Conformationally constrained lipid a mimetics for exploration of structural basis of TLR4/MD-2 activation by lipopolysaccharide

ACS Chemical Biology

Volumn 8, Issue 11, 2013, Pages 2423-2432

  Artner, Daniel ^a   Oblak, Alja ^b   Ittig, Simon ^c   Garate, Jose Antonio ^a   Horvat, Simon ^b   Arrieumerlou, Cécile ^c   Hofinger, Andreas ^a   Oostenbrink, Chris ^a   Jerala, Roman ^b   Kosma, Paul ^a   Zamyatina, Alla ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; LIPID A; LIPOPOLYSACCHARIDE; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; MD-2 MIMETIC PEPTIDE; PEPTIDE; PROTEIN BINDING; TLR4 PROTEIN, HUMAN;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARBOHYDRATE ANALYSIS; CHEMICAL STRUCTURE; CONFORMATION; CONFORMATIONAL TRANSITION; DIMERIZATION; ENZYME PHOSPHORYLATION; GLYCOSYLATION; HUMAN; HUMAN CELL; HYDROGENATION; IMMUNE RESPONSE; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BIOMIMETICS; CHEMISTRY; DOSE RESPONSE; ESCHERICHIA COLI; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; X RAY CRYSTALLOGRAPHY;

ANIMALS; BIOMIMETICS; CRYSTALLOGRAPHY, X-RAY; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; HEK293 CELLS; HUMANS; INTERLEUKIN-6; LIPID A; LIPOPOLYSACCHARIDES; MALE; MICE; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; PEPTIDES; PROTEIN BINDING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84887938025     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb4003199     Document Type: Article

References (42)

