Bordetella pertussis lipid A recognition by toll-like receptor 4 and MD-2 is dependent on distinct charged and uncharged interfaces

Journal of Biological Chemistry

Volumn 290, Issue 21, 2015, Pages 13440-13453

  Maeshima, Nina ^a,c   Evans Atkinson, Tara ^a   Hajjar, Adeline M ^b   Fernandez, Rachel C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF WASHINGTON   (United States)

^c STEMCELL Technologies   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; AMINO ACIDS; BACTERIA; CHEMICAL ACTIVATION; ESCHERICHIA COLI; MAMMALS;

CAUSATIVE AGENTS; CHARGED AMINO ACIDS; GRAM-NEGATIVE BACTERIA; INNATE IMMUNITY; RECEPTOR COMPLEX; RECEPTOR-LIGAND INTERACTIONS; SITE DIRECTED MUTAGENESIS; TOLL-LIKE RECEPTOR 4;

IMMUNE SYSTEM;

BACTERIUM LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID A; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; AMINO ACID; GLUCOSAMINE;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL STRAIN; BORDETELLA PERTUSSIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ANIMAL; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; HEK293 CELL LINE; HOST RANGE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MOUSE; MUTATION; PROTEIN CONFORMATION; WESTERN BLOTTING;

BORDETELLA PERTUSSIS; ESCHERICHIA COLI; NEGIBACTERIA;

AMINO ACIDS; ANIMALS; BLOTTING, WESTERN; BORDETELLA PERTUSSIS; CELLS, CULTURED; GLUCOSAMINE; HEK293 CELLS; HOST SPECIFICITY; HUMANS; IMMUNITY, INNATE; LIPID A; LYMPHOCYTE ANTIGEN 96; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84929996030     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.653881     Document Type: Article

References (34)

