Unique properties of the chicken TLR4/MD-2 complex: Selective lipopolysaccharide activation of the MyD88-dependent pathway

Journal of Immunology

Volumn 181, Issue 6, 2008, Pages 4354-4362

  Marijke Keestra, A ^a   Van Putten, Jos P M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BETA INTERFERON; GLUTAMINE; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID A; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN MD 2; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; TYROSINE; AVIAN PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ACTIVATION; CELL STRAIN HEK293; CHICKEN; CHIMERA; CLONING; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MAMMAL; MURINAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; SPECIES DIFFERENCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; AVIAN PROTEINS; CELL LINE; CHICKENS; HELA CELLS; HUMANS; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; MICE; MOLECULAR SEQUENCE DATA; MYELOID DIFFERENTIATION FACTOR 88; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 56149107708     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.6.4354     Document Type: Article

References (65)

1. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
2. Palsson-McDermott, E. M., and L. A. O'Neill. 2004. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113: 153-162. (Pubitemid 39312442)
3. Kim, H. M., B. S. Park, J. I. Kim, S. E. Kim, J. Lee, S. C. Oh, P. Enkhbayar, N. Matsushima, H. Lee, O. J. Yoo, and J. O. Lee. 2007. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130: 906-917.
4. Ohto, U., K. Fukase, K. Miyake, and Y. Satow. 2007. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316: 1632-1634.
5. Nagai, Y., S. Akashi, M. Nagafuku, M. Ogata, Y. Iwakura, S. Akira, T. Kitamura, A. Kosugi, M. Kimoto, and K. Miyake. 2002. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3: 667-672. (Pubitemid 34752476)
6. 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: 2085-2088. (Pubitemid 29001265)
7. Yamamoto, M., S. Sato, H. Hemmi, S. Uematsu, K. Hoshino, T. Kaisho, O. Takeuchi, K. Takeda, and S. Akira. 2003. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4: 1144-1150. (Pubitemid 37428043)
8. Kagan, J. C., T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 9: 361-368.
9. Tanimura, N., S. Saitoh, F. Matsumoto, S. Akashi-Takamura, and K. Miyake. 2008. Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 368: 94-99.
10. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643. (Pubitemid 36927946)
11. Meijer, A. H., S. F. Gabby Krens, I. A. Medina Rodriguez, S. He, W. Bitter, B. Ewa Snaar-Jagalska, and H. P. Spaink. 2004. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol. Immunol. 40: 773-783.
12. Roach, J. C., G. Glusman, L. Rowen, A. Kaur, M. K. Purcell, K. D. Smith, L. E. Hood, and A. Aderem. 2005. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 102: 9577-9582.
13. Adler, H. E., and A. J. DaMassa. 1979. Toxicity of endotoxin to chicks. Avian Dis. 23: 174-178.
14. Berczi, I., L. Bertok, and T. Bereznai. 1966. Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can. J. Microbiol. 12: 1070-1071.
15. Iliev, D. B., J. C. Roach, S. Mackenzie, J. V. Planas, and F. W. Goetz. 2005. Endotoxin recognition: in fish or not in fish? FEBS Lett. 579: 6519-6528.