1. Miyake, K. (2006) Roles for accessory molecules in microbial recognition by Toll-like receptors J. Endotoxin Res. 12, 195-204
2. Prohinar, P., Re, F., Widstrom, R., Zhang, D., Teghanemt, A., Weiss, J. P., and Gioannini, T. L. (2007) Specific high affinity interactions of monomeric endotoxin-protein complexes with Toll-like receptor 4 ectodomain J. Biol. Chem. 282, 1010-1017
3. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex Nature 458, 1191-1195
4. Munford, R. S. (2008) Sensing Gram-negative bacterial lipopolysaccharides: A human disease determinant? Infect. Immun. 76, 454-465
5. Park, S. H., Kim, N. D., Jung, J. K., Lee, C. K., Han, S. B., and Kim, Y. (2012) Myeloid differentiation 2 as a therapeutic target of inflammatory disorders Pharmacol.Ther. 133, 291-298
6. Opal, S. M. (2007) The host response to endotoxin, antilipopolysaccharide strategies, and the management of severe sepsis Int. J. Med. Microbiol. 297, 365-377
7. Hammad, H., Chieppa, M., Perros, F., Willart, M. A., Germain, R. N., and Lambrecht, B. N. (2009) House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells Nat. Med. 15, 410-416
8. Abdollahi-Roodsaz, S., Joosten, L. A. B., Roelofs, M. F., Radstake, T. R. D. J., Matera, G., Popa, C., Van der Meer, J. W. M., Netea, M. G., and van den Berg, W. B. (2007) Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis Arthritis Rheum. 56, 2957-2967
9. Abreu, M. T. and Arditi, M. (2004) Innate immunity and toll-like receptors: Clinical implications of basic science research J. Pediatr. 144, 421-429
10. Reisser, D. and Jeannin, J.-F. (2009) Lipid A in cancer therapies: Preclinical studies. In Lipid A in Cancer Therapy, pp 101-110, Springer, Landes Bioscience, New York.
11. Ohto, U., Fukase, K., Miyake, K., and Satow, Y. (2007) Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa Science 316, 1632-1634
12. Takayama, K., Qureshi, N., Beutler, B., and Kirkland, T. N. (1989) Diphosphoryl lipid A from Rhodopseudomonas sphaeroides ATCC 17023 blocks induction of cachectin in macrophages by lipopolysaccharide Infect. Immun. 57, 1336-1338
13. Christ, W. J., McGuinness, P. D., Asano, O., Wang, Y., Mullarkey, M. A., Perez, M., Hawkins, L. D., Blythe, T. A., Dubuc, G. R., and Robidoux, A. L. (1994) Total synthesis of the proposed structure of Rhodobacter sphaeroides Lipid A resulting in the synthesis of new potent lipopolysaccharide antagonists J. Am. Chem. Soc. 116, 3637-3638
14. Hawkins, L. D., Christ, W. J., and Rossignol, D. P. (2004) Inhibition of endotoxin response by synthetic TLR4 antagonists Curr. Top. Med. Chem. 4, 1147-1171
15. Shirey, K. A., Lai, W., Scott, A. J., Lipsky, M., Mistry, P., Pletneva, L. M., Karp, C. L., McAlees, J., Gioannini, T. L., Weiss, J., Chen, W. H., Ernst, R. K., Rossignol, D. P., Gusovsky, F., Blanco, J. C. G., and Vogel, S. N. (2013) The TLR4 antagonist Eritoran protects mice from lethal influenza infection Nature 497, 498-502
16. Kim, H. M., Park, B. S., Kim, J. I., Kim, S. E., Lee, J., Oh, S. C., Enkhbayar, P., Matsushima, N., Lee, H., Yoo, O. J., and Lee, J. O. (2007) Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran Cell 130, 906-917
17. Meng, J., Gong, M., Björkbacka, H., and Golenbock, D. T. (2011) Genome-wide expression profiling and mutagenesis studies reveal that lipopolysaccharide responsiveness appears to be absolutely dependent on TLR4 and MD-2 expression and is dependent upon intermolecular ionic interactions J. Immunol. 187, 3683-3693
18. Teghanemt, A., Re, F., Prohinar, P., Widstrom, R., Gioannini, T. L., and Weiss, J. P. (2008) Novel roles in human MD-2 of phenylalanines 121 and 126 and tyrosine 131 in activation of Toll-like receptor 4 by endotoxin J. Biol. Chem. 283, 1257-1266
19. Resman, N., Vasl, J., Oblak, A., Pristovsek, P., Gioannini, T. L., Weiss, J. P., and Jerala, R. (2009) Essential roles of hydrophobic residues in both MD-2 and Toll-like receptor 4 in activation by endotoxin J. Biol. Chem. 284, 15052-15060
20. Ohto, U., Fukase, K., Miyake, K., and Shimizu, T. (2012) Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2 Proc. Natl. Acad. Sci. U.S.A. 109, 7421-7426
21. Meng, J., Lien, E., and Golenbock, D. T. (2010) MD-2-mediated ionic interactions between Lipid A and TLR4 are essential for receptor activation J. Biol. Chem. 285, 8695-8702
