Lipoprotein LprI of mycobacterium tuberculosis acts as a lysozyme inhibitor

Journal of Biological Chemistry

Volumn 291, Issue 6, 2016, Pages 2938-2953

  Sethi, Deepti ^a   Mahajan, Sahil ^a   Singh, Chaahat ^a   Lama, Amrita ^a   Hade, Mangesh Dattu ^a   Gupta, Pawan ^a   Dikshit, Kanak L ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; BACTERIA; CELL CULTURE; ESCHERICHIA COLI; GENE ENCODING; GENE EXPRESSION; GENES; IMMUNOLOGY; LIPOPROTEINS; MACROPHAGES; TUBES (COMPONENTS);

DEFENSE STRATEGY; INTRACELLULAR SURVIVAL; LYSOZYME INHIBITOR; M. TUBERCULOSIS; MONOCYTE-DERIVED MACROPHAGES; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; SECONDARY CELLS;

ENZYMES;

BACTERIAL PROTEIN; LPRI PROTEIN; UNCLASSIFIED DRUG; ENZYME INHIBITOR; LIPOPROTEIN; LYSOZYME; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION; LPRI GENE; MICROCOCCUS LUTEUS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CHEMISTRY; GENETICS; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; ENZYME INHIBITORS; LIPOPROTEINS; MACROPHAGES; MICE; MURAMIDASE; MYCOBACTERIUM TUBERCULOSIS; RECOMBINANT PROTEINS;

EID: 84958211633     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.662593     Document Type: Article

References (62)

