Med. 187:1069.
49. Bengoechea, J. A., Brandenburg, K., Arraiza, M. D., Seydel, U., Skurnik, M., and Moriyón, I. 2003. Pathogenic Yersinia enterocolitica strains increase the outer membrane permeability in response to environmental stimuli by modulating lipopolysaccharide fluidity and lipid A structure. Infect. Immun. 71:2014.
50. Hirschfeld, M., Weis, J. J., Toshchakov, V., Salkowski, C. A., Cody, M. J., Ward, D. C., Qureshi, N., Michalek, S. M. and Vogel, S. N. 2001. Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect. Immun. 69:1477.
51. Ogawa, T., Asai, Y., Hashimoto, M., Takeuchi, O., Kurita, T., Yoshikai, Y., Miyake, K. and Akira, S. 2002. Cell activation by Porphyromonas gingivalis lipid A molecule through Toll-like receptor 4- and myeloid differentiation factor 88-dependent signaling pathway. Int. Immunol. 14:1325.
52. Hashimoto, M., Asai, Y., Tamai, R., Jinno, T., Umatani, K. and Ogawa, T. 2003. Chemical structure and immunobiological activity of lipid A from Prevotella intermedia ATCC 25611 lipopolysaccharide. FEBS Lett. 543:98.
53. Picard, C., Puel, A., Bonnet, M. et al. 2003. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299:2076.