Reconstruction of LPS Transfer Cascade Reveals Structural Determinants within LBP, CD14, and TLR4-MD2 for Efficient LPS Recognition and Transfer

Immunity

Volumn 46, Issue 1, 2017, Pages 38-50

  Ryu, Je Kyung ^a   Kim, Soo Jin ^a   Rah, Sang Hyun ^a,c   Kang, Ji In ^a   Jung, Hi Eun ^a   Lee, Dongsun ^a   Lee, Heung Kyu ^a   Lee, Jie Oh ^a   Park, Beom Seok ^b   Yoon, Tae Young ^a,c   Kim, Ho Min ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Eulji University   (South Korea)

^c Yonsei University   (South Korea)

Author keywords

CD14; innate immunity; LBP; LPS recognition; LPS transfer; negative stain EM; single molecule fluorescence analysis; TLR4 MD2

Indexed keywords

CD14 ANTIGEN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; ACUTE PHASE PROTEIN; CARRIER PROTEIN; LIPOPOLYSACCHARIDE-BINDING PROTEIN; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BONE MARROW DERIVED DENDRITIC CELL; CARBOHYDRATE TRANSPORT; CARBOXY TERMINAL SEQUENCE; CATALYST; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE; IMMUNE RESPONSE; IN VITRO STUDY; INNATE IMMUNITY; MICELLE; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; STATIC ELECTRICITY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; HUMAN; IMMUNOLOGY; MOUSE; SIGNAL TRANSDUCTION;

ACUTE-PHASE PROTEINS; ANIMALS; ANTIGENS, CD14; CARRIER PROTEINS; HUMANS; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 85008173357     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.11.007     Document Type: Article

References (30)