1. World Health Organization (2013) Global Tuberculosis Report 2013, World Health Organization, Geneva.
2. Ahmad, S. (2011) Pathogenesis, immunology, and diagnosis of latent Mycobacterium tuberculosis infection. Clin. Dev. Immunol. 2011, 814943.
3. Torrelles, J. B. (2012) Broadening our view about the role of Mycobacterium tuberculosis cell envelope components during infection: A battle for survival. in Understanding Tuberculosis-Analyzing the Origin of Mycobacterium tuberculosis Pathogenicity (Cardona, P.-J., ed) pp. 77-122, In- Tech, Rijeka, Croatia.
4. Sander, P., Rezwan, M., Walker, B., Rampini, S. K., Kroppenstedt, R. M., Ehlers, S., Keller, C., Keeble, J. R., Hagemeier, M., and Colston, M. J. (2004) Lipoprotein processing is required for virulence of Mycobacterium tuberculosis. Mol. Microbiol. 52, 1543-1552.
5. Sutcliffe, I. C., and Harrington, D. J. (2004) Lipoproteins of Mycobacterium tuberculosis: An abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 28, 645-659.
6. Nguyen, H. T., Wolff, K. A., Cartabuke, R. H., Ogwang, S., and Nguyen, L. (2010) A lipoprotein modulates activity of the MtrAB two-component system to provide intrinsic multidrug resistance, cytokinetic control and cell wall homeostasis in mycobacterium. Mol. Microbiol. 76, 348-364.
7. Couture, M., Yeh, S. R., Wittenberg, B. A., Wittenberg, J. B., Ouellet, Y., Rousseau, D. L., and Guertin, M. (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 96, 11223-11228.
8. Pathania, R., Navani, N. K., Gardner, A. M., Gardner, P. R., and Dikshit, K. L. (2002) Nitric oxide scavenging and detoxification by the Mycobacterium tuberculosis haemoglobin, HbN in Escherichia coli. Mol. Microbiol. 45, 1303-1314.
9. Ouellet, H., Ouellet, Y., Richard, C., Labarre, M., Wittenberg, B., Wittenberg, J., and Guertin, M. (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 99, 5902-5907.
10. Lama, A., Pawaria, S., and Dikshit, K. L. (2006) Oxygen binding and NO scavenging properties of truncated hemoglobin, HbN, of Mycobacterium smegmatis. FEBS Lett. 580, 4031-4041.
11. Arya, S., Sethi, D., Singh, S., Hade, M. D., Singh, V., Raju, P., Chodisetti, S. B., Verma, D., Varshney, G. C., Agrewala, J. N., and Dikshit, K. L. (2013) Truncated hemoglobin, HbN, is post-translationally modified in Mycobacterium tuberculosis and modulates host-pathogen interactions during intracellular infection. J. Biol. Chem. 288, 29987-29999.
12. Farrow, M. F., and Rubin, E. J. (2008) Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein. J. Bacteriol. 190, 1783-1791.
13. Callewaert, L., Aertsen, A., Deckers, D., Vanoirbeek, K. G., Vanderkelen, L., Van Herreweghe, J. M., Masschalck, B., Nakimbugwe, D., Robben, J., and Michiels, C. W. (2008) A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog. 4, e1000019.
14. Cohn, Z. A., and Wiener, E. (1963) The particulate hydrolases of macrophages. I. Comparative enzymology, isolation, and properties. J. Exp. Med. 118, 991-1008.
15. Sorber, W. A., Leake, E. S., and Myrvik, Q. N. (1973) Comparative densities of hydrolase-containing granules from normal and BCG-induced alveolar macrophages. Infect. Immun. 7, 86-92.
16. Keshav, S., Chung, P., Milon, G., and Gordon, S. (1991) Lysozyme is an inducible marker of macrophage activation in murine tissues as demon-strated by in situ hybridization. J. Exp. Med. 174, 1049-1058.
17. Near, K. A., and Lefford, M. J. (1992) Use of serum antibody and lysozyme levels for diagnosis of leprosy and tuberculosis. J. Clin. Microbiol. 30, 1105-1110.
18. Jena, P., Mohanty, S., Mohanty, T., Kallert, S., Morgelin, M., Lindstrøm, T., Borregaard, N., Stenger, S., Sonawane, A., and Sørensen, O. E. (2012) Azurophil granule proteins constitute the major mycobactericidal proteins in human neutrophils and enhance the killing of mycobacteria in macrophages. PLoS One 7, e50345.
19. Callewaert, L., Van Herreweghe, J. M., Vanderkelen, L., Leysen, S., Voet, A., and Michiels, C. W. (2012) Guards of the great wall: bacterial lysozyme inhibitors. Trends Microbiol. 20, 501-510.
