Essential calcium-binding cluster of Leptospira LipL32 protein for inflammatory responses through the Toll-like receptor 2 pathway

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 12335-12344

  Lo, Yueh Yu ^a   Hsu, Shen Hsing ^b   Ko, Yi Ching ^b   Hung, Cheng Chieh ^b   Chang, Ming Yang ^b   Hsu, Hsiang Hao ^b   Pan, Ming Jeng ^c   Chen, Yen Wei ^a   Lee, Ching Hung ^a   Tseng, Fan Gang ^a   Sun, Yuh Ju ^a   Yang, Chih Wei ^b   Pan, Rong Long ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CENTRAL TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING CAPABILITY; BINDING RESIDUES; CALCIUM BINDING; INFLAMMATORY RESPONSE; OUTER MEMBRANE; SITE DIRECTED MUTAGENESIS; TOLL-LIKE RECEPTOR 2; X-RAY CRYSTALLOGRAPHIC STRUCTURES;

ATOMIC FORCE MICROSCOPY; CALCIUM;

PROTEINS;

ALANINE; INTERLEUKIN 8; MATRILYSIN; MONOCYTE CHEMOTACTIC PROTEIN 1; OUTER MEMBRANE PROTEIN LIPL32; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL VIRULENCE; BINDING AFFINITY; CALCIUM BINDING; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE; CHEMOKINE CCL2; HUMANS; INFLAMMATION; INTERLEUKIN-8; KIDNEY; LEPTOSPIRA; LEPTOSPIROSIS; LIPOPROTEINS; MATRIX METALLOPROTEINASE 7; MUTAGENESIS, SITE-DIRECTED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR-ALPHA;

LEPTOSPIRA;

EID: 84876891567     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.418699     Document Type: Article

References (40)

