1887

Abstract

Lipoproteins are a functionally diverse class of secreted bacterial proteins characterized by an N-terminal lipid moiety. The lipid moiety serves to anchor these proteins to the cell surface. Lipoproteins are synthesized as pre-prolipoproteins and mature by post-translational modifications. The post-translational modifications are directed by the lipobox motif located within the signal peptide. Enzymes involved in lipoprotein synthesis are essential in Gram-negative bacteria but not in Gram-positve bacteria. Inactivation of genes involved in lipoprotein synthesis attenuates a variety of Gram-positive pathogens, including . The attenuated phenotype of these mutants indicates an important role of lipoproteins and lipoprotein synthesis in bacterial virulence. , the causative agent of tuberculosis, is one of the most devastating pathogens in the world. This article reviews recent findings on the synthesis, localization and function of lipoproteins in mycobacteria.

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2007-03-01
2024-03-28
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References

  1. Babu M. M., Priya M. L., Selvan A. T., Madera M., Gough J., Aravind L., Sankaran K. 2006; A database of bacterial lipoproteins (DOLOP) with functional assignments to predict lipoproteins. J Bacteriol 188:2761–2773 [CrossRef]
    [Google Scholar]
  2. Banaiee N., Kincaid E. Z., Buchwald U., Jacobs W. R., Ernst J. D. 2006; Potent inhbition of macrophage responses to IFN- γ by live virulent Mycobacterium tuberculosis is independent of mature lipoproteins but dependent on TLR2. J Immunol 176:3019–3027 [CrossRef]
    [Google Scholar]
  3. Baulard A. R., Gurcha S. S., Engohang-Ndong J., Gouffi K., Locht C., Besra G. S. 2003; In vivo interaction between the polyprenol phosphate mannose synthase Ppm1 and the integral membrane protein Ppm2 from Mycobacterium smegmatis revealed by a bacterial two-hybrid system. J Biol Chem 278:2242–2248 [CrossRef]
    [Google Scholar]
  4. Bigi F., Gioffre A., Klepp L., Santangelo M. P., Alito A., Caimi K., Meikle V., Zamarrago M. other authors 2004; The knockout of the lprG-Rv1410 operon produces strong attenuation of Mycobacterium tuberculosis . Microbes Infect 6:182–187 [CrossRef]
    [Google Scholar]
  5. Boshoff H. I., Myer T. G., Copp B. R., McNeil M. R., Wilson M. A., Barry C. E. 2004; The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem 279:40174–40184 [CrossRef]
    [Google Scholar]
  6. Brennan P. J., Nikaido H. 1995; The envelope of mycobacteria. Annu Rev Biochem 64:29–63 [CrossRef]
    [Google Scholar]
  7. Diaz-Silvestre H., Espinosa-Cueto P., Sanchez-Gonzalez A., Esparza-Ceron M. A., Pereira-Suarez A. L., Bernal-Fernandez G., Espitia C., Mancilla R. 2005; The 19-kDa antigen of Mycobacterium tuberculosis is a major adhesin that binds the mannose receptor of THP-1 monocytic cells and promotes phagocytosis of mycobacteria. Microb Pathog 39:97–107 [CrossRef]
    [Google Scholar]
  8. Gao B., Paramanathan R., Gupta R. S. 2006; Signature proteins that are distinctive characteristics of Actinobacteria and their subgroups. Antonie van Leeuwenhoek 90:69–91 [CrossRef]
    [Google Scholar]
  9. Gurcha S. S., Baulard A. R., Kremer L., Locht C., Moody D. B., Muhlecker W., Costello C. E., Crick D. C., Brennan P. J., Besra G. S. 2002; Ppm1, a novel polyprenol monophosphomannose synthase from Mycobacterium tuberculosis . Biochem J 365:441–450 [CrossRef]
    [Google Scholar]
  10. Harboe M., Wiker H. G., Ulvund G., Lund-Pedersen B., Andersen A. B., Hewinson R. G., Nagai S. 1998; Mpb70 and Mpb83 as indicators of protein localization in mycobacterial cells. Infect Immun 66:289–296
    [Google Scholar]