1. Akashi, S., Nagai, Y., Ogata, H., Oikawa, M., Fukase, K., Kusumoto, S., Kawasaki, K., Nishijima, M., Hayashi, S., Kimoto, M., Miyake, K., Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Int. Immunol. 13 (2001), 1595–1599.
2. Akashi, S., Saitoh, S., Wakabayashi, Y., Kikuchi, T., Takamura, N., Nagai, Y., Kusumoto, Y., Fukase, K., Kusumoto, S., Adachi, Y., et al. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J. Exp. Med. 198 (2003), 1035–1042.
3. Beamer, L.J., Carroll, S.F., Eisenberg, D., Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 276 (1997), 1861–1864.
4. Beutler, B., Rietschel, E.T., Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3 (2003), 169–176.
5. Beveridge, T.J., Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181 (1999), 4725–4733.
6. Bruce, C., Beamer, L.J., Tall, A.R., The implications of the structure of the bactericidal/permeability-increasing protein on the lipid-transfer function of the cholesteryl ester transfer protein. Curr. Opin. Struct. Biol. 8 (1998), 426–434.
7. Eckert, J.K., Kim, Y.J., Kim, J.I., Gürtler, K., Oh, D.Y., Sur, S., Lundvall, L., Hamann, L., van der Ploeg, A., Pickkers, P., et al. The crystal structure of lipopolysaccharide binding protein reveals the location of a frequent mutation that impairs innate immunity. Immunity 39 (2013), 647–660.
8. Georgel, P., Macquin, C., Bahram, S., The heterogeneous allelic repertoire of human toll-like receptor (TLR) genes. PLoS ONE, 4, 2009, e7803.
9. Gioannini, T.L., Teghanemt, A., Zhang, D., Coussens, N.P., Dockstader, W., Ramaswamy, S., Weiss, J.P., Isolation of an endotoxin-MD-2 complex that produces Toll-like receptor 4-dependent cell activation at picomolar concentrations. Proc. Natl. Acad. Sci. USA 101 (2004), 4186–4191.
10. Hailman, E., Lichenstein, H.S., Wurfel, M.M., Miller, D.S., Johnson, D.A., Kelley, M., Busse, L.A., Zukowski, M.M., Wright, S.D., Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J. Exp. Med. 179 (1994), 269–277.
11. Hajjar, A.M., Ernst, R.K., Tsai, J.H., Wilson, C.B., Miller, S.I., Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3 (2002), 354–359.
12. Han, J., Mathison, J.C., Ulevitch, R.J., Tobias, P.S., Lipopolysaccharide (LPS) binding protein, truncated at Ile-197, binds LPS but does not transfer LPS to CD14. J. Biol. Chem. 269 (1994), 8172–8175.
13. Iovine, N., Eastvold, J., Elsbach, P., Weiss, J.P., Gioannini, T.L., The carboxyl-terminal domain of closely related endotoxin-binding proteins determines the target of protein-lipopolysaccharide complexes. J. Biol. Chem. 277 (2002), 7970–7978.
14. Juan, T.S., Hailman, E., Kelley, M.J., Wright, S.D., Lichenstein, H.S., Identification of a domain in soluble CD14 essential for lipopolysaccharide (LPS) signaling but not LPS binding. J. Biol. Chem. 270 (1995), 17237–17242.
15. Kelley, S.L., Lukk, T., Nair, S.K., Tapping, R.I., The crystal structure of human soluble CD14 reveals a bent solenoid with a hydrophobic amino-terminal pocket. J. Immunol. 190 (2013), 1304–1311.
16. Kim, J.I., Lee, C.J., Jin, M.S., Lee, C.H., Paik, S.G., Lee, H., Lee, J.O., Crystal structure of CD14 and its implications for lipopolysaccharide signaling. J. Biol. Chem. 280 (2005), 11347–11351.
17. 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., Lee, J.O., Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130 (2007), 906–917.
18. Lamping, N., Hoess, A., Yu, B., Park, T.C., Kirschning, C.J., Pfeil, D., Reuter, D., Wright, S.D., Herrmann, F., Schumann, R.R., Effects of site-directed mutagenesis of basic residues (Arg 94, Lys 95, Lys 99) of lipopolysaccharide (LPS)-binding protein on binding and transfer of LPS and subsequent immune cell activation. J. Immunol. 157 (1996), 4648–4656.
19. Park, B.S., Song, D.H., Kim, H.M., Choi, B.S., Lee, H., Lee, J.O., The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458 (2009), 1191–1195.
20. Qiu, X., Mistry, A., Ammirati, M.J., Chrunyk, B.A., Clark, R.W., Cong, Y., Culp, J.S., Danley, D.E., Freeman, T.B., Geoghegan, K.F., et al. Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules. Nat. Struct. Mol. Biol. 14 (2007), 106–113.
21. Raetz, C.R., Reynolds, C.M., Trent, M.S., Bishop, R.E., Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76 (2007), 295–329.
22. Ryu, J.K., Min, D., Rah, S.H., Kim, S.J., Park, Y., Kim, H., Hyeon, C., Kim, H.M., Jahn, R., Yoon, T.Y., Spring-loaded unraveling of a single SNARE complex by NSF in one round of ATP turnover. Science 347 (2015), 1485–1489.
23. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
24. Tan, Y., Kagan, J.C., A cross-disciplinary perspective on the innate immune responses to bacterial lipopolysaccharide. Mol. Cell 54 (2014), 212–223.
25. Tobias, P.S., Soldau, K., Ulevitch, R.J., Isolation of a lipopolysaccharide-binding acute phase reactant from rabbit serum. J. Exp. Med. 164 (1986), 777–793.
26. Tobias, P.S., Soldau, K., Gegner, J.A., Mintz, D., Ulevitch, R.J., Lipopolysaccharide binding protein-mediated complexation of lipopolysaccharide with soluble CD14. J. Biol. Chem. 270 (1995), 10482–10488.
27. Walsh, C., Gangloff, M., Monie, T., Smyth, T., Wei, B., McKinley, T.J., Maskell, D., Gay, N., Bryant, C., Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa. J. Immunol. 181 (2008), 1245–1254.
28. Yu, B., Wright, S.D., Catalytic properties of lipopolysaccharide (LPS) binding protein. Transfer of LPS to soluble CD14. J. Biol. Chem. 271 (1996), 4100–4105.
29. Zanoni, I., Ostuni, R., Marek, L.R., Barresi, S., Barbalat, R., Barton, G.M., Granucci, F., Kagan, J.C., CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147 (2011), 868–880.
30. Zhang, L., Yan, F., Zhang, S., Lei, D., Charles, M.A., Cavigiolio, G., Oda, M., Krauss, R.M., Weisgraber, K.H., Rye, K.A., et al. Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein. Nat. Chem. Biol. 8 (2012), 342–349.