NMR studies of hexaacylated endotoxin bound to wild-type and F126A mutant MD-2 and MD-2·TLR4 ectodomain complexes

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16346-16355

  Yu, Liping ^a   Phillips, Rachel L ^a   Zhang, DeSheng ^a   Teghanemt, Athmane ^a   Weiss, Jerrold P ^a   Gioannini, Theresa L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC SIDE CHAINS; CHEMICAL SHIFT PERTURBATIONS; ECTODOMAIN; FATTY ACYL CHAINS; GRAM-NEGATIVE BACTERIA; HOST RESPONSE; HYDROPHOBIC POCKETS; HYDROPHOBIC SWITCHES; METABOLIC LABELING; MYELOID DIFFERENTIATION; NEISSERIA MENINGITIDIS; NMR STUDIES; RE-ARRANGEMENT; RE-ORIENTATION; TERNARY COMPLEX; TOLL-LIKE RECEPTOR 4; WILD TYPES;

BIOCHEMISTRY; BIOLOGY;

PARAMAGNETISM;

ACETIC ACID; CARBON 13; ENDOTOXIN; HEXAACYLATED ENDOTOXIN; MUTANT PROTEIN; MYELOID DIFFERENTIATION FACTOR 2; PHENYLALANINE; PROTEIN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; COMPLEX FORMATION; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROPHOBICITY; ISOTOPE LABELING; NEISSERIA MENINGITIDIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS;

ACETYLATION; AMINO ACID SUBSTITUTION; ENDOTOXINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LYMPHOCYTE ANTIGEN 96; MUTATION, MISSENSE; NEISSERIA MENINGITIDIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; TOLL-LIKE RECEPTOR 4;

NEGIBACTERIA; NEISSERIA MENINGITIDIS;

EID: 84860870432     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.343467     Document Type: Article

References (37)