  11. Harrington D. J., Greated J. S., Chanter N., Sutcliffe I. C. 2000; Identification of lipoprotein homologues of pneumococcal PsaA in the equine pathogens Streptococcus equi and Streptococcus zooepidemicus . Infect Immun 68:6048–6051 [CrossRef]
    [Google Scholar]
  12. Hoskisson P. A., Hutchings M. I. 2006; MtrAB-LpqB: a conserved three-component system in actinobacteria?. Trends Microbiol 14:444–449 [CrossRef]
    [Google Scholar]
  13. Hovav A.-H., Davidovitch L., Nussbaum G., Mullerad J., Fishman Y., Bercovier H. 2004; Mitogenicity of the recombinant mycobacterial 27-kilodalton lipoprotein is not connected to its antiprotective effect. Infect Immun 72:3383–3390 [CrossRef]
    [Google Scholar]
  14. Inukai M., Nakajima M., Osawa M., Haneishi T., Arai M. 1978; Globomycin, a new peptide antibiotic with spheroblast-forming activity. Isolation and physico-chemical and biological characterization. J Antibiot 31:421–426 [CrossRef]
    [Google Scholar]
  15. Juncker A. S., Willenbrock H., von Heinje G., Nielsen H., Brunak S., Krogh A. 2003; Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12:1652–1662 [CrossRef]
    [Google Scholar]
  16. Karakousis P. C., Bishai W. R., Dorman S. E. 2004; Mycobacterium tuberculosis cell envelope lipids and the host immune response. Cell Microbiol 6:105–116 [CrossRef]
    [Google Scholar]
  17. Keep N. H., Ward J. M., Cohen-Gonsaud M., Henderson B. 2006; Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol 14:271–276 [CrossRef]
    [Google Scholar]
  18. Kiho T., Nakayama M., Ysuda K., Miyakoshi S., Inukai M., Kogen H. 2004; Structure-activity relationships of globomycin analogues as antibiotics. Bioorg Med Chem 12:337–361 [CrossRef]
    [Google Scholar]
  19. Kovacevic S., Anderson D., Morita Y. S., Patterson J., Haites R., McMillan B. N. I., Coppel R., McConville M. J., Billman-Jacobe H. 2006; Identification of a novel protein with a role in lipoarabinomannan biosynthesis in mycobacteria. J Biol Chem 281:9011–9017 [CrossRef]
    [Google Scholar]
  20. Kriakov J., Lee S. H., Jacobs W. R., Jr. 2003; Identification of a regulated alkaline phosphatase, a cell surface-associated lipoprotein, in Mycobacterium smegmatis . J Bacteriol 185:4983–4991 [CrossRef]
    [Google Scholar]
  21. Leskela S., Wahlstrom E., Kontinen V. P., Sarvas M. 1999; Lipid modification of prelipoproteins is dispensable for growth but essential for efficient protein secretion in Bacillus subtilis : characterization of the lgt gene. Mol Microbiol 31:1075–1085 [CrossRef]
    [Google Scholar]
  22. Marland Z., Beddoe T., Zaker-Tabrizi L., Lucet I. S., Brammananth R., Whisstock J. C., Wilce M. C. J., Coppel R. L., Crellin P. K., Rossjohn J. 2006; Hijacking of a substrate-binding protein scaffold for use in mycobacterial cell wall biosynthesis. J Mol Biol 359:983–997 [CrossRef]
    [Google Scholar]
  23. Mawuenyega K. G., Forst C. V., Dobos K. M., Belisle J. T., Chen J., Bradbury E. M., Bradbury A. R. M., Chen X. 2005; Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol Biol Cell 16:396–404
    [Google Scholar]
  24. McDonough J. A., Hacker K. E., Flores A. R., Pavelka M. S., Braunstein M. 2005; The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial lactamases. J Bacteriol 187:7667–7679 [CrossRef]
    [Google Scholar]
  25. Narita S., Matsuyama S., Tokuda H. 2004; Lipoprotein trafficking in Escherichia coli . Arch Microbiol 182:1–6 [CrossRef]
    [Google Scholar]
  26. Peirs P., Lefevre P., Boarbi S., Wang X. M., Denis O., Braibant M., Pethe K., Locht C., Huygen K., Content J. 2005; Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun 73:1898–1902 [CrossRef]
    [Google Scholar]
  27. Rengarajan J., Bloom B. R., Rubin E. J. 2005; Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102:8327–8332 [CrossRef]
    [Google Scholar]
  28. Rezwan M., Laneelle M. A., Sander P., Daffé M. 2006; Breaking down the wall: fractionation of mycobacteria. J Microbiol Methods (in press).