1. Levett, P. N. (2001) Leptospirosis. Clin. Microbiol. Rev. 14, 296-326
2. Yang, C. W. (2007) Leptospirosis renal disease: understanding the initiation by Toll-like receptors. Kidney Int. 72, 918-925
3. Dolhnikoff, M., Mauad, T., Bethlem, E. P., and Carvalho, C. R. (2007) Pathology and pathophysiology of pulmonary manifestations in leptospi-rosis. Braz. J. Infect. Dis. 11, 142-148
4. Farr, R. W. (1995) Leptospirosis. Clin. Infect. Dis. 21, 1-8
5. Yang, C. W., Wu, M. S., and Pan, M. J. (2001) Leptospirosis renal disease. Nephrol. Dial. Transplant. 16, 73-77
6. Yang, C. W., Wu, M. S., Pan, M. J., Hong, J. J., Yu, C. C, Vandewalle, A., and Huang, C. C. (2000) Leptospira outer membrane protein activates NF-κB and downstream genes expressed in medullary thick ascending limb cells. J. Am. Soc. Nephrol. 11, 2017-2026
7. Hung, C. C, Chang, C. T., Chen, K. H., Tian, Y. C, Wu, M. S., Pan, M. J., Vandewalle, A., and Yang, C. W. (2006) Up-regulation of chemokine CXCL1/KC by leptospiral membrane lipoprotein preparation in renal tubule epithelial cells. Kidney Int. 69, 1814-1822
8. Patti, J. M., Allen, B. L., McGavin, M. J., and Hoök, M. (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617
9. Werts, C., Tapping, R. I., Mathison, J. C, Chuang, T. H, Kravchenko, V., Saint Girons, I., Haake, D. A., Godowski, P. J., Hayashi, F., Ozinsky, A., Underhill, D. M., Kirschning, C. J., Wagner, H., Aderem, A., Tobias, P. S., and Ulevitch, R. J. (2001) Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immunol. 2, 346-352
10. Yang, C. W., Wu, M. S., Pan, M. J., Hsieh, W. J., Vandewalle, A., and Huang, C. C. (2002) The Leptospira outer membrane protein LipL32 induces tubulointerstitial nephritis-mediated gene expression in mouse proximal tubule cells. J. Am. Soc. Nephrol. 13, 2037-2045
11. Matsunaga, J., Barocchi, M. A., Croda, J., Young, T. A., Sanchez, Y., Siqueira, I., Bolin, C A., Reis, M. G., Riley, L. W., Haake, D. A, and Ko, A. I. (2003) Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol. Microbiol. 49, 929-945
12. Stevenson, B., Choy, H. A., Pinne, M., Rotondi, M. L., Miller, M. C, De-moll, E., Kraiczy, P., Cooley, A. E., Creamer, T. P., Suchard, M. A., Bris-sette, C. A., Verma, A., and Haake, D. A. (2007) Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin, and regulators of complement. PLoS One 2, e1188
13. Ristow, P., Bourhy, P., da Cruz McBride, F. W., Figueira, C. P., Huerre, M., Ave, P., Girons, I. S., Ko, A. I., and Picardeau, M. (2007) The OmpA-like protein Loa22 is essential for leptospiral virulence. PLoS Pathog. 3, e97
14. Haake, D. A., Chao, G., Zuerner, R. L., Barnett, J. K., Barnett, D., Mazel, M., Matsunaga, J., Levett, P. N., and Bolin, C A. (2000) The leptospiral major outer membrane protein LipL32 is a lipoprotein expressed during mammalian infection. Infect. Immun. 68, 2276-2285
15. Lee, S. H., Kim, K. A., Park, Y. G., Seong, I. W., Kim, M. J., and Lee, Y. J. (2000) Identification and partial characterization of a novel hemolysin from Leptospira interrogans serovar lai. Gene 254, 19-28
16. Hauk, P., Guzzo, C. R., Roman Ramos, H., Ho, P. L., and Farah, C S. (2009) Structure and calcium-binding activity of LipL32, the major surface antigen of pathogenic Leptospira sp. J. Mol. Biol. 390, 722-736
17. Tung, J. Y., Yang, C. W., Chou, S. W., Lin, C. C, and Sun, Y. J. (2010) Calcium binds to LipL32, a lipoprotein from pathogenic Leptospira, and modulates fibronectin binding. J. Biol. Chem. 285, 3245-3252
18. Vivian, J. P., Beddoe, T., McAlister, A. D., Wilce, M. C, Zaker-Tabrizi, L., Troy, S., Byres, E., Hoke, D. E., Cullen, P. A., Lo, M., Murray, G. L., Adler, B., and Rossjohn, J. (2009) Crystal structure of LipL32, the most abundant surface protein of pathogenic Leptospira spp. J. Mol. Biol. 387, 1229-1238
19. Hauk, P., Barbosa, A. S., Ho, P. L., and Farah, C. S. (2012) Calcium binding to Leptospira outer membrane antigen LipL32 is not necessary for its interaction with plasma fibronectin, collagen type IV, and plasminogen. J. Biol. Chem. 287, 4826-4834