1. Beutler, B., and Rietschel, E. T. (2003) Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3, 169-176 (Pubitemid 37328694)
2. Miller, S. I., Ernst, R. K., and Bader, M. W. (2005) LPS, TLR4, and infectious disease diversity. Nat. Rev. Microbio.l 3, 36-46 (Pubitemid 40028467)
3. Gioannini, T. L., Teghanemt, A., Zhang, D., Levis, E. N., and Weiss, J. P. (2005) Monomeric endotoxin:protein complexes are essential for TLR4-dependent cell activation. J. Endotoxin Res. 11, 117-123 (Pubitemid 40711488)
4. Miyake, K. (2003) Innate recognition of lipopolysaccharide by CD14 and toll-like receptor 4-MD-2: unique roles for MD-2. Int. Immunopharmacol. 3, 119-128
5. Ulevitch, R. J., and Tobias, P. S. (1999) Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immuno.l 11, 19-22 (Pubitemid 29082331)
6. Akira, S. (2009) Pathogen recognition by innate immunity and its signaling. Pro.c Jpn. Acad. Ser. B. Phys. Bio.l. Sc.i 85, 143-156
7. Fitzgerald, K. A., and Chen, Z. J. (2006) Sorting out Toll signals. Cell 125, 834-836 (Pubitemid 43795201)
8. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Na.t Immunol. 11, 373-384
9. Ostuni, R., Zanoni, I., and Granucci, F. (2010) Deciphering the complexity of Toll-like receptor signaling. Cell Mol. Life Sc.i 67, 4109-4134
10. Yamamoto, M., and Akira, S. (2009) Lipid A receptor TLR4-mediated signaling pathways. Adv. Exp. Med. Biol. 667, 59-68
11. Meng, J., Gong, M., Bjorkbacka, 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
12. Gioannini, T. L., Teghanemt, A., Zhang, D., Coussens, N. P., Dockstader, W., Ramaswamy, S., and Weiss, J. P. (2004) Isolation of an endotoxin-MD-2 complex that produces Toll-like receptor 4-dependent cell activation at picomolar concentrations. Proc. Natl. Acad. Sci. U.S.A. 101, 4186-4191 (Pubitemid 38405904)
13. 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 (Pubitemid 47076551)
14. Teghanemt, A., Zhang, D., Levis, E. N., Weiss, J. P., and Gioannini, T. L. (2005) Molecular basis of reduced potency of underacylated endotoxins. J. Immuno.l 175, 4669-4676 (Pubitemid 41362008)
15. 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 (Pubitemid 47332573)
16. 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 (Pubitemid 46982039)
17. 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
18. 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
19. Gruber, A., Mancek, M., Wagner, H., Kirschning, C. J., and Jerala, R. (2004) Structural model of MD-2 and functional role of its basic amino acid clusters involved in cellular lipopolysaccharide recognition. J. Biol. Chem. 279, 28475-28482 (Pubitemid 38900129)
20. 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
21. Kawasaki, K., Nogawa, H., and Nishijima, M. (2003) Identification of mouse MD-2 residues important for forming the cell surface TLR4-MD-2 complex recognized by anti-TLR4-MD-2 antibodies, and for conferring LPS and taxol responsiveness on mouse TLR4 by alanine-scanning mutagenesis. J. Immunol. 170, 413-420 (Pubitemid 36026166)
22. 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
23. Kobayashi, M., Saitoh, S., Tanimura, N., Takahashi, K., Kawasaki, K., Nishijima, M., Fujimoto, Y., Fukase, K., Akashi-Takamura, S., and Miyake, K. (2006) Regulatory roles for MD-2 and TLR4 in ligand-induced receptor clustering. J. Immunol. 176, 6211-6218
24. Giardina, P. C., Gioannini, T., Buscher, B. A., Zaleski, A., Zheng, D. S., Stoll, L., Teghanemt, A., Apicella, M. A., and Weiss, J. (2001) Construction of acetate auxotrophs of Neisseria meningitidis to study host-meningococcal endotoxin interactions. J. Biol. Chem. 276, 5883-5891
25. Post, D. M., Zhang, D., Weiss, J. P., and Gibson, B. W. (2006) Stable isotope metabolic labeling of Neisseria meningitidis lipooligosaccharide. J. Endotoxin Res. 12, 93-98 (Pubitemid 47470159)
26. Esparza, G. A., Teghanemt, A., Zhang, D., Gioannini, T. L., and Weiss, J. P. (2012) Endotoxin:albumin complexes transfer endotoxin monomers to MD-2 resulting in activation of TLR4. Innate Immun., in press
27. Teghanemt, A., Widstrom, R. L., Gioannini, T. L., and Weiss, J. P. (2008) Isolation of monomeric and dimeric secreted MD-2. Endotoxin.sCD14 and Toll-like receptor 4 ectodomain selectively react with the monomeric form of secreted MD-2. J. Biol. Chem. 283, 21881-21889
28. Lewis. K. E., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665
29. Iwahara, J., Tang, C., and Marius Clore, G. (2007) Practical aspects of (1)H transverse paramagnetic relaxation enhancement measurements on macromolecules. J. Magn. Reson. 184, 185-195 (Pubitemid 46177665)
30. Pintacuda, G., and Otting, G. (2002) Identification of protein surfaces by NMRmeasurements with a pramagnetic Gd(III) chelate. J. Am. Chem. Soc. 124, 372-373 (Pubitemid 34084122)
31. Respondek, M., Madl, T., Göbl, C., Golser, R., and Zangger, K. (2007) Mapping the orientation of helices in micelle-bound peptides by paramagnetic relaxation waves. J. Am. Chem. Soc. 129, 5228-5234 (Pubitemid 46651400)
32. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
33. Johnson, B. A., and Blevins, R. A. (1994) NMR View: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614
34. 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. Immuno.l 49, 124-133
35. Madl, T., Bermel, W., and Zangger, K. (2009) Use of relaxation enhancements in a paramagnetic environment for the structure determination of proteins using NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 48, 8259-8262
36. Wang, Y., Liu, L., Davies, D. R., and Segal, D. M. (2010) Dimerization of Toll-like receptor 3 (TLR3) is required for ligand binding. J. Biol. Chem. 285, 36836-36841
37. Panter, G., and Jerala, R. (2011) The ectodomain of the Toll-like receptor 4 prevents constitutive receptor activation. J. Biol. Chem. 286, 23334-23344