Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism

Nature Immunology

Volumn 2, Issue 4, 2001, Pages 346-352

  Werts, Catherine ^a,b   Tapping, Richard I ^a   Mathison, John C ^a   Chuang, Tsung Hsien ^a   Kravchenko, Vladimir ^a   Saint Girons, Isabelle ^b   Haake, David A ^c   Godowski, Paul J ^d   Hayashi, Fumitaka ^e   Ozinsky, Adrian ^e   Underhill, David M ^e   Kirschning, Carsten J ^f   Wagner, Hermann ^f   Aderem, Alan ^e   Tobias, Peter S ^a   Ulevitch, Richard J ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b INSTITUT PASTEUR   (France)

^c VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^d GENENTECH INC   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; LIPOPOLYSACCHARIDE; LIPOPROTEIN; MEMBRANE PROTEIN; TLR2 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL; ARTICLE; CELL LINE; CHO CELL; DRUG EFFECT; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; LEPTOSPIRA INTERROGANS; LEPTOSPIROSIS; MACROPHAGE ACTIVATION; METABOLISM; MOUSE; MOUSE MUTANT; PATHOGENICITY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD14; CELL LINE; CHO CELLS; CRICETINAE; DROSOPHILA PROTEINS; HUMANS; LEPTOSPIRA INTERROGANS; LEPTOSPIROSIS; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MACROPHAGE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 5944225473     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/86354     Document Type: Article

References (57)