16. Dil, N., and M. A. Qureshi. 2002. Differential expression of inducible nitric oxide synthase is associated with differential Toll-like receptor-4 expression in chicken macrophages from different genetic backgrounds. Vet. Immunol. Immunopathol. 84: 191-207. (Pubitemid 34037116)
17. Fukui, A., N. Inoue, M. Matsumoto, M. Nomura, K. Yamada, Y. Matsuda, K. Toyoshima, and T. Seya. 2001. Molecular cloning and functional characterization of chicken Toll-like receptors: a single chicken Toll covers multiple molecular patterns. J. Biol. Chem. 276: 47143-47149. (Pubitemid 37373090)
18. He, H., K. J. Genovese, D. J. Nisbet, and M. H. Kogut. 2006. Profile of Toll-like receptor expressions and induction of nitric oxide synthesis by Toll-like receptor agonists in chicken monocytes. Mol. Immunol. 43: 783-789. (Pubitemid 41814395)
19. Higgs, R., P. Cormican, S. Cahalane, B. Allan, A. T. Lloyd, K. Meade, T. James, D. J. Lynn, L. A. Babiuk, and C. O'Farrelly. 2006. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74: 1692-1698. (Pubitemid 43346802)
20. Higuchi, M., A. Matsuo, M. Shingai, K. Shida, A. Ishii, K. Funami, Y. Suzuki, H. Oshiumi, M. Matsumoto, and T. Seya. 2007. Combinational recognition of bacterial lipoproteins and peptidoglycan by chicken Toll-like receptor 2 subfamily. Dev. Comp. Immunol. 32: 147-155. (Pubitemid 350160923)
21. Iqbal, M., V. J. Philbin, G. S. Withanage, P. Wigley, R. K. Beal, M. J. Goodchild, P. Barrow, I. McConnell, D. J. Maskell, J. Young, et al. 2005. Identification and functional characterization of chicken Toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar Typhimurium. Infect. Immun. 73: 2344-2350. (Pubitemid 40470837)
22. Keestra, A. M., M. R. de Zoete, R. A. van Aubel, and J. P. M. van Putten. 2007. The central leucine-rich repeat region of chicken TLR16 dictates unique ligand specificity and species-specific interaction with TLR2. J. Immunol. 178: 7110-7119.
23. Keestra, A. M., M. R. de Zoete, R. A. van Aubel, and J. P. M. van Putten. 2008. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Mol. Immunol. 45: 1298-1307.
24. Philbin, V. J., M. Iqbal, Y. Boyd, M. J. Goodchild, R. K. Beal, N. Bumstead, J. Young, and A. L. Smith. 2005. Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 114: 507-521.
25. Schwarz, H., K. Schneider, A. Ohnemus, M. Lavric, S. Kothlow, S. Bauer, B. Kaspers, and P. Staeheli. 2007. Chicken Toll-like receptor 3 recognizes its cognate ligand when ectopically expressed in human cells. J. Interferon Cytokine Res. 27: 97-101. (Pubitemid 46294431)
26. Scott, T., and M. D. Owens. 2007. Thrombocytes respond to lipopolysaccharide through Toll-like receptor-4, and MAP kinase and NF-κB pathways leading to expression of interleukin-6 and cyclooxygenase-2 with production of prostaglandin E2. Mol. Immunol. 45: 1001-1008. (Pubitemid 350016336)
27. Leveque, G., V. Forgetta, S. Morroll, A. L. Smith, N. Bumstead, P. Barrow, J. C. Loredo-Osti, K. Morgan, and D. Malo. 2003. Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar Typhimurium infection in chickens. Infect. Immun. 71: 1116-1124. (Pubitemid 36254291)
28. Malek, M., J. R. Hasenstein, and S. J. Lamont. 2004. Analysis of chicken TLR4, CD28, MIF, MD-2, and LITAF genes in a Salmonella enteritidis resource population. Poult. Sci. 83: 544-549. (Pubitemid 39197221)
29. Dil, N., and M. A. Qureshi. 2002. Involvement of lipopolysaccharide related receptors and nuclear factor κB in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds. Vet. Immunol. Immunopathol. 88: 149-161. (Pubitemid 34786756)
30. Farnell, M. B., T. L. Crippen, H. He, C. L. Swaggerty, and M. H. Kogut. 2003. Oxidative burst mediated by Toll like receptors (TLR) and CD14 on avian heterophils stimulated with bacterial Toll agonists. Dev. Comp. Immunol. 27: 423-429.
31. Kogut, M. H., C. Swaggerty, H. He, I. Pevzner, and P. Kaiser. 2006. Toll-like receptor agonists stimulate differential functional activation and cytokine and chemokine gene expression in heterophils isolated from chickens with differential innate responses. Microbes Infect. 8: 1866-1874.
