Novel roles of lysines 122, 125, and 58 in functional differences between human and murine MD-2

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 5138-5145

  Vašl, Jožica ^a   Oblak, Alja ^a   Gioannini, Theresa L ^b,c   Weiss, Jerrold P ^b   Jerala, Roman ^a,d  

^a NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; CD14 ANTIGEN; ENDOTOXIN; GLUTAMIC ACID; LEUCINE; LYSINE 122; LYSINE 125; LYSINE 58; LYSINE DERIVATIVE; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES DIFFERENCE; WILD TYPE;

ANIMALS; CELL LINE; ENDOTOXINS; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE ANTIGEN 96; LYSINE; MICE; MUTAGENESIS, SITE-DIRECTED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TRANSFECTION;

EID: 77954100856     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901544     Document Type: Article

References (40)

1. Beutler, B., and E. T. Rietschel. 2003. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3: 169-176.
2. Jerala, R. 2007. Structural biology of the LPS recognition. Int. J. Med Microbiol. 297: 353-363.
3. Gioannini, T. L., and J. P. Weiss. 2007. Regulation of interactions of Gram-negative bacterial endotoxins with mammalian cells. Immunol. Res. 39: 249-260.
4. Tobias, P. S., K. Soldau, J. A. Gegner, D. Mintz, and R. J. Ulevitch. 1995. Lipopolysaccharide binding protein-mediated complexation of lipopolysaccharide with soluble CD14. J. Biol. Chem. 270: 10482-10488.
5. Gioannini, T. L., A. Teghanemt, D. Zhang, E. N. Levis, and J. P. Weiss. 2005. Monomeric endotoxin:protein complexes are essential for TLR4-dependent cell activation. J. Endotoxin Res. 11: 117-123.
6. Re, F., and J. L. Strominger. 2002. Monomeric recombinant MD-2 binds toll-like receptor 4 tightly and confers lipopolysaccharide responsiveness. J. Biol. Chem. 277: 23427-23432.
7. Miyake, K. 2004. Endotoxin recognition molecules, Toll-like receptor 4-MD-2. Semin. Immunol. 16: 11-16. (Pubitemid 38147428)
8. 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.
9. Viriyakosol, S., P. S. Tobias, R. L. Kitchens, and T. N. Kirkland. 2001. MD-2 binds to bacterial lipopolysaccharide. J. Biol. Chem. 276: 38044-38051.
10. 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.
11. Kawasaki, K., S. Akashi, R. Shimazu, T. Yoshida, K. Miyake, and M. Nishijima. 2001. Involvement of TLR4/MD-2 complex in species-specific lipopolysaccharide-mimetic signal transduction by Taxol. J. Endotoxin Res. 7: 232-236.
12. Shimazu, R., S. Akashi, H. Ogata, Y. Nagai, K. Fukudome, K. Miyake, and M. Kimoto. 1999. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189: 1777-1782. (Pubitemid 29272694)
13. Visintin, A., K. A. Halmen, N. Khan, B. G. Monks, D. T. Golenbock, and E. Lien. 2006. MD-2 expression is not required for cell surface targeting of Toll-like receptor 4 (TLR4). J. Leukocyte Biol. 80: 1584-1592.
14. Saitoh, S., S. Akashi, T. Yamada, N. Tanimura, F. Matsumoto, K. Fukase, S. Kusumoto, A. Kosugi, and K. Miyake. 2004. Ligand-dependent Toll-like receptor 4 (TLR4)-oligomerization is directly linked with TLR4-signaling. J. Endotoxin Res. 10: 257-260.
15. 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.
16. Kawasaki, K., K. Gomi, Y. Kawai, M. Shiozaki, and M. Nishijima. 2003. Molecular basis for lipopolysaccharide mimetic action of Taxol and flavolipin. J. Endotoxin Res. 9: 301-307.
17. Kawasaki, K., S. Akashi, R. Shimazu, T. Yoshida, K. Miyake, and M. Nishijima. 2000. Mouse toll-like receptor 4.MD-2 complex mediates lipopolysaccharidemimetic signal transduction by Taxol. J. Biol. Chem. 275: 2251-2254.
18. Resman, N., H. Gradisar, J. Vasl, M. M. Keber, P. Pristovsek, and R. Jerala. 2008. Taxanes inhibit human TLR4 signaling by binding to MD-2. FEBS Lett. 582: 3929-3934.