20. Daigle, F., Graham, J. E., and Curtiss, R. 3rd. (2001) Identification of Salmonella typhi genes expressed within macrophages by selective capture of transcribed sequences (SCOTS). Mol. Microbiol. 41, 1211-1222.
21. Voet, A., Callewaert, L., Ulens, T., Vanderkelen, L., Vanherreweghe, J. M., Michiels, C. W., and De Maeyer, M. (2011) Structure based discovery of small molecule suppressors targeting bacterial lysozyme inhibitors. Biochem. Biophys. Res. Commun. 405, 527-532.
22. Kanetsuna, F. (1980) Effect of lysozyme on mycobacteria. Microbiol. Immunol. 24, 11511162.
23. Myrvik, Q. N., Weiser, R. S. and Agar, H. D. (1953) Lethal and cytologic effects of lysozyme on tubercle bacilli. Am. Rev. Tuberc. 67, 217-231.
24. Callewaert, L., and Michiels, C. W. (2010) Lysozymes in the animal kingdom. J. Biosci. 35, 127-160.
25. de Castro, E., Sigrist, C. J., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P. S., Gasteiger, E., Bairoch, A., and Hulo, N. (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362-W365.
26. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., (2004) The Pfam protein families database. Nucleic Acids Res. 32, D138-D141.
27. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gramnegative bacteria. Protein Sci. 12, 1652-1662.
28. Madan Babu, M., and Sankaran, K. (2002) DOLOP-database of bacterial lipoproteins. Bioinformatics 18, 641-643.
29. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40.
30. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
31. DeLano, W. L. (2012) The PyMOL Molecular Graphics System, Schrödinger, LLC, New York.
32. Mawuenyega, K. G., Forst, C. V., Dobos, K. M., Belisle, J. T., Chen, J., Bradbury, E. M., Bradbury, A. R., and Chen, X. (2005) Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol. Biol. Cell 16, 396-404.
33. Bordier, C. (1981) Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256, 1604-1607.
34. Severin, A., Nickbarg, E., Wooters, J., Quazi, S. A., Matsuka, Y. V., Murphy, E., Moutsatsos, I. K., Zagursky, R. J., and Olmsted, S. B. (2007) Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J. Bacteriol. 189, 1514-1522.
35. Helal, R., and Melzig, M. (2008) Determination of lysozyme activity by a fluorescence technique in comparison with the classical turbidity assay. Pharmazie 63, 415-419.
36. Mahajan, S., Saini, A., Chandra, V., Nanduri, R., Kalra, R., Bhagyaraj, E., Khatri, N., and Gupta, P. (2015) Nuclear receptor Nr4a2 promotes alternative polarization of macrophages and confer protection in sepsis. J. Biol. Chem. 290, 18304-18314.
37. Dkhar, H. K., Nanduri, R., Mahajan, S., Dave, S., Saini, A., Somavarapu, A. K., Arora, A., Parkesh, R., Thakur, K. G., Mayilraj, S., and Gupta, P. (2014) Mycobacterium tuberculosis keto-mycolic acid and macrophage nuclear receptor TR4 modulate foamy biogenesis in granulomas: A case of a heterologous and noncanonical ligand-receptor pair. J. Immunol. 193, 295-305.
38. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E. 3rd, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544.
39. Yum, S., Kim, M. J., Xu, Y., Jin, X. L., Yoo, H. Y., Park, J. W., Gong, J. H., Choe, K. M., Lee, B. L., and Ha, N. C. (2009) Structural basis for the recognition of lysozyme by MliC, a periplasmic lysozyme inhibitor in Gram-negative bacteria. Biochem. Biophys. Res. Commun. 378, 244-248.
40. Kopácek, P., Vogt, R., Jindrák, L., Weise, C., and Safarík, I. (1999) Purification and characterization of the lysozyme from the gut of the soft tick Ornithodoros moubata. Insect Biochem. Mol. Biol. 29, 989-997.
41. Monchois, V., Abergel, C., Sturgis, J., Jeudy, S., and Claverie, J. M. (2001) Escherichia coli ykfE ORFan gene encodes a potent inhibitor of C-type lysozyme. J. Biol. Chem. 276, 18437-18441.
42. Liu, C.-F., Tonini, L., Malaga, W., Beau, M., Stella, A., Bouyssié, D., Jackson, M. C., Nigou, J., Puzo, G., Guilhot, C., Burlet-Schiltz, O., and Rivière, M. (2013) Bacterial protein-O-mannosylating enzyme is crucial for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 110, 6560-6565.