    [Google Scholar]
  29. Rogall T., Wolters J., Flohr T., Böttger E. C. 1990; Towards a phylogeny and definition of species at the molecular level within the genus Mycobacterium . Int J Syst Bacteriol 40:323–330 [CrossRef]
    [Google Scholar]
  30. Romano M., Roupie V., Hamard M., Huygen K. 2006; Evaluation of the immunogenicity of pBudCE4.1 plasmids encoding mycolyl-transferase Ag85A and phosphate transport receptor PstS-3 from Mycobacterium tuberculosis . Vaccine 24:3353–3364 [CrossRef]
    [Google Scholar]
  31. Sander P., Rezwan M., Walker B., Rampini S. K., Kroppenstedt R. M., Ehlers S., Keller C., Keeble R. J., Hagemeier M. other authors 2004; Lipoprotein processing is required for virulence of Mycobacterium tuberculosis . Mol Microbiol 52:1543–1552 [CrossRef]
    [Google Scholar]
  32. Sassetti C. M., Rubin E. J. 2003; Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100:12989–12994 [CrossRef]
    [Google Scholar]
  33. Schulze R. J., Zuckert W. R. 2006; Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol Microbiol 59:1473–1484 [CrossRef]
    [Google Scholar]
  34. Stewart G. R., Wilkinson K. A., Newton S. M., Sullivan S. M., Neyrolles O., Wain J. R., Patel J., Pool K. L., Young D. B., Wilkinson R. J. 2005; Effect of deletion or overexpression of the 19-kilodalton lipoprotein Rv3763 on the innate response to Mycobacterium tuberculosis . Infect Immun 73:6831–6837 [CrossRef]
    [Google Scholar]
  35. Sulzenbacher G., Canaan S., Bordat Y., Neyrolles O., Stadthagen G., Roig-Zamboni V., Rauzier J., Maurin D., Laval F. other authors 2006; LppX is a lipoprotein required for translocation of phthiocerol dimycocerosates to the surface of Mycobacterium tuberculosis . EMBO J 25:1436–1444 [CrossRef]
    [Google Scholar]
  36. Sutcliffe I. C., Harrington D. J. 2004; Lipoproteins of Mycobacterium tuberculosis : an abundant and functionally diverse class of cell envelope components. FEMS Microbiol Rev 28:645–659 [CrossRef]
    [Google Scholar]
  37. Sutcliffe I. C., Russell R. R. B. 1995; Lipoproteins of Gram-positive bacteria. J Bacteriol 177:1123–1128
    [Google Scholar]
  38. Thoma-Uszynski S., Stenger S., Takeuchi O., Ochoa M. T., Engele M., Sieling P. A., Barnes P. F., Röllinghoff M., Bölsckei P. L. other authors 2001; Induction of direct antimicrobial activity through mammalian Toll-like receptors. Science 291:1544–1547 [CrossRef]
    [Google Scholar]
  39. Tokuda H., Matsuyama S.-i. 2004; Sorting of lipoproteins to the outer membrane in E. coli . Biochim Biophys Acta 16935–13 [CrossRef]
    [Google Scholar]
  40. Tufariello J. A. M., Mi K., Xu J., Manabe Y. C., Kesavan A. K., Drumm J., Tanaka K., Jacobs W. R., Chan J. 2006; Deletion of the Mycobacterium tuberculosis resuscitation-promotion factor Rv1009 gene results in delayed reactivation from chronic tuberculosis. Infect Immun 74:2985–2995 [CrossRef]
    [Google Scholar]
  41. Vosloo W., Tippoo P., Hughes J. E., Harriman N., Emms M., Beatty D. W., Zappe H., Steyn L. M. 1997; Characterisation of a lipoprotein in Mycobacterium bovis (BCG) with sequence similarity to the secreted protein MPB70. Gene 188:123–128 [CrossRef]
    [Google Scholar]
  42. Wu H. C. 1996; Biosynthesis of lipoproteins. In Escherichia coli and Salmonella typhimurium pp. 1005–1014 Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  43. Young D. B., Garbe T. 1991; Lipoprotein antigens of Mycobacterium tuberculosis . Res Microbiol 142:55–65 [CrossRef]
    [Google Scholar]
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