Molecular characterization and subcellular localization of macrophage infectivity potentiator, a Chlamydia trachomatis lipoprotein

Journal of Bacteriology

Volumn 189, Issue 13, 2007, Pages 4739-4748

  Neff, Laurence ^a,b   Daher, Sawsan ^c   Muzzin, Patrick ^b   Spenato, Ursula ^a   Gülaçar, Fazil ^c   Gabay, Cem ^a,b   Bas, Sylvette ^a,d  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; GLOBOMYCIN; GLYCEROL DERIVATIVE; LIPOPROTEIN; PALMITIC ACID;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; BIOTINYLATION; CELLULAR DISTRIBUTION; CHLAMYDIA TRACHOMATIS; FATTY ACID METABOLISM; IMMUNOPRECIPITATION; ISOTOPE LABELING; MACROPHAGE ACTIVATION; METHANOLYSIS; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; COMPUTATIONAL BIOLOGY; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIPOPROTEINS; MOLECULAR SEQUENCE DATA; PALMITIC ACID; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID;

CHLAMYDIA TRACHOMATIS; PROKARYOTA;

EID: 34347375108     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01889-06     Document Type: Article

References (73)

1. Bas, S., P. Muzzin, B. Ninet, J. E. Bornand, C. Scieux, and T. L. Vischer. 2001. Chlamydial serology: comparative diagnostic value of immunoblotting, microimmunofluorescence test, and immunoassays using different recombinant proteins as antigens. J. Clin. Microbiol. 39:1368-1377.
2. Bavoil, P., R. S. Stephens, and S. Falkow. 1990. A soluble 60 kiloDalton antigen of Chlamydia spp. is a homologue of Escherichia coli GroEL. Mol. Microbiol. 4:461-469.
3. Bidawid, S., S. Chou, C. W. Ng, E. Perry, and S. Kasatiya. 1989. Fatty acid profiles of Chlamydia using capillary gas chromatography. Antonie Leeuwenhoek 55:123-131.
4. Blanco, D. R., K. Reimann, J. Skare, C. I. Champion, D. Foley, M. M. Exner, R. E. Hancock, J. N. Miller, and M. A. Lovett. 1994. Isolation of the outer membranes from Treponema pallidum and Treponema vincentii. J. Bacteriol. 176:6088-6099.
5. Boleti, H., A. Benmerah, D. M. Ojcius, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Chlamydia infection of epithelial cells expressing dynamin and Eps15 mutants: clathrin-independent entry into cells and dynamin-dependent productive growth. J. Cell Sci. 112:1487-1496.
6. Bouchon, B., M. Klein, R. Bischoff, A. Van Dorsselaer, and C. Roitsch. 1997. Analysis of the lipidated recombinant outer surface protein A from Borrelia burgdorferi by mass spectrometry. Anal. Biochem. 246:52-61.
7. Bouchon, B., A. Van Dorsselaer, and C. Roitsch. 1993. Characterization of multiple acylation sites on a recombinant protein by electrospray mass spectrometry. Biol. Mass Spectrom. 22:358-360.
8. Brightbill, H. D., D. H. Libraty, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, P. J. Brennan, B. R. Bloom, P. J. Godowski, and R. L. Modlin. 1999. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285:732-736.
9. Brusca, J. S., A. W. McDowall, M. V. Norgard, and J. D. Radolf. 1991. Localization of outer surface proteins A and B in both the outer membrane and intracellular compartments of Borrelia burgdorferi. I. Bacteriol. 173: 8004-8008.
10. Caldwell, H. D., J. Kromhout, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:1161-1176.
11. Centers for Disease Control and Prevention. 1997. Chlamydia trachomatis genital infections - United States, 1995. JAMA 277:952-953.
12. Corsaro, D., and G. Greub. 2006. Pathogenic potential of novel chlamydiae and diagnostic approaches to infections due to these obligate [sic] intracellular bacteria. Clin. Microbiol. Rev. 19:283-297.
13. Cullen, P. A., M. Lo, D. M. Bulach, S. J. Cordwell, and B. Adler. 2003. Construction and evaluation of a plasmid vector for the expression of recombinant lipoproteins in Escherichia coli. Plasmid 49:18-29.
