Mycobacterium tuberculosis lipoprotein LprG (Rv1411c) binds triacylated glycolipid agonists of Toll-like receptor 2

Nature Structural and Molecular Biology

Volumn 17, Issue 9, 2010, Pages 1088-1095

  Drage, Michael G ^a   Tsai, Han Chun ^b   Pecora, Nicole D ^a   Cheng, Tan Yun ^c   Arida, Ahmad R ^a   Shukla, Supriya ^a   Rojas, Roxana E ^a   Seshadri, Chetan ^c   Moody, D Branch ^c   Boom, W Henry ^a   Sacchettini, James C ^b   Harding, Clifford V ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOARABINOMANNAN; PHOSPHATIDYLINOSITOL; PROTEIN LPRG; UNCLASSIFIED DRUG; GLYCOLIPID; LIPOMANNAN; LIPOPOLYSACCHARIDE; LIPOPROTEIN; PHOSPHATIDYLINOSITOL MANNOSIDE; PROTEIN BINDING; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ARTICLE; CRYSTAL STRUCTURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; ACYLATION; AGONISTS; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN TERTIARY STRUCTURE;

ACYLATION; BACTERIAL PROTEINS; CELL LINE; GLYCOLIPIDS; HUMANS; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MODELS, MOLECULAR; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TOLL-LIKE RECEPTOR 2;

BACTERIA (MICROORGANISMS); MUS; MYCOBACTERIUM TUBERCULOSIS;

EID: 77956340123     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1869     Document Type: Article

References (44)

1. Flynn, J.L. & Chan, J. Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129 (2001).
2. Janeway, C.A. Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54, 1-13 (1989).
3. Chan, J. et al. Microbial glycolipids: possible virulence factors that scavenge oxygen radicals. Proc. Natl. Acad. Sci. USA 86, 2453-2457 (1989).
4. Fratti, R.A., Chua, J., Vergne, I. & Deretic, V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100, 5437-5442 (2003).
5. Vergne, I. et al. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol. Biol. Cell 15, 751-760 (2004).
6. Cole, S.T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998).
7. Sutcliffe, I.C. & Harrington, D.J. Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 28, 645-659 (2004).
8. Bigi, F. et al. The knockout of the lprG-Rv1410 operon produces strong attenuation of Mycobacterium tuberculosis. Microbes Infect. 6, 182-187 (2004).
9. Rengarajan, J., Bloom, B.R. & Rubin, E.J. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. USA 102, 8327-8332 (2005).
10. Sassetti, C.M. & Rubin, E.J. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. USA 100, 12989-12994 (2003).
11. Farrow, M.F. & Rubin, E.J. Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein. J. Bacteriol. 190, 1783-1791 (2008).
12. Sulzenbacher, G. et al. LppX is a lipoprotein required for the translocation of phthiocerol dimycocerosates to the surface of Mycobacterium tuberculosis. EMBO J. 25, 1436-1444 (2006).
13. Jones, B.W. et al. Different Toll-like receptor agonists induce distinct macrophage responses. J. Leukoc. Biol. 69, 1036-1044 (2001).
14. Gilleron, M., Quesniaux, V.F. & Puzo, G. Acylation state of the phosphatidyl inositol hexamannosides from Mycobacterium bovis BCG and Mycobacterium tuberculosis H37Rv and its implication in TLR response. J. Biol. Chem. 278, 29880-29889 (2003).
15. Elass, E. et al. Mycobacterial lipomannan induces matrix metalloproteinase-9 expression in human macrophagic cells through a toll-like receptor 1 (TLR1)/TLR2-and CD14-dependent mechanism. Infect. Immun. 73, 7064-7068 (2005).
16. Tapping, R.I. & Tobias, P.S. Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling. J. Endotoxin Res. 9, 264-268 (2003).
17. Bhatt, K. & Salgame, P. Host innate immune response to Mycobacterium tuberculosis. J. Clin. Immunol. 27, 347-362 (2007).
18. Pai, R.K., Convery, M., Hamilton, T.A., Boom, W.H. & Harding, C.V. Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J. Immunol. 171, 175-184 (2003).
19. Noss, E.H. et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19 kD lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167, 910-918 (2001).
20. Brightbill, H.D. et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732-736 (1999).
21. Takeuchi, O. et al. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169, 10-14 (2002).
22. Nigou, J. et al. Mannan chain length controls lipoglycans signaling via and binding to TLR2. J. Immunol. 180, 6696-6702 (2008).
23. Pecora, N.D., Gehring, A.J., Canaday, D.H., Boom, W.H. & Harding, C.V. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J. Immunol. 177, 422-429 (2006).
24. Gehring, A.J., Dobos, K.M., Belisle, J.T., Harding, C.V. & Boom, W.H. Mycobacterium tuberculosis LprG (Rv1411c): A novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J. Immunol. 173, 2660-2668 (2004).
25. Jung, S.B. et al. The mycobacterial 38-kilodalton glycolipoprotein antigen activates the mitogen-activated protein kinase pathway and release of proinfammatory cytokines through Toll-like receptors 2 and 4 in human monocytes. Infect. Immun. 74, 2686-2696 (2006).
26. Jin, M.S. et al. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130, 1071-1082 (2007).
27. Rezwan, M., Grau, T., Tschumi, A. & Sander, P. Lipoprotein synthesis in mycobacteria. Microbiology 153, 652-658 (2007).
28. Nigou, J., Gilleron, M. & Puzo, G. Lipoarabinomannans: characterization of the multiacylated forms of the phosphatidyl-myo-inositol anchor by NMR spectroscopy. Biochem. J. 337, 453-460 (1999).
29. Bigi, F. et al. The gene encoding P27 lipoprotein and a putative antibiotic-resistance gene form an operon in Mycobacterium tuberculosis and Mycobacterium bovis. Microbiology 146, 1011-1018 (2000).
30. Gilleron, M., Nigou, J., Nicolle, D., Quesniaux, V. & Puzo, G. The acylation state of mycobacterial lipomannans modulates innate immunity response through toll-like receptor 2. Chem. Biol. 13, 39-47 (2006).
31. Kang, J.Y. et al. Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31, 873-884 (2009).
32. Berg, S., Kaur, D., Jackson, M. & Brennan, P.J. The glycosyltransferases of Mycobacterium tuberculosis\roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates. Glycobiology 17, 35R-56R (2007).
33. Finberg, R.W., Re, F., Popova, L., Golenbock, D.T. & Kurt-Jones, E.A. Cell activation by Toll-like receptors: role of LBP and CD14. J. Endotoxin Res. 10, 413-418 (2004).
34. Jiang, Z. et al. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6, 565-570 (2005).
35. Sklar, M.D., Tereba, A., Chen, B.D. & Walker, W.S. Transformation of mouse bone marrow cells by transfection with a human oncogene related to c-myc is associated with the endogenous production of macrophage colony stimulating factor 1. J. Cell. Physiol. 125, 403-412 (1985).
36. Flo, T.H. et al. Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 277, 35489-35495 (2002).
37. Latz, E. et al. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277, 47834-47843 (2002).
38. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
39. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
40. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
41. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
42. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
43. Pettersen, E.F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
44. Dundas, J. et al. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34, W116-8 (2006).