32. Kogut, M. H., H. He, and P. Kaiser. 2005. Lipopolysaccharide binding protein/CD14/ TLR4-dependent recognition of Salmonella LPS induces the functional activation of chicken heterophils and up-regulation of pro-inflammatory cytokine and chemokine gene expression in these cells. Anim. Biotechnol. 16: 165-181.
33. Beug, H., A. von Kirchbach, G. Doderlein, J. F. Conscience, and T. Graf. 1979. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18: 375-390. (Pubitemid 10248363)
34. 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. (Pubitemid 30134039)
35. Rodriguez, M. S., J. Thompson, R. T. Hay, and C. Dargemont. 1999. Nuclear retention of IκBα protects it from signal-induced degradation and inhibits nuclear factor κB transcriptional activation. J. Biol. Chem. 274: 9108-9115.
36. Horton, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. BioTechniques 8: 528-535.
37. Johnson, K. G., and M. B. Perry. 1976. Improved techniques for the preparation of bacterial lipopolysaccharides. Can. J. Microbiol. 22: 29-34.
38. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165: 618-622. (Pubitemid 30484724)
39. van Aubel, R. A., A. M. Keestra, D. J. Krooshoop, W. van Eden, and J. P. M. van Putten. 2007. Ligand-induced differential cross-regulation of Toll-like receptors 2, 4 and 5 in intestinal epithelial cells. Mol. Immunol. 44: 3702-3714. (Pubitemid 46817666)
40. Karpala, A. J., J. W. Lowenthal, and A. G. Bean. 2008. Activation of the TLR3 pathway regulates IFNβ production in chickens. Dev. Comp. Immunol. 32: 435-444.
41. Smith, C. K., P. Kaiser, L. Rothwell, T. Humphrey, P. A. Barrow, and M. A. Jones. 2005. Campylobacter jejuni-induced cytokine responses in avian cells. Infect. Immun. 73: 2094-2100. (Pubitemid 40470807)
42. da Silva Correia, J., and R. J. Ulevitch. 2002. MD-2 and TLR4 N-linked glycosylations are important for a functional lipopolysaccharide receptor. J. Biol. Chem. 277: 1845-1854.
43. Ohnishi, T., M. Muroi, and K. Tanamoto. 2003. MD-2 is necessary for the Toll-like receptor 4 protein to undergo glycosylation essential for its translocation to the cell surface. Clin. Diagn. Lab. Immunol. 10: 405-410. (Pubitemid 36592967)
44. 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. (Pubitemid 36418132)
45. 114 of human MD-2 are required for Toll-like receptor 4-mediated activation of NF-κB by lipopolysaccharide. J. Immunol. 167: 3354-3359.
46. Akashi, S., Y. Nagai, H. Ogata, M. Oikawa, K. Fukase, S. Kusumoto, K. Kawasaki, M. Nishijima, S. Hayashi, M. Kimoto, and K. Miyake. 2001. Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Int. Immunol. 13: 1595-1599. (Pubitemid 33133886)
47. Steeghs, L., A. M. Keestra, A. van Mourik, H. Uronen-Hansson, P. van der Ley, R. Callard, N. Klein, and J. P. M. van Putten. 2008. Differential activation of human and mouse Toll-like receptor 4 by the adjuvant candidate LpxL1 of Neisseria meningitidis. Infect. Immun. 76: 3801-3807.
48. Lehmann, V. 1977. Isolation, purification and properties of an intermediate in 3-deoxy-D-manno-octulosonic acid: lipid A biosynthesis. Eur. J. Biochem. 75: 257-266. (Pubitemid 8080836)
49. Mata-Haro, V., C. Cekic, M. Martin, P. M. Chilton, C. R. Casella, and T. C. Mitchell. 2007. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316: 1628-1632. (Pubitemid 46982038)
50. Golenbock, D. T., R. Y. Hampton, N. Qureshi, K. Takayama, and C. R. Raetz. 1991. Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J. Biol. Chem. 266: 19490-19498.