14. De, B. K., J. S. Sampson, E. W. Ades, R. C. Huebner, D. L. Jue, S. E. Johnson, M. Espina, A. R. Stinson, D. E. Briles, and G. M. Carlone. 2000. Purification and characterization of Streptococcus pneumoniae palmitoylated pneumococcal surface adhesin A expressed in Escherichia coli. Vaccine 18: 1811-1821.
15. De, B. K., A. R. Woolfitt, J. R. Barr, M. I. Daneshvar, J. S. Sampson, E. W. Ades, and G. M. Carlone. 2003. Analysis of recombinant acylated pneumococcal surface adhesin A of Streptococcus pneumoniae by mass spectrometry. Arch. Biochem. Biophys. 419:147-157.
16. Driessen, A. J., P. Fekkes, and J. P. van der Wolk. 1998. The Sec system. Curr. Opin. Microbiol. 1:216-222.
17. Erdile, L. F., M. A. Brandt, D. J. Warakomski, G. J. Westrack, A Sadziene, A. G. Barbour, and J. P. Mays. 1993. Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect. Immun. 61:81-90.
18. Everett, K. D., and T. P. Hatch. 1995. Architecture of the cell envelope of Chlamydia psittaci 6BC. J. Bacteriol. 177:877-882.
19. Fan, V. S., and H. M. Jenkin. 1974. Lipid metabolism of monkey kidney cells (LLC-MK-2) infected with Chlamydia trachomatis strain lymphogranuloma venereum. Infect. Immun. 10:464-470.
20. Filip, C., G. Fletcher, J. L. Wulff, and C. F. Earhart. 1973. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 115:717-722.
21. Flo, T. H., O. Halaas, E. Lien, L. Ryan, G. Teti, D. T. Golenbock, A. Sundan, and T. Espevik. 2000. Human toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B streptococci or lipopolysaccharide. J. Immunol. 164:2064-2069.
22. Gaston, J. S. 2000. Immunological basis of Chlamydia induced reactive arthritis. Sex. Transm. Infect. 76:156-161.
23. Haake, D. A. 2000. Spirochaetal lipoproteins and pathogenesis. Microbiology 146:1491-1504.
24. Hahn, D. L., R. W. Dodge, and R. Golubjatnikov. 1991. Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA 266:225-230.
25. Hantke, K., and V. Braun. 1973. Covalent binding of lipid to protein. Diglyceride and amide-linked fatty acid at the N-terminal end of the murein-lipoprotein of the Escherichia coli outer membrane. Eur. J. Biochem. 34: 284-296.
26. Hayashi, S., and H. C. Wu. 1990. Lipoproteins in bacteria. J. Bioenerg. Biomembr. 22:451-471.
27. Hefty, P. S., S. E. Jolliff, M. J. Caimano, S. K. Wikel, and D. R. Akins. 2002. Changes in temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 70:3468-3478.
28. Horn, M., A. Collingro, S. Schmitz-Esser, C. L. Beier, U. Purkhold, B. Fartmann, P. Brandt, G. J. Nyakatura, M. Droege, D. Frishman, T. Rattei, H. W. Mewes, and M. Wagner. 2004. Illuminating the evolutionary history of chlamydiae. Science 304:728-730.
29. Huang, X. Q., R. C. Hardison, and W. Miller. 1990. A space-efficient algorithm for local similarities. Comput. Appl. Biosci. 6:373-381.
30. Hulo, N., C. J. Sigrist, V. Le Saux, P. S. Langendijk-Genevaux, L. Bordoli, A. Gattiker, E. De Castro, P. Bucher, and A. Bairoch. 2004. Recent improvements to the PROSITE database. Nucleic Acids Res. 32:D134-D137.
31. Inukai, M., M. Takeuchi, K. Shimizu, and M. Arai. 1978. Mechanism of action of globomycin. J. Antibiot. (Tokyo) 31:1203-1205.
32. Jin, S., Y. C. Song, A. Emili, P. M. Sherman, and V. L. Chan. 2003. JlpA of Campylobacter jejuni interacts with surface-exposed heat shock protein 90α and triggers signalling pathways leading to the activation of NF-κB and p38 MAP kinase in epithelial cells. Cell. Microbiol. 5:165-174.
33. Juncker, A. S., H. Willenbrock, G. Von Heijne, S. Brunak, H. Nielsen, and A. Krogh. 2003. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12:1652-1662.
34. Kalayoglu, M. V., P. Libby, and G. I. Byrne. 2002. Chlamydia pneumoniae as an emerging risk factor in cardiovascular disease. JAMA 288:2724-2731.