19. Fujimoto, T., S. Yamazaki, A. Eto-Kimura, K. Takeshige, and T. Muta. 2004. The amino-terminal region of toll-like receptor 4 is essential for binding to MD-2 and receptor translocation to the cell surface. J. Biol. Chem. 279: 47431-47437.
20. Park, B. S., D. H. Song, H. M. Kim, B. S. Choi, H. Lee, and J. O. Lee. 2009. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
21. 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.
22. 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.
23. Gruber, A., M. Mancek, H. Wagner, C. J. Kirschning, and R. Jerala. 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.
24. Gangloff, M., and N. J. Gay. 2004. MD-2: the Toll 'gatekeeper' in endotoxin signalling. Trends Biochem. Sci. 29: 294-300.
25. Giardina, P. C., T. Gioannini, B. A. Buscher, A. Zaleski, D. S. Zheng, L. Stoll, A. Teghanemt, M. A. Apicella, and J. Weiss. 2001. Construction of acetate auxotrophs of Neisseria meningitidis to study host-meningococcal endotoxin interactions. J. Biol. Chem. 276: 5883-5891.
26. Vasl, J., P. Prohinar, T. L. Gioannini, J. P. Weiss, and R. Jerala. 2008. Functional activity of MD-2 polymorphic variant is significantly different in soluble and TLR4-bound forms: decreased endotoxin binding by G56R MD-2 and its rescue by TLR4 ectodomain. J. Immunol. 180: 6107-6115.
27. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249: 1431-1433. (Pubitemid 20341908)
28. Teghanemt, A., R. Fabio, P. Prohinar, R. Widstrom, T. L. Gioannini, and J. P. Weiss. 2007. Novel roles in human MD-2 of phenylalanine 121 and 126 and tyrosine 131 in activation of Toll-like receptor 4 by endotoxin. J. Biol. Chem. 283: 1257-1266.
29. Visintin, A., K. A. Halmen, E. Latz, B. G. Monks, and D. T. Golenbock. 2005. Pharmacological inhibition of endotoxin responses is achieved by targeting the TLR4 coreceptor, MD-2. J. Immunol. 175: 6465-6472. (Pubitemid 41598888)
30. Prohinar, P., F. Re, R. Widstrom, D. S. Zhang, A. Teghanemt, J. P. Weiss, and T. L. Gioannini. 2007. Specific high affinity interactions of monomeric endotoxin: protein complexes with Toll-like receptor 4 ectodomain. J. Biol. Chem. 282: 1010-1017.
31. Muroi, M., and K. Tanamoto. 2006. Structural regions of MD-2 that determine the agonist-antagonist activity of lipid IVa. J. Biol. Chem. 281: 5484-5491.
32. Walsh, C., M. Gangloff, T. Monie, T. Smyth, B. Wei, T. J. McKinley, D. Maskell, N. Gay, and C. Bryant. 2008. Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa. J. Immunol. 181: 1245-1254.
33. Kawasaki, K., H. Nogawa, and M. Nishijima. 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)
34. Kennedy, M. N., G. E. Mullen, C. A. Leifer, C. Lee, A. Mazzoni, K. N. Dileepan, and D. M. Segal. 2004. A complex of soluble MD-2 and lipopolysaccharide serves as an activating ligand for Toll-like receptor 4. J. Biol. Chem. 279: 34698-34704.
35. Teghanemt, A., R. L. Widstrom, T. L. Gioannini, and J. P. Weiss. 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.
36. Visintin, A., A. Mazzoni, J. A. Spitzer, and D. M. Segal. 2001. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proc. Natl. Acad. Sci. USA 98: 12156-12161.
37. Resman, N., J. Vasl, A. Oblak, P. Pristovsek, T. L. Gioannini, J. P. Weiss, and R. Jerala. 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.
38. Wolfs, T. G., I. Dunn-Siegrist, C. van't Veer, C. M. Hodin, W. T. Germeraad, M. A. van Zoelen, R. J. van Suylen, C. J. Peutz-Kootstra, G. Elson, J. Pugin, and W. A. Buurman. 2008. Increased release of sMD-2 during human endotoxemia and sepsis: a role for endothelial cells. Mol. Immunol. 45: 3268-3277.
39. Jia, H. P., J. N. Kline, A. Penisten, M. A. Apicella, T. L. Gioannini, J. Weiss, and P. B. McCray, Jr. 2004. Endotoxin responsiveness of human airway epithelia is limited by low expression of MD-2. Am. J. Physiol. 287: L428-L437.
40. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.