51. Lien, E., T. K. Means, H. Heine, A. Yoshimura, S. Kusumoto, K. Fukase, M. J. Fenton, M. Oikawa, N. Qureshi, B. Monks, et al. 2000. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J. Clin. Invest. 105: 497-504. (Pubitemid 30127250)
52. Sauter, K. S., M. Brcic, M. Franchini, and T. W. Jungi. 2007. Stable transduction of bovine TLR4 and bovine MD-2 into LPS-nonresponsive cells and soluble CD14 promote the ability to respond to LPS. Vet. Immunol. Immunopathol. 118: 92-104.
53. Delude, R. L., R. Savedra, Jr., H. Zhao, R. Thieringer, S. Yamamoto, M. J. Fenton, and D. T. Golenbock. 1995. CD14 enhances cellular responses to endotoxin without imparting ligand-specific recognition. Proc. Natl. Acad. Sci. USA 92: 9288-9292.
54. Takayama, K., N. Qureshi, B. Beutler, and T. N. Kirkland. 1989. Diphosphoryl lipid A from Rhodopseudomonas sphaeroides ATCC 17023 blocks induction of cachectin in macrophages by lipopolysaccharide. Infect. Immun. 57: 1336-1338. (Pubitemid 19087890)
55. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
56. Re, F., and J. L. Strominger. 2003. Separate functional domains of human MD-2 mediate Toll-like receptor 4-binding and lipopolysaccharide responsiveness. J. Immunol. 171: 5272-5276. (Pubitemid 37432812)
57. Hajjar, A. M., R. K. Ernst, J. H. Tsai, C. B. Wilson, and S. I. Miller. 2002. Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3: 354-359.
58. Muroi, M., T. Ohnishi, and K. Tanamoto. 2002. MD-2, a novel accessory molecule, is involved in species-specific actions of Salmonella lipid A. Infect. Immun. 70: 3546-3550. (Pubitemid 34665991)
59. Harper, M., A. D. Cox, F. St. Michael, I. W. Wilkie, J. D. Boyce, and B. Adler. 2004. A heptosyltransferase mutant of Pasteurella multocida produces a truncated lipopolysaccharide structure and is attenuated in virulence. Infect. Immun. 72: 3436-3443. (Pubitemid 38697769)
60. Arbour, N. C., E. Lorenz, B. C. Schutte, J. Zabner, J. N. Kline, M. Jones, K. Frees, J. L. Watt, and D. A. Schwartz. 2000. TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat. Genet. 25: 187-191.
61. Erridge, C., J. Stewart, and I. R. Poxton. 2003. Monocytes heterozygous for the Asp299Gly and Thr399Ile mutations in the Toll-like receptor 4 gene show no deficit in lipopolysaccharide signalling. J. Exp. Med. 197: 1787-1791. (Pubitemid 36745353)
62. van der Graaf, C., B. J. Kullberg, L. Joosten, T. Verver-Jansen, L. Jacobs, J. W. Van der Meer, and M. G. Netea. 2005. Functional consequences of the Asp299Gly Toll-like receptor-4 polymorphism. Cytokine 30: 264-268. (Pubitemid 40775845)
63. Jiang, Z., P. Georgel, X. Du, L. Shamel, S. Sovath, S. Mudd, M. Huber, C. Kalis, S. Keck, C. Galanos, et al. 2005. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6: 565-570. (Pubitemid 41710726)
64. Kato, A., T. Ogasawara, T. Homma, H. Saito, and K. Matsumoto. 2004. Lipopolysaccharide-binding protein critically regulates lipopolysaccharide- induced IFN-β signaling pathway in human monocytes. J. Immunol. 172: 6185-6194. (Pubitemid 38621224)
65. Karaghiosoff, M., R. Steinborn, P. Kovarik, G. Kriegshauser, M. Baccarini, B. Donabauer, U. Reichart, T. Kolbe, C. Bogdan, T. Leanderson, et al. 2003. Central role for type I interferons and Tyk2 in lipopolysaccharide- induced endotoxin shock. Nat. Immunol. 4: 471-477. (Pubitemid 36592440)