Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria chlamydia and wolbachia: Why is lipid II needed?

Molecular Microbiology

Volumn 73, Issue 5, 2009, Pages 913-923

  Henrichfreise, Beate ^a   Schiefer, Andrea ^a   Schneider, Tanja ^a   Nzukou, Edith ^a   Poellinger, Christina ^a   Hoffmann, Theo Julian ^a   Johnston, Kelly L ^b   Moelleken, Katja ^c   Wiedemann, Lmke ^a   Pfarr, Kenneth ^a   Hoerauf, Achim ^a   Sahl, Hans Georg ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; FOSFOMYCIN; LIPID; LIPID II; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CATALYSIS; CELL DIVISION; CELL GROWTH; CELL ISOLATION; CELL MEMBRANE; CELL WALL; CHLAMYDIA; CONTROLLED STUDY; GENOME; IN VITRO SELECTION; LIPOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROKARYOTE; PROKARYOTIC CELL; WOLBACHIA;

ALKYL AND ARYL TRANSFERASES; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; CELL MEMBRANE; CHLAMYDIA; ENZYME INHIBITORS; FOSFOMYCIN; GENES, BACTERIAL; GENES, ESSENTIAL; MODELS, BIOLOGICAL; MONOSACCHARIDES; N-ACETYLGLUCOSAMINYLTRANSFERASES; OLIGOPEPTIDES; TRANSFERASES; URIDINE DIPHOSPHATE N-ACETYLMURAMIC ACID; WOLBACHIA;

CHLAMYDIA; PROKARYOTA; WOLBACHIA;

EID: 70350139038     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06815.x     Document Type: Article

References (41)