35. Kalman, S., W. Mitchell, R. Marathe, C. Lammel, J. Fan, R. W. Hyman, L. Olinger, J. Grimwood, R. W. Davis, and R. S. Stephens. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21:385-389.
36. Legrain, M., D. Speck, and E. Jacobs. 1995. Production of lipidated meningococcal transferrin binding protein 2 in Escherichia coli. Protein Expr. Purif. 6:570-578.
37. Longbottom, D., M. Russell, S. M. Dunbar, G. E. Jones, and A. J. Herring. 1998. Molecular cloning and characterization of the genes coding for the highly immunogenic cluster of 90-kilodalton envelope proteins from the Chlamydia psittaci subtype that causes abortion in sheep. Infect. Immun. 66:1317-1324.
38. Lundemose, A. G., S. Birkelund, S. J. Fey, P. M. Larsen, and G. Christiansen. 1991. Chlamydia trachomatis contains a protein similar to the Legionella pneumophila mip gene product. Mol. Microbiol. 5:109-115.
39. Lundemose, A. G., S. Birkelund, P. M. Larsen, S. J. Fey, and G. Christiansen. 1990. Characterization and identification of early proteins in Chlamydia trachomatis serovar L2 by two-dimensional gel electrophoresis. Infect. Immun. 58:2478-2486.
40. Lundemose, A. G., J. E. Kay, and J. H. Pearce. 1993. Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol. Microbiol. 7:777-783.
41. Lundemose, A. G., D. A. Rouch, S. Birkelund, G. Christiansen, and J. H. Pearce. 1992. Chlamydia trachomatis Mip-like protein. Mol. Microbiol. 6:2539-2548.
42. Lundemose, A. G., D. A. Rouch, C. W. Penn, and J. H. Pearce. 1993. The Chlamydia trachomatis Mip-like protein is a lipoprotein. J. Bacteriol. 175: 3669-3671.
43. Mabey, D. C., A. W. Solomon, and A. Foster. 2003. Trachoma. Lancet 362:223-229.
44. Madan Babu, M., and K. Sankaran. 2002. DOLOP - database of bacterial lipoproteins. Bioinformatics 18:641-643.
45. Montigiani, S., F. Falugi, M. Scarselli, O. Finco, R. Petracca, G. Galli, M. Mariani, R. Manetti, M. Agnusdei, R. Cevenini, M. Donati, R. Nogarotto, N. Norais, I. Garaguso, S. Nuti, G. Saletti, D. Rosa, G. Ratti, and G. Grandi. 2002. Genomic approach for analysis of surface proteins in Chlamydia pneumoniae. Infect. Immun. 70:368-379.
46. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143-190.
47. Olson, E. N., D. A. Towler, and L. Glaser. 1985. Specificity of fatty acid acylation of cellular proteins. J. Biol. Chem. 260:3784-3790.
48. Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734-740.
49. Pal, S., I. Theodor, E. M. Peterson, and L. M. de la Maza. 1997. Immunization with an acellular vaccine consisting of the outer membrane complex of Chlamydia trachomatis induces protection against a genital challenge. Infect. Immun. 65:3361-3369.
50. Probert, W. S., and B. J. Johnson. 1998. Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol. Microbiol. 30:1003-1015.
51. Radolf, J. D., L. L. Arndt, D. R. Akins, L. L. Curetty, M. E. Levi, Y. Shen, L. S. Davis, and M. V. Norgard. 1995. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154:2866-2877.
52. Read, T. D., R. C. Brunham, C. Shen, S. R. Gill, J. F. Heidelberg, O. White, E. K. Hickey, J. Peterson, T. Utterback, K. Berry, S. Bass, K. Linher, J. Weidman, H. Khouri, B. Craven, C. Bowman, R. Dodson, M. Gwinn, W. Nelson, R. DeBoy, J. Kolonay, G. McClarty, S. L. Salzberg, J. Eisen, and C. M. Fraser. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397-1406.
53. Read, T. D., G. S. Myers, R. C. Brunham, W. C. Nelson, I. T. Paulsen, J. Heidelberg, E. Holtzapple, H. Khouri, N. B. Federova, H. A. Carty, L. A. Umayam, D. H. Haft, J. Peterson, M. J. Beanan, O. White, S. L. Salzberg, R. C. Hsia, G. McClarty, R. G. Rank, P. M. Bavoil, and C. M. Fraser. 2003. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31:2134-2147.