1. Pereira, M. M. et al. A clonal subpopulation of Leptospira interrogans sensu stricto is the major cause of leptospirosis outbreaks in Brazil. J. Clin. Microbiol. 38, 450-452 (2000).
2. Barnett, J. K. et al. Expression and distribution of leptospiral outer membrane components during renal infection of hamsters. Infect. Immun. 67, 853-861 (1999).
3. Faine, S. Adler, B., Bolin, C. & Perolat, P. Leptospira and Leptospirosis 2nd edn (Monash University Press, Melbourne, Australia, 1999).
4. Chu, K. M., Rathinam, R., Namperumalsamy, P. & Dean, D. Identification of Leptospira species in the pathogenesis of uveitis and determination of clinical ocular characteristics in South India. J. Infect. Dis. 177, 1314-1321 (1998).
5. Adler, B. & Faine, S. The antibodies involved in the human immune response to leptospiral infection. J. Med. Microbiol. 11, 387-400 (1978).
6. de Souza, L. & Koury, M. C. Isolation and biological activities of endotoxin from Leptospira interrogans. Can. J. Microbiol. 38, 284-289 (1992).
7. Mitchison, M. et al. Identification and characterization of the dTDP-rhamnose biosynthesis and transfer genes of the lipopolysaccharide-related rfb locus in Leptospira interrogans serovar copenhageni. J. Bacteriol. 179, 1262-1267 (1997).
8. Kalambaheti, T., Bulach, D. M., Rajakumar, K. & Adler, B. Genetic organization of the lipopolysaccharide O-antigen biosynthetic locus of leptospira borgpetersenii serovar hardjobovis. Micro. Pathogen. 27, 105-117 (1999).
9. Bulach, D. M., Kalambaheti, T., da la Pena-Moctezuma, A. & Adler, B. Functional analysis of genes in the rfb locus of Leptospira borgpetersenii serovar hardjo subtype hardjobovis. Infect. Immun. 68, 3793-3798 (2000).
10. Bulach, D. M., Kalambaheti, T., de la Pena-Moctezuma, A. & Adler, B. Lipopolysaccharide biosynthesis in Leptospira. J. Mol. Microbiol. Biotechnol. 2, 375-380 (2000).
11. Haake, D. A. et al. Characterization of leptospiral outer membrane lipoprotein LipL36: downregulation associated with late log-phase growth and mammalian infection. Infect. Immun. 66, 1579-1587 (1998).
12. Shang, E. S., Summers, T. A. & Haake, D. A. Molecular cloning and sequence analysis of the gene encoding LipL41, a surface-exposed lipoprotein of pathogenic Leptospira species. Infect. Immun. 64, 2322-2330 (1996).
13. Haake, D. A. et al. The leptospiral major outer membrane protein LipL32 is a lipoprotein expressed during mammalian infection. Infect. Immun. 68, 2276-2285 (2000).
14. Ulevitch, R. J. & Tobias, P. S. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13, 437-457 (1995).
15. Ulevitch, R. J. Toll gates for pathogen selection. Nature 401, 755-756 (1999).
16. Ulevitch, R. J. Endotoxin opens the Toll gates of innate immunity. Nature Med. 5, 144-145 (1999).
17. Poltorak, A. et al. Defective LPS signaling in C3H/HeJ and C57B/10ScCr mice:mutations in Tlr4 gene. Science 282, 2085-2088 (1998).
18. Beutler, B. Tlr4: central component of the sole mammalian LPS sensor. Curr. Opin. Immunol. 12, 20-26 (2000).
19. Aderem, A. & Ulevitch, R. J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787 (2000).
20. Hirschfeld, M., Ma, Y., Weis, J. H., Vogel, S. N. & Weis, J. J. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J. Immunol. 165, 618-622 (2000).
21. Tapping, R. I. Akashi, S., Miyake, K. Godowski, P. & Tobias, P. S. Toll-like receptor 4, but not Toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella LPSs. J. Immunol. 165, 5780-5787 (2000).
22. Leturcq, D. J. et al. Antibodies against CD14 protect primates from endotoxin-induced shock. J. Clin. Invest. 98, 1533-1533 (1996).
23. Heine, H. et al. Cutting edge: cells that carry a null allele for toll-like receptor 2 are capable of responding to endotoxin. J. Immunol. 162, 6971-6975 (1999).
24. Underhill, D. M. et al. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401, 811-615 (1999).
25. Kirschning, C. J., Wesche, H., Merrill, A. T. & Rothe, M. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 188, 2091-2097 (1998).
26. Lien, E. et al. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274, 33419-33425 (1999).
27. Sellati, T. J. et al. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J. Immunol. 160, 5455-5464 (1998).
28. Brightbill, H. D. et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732-736 (1999).
29. Akashi, S. et al. 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 (2000).
30. Radolf, J. D. et al. Lipoproteins of Borrelia burgdorferi and Treponema pallidum activate cachectin/tumor necrosis factor synthesis. Analysis using a CAT reporter construct. J. Immunol. 147, 1968-1974 (1991).
31. Manthey, C. L. & Vogel, S. L. Elimination of trace endotoxin protein from rough chemotype LPS. J. Endotoxin Res. 1, 84-91 (1994).
32. Isogai, E., Kitagawa, H., Isogai, H., Kurebayashi, Y. & Ito, N. Phagocytosis as a defense mechanism against infection with leptospira. Zentralbt Bakteriol Mikrobiol Hyg [A] 261, 65-74 (1986).
33. Vinetz, J. M., Glass, G. E., Flexner, C. E., Mueller, P. & Kaslow, D. C. Sporadic urban leptospirosis. Ann. Intern. Med. 125, 794-798 (1996).
34. Arean, V. M. The pathologic anatomy and pathogenesis of fatal human leptospirosis (Weils disease). Am. J. Pathol. 40, 393-423 (1962).
35. Vinh, T., Adler, B. & Faine, S. Ultrastructure and chemical composition of lipopolysaccharide extracted from Leptospira interrogans serovar Copenhageni. J. Gen. Microbiol. 132, 103-109 (1986).
36. Vinh, T. U., Shi, M. H., Adler, B. & Faine, S. Characterization and toxonomic significance of lipopolysaccharides of Leptospira interrogans serovar hardjo. J. Gen. Microbiol. 135, 2663-2673 (1989).
37. Norgard, M. V. et al. Activation of human monocytic cells by Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides proceeds via a pathway distinct from that of lipopolysaccharide but involves the transcriptional activator NF-kappa B. Infect. Immun. 64, 3845-3852 (1996).
38. Beutler, B. Endotoxin, toll-like receptor 4, and the afferent limb of innate immunity. Curr. Opin. Microbiol. 3, 23-28 (2000).
39. Hoshino, K. et al. Cutting edge:Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162, 3749-3752 (1999).
40. Takeuchi, O. et al. Differential roles of Toll-like receptor (TLR) 2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11, 443-451 (1999).
41. Lien, E. et al. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J. Clin. Invest. 105, 497-504 (2000).
42. Poltorak, A., Ricciardi-Castagnoli, P., Citterio, S. & Beutler, B. Physical contact between lipopolysaccharide and toll-like receptor 4 revealed by genetic complementation. Proc. Natl Acad. Sci. USA 97, 2163-2167 (2000).
43. Baril, C. & Saint Girons I. Sizing of the Leptospira genome by pulsed-field agarose gel electrophoresis. FEMS Microbiol. Lett. 71, 100 (1990).
44. Zuerner, R. L. Knudtson, W., Bolin, C. A. & Trueba, B. Characterization of outer membrane and secreted proteins of leptospira interrogans serovar pomona. Microb. Pathog. 10, 311-322 (1991).
45. Fraser, C. M. et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586 (1997).
46. Ellinghausen, H. C. & McCulloch, W. G. Nutrition of leptospira pomona and growth of 13 other serotypes: fractionation of oleic albumin complex and a medium of bovine albumin and polysorbate 80. Am. J. Vet. Res. 26, 45-51 (1965).
47. Johnson, R. C. & Harris, V. G. Differentiation of pathogenic and saprophytic leptospires. I. Growth at low temperatures. J. Bacteriol. 94, 27-31 (1967).
48. Westphal, O. & Jann, K. Bacterial lipopolysaccharides: extraction with phenol-water and further application of the procedure. Methods in Carbohydrate Chem. 5, 83-91 (1965).
49. Mathison, J. C. et al. Adaptation to bacterial lipopolysaccharide (LPS) controls LPS-induced tumor necrosis factor production in rabbit macrophages. J. Clin. Invest. 85, 1108-1118 (1990).
50. Lee, C.-H. & Tsai, C.-M. Quantification of bacterial lipopolysaccharides by the purpald assay: measuring formaldehyde generated from 2-keto-deoxyoctonate and heptose at the inner core by periodate oxidation. Anal. Biochem. 267, 161-168 (1999).
51. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 (1970).
52. Tsai, C.-M. & Frasch, C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119, 115-119 (1982).
53. Kirkland, T. N. et al. Analysis of lipopolysaccharide binding by CD14. J. Biol. Chem. 268, 24818-24823 (1993).
54. Yang, R. B. et al. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395, 284-288 (1998).
55. Pugin, J. et al. Cell activation mediated by glycosylphosphatidylinositol-anchored or transmembrane forms of CD14. Infect. Immun. 66, 1174-1180 (1998).
56. Kravchenko, V. V. et al. Platelet-activating factor induces NF-κB activation through a G protein-coupled pathway. J. Biol. Chem. 270, 14928-14934 (1995).
57. Kravchenko, V. V., Steinemann, S., Kline, L. Feng, L. & Ulevitch, R. J. Endotoxin tolerance is induced in Chinese hamster ovary cell lines expressing human CD14. Shock 5, 194-201 (1996).