1. Bandi, C., McCall, J. W., Genchi, C., Corona, S., Venco, L., and Sacchi, L. (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29: 357-364.
2. Barker, L. F. (1968) Determination of antibiotic susceptibility of Rickettsiae and Chlamydiae. BS-C-1 cell cultures. Antimicrob Agents Chemother (Bethesda) 8: 425-428.
3. Casiraghi, M., McCall, J. W., Simoncini, L., Kramer, L. H., Sacchi, L., Genchi, C., et al. (2002) Tetracycline treatment and sex-ratio distortion: a role for Wolbachia in the moulting of filarial nematodes? Int J Parasitol 32: 1457-1468.
4. Chopra, I., Storey, C., Falla, T. J., and Pearce, J. H. (1998) Antibiotics, peptidoglycan synthesis and genomics: the chlamydial anomaly revisited. Microbiology 144: 2673-2678.
5. Crouvoisier, M., Auger, G., Blanot, D., and Mengin-Lecreulx, D. (2007) Role of the amino acid invariants in the active site of MurG as evaluated by site-directed mutagenesis. Biochimie 89: 1498-1508.
6. Errington, J., Daniel, R. A., and Scheffers, D. J. (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52-65, table of contents.
7. Feldhaar, H., and Gross, R. (2009) Insects as hosts for mutualistic bacteria. Int J Med Microbiol 299: 1-8.
8. Foster, J., Ganatra, M., Kamal, I., Ware, J., Makarova, K., Ivanova, N., et al. (2005) The Wolbachia genome of Brugia malayr. endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: e121.
9. Ghuysen, J. M., and Goffin, C. (1999) Lack of cell wall peptidoglycan versus penicillin sensitivity: new insights into the chlamydial anomaly. Antimicrob Agents Chemother 43: 2339-2344.
10. Gordon, F. B., and Quan, A. L. (1972) Susceptibility of Chlamydia to antibacterial drugs: test in cell cultures. Antimicrob Agents Chemother 2: 242-244.
11. Ha, S., Walker, D., Shi, Y., and Walker, S. (2000) The 1.9 A crystal structure of Escherichia coli MurG, a membraneassociated glycosyltransferase involved in peptidoglycan biosynthesis. Protein Sci. 9: 1045-1052.
12. Hasper, H. E., Kramer, N. E., Smith, J. L., Hillman, J. D., Zachariah, C., Kuipers, O. P., et al. (2006) An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313: 1636-1637.
13. Hesse, L., Bostock, J., Dementin, S., Blanot, D., MenginLecreulx, D., and Chopra, I. (2003) Functional and biochemical analysis of Chlamydia trachomatis MurC, an enzyme displaying UDP-N-acetylmuramate: amino acid ligase activity. J Bacteriol 185: 6507-6512.
14. Hoerauf, A. (2008) Filariasis: new drugs and new opportunities for lymphatic filariasis and onchocerciasis. Curr Opin Infect Dis 21: 673-681.
15. Hoerauf, A., Nissen-Pahle, K., Schmetz, C., Henkle-Duhrsen, K., Blaxter, M. L., Buttner, D. W., et al. (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103: 11-18.
16. Hoerauf, A., Volkmann, L., Hamelmann, C., Adjei, O., Autenrieth, I. B., Fleischer, B., and Buttner, D. W. (2000) Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 355: 1242-1243.
17. Hyde, A. J., Parisot, J., McNichol, A., and Bonev, B. B. (2006) Nisin-induced changes in Bacillus morphology suggest a paradigm of antibiotic action. Proc Natl Acad Sci. USA 103: 19896-19901.
18. Jantos, C. A., Heck, S., Roggendorf, R., Sen-Gupta, M., and Hegemann, J. H. (1997) Antigenic and molecular analyses of different Chlamydia pneumoniae strains. J Clin Microbiol 35: 620-623.
19. McCoy, A. J., and Maurelli, A. T. (2005) Characterization of Chlamydia MurC-Ddl, a fusion protein exhibiting D-alanyl-D-alanine ligase activity involved in peptidoglycan synthesis and D-cycloserine sensitivity. Mol Microbiol 57: 41-52.
20. McCoy, A. J., and Maurelli, A. T. (2006) Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends Microbiol 14: 70-77.
21. McCoy, A. J., Sandlin, R. C., and Maurelli, A. T. (2003) In vitro and in vivo functional activity of Chlamydia MurA, a UDPN-acetylglucosamine enolpyruvyl transferase involved in peptidoglycan synthesis and fosfomycin resistance. J Bacteriol 185: 1218-1228.
22. McCoy, A. J., Adams, N. E., Hudson, A. O., Gilvarg, C., Leustek, T., and Maurelli, A. T. (2006) L,L-diaminopimelate aminotransferase, a trans-kingdom enzyme shared by Chlamydia and plants for synthesis of diaminopimelate/ lysine. Proc Natl Acad Sci. USA 103: 17909-17914.
23. Machida, M., Takechi, K., Sato, H., Chung, S. J., Kuroiwa, H., Takio, S., et al. (2006) Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci. USA 103: 6753-6758.
24. Makepeace, B. L., Rodgers, L., and Trees, A. J. (2006) Rate of elimination of Wolbachia pipientis by doxycycline in vitro increases following drug withdrawal. Antimicrob Agents Chemother 50: 922-927.
25. Moulder, J. W. (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55: 143-190.
26. Moulder, J. W. (1993) Why is Chlamydia sensitive to penicillin in the absence of peptidoglycan? Infect Agents Dis 2: 87-99.
27. Pfarr, K., and Hoerauf, A. (2005) The annotated genome of Wolbachia from the filarial nematode Brugia malayr what it means for progress in antifilarial medicine. PLoS Med 2: e110.
28. Pinho, M. G., and Errington, J. (2005) Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol Microbiol 55: 799-807.
29. Rasgon, J. L., Gamston, C. E., and Ren, X. (2006) Survival of Wolbachia pipientis in cell-free medium. Appl Environ Microbiol 72: 6934-6937.
30. Rick, P. D., Hubbard, G. L., Kitaoka, M., Nagaki, H., Kinoshita, T., Dowd, S., et al. (1998) Characterization of the lipidcarrier involved in the synthesis of enterobacterial common antigen (ECA) and identification of a novel phosphoglyceride in a mutant of Salmonella typhimurium defective in ECA synthesis. Glycobiology 8: 557-567.
31. Scheffers, D. J., and Pinho, M. G. (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69: 585-607.
32. Schneider, T., Senn, M. M., Berger-Bachi, B., Tossi, A., Sahl, H. G., and Wiedemann, I. (2004) In vitro assembly of a complete, pentaglycine interpeptide bridge containing cell wall precursor (lipid II-Gly5) of Staphylococcus aureus. Mol Microbiol 53: 675-685.
33. Schneider, T., Gries, K., Josten, M., Wiedemann, I., Pelzer, S., Labischinski, H., and Sahl, H. G. (2009) The Lipopeptide Antibiotic Friulimicin B Inhibits Cell Wall Biosynthesis through Complex Formation with Bactoprenol-Phosphate. Antimicrob Agents Chemother 53: 1610-1618.
34. Stephens, R. S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L., et al. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754-759.
35. Tatar, L. D., Marolda, C. L., Polischuk, A. N., van Leeuwen, D., and Valvano, M. A. (2007) An Escherichia coli undecaprenyl-pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology 153: 2518-2529.
36. Turner, J. D., Langley, R. S., Johnston, K. L., Egerton, G., Wanji, S., and Taylor, M. J. (2006) Wolbachia endosymbiotic bacteria of Brugia malayi mediate macrophage tolerance to TLR- and CD40-specific stimuli in a MyD88/ TLR2-dependent manner. J lmmunol 177: 1240-1249.
37. Vicente, M., and Rico, A. I. (2006) The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol 61: 5-8.
38. Ward, M. E. (1983) Chlamydial classification, development and structure. Br Med Bull 39: 109-115.
39. WHO (2006) Global programme to eliminate lymphatic filariasis. Wkly Epidemiol Rec 81: 221-232.
40. WHO (2007) Meeting of the international task force for disease eradication. Wkly Epidemiol Rec 82: 197-202.
41. Wu, M., Sun, L. V., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J. C., et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: E69.