Leucine-rich repeat 11 of toll-like receptor 9 can tightly bind to CpG-containing oligodeoxynucleotides, and the positively charged residues are critical for the high affinity

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30596-30609

  Pan, Xichun ^a   Yue, Junjie ^b   Ding, Guofu ^a   Li, Bin ^a   Liu, Xin ^a   Zheng, Xinchuan ^a   Yu, Mengchen ^a   Li, Jun ^a   Jiang, Weiwei ^a   Wu, Chong ^a   Zheng, Jiang ^a   Zhou, Hong ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR RESPONSE; CHARGE RESIDUE; CPG-ODN; CYTOKINES; DELETION MUTANTS; EXTRACELLULAR DOMAINS; HIGH AFFINITY; IN-VITRO; LEUCINE-RICH REPEATS; LIGAND BINDING; OLIGODEOXYNUCLEOTIDES; PERITONEAL MACROPHAGE; POSITIVELY CHARGED; PRE-INCUBATION; TOLL-LIKE RECEPTOR 9;

HYDROGEN BONDS; OLIGONUCLEOTIDES;

AMINO ACIDS;

ARGININE; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; HISTIDINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LEUCINE RICH REPEAT 11 PROTEIN; LEUCINE RICH REPEAT 2 PROTEIN; LEUCINE RICH REPEAT 5 PROTEIN; LEUCINE RICH REPEAT 8 PROTEIN; LYSINE; MESSENGER RNA; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL ISOLATION; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE RELEASE; HYDROGEN BOND; IN VITRO STUDY; INTERNALIZATION; LIGAND BINDING; MOUSE; MUTANT; MUTATION; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BINDING SITES; HEK293 CELLS; HUMANS; MACROPHAGES, PERITONEAL; MICE; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN BINDING; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE DELETION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

BACTERIA (MICROORGANISMS);

EID: 84865788432     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.396432     Document Type: Article

References (28)

1. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
2. Uematsu, S., and Akira, S. (2007) Toll-like receptors and Type I interferons. J. Biol. Chem. 282, 15319-15323
3. Jin, M. S., and Lee, J. O. (2008) Structures of TLR-ligand complexes. Curr. Opin Immunol. 20, 414-419
4. Akira, S., and Takeda, K. (2004) Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511
5. Bell, J. K., Mullen, G. E., Leifer, C. A., Mazzoni, A., Davies, D. R., and Segal, D. M. (2003) Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol. 24, 528-533
6. Lee, J. H., Voo, K. S., and Skalnik, D. G. (2001) Identification and characterization of the DNA binding domain of CpG-binding protein. J. Biol. Chem. 276, 44669-44676
7. Ewald, S. E., Lee, B. L., Lau, L., Wickliffe, K. E., Shi, G. P., Chapman, H. A., and Barton, G. M. (2008) The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456, 658-662
8. Park, B., Brinkmann, M. M., Spooner, E., Lee, C. C., Kim, Y. M., and Ploegh, H. L. (2008) Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 9, 1407-1414
9. Peter, M. E., Kubarenko, A. V., Weber, A. N., and Dalpke, A. H. (2009) Identification of an N-terminal recognition site in TLR9 that contributes to CpG-DNA-mediated receptor activation. J. Immunol. 182, 7690-7697
10. Kubarenko, A. V., Ranjan, S., Rautanen, A., Mills, T. C., Wong, S., Vannberg, F., Neumaier, M., Bekeredjian-Ding, I., Hill, A. V., Ahmad-Nejad, P., and Weber, A. N. (2010) A naturally occurring variant in human TLR9, P99L, is associated with loss of CpG oligonucleotide responsiveness. J. Biol. Chem. 285, 36486-36494
11. Yibin, G., Jiang, Z., Hong, Z., Gengfa, L., Liangxi, W., Guo, W., and Yongling, L. (2005) A synthesized cationic tetradecapeptide from hornet venom kills bacteria and neutralizes lipopolysaccharide in vivo and in vitro. Biochem. Pharmacol. 70, 209-219
12. Li, B., Zhang, R., Li, J., Zhang, L., Ding, G., Luo, P., He, S., Dong, Y., Jiang, W., Lu, Y., Cao, H., Zheng, J., and Zhou, H. (2008) Antimalarial artesunate protects sepsis model mice against heat-killed Escherichia coli challenge by decreasing TLR4 and TLR9 mRNA expressions and transcription factor NF-κB activation. Int. Immunopharmacol. 8, 379-389
13. Liu, X., Cheng, J., Zheng, X., Chen, Y., Wu, C., Li, B., Fu, J., Cao, H., Lu, Y., Li, J., Zheng, J., and Zhou, H. (2009) Targeting CpG DNA to screen and isolate anti-sepsis fraction and monomers from traditional Chinese herbs using affinity biosensor technology. Int. Immunopharmacol. 9, 1021-1031
14. Wang, J., Xu, X., Zhang, Z., Yang, F., and Yang, X. (2009) Real-time study of genomic DNA structural changes upon interaction with small molecules using dual-polarization interferometry. Anal Chem. 81, 4914-4921
15. Kuznik, A., Bencina, M., Svajger, U., Jeras, M., Rozman, B., and Jerala, R. (2011) Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J. Immunol. 186, 4794-4804
16. Hong, Z., Jiang, Z., Liangxi, W., Guofu, D., Ping, L., Yongling, L., Wendong, P., and Minghai, W. (2004) Chloroquine protects mice from challenge with CpG ODN and LPS by decreasing proinflammatory cytokine release. Int. Immunopharmacol. 4, 223-234
17. Liu, X., Zheng, X., Wang, N., Cao, H., Lu, Y., Long, Y., Zhao, K., Zhou, H., and Zheng, J. (2011) Kukoamine B, a novel dual inhibitor of LPS and CpG DNA, is a potential candidate for sepsis treatment. Br. J. Pharmacol. 162, 1274-1290
18. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25, 402-408
19. Jung, I., Lee, J., Lee, S. Y., and Kim, D. (2008) Application of nonnegative matrix factorization to improve profile-profile alignment features for -fold recognition and remote homolog detection. BMC Bioinformatics 9, 298
20. Kelm, S., Shi, J., and Deane, C. M. (2010) MEDELLER. Homology-based coordinate generation for membrane proteins. Bioinformatics 26, 2833-2840
21. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR. An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-W667
22. Li, H., Robertson, A. D., and Jensen, J. H. (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61, 704-721
23. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems. Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
24. Rutz, M., Metzger, J., Gellert, T., Luppa, P., Lipford, G. B., Wagner, H., and Bauer, S. (2004) Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 34, 2541-2550
25. Ritchie, D. W. (2003) Evaluation of protein docking predictions using Hex 3.1 in CAPRI rounds 1 and 2. Proteins 52, 98-106
26. González-Navajas, J. M., Law, J., Nguyen, K. P., Bhargava, M., Corr, M. P., Varki, N., Eckmann, L., Hoffman, H. M., Lee, J., and Raz, E. (2010) Interleukin 1 receptor signaling regulates DUBA expression and facilitates Toll-like receptor 9-driven anti-inflammatory cytokine production. J. Exp. Med. 207, 2799-2807
27. Liu, L., Botos, I., Wang, Y., Leonard, J. N., Shiloach, J., Segal, D. M., and Davies, D. R. (2008) Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320, 379-381
28. Choe, J., Kelker, M. S., and Wilson, I. A. (2005) Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309, 581-585