1. O'Neill, L. A., Golenbock, D., and Bowie, A. G. (2013) The history of Toll-like receptors: redefining innate immunity. Nat. Rev. Immunol. 13, 453-460
2. Muta, T., and Takeshige, K. (2001) Essential roles of CD14 and lipopoly-saccharide-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, 4580-4589
3. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700
4. 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
5. 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
6. Lu, Y. C., Yeh, W. C., and Ohashi, P. S. (2008) LPS/TLR4 signal transduction pathway. Cytokine 42, 145-151
7. 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-2and toll-like receptor 4 in activation by endotoxin. J. Biol. Chem. 284, 15052-15060
8. Resman, N., Oblak, A., Gioannini, T. L., Weiss, J. P., and Jerala, R. (2014)Tetraacylated lipid A and paclitaxel-selective activation of TLR4/MD-2conferred through hydrophobic interactions. J. Immunol. 192, 1887-1895
9. Needham, B. D., Carroll, S. M., Giles, D. K., Georgiou, G., Whiteley, M., and Trent, M. S. (2013) Modulating the innate immune response by combinatorial engineering of endotoxin. Proc. Natl. Acad. Sci. U.S.A. 110, 1464-1469
10. Bryant, C. E., Spring, D. R., Gangloff, M., and Gay, N. J. (2010) The molecular basis of the host response to lipopolysaccharide. Nat. Rev. Microbiol. 8, 8-14
11. 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
12. Hajjar, A. M., Ernst, R. K., Fortuno, E. S., 3rd, Brasfield, A. S., Yam, C. S., Newlon, L. A., Kollmann, T. R., Miller, S. I., and Wilson, C. B. (2012)Humanized TLR4/MD-2 mice reveal LPS recognition differentially impacts susceptibility to Yersinia pestis and Salmonella enterica. PLoS Pathog. 8, e1002963
13. Hajjar, A. M., Ernst, R. K., Tsai, J. H., Wilson, C. B., and Miller, S. I. (2002)Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3, 354-359
14. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B., and Matsuura, M. (2002) Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70, 4092-4098
15. Marr, N., Hajjar, A. M., Shah, N. R., Novikov, A., Yam, C. S., Caroff, M., and Fernandez, R. C. (2010) Substitution of the Bordetella pertussis lipidA phosphate groups with glucosamine is required for robust NF-kB activation and release of proinflammatory cytokines in cells expressing human but not murine Toll-like receptor 4-MD-2-CD14. Infect. Immun. 78, 2060-2069
16. Tanamoto, K., and Azumi, S. (2000) Salmonella-type heptaacylated lipidA is inactive and acts as an antagonist of lipopolysaccharide action on human line cells. J. Immunol. 164, 3149-3156
17. Marr, N., Tirsoaga, A., Blanot, D., Fernandez, R., and Caroff, M. (2008)Glucosamine found as a substituent of both phosphate groups in Bordetella lipid A backbones: role of a BvgAS-activated ArnT ortholog. J Bacteriol 190, 4281-4290
18. Shah, N. R., Albitar-Nehme, S., Kim, E., Marr, N., Novikov, A., Caroff, M., and Fernandez, R. C. (2013) Minor modifications to the phosphate groups and the C3- acyl chain length of lipid A in two Bordetella pertussis strains, BP338 and 18-323, independently affect Toll-like receptor 4 activation. J. Biol. Chem. 288, 11751-11760
19. Fedele, G., Nasso, M., Spensieri, F., Palazzo, R., Frasca, L., Watanabe, M., and Ausiello, C. M. (2008) Lipopolysaccharides from Bordetella pertussis and Bordetella parapertussis differently modulate human dendritic cell functions resulting in divergent prevalence of Th17-polarized responses. J. Immunol. 181, 208-216
20. Marr, N., Novikov, A., Hajjar, A. M., Caroff, M., and Fernandez, R. C. (2010) Variability in the lipooligosaccharide structure and endotoxicity among Bordetella pertussis strains. J. Infect. Dis. 202, 1897-1906
21. Akashi, S., Nagai, Y., Ogata, H., Oikawa, M., Fukase, K., Kusumoto, S., Kawasaki, K., Nishijima, M., Hayashi, S., Kimoto, M., and Miyake, K. (2001) Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Int. Immunol. 13, 1595-1599
22. Hajjar, A. M., Ernst, R. K., Fortuno, E. S., 3rd, Brasfield, A. S., Yam, C. S., Newlon, L. A., Kollmann, T. R., Miller, S. I., and Wilson, C. B. (2012)Humanized TLR4/MD-2 mice reveal LPS recognition differentially impacts susceptibility to Yersinia pestis and Salmonella enterica. PLoS Pathog. 8, e1002963
23. 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
24. Heckman, K. L., and Pease, L. R. (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2, 924-932
25. Meng, J., Lien, E., and Golenbock, D. T. (2010) MD-2-mediated ionicinteractions between lipid A and TLR4 are essential for receptor activation. J. Biol. Chem. 285, 8695-8702
26. Muroi, M., and Tanamoto, K. (2006) Structural regions of MD-2 that determine the agonist-antagonist activity of lipid IVa. J. Biol. Chem. 281, 5484-5491
27. 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/TLR4interface required for signaling by lipid IVa. J. Immunol. 181, 1245-1254
28. Meng, J., Gong, M., Björkbacka, H., and Golenbock, D. T. (2011) Genomewide 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
29. Meng, J., Drolet, J. R., Monks, B. G., and Golenbock, D. T. (2010) MD-2residues tyrosine 42, arginine 69, aspartic acid 122, and leucine 125 provide species specificity for lipid IVA. J. Biol. Chem. 285, 27935-27943
30. Raetz, C. R., Reynolds, C. M., Trent, M. S., and Bishop, R. E. (2007) Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329
31. Fornusková, A., Vinkler, M., Pagès, M., Galan, M., Jousselin, E., Cerqueira, F., Morand, S., Charbonnel, N., Bryja, J., and Cosson, J. F. (2013) Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE). BMC Evol. Biol. 13, 194
32. Mata-Haro, V., Cekic, C., Martin, M., Chilton, P. M., Casella, C. R., and Mitchell, T. C. (2007) The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316, 1628-1632
33. Chilton, P. M., Hadel, D. M., To, T. T., Mitchell, T. C., and Darveau, R. P. (2013) Adjuvant activity of naturally occurring monophosphoryl lipopolysaccharide preparations from mucosa-associated bacteria. Infect. Immun. 81, 3317-3325
34. Cui, W., Joshi, N. S., Liu, Y., Meng, H., Kleinstein, S. H., and Kaech, S. M. (2014) TLR4 ligands lipopolysaccharide and monophosphoryl lipid a differentially regulate effector and memory CD8+ T Cell differentiation. J. Immunol. 192, 4221-4232