54. Reindl, M., B. Redl, and G. Stoffler. 1993. Isolation and analysis of a linear plasmid-located gene of Borrelia burgdorferi B29 encoding a 27 kDa surface lipoprotein (P27) and its overexpression in Escherichia coli. Mol. Microbiol. 8:1115-1124.
55. Rockey, D. D., B. B. Chesebro, R. A. Heinzen, and T. Hackstadt. 1996. A 28 kDa major immunogen of Chlamydia psittaci shares identity with Mip proteins of Legionella spp. and Chlamydia trachomatis - cloning and characterization of the C. psittaci mip-like gene. Microbiology 142:945-953.
56. Sankaran, K., and H. C. Wu. 1994. Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J. Biol. Chem. 269:19701-19706.
57. Schulze, R. J., and W. R. Zuckert. 2006. Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol. Microbiol. 59:1473-1484.
58. Shang, E. S., T. A. Summers, and D. A. Haake. 1996. Molecular cloning and sequence analysis of the gene encoding LipL41, a surface-exposed lipoprotein of pathogenic Leptospira species. Infect. Immun. 64:2322-2330.
59. Shirai, M., H. Hirakawa, M. Kimoto, M. Tabuchi, F. Kishi, K. Ouchi, T. Shiba, K. Ishii, M. Hattori, S. Kuhara, and T. Nakazawa. 2000. Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res. 28:2311-2314.
60. Shuto, T., H. Xu, B. Wang, J. Han, H. Kai, X. X. Gu, T. F. Murphy, D. J. Lim, and J. D. Li. 2001. Activation of NF-κB by nontypeable Haemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKKα/β-IκBα and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc. Natl. Acad. Sci. USA 98:8774-8779.
61. Skare, J. T., T. A. Mirzabekov, E. S. Shang, D. R. Blanco, H. Erdjument-Bromage, J. Bunikis, S. Bergstrom, P. Tempst, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1997. The Oms66 (p66) protein is a Borrelia burgdorferi porin. Infect. Immun. 65:3654-3661.
62. Stephens, R. S. 2003. The cellular paradigm of chlamydial pathogenesis. Trends Microbiol. 11:44-51.
63. Stephens, R. S., S. Kalman, C. Lammel, J. Fan, R. Marathe, L. Aravind, W. Mitchell, L. Olinger, R. L. Tatusov, Q. Zhao, E. V. Koonin, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
64. Stoll, H., J. Dengjel, C. Nerz, and F. Gotz. 2005. Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immun. 73:2411-2423.
65. Takeuchi, O., A. Kaufmann, K. Grote, T. Kawai, K. Hoshino, M. Morr, P. F. Muhlradt, and S. Akira. 2000. Preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164:554-557.
66. Tanzer, R. J., and T. P. Hatch. 2001. Characterization of outer membrane proteins in Chlamydia trachomatis LGV serovar L2. J. Bacteriol. 183:2686-2690.
67. Tanzer, R. J., D. Longbottom, and T. P. Hatch. 2001. Identification of polymorphic outer membrane proteins of Chlamydia psittaci 6BC. Infect. Immun. 69:2428-2434.
68. Thoma-Uszynski, S., S. Stenger, O. Takeuchi, M. T. Ochoa, M. Engele, P. A. Sieling, P. F. Barnes, M. Rollinghoff, P. L. Bolcskei, M. Wagner, S. Akira, M. V. Norgard, J. T. Belisle, P. J. Godowski, B. R. Bloom, and R. L. Modlin. 2001. Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 291:1544-1547.
69. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 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.
70. Turner, S., E. Reid, H. Smith, and J. Cole. 2003. A novel cytochrome c peroxidase from Neisseria gonorrhoeae: a lipoprotein from a Gram-negative bacterium. Biochem. J. 373:865-873.
71. Yakushi, T., K. Masuda, S. Narita, S. Matsuyama, and H. Tokuda. 2000. A new ABC transporter mediating the detachment of lipid-modified proteins from membranes. Nat. Cell Biol. 2:212-218.
72. Yamaguchi, K., F. Yu, and M. Inouye. 1988. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53:423-432.
73. Zuckert, W. R., J. E. Lloyd, P. E. Stewart, P. A. Rosa, and A. G. Barbour. 2004. Cross-species surface display of functional spirochetal lipoproteins by recombinant Borrelia burgdorferi. Infect. Immun. 72:1463-1469.