20. Akira, S., Takeda, K., and Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680
21. Anders, H. J., Banas, B., and Schlondorff, D. (2004) Signaling danger: Tolllike receptors and their potential roles in kidney disease. J. Am. Soc. Nephrol. 15, 854-867
22. Takeda, K., Kaisho, T., and Akira, S. (2003) TLR signaling pathways. Annu. Rev. Immunol. 21, 335-376
23. Hsu, S. H, Lo, Y. Y., Tung, J. Y., Ko, Y. C, Sun, Y. J., Hung, C C., Yang, C. W, Tseng, F. G, Fu, C C., and Pan, R. L. (2010) Leptospiral outer membrane lipoprotein LipL32 binding on toll-like receptor 2 of renal cells as determined with an atomic force microscope. Biochemistry 49, 5408-5417
24. Alexopoulou, L., Thomas, V., Schnare, M., Lobet, Y., Anguita, J., Schoen, R. T., Medzhitov, R., Fikrig, E., and Flavell, R. A. (2002) Hyporesponsive-ness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1-and TLR2-deficient mice. Nat Med. 8, 878-884
25. Kirsch, R. D., and Joly, E. (1998) An improved PCR mutagenesis strategy for two-site mutagenesis or sequence swapping between related genes. Nucleic Acids Res. 26, 1848-1850
26. +-pyrophosphatase expressed in yeast. Bot. Stud. 50, 291-301
27. Gasparian, M. E., Bychkov, M. L., Dolgikh, D. A., and Kirpichnikov, M. P. (2011) Strategy for improvement of enteropeptidase efficiency in tag removal processes. Protein Expr. Purif 79, 191-196
28. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Res. 22, 4673-4680
29. Sharma, Y., Rao, C. M., Rao, S. C, Krishna, A. G., Somasundaram, T., and Balasubramanian, D. (1989) Calcium ion binding to crystallins: the presence of the EF-hand motif in S-crystallin that aids in calcium ion binding. J. Biol. Chem. 264, 20923-20927
30. Lin, Y. P., Raman, R., Sharma, Y., and Chang, Y. F. (2008) Calcium binds to leptospiral immunoglobulin-like protein, LigB, and modulates fibronectin binding. J. Biol. Chem. 283, 25140-25149
31. Rajini, B., Shridas, P., Sundari, C. S., Muralidhar, D., Chandani, S., Thomas, F., and Sharma, Y. (2001) Calcium binding properties of 7-crystallin: calcium ion binds at the Greek key β7-crystallin fold. J. Biol. Chem. 276, 38464-38471
32. Hung, C C, Chang, C. T., Tian, Y. C, Wu, M. S., Yu, C C, Pan, M. J., Vandewalle, A., and Yang, C. W. (2006) Leptospiral membrane proteins stimulate pro-inflammatory chemokines secretion by renal tubule epithelial cells through Toll-like receptor 2 and p38 mitogen-activated protein kinase. Nephrol. Dial. Transplant. 21, 898-910
33. Yang, C. W., Hung, C C, Wu, M. S., Tian, Y. C, Chang, C. T., Pan, M. J., and Vandewalle, A. (2006) Toll-like receptor 2 mediates early inflammation by leptospiral outer membrane proteins in proximal tubule cells. Kidney Int. 69, 815-822
34. Pathirana, R. D., O'Brien-Simpson, N. M., Veith, P. D., Riley, P. F., and Reynolds, E. C. (2006) Characterization of proteinase-adhesin complexes of Porphyromonas gingivalis. Microbiology 152, 2381-2394
35. Brosh, R. M., Jr., Li, J. L., Kenny, M. K., Karow, J. K., Cooper, M. P., Ku-reekattil, R. P., Hickson, I. D., and Bohr, V. A. (2000) Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275, 23500-23508
36. Allen, S., Chen, X., Davies, J., Davies, M. C, Dawkes, A. C, Edwards, J. C, Roberts, C. J., Sefton, J., Tendler, S. J., and Williams, P. M. (1997) Detection of antigen-antibody binding events with the atomic force microscope. Biochemistry 36, 7457-7463
37. Wang, H., Bash, R., Yodh, J. G., Hager, G. L., Lohr, D., and Lindsay, S. M. (2002) Glutaraldehyde modified mica: a new surface for atomic force microscopy of chromatin. Biophys. J. 83, 3619-3625
38. Stroh, C., Wang, H., Bash, R., Ashcroft, B., Nelson, J., Gruber, H., Lohr, D., Lindsay, S. M., and Hinterdorfer, P. (2004) Single-molecule recognition imaging microscopy. Proc. Natl. Acad. Sci. U. S. A. 101, 12503-12507
39. Kim, H., Arakawa, H., Hatae, N., Sugimoto, Y., Matsumoto, O., Osada, T., Ichikawa, A., and Ikai, A. (2006) Quantification of the number of EP3 receptors on a living CHO cell surface by the AFM. Ultramicroscopy 106, 652-662
40. + antiporter-deficient strains by the overex-pressed gene. J. Biol. Chem. 268, 11296-11303