22. Walsh, C., Gangloff, M., Monie, T., Smyth, T., Wei, B., McKinley, T. J., Maskell, D., Gay, N., and Bryant, C. (2008) Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa J. Immunol. 181, 1245-1254
23. Meng, J., Drolet, J. R., Monks, B. G., and Golenbock, D. T. (2010) MD-2 residues Tyrosine 42, Arginine 69, Aspartic acid 122, and Leucine 125 provide species specificity for lipid IVa J. Biol. Chem. 285, 27935-27943
24. Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., and Stephens, D. S. (2005) Differential induction of the Toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins Infect. Immun. 73, 2940-2950
25. Trent, M. S., Stead, C. M., Tran, A. X., and Hankins, J. V. (2006) Diversity of endotoxin and its impact on pathogenesis J. Endotoxin Res. 12, 205-223
26. Akamatsu, M., Fujimoto, Y., Kataoka, M., Suda, Y., Kusumoto, S., and Fukase, K. (2006) Synthesis of lipid A monosaccharide analogues containing acidic amino acid: Exploring the structural basis for the endotoxic and antagonistic activities Bioorg. Med. Chem. 14, 6759-6777
27. Fujimoto, Y., Adachi, Y., Akamatsu, M., Fukase, Y., Kataoka, M., Suda, Y., Fukase, K., and Kusumoto, S. (2005) Synthesis of lipid A and its analogues for investigation of the structural basis for their bioactivity J. Endotoxin Res. 11, 341-347
28. Zhang, Y., Gaekwad, J., Wolfert, M. A., and Boons, G. J. (2007) Modulation of innate immune responses with synthetic Lipid A derivatives J. Am. Chem. Soc. 129, 5200-5216
29. Bazin, H. G., Murray, T. J., Bowen, W. S., Mozaffarian, A., Fling, S. P., Bess, L. S., Livesay, M. T., Arnold, J. S., Johnson, C. L., Ryter, K. T., Cluff, C. W., Evans, J. T., and Johnson, D. A. (2008) The "Ethereal" nature of TLR4 agonism and antagonism in the AGP class of lipid A mimetics Bioorg. Med. Chem. Lett. 18, 5350-5354
30. 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, 3032-3039
31. Rao, V. S. R., Qasba, P. K., Balaji, P. V., and Chandrasekaran, R. (1998) Conformation of disaccharides. In Conformation of Carbohydrates, pp 91-130, OPA: Overseas Publishers Association, Harwood Academic Publishers, Amsterdam.
32. Oikawa, M., Shintaku, T., Fukuda, N., Sekljic, H., Fukase, Y., Yoshizaki, H., Fukase, K., and Kusumoto, S. (2004) NMR conformational analysis of biosynthetic precursor-type lipid A: monomolecular state and supramolecular assembly Org. Biomol. Chem. 2, 3557-3565
33. 15N-labeled lipopolysaccharides in a membrane mimetic Angew. Chem. Int. Ed. 47, 9870-9874
34. Taga, T., Miwa, Y., and Min, Z. (1997) α,β-Trehalose monohydrate Acta Crystallogr., Sect. C: Cryst. Struct. Commun. 53, 234-236
35. Dowd, M. K., Reilly, P. J., and French, A. D. (1992) Conformational analysis of trehalose disaccharides and analogues using MM3 J. Comput. Chem. 13, 102-114
36. Peric-Hassler, L., Hansen, H. S., Baron, R., and Hünenberger, P. H. (2010) Conformational properties of glucose-based disaccharides investigated using molecular dynamics simulations with local elevation umbrella sampling Carbohydr. Res. 345, 1781-1801
37. Gaekwad, J., Zhang, Y., Zhang, W., Reeves, J., Wolfert, M. A., and Boons, G. J. (2010) Differential induction of innate immune responses by synthetic Lipid A derivatives J. Biol. Chem. 285, 29375-29386
38. Fukase, K., Fukase, Y., Oikawa, M., Liu, W. C., Suda, Y., and Kusumoto, S. (1998) Divergent synthesis and biological activities of lipid A analogues of shorter acyl chains Tetrahedron 54, 4033-4050
39. DeMarco, M. L. and Woods, R. J. (2011) From agonist to antagonist: Structure and dynamics of innate immune glycoprotein MD-2 upon recognition of variably acylated bacterial endotoxins Mol. Immunol. 49, 124-133
40. Yu, L., Phillips, R. L., Zhang, D., Teghanemt, A., Weiss, J. P., and Gioannini, T. L. (2012) NMR studies of hexaacylated endotoxin bound to wild-type and F126A mutant MD-2 and MD-2-TLR4 ectodomain complexes J. Biol. Chem. 287, 16346-16355
41. Barochia, A., Solomon, S., Cui, X., Natanson, C., and Eichacker, P. Q. (2011) Eritoran tetrasodium (E5564) treatment for sepsis: Review of preclinical and clinical studies Expert Opin. Drug Metab. Toxicol. 7, 479-494
42. Fleischer, J. G., Rossignol, D., Francis, G. A., Chan, T., Lynn, M., and Wasan, K. M. (2012) Deactivation of the lipopolysaccharide antagonist eritoran (E5564) by high-density lipoprotein-associated apolipoproteins Innate Immun. 18, 171-178