43. Hansen, J. E., Lund, O., Tolstrup, N., Gooley, A. A., Williams, K. L., Brunak, S. (1998) NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj. J. 15, 115-130.
44. Espitia, C., Servín-González, L., and Mancilla, R. (2010) New insights into protein O-mannosylation in actinomycetes. Mol. BioSyst. 6, 775-781.
45. Bartels, K.-M., Funken, H., Knapp, A., Brocker, M., Bott, M., Wilhelm, S., Jaeger, K.-E., and Rosenau, F. (2011) Glycosylation is required for outer membrane localization of the lectin LecB in Pseudomonas aeruginosa. J. Bacteriol. 193, 1107-1113.
46. Martin, A., Portaels, F., and Palomino, J. C. (2007) Colorimetric redoxindicator methods for the rapid detection of multidrug resistance in Mycobacterium tuberculosis: A systematic review and meta-analysis. J. Antimicrob. Chemother. 59, 175-183.
47. Chaturvedi, V., Dwivedi, N., Tripathi, R. P., and Sinha, S. (2007) Evaluation of Mycobacterium smegmatis as a possible surrogate screen for selecting molecules active against multi-drug resistant Mycobacterium tuberculosis. J. Gen. Appl. Microbiol. 53, 333-337.
48. Garbe, T., Harris, D., Vordermeier, M., Lathigra, R., Ivanyi, J., and Young, D. (1993) Expression of the Mycobacterium tuberculosis 19-kilodalton antigen in Mycobacterium smegmatis: immunological analysis and evidence of glycosylation. Infect. Immun. 61, 260-267.
49. Klockars, M., and Reitamo, S. (1975) Tissue distribution of lysozyme in man. J. Histochem. Cytochem. 23, 932-940.
50. Dajani, R., Zhang, Y., Taft, P. J., Travis, S. M., Starner, T. D., Olsen, A., Zabner, J., Welsh, M. J., and Engelhardt, J. F. (2005) Lysozyme secretion by submucosal glands protects the airway from bacterial infection. Am. J. Respir. Cell Mol. Biol. 32, 548-552.
51. Kasukabe, T., Honma, Y., and Hozumi, M. (1979) Characterization of lysozyme synthesized by differentiated mouse myeloid leukemia cells. Biochim. Biophys. Acta 586, 615-623.
52. Smith, J. B., Hassan, N. F., Douglas, S. D., and Polin, R. A. (1991) Effects of indomethacin and prostaglandin E1 on the production of fibronectin and lysozyme by monocyte-derived macrophages in vitro. J. Clin. Lab Immunol. 35, 147-155.
53. Vanderkelen, L., Van Herreweghe, J. M., Vanoirbeek, K. G., Baggerman, G., Myrnes, B., Declerck, P. J., Nilsen, I. W., Michiels, C. W., and Callewaert, L. (2011) Identification of a bacterial inhibitor against g-type lysozyme. Cell. Mol. Life Sci. 68, 1053-1064.
54. Um, S.-H., Kim, J.-S., Kim, K., Kim, N., Cho, H.-S., and Ha, N.-C. (2013) Structural basis for the inhibition of human lysozyme by PliC from Brucella abortus. Biochemistry 52, 9385-9393.
55. Haneberg, B., Glette, J., Talstad, I., Sørnes, S., and Solberg, C. (1984) In vitro release of lysozyme from monocytes and granulocytes. J. Leukoc. Biol. 35, 573-582.
56. Dubnau, E., Chan, J., Mohan, V. P., and Smith, I. (2005) Responses of Mycobacterium tuberculosis to growth in the mouse lung. Infect. Immun. 73, 3754-3757.
57. Ralph, P., Moore, M. A., and Nilsson, K. (1976) Lysozyme synthesis by established human and murine histiocytic lymphoma cell lines. J. Exp. Med. 143, 1528-1533.
58. Raschke, W. C., Baird, S., Ralph, P., and Nakoinz, I. (1978) Functional macrophage cell lines transformed by Abelson leukemia virus. Cell 15, 261-267.
59. Davis, K. M., Akinbi, H. T., Standish, A. J., and Weiser, J. N. (2008) Resistance to mucosal lysozyme compensates for the fitness deficit of peptidoglycan modifications by Streptococcus pneumoniae. PLoS Pathog. 4, e1000241.
60. Klockars, M., Pettersson, T., Riska, H., Hellström, P.-E., and Norhagen, A. (1979) Pleural fluid lysozyme in human disease. Arch. Intern. Med. 139, 73-77.
61. Herrmann, J. L., O'Gaora, P., Gallagher, A., Thole, J. E., and Young, D. B. (1996) Bacterial glycoproteins: A link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J. 15, 3547-3554.
62. Gut, A., Kappeler, F., Hyka, N., Balda, M. S., Hauri, H. P., and Matter, K. (1998) Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J. 17, 1919-1929.