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. 1996 Sep;40(9):2173–2177. doi: 10.1128/aac.40.9.2173

Location of N-acetylmuramyl-L-alanyl-D-glutamylmesodiaminopimelic acid, presumed signal molecule for beta-lactamase induction, in the bacterial cell.

H Dietz 1, D Pfeifle 1, B Wiedemann 1
PMCID: PMC163493  PMID: 8878601

Abstract

Using a chromatographic method for the isolation and detection of periplasmic and cytoplasmic muropeptides avoiding radioactive labeling, we found that in the ampD-negative strain JRG582 the anhydromuropeptide N-acetylmuramyl-L-alanyl-D-glutamylmesodiaminopimelic acid (anhMurNAc tripeptide) accumulates not only in the cytoplasm but also in the periplasm. Simultaneously JRG582 carrying the Enterobacter cloacae genes ampC and ampR, which are necessary for the induction of beta-lactamase expression, overproduces beta-lactamase. We confirmed that the transmembrane protein AmpG transports a precursor muropeptide into the cytoplasm and that the formation of the anhMurNAc tripeptide takes place in the cytoplasm. anhMurNAc tripeptide can then be secreted into the periplasm. Therefore, the amount of anhMurNAc tripeptide in the cytoplasm is reduced not only by AmpD but also by transport out of the cell.

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Selected References

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  1. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  2. Broome-Smith J. K., Spratt B. G. A vector for the construction of translational fusions to TEM beta-lactamase and the analysis of protein export signals and membrane protein topology. Gene. 1986;49(3):341–349. doi: 10.1016/0378-1119(86)90370-7. [DOI] [PubMed] [Google Scholar]
  3. Fleming T. J., Wallsmith D. E., Rosenthal R. S. Arthropathic properties of gonococcal peptidoglycan fragments: implications for the pathogenesis of disseminated gonococcal disease. Infect Immun. 1986 May;52(2):600–608. doi: 10.1128/iai.52.2.600-608.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Glauner B., Höltje J. V., Schwarz U. The composition of the murein of Escherichia coli. J Biol Chem. 1988 Jul 25;263(21):10088–10095. [PubMed] [Google Scholar]
  5. Goodell E. W. Recycling of murein by Escherichia coli. J Bacteriol. 1985 Jul;163(1):305–310. doi: 10.1128/jb.163.1.305-310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Guest J. R., Stephens P. E. Molecular cloning of the pyruvate dehydrogenase complex genes of Escherichia coli. J Gen Microbiol. 1980 Dec;121(2):277–292. doi: 10.1099/00221287-121-2-277. [DOI] [PubMed] [Google Scholar]
  7. Höltje J. V., Kopp U., Ursinus A., Wiedemann B. The negative regulator of beta-lactamase induction AmpD is a N-acetyl-anhydromuramyl-L-alanine amidase. FEMS Microbiol Lett. 1994 Sep 15;122(1-2):159–164. doi: 10.1111/j.1574-6968.1994.tb07159.x. [DOI] [PubMed] [Google Scholar]
  8. Jacobs C., Huang L. J., Bartowsky E., Normark S., Park J. T. Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. EMBO J. 1994 Oct 3;13(19):4684–4694. doi: 10.1002/j.1460-2075.1994.tb06792.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jacobs C., Joris B., Jamin M., Klarsov K., Van Beeumen J., Mengin-Lecreulx D., van Heijenoort J., Park J. T., Normark S., Frère J. M. AmpD, essential for both beta-lactamase regulation and cell wall recycling, is a novel cytosolic N-acetylmuramyl-L-alanine amidase. Mol Microbiol. 1995 Feb;15(3):553–559. doi: 10.1111/j.1365-2958.1995.tb02268.x. [DOI] [PubMed] [Google Scholar]
  10. Kopp U., Wiedemann B., Lindquist S., Normark S. Sequences of wild-type and mutant ampD genes of Citrobacter freundii and Enterobacter cloacae. Antimicrob Agents Chemother. 1993 Feb;37(2):224–228. doi: 10.1128/aac.37.2.224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Korfmann G., Sanders C. C. ampG is essential for high-level expression of AmpC beta-lactamase in Enterobacter cloacae. Antimicrob Agents Chemother. 1989 Nov;33(11):1946–1951. doi: 10.1128/aac.33.11.1946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Korfmann G., Wiedemann B. Genetic control of beta-lactamase production in Enterobacter cloacae. Rev Infect Dis. 1988 Jul-Aug;10(4):793–799. doi: 10.1093/clinids/10.4.793. [DOI] [PubMed] [Google Scholar]
  13. Krueger J. M., Pappenheimer J. R., Karnovsky M. L. Sleep-promoting effects of muramyl peptides. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6102–6106. doi: 10.1073/pnas.79.19.6102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lindberg F., Lindquist S., Normark S. Inactivation of the ampD gene causes semiconstitutive overproduction of the inducible Citrobacter freundii beta-lactamase. J Bacteriol. 1987 May;169(5):1923–1928. doi: 10.1128/jb.169.5.1923-1928.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lindberg F., Normark S. Common mechanism of ampC beta-lactamase induction in enterobacteria: regulation of the cloned Enterobacter cloacae P99 beta-lactamase gene. J Bacteriol. 1987 Feb;169(2):758–763. doi: 10.1128/jb.169.2.758-763.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lindquist S., Galleni M., Lindberg F., Normark S. Signalling proteins in enterobacterial AmpC beta-lactamase regulation. Mol Microbiol. 1989 Aug;3(8):1091–1102. doi: 10.1111/j.1365-2958.1989.tb00259.x. [DOI] [PubMed] [Google Scholar]
  17. Lindquist S., Lindberg F., Normark S. Binding of the Citrobacter freundii AmpR regulator to a single DNA site provides both autoregulation and activation of the inducible ampC beta-lactamase gene. J Bacteriol. 1989 Jul;171(7):3746–3753. doi: 10.1128/jb.171.7.3746-3753.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lindquist S., Weston-Hafer K., Schmidt H., Pul C., Korfmann G., Erickson J., Sanders C., Martin H. H., Normark S. AmpG, a signal transducer in chromosomal beta-lactamase induction. Mol Microbiol. 1993 Aug;9(4):703–715. doi: 10.1111/j.1365-2958.1993.tb01731.x. [DOI] [PubMed] [Google Scholar]
  19. Lodge J. M., Piddock L. J. The control of class I beta-lactamase expression in Enterobacteriaceae and Pseudomonas aeruginosa. J Antimicrob Chemother. 1991 Aug;28(2):167–172. doi: 10.1093/jac/28.2.167. [DOI] [PubMed] [Google Scholar]
  20. Nossal N. G., Heppel L. A. The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J Biol Chem. 1966 Jul 10;241(13):3055–3062. [PubMed] [Google Scholar]
  21. Peter K., Korfmann G., Wiedemann B. Impact of the ampD gene and its product on beta-lactamase production in Enterobacter cloacae. Rev Infect Dis. 1988 Jul-Aug;10(4):800–805. doi: 10.1093/clinids/10.4.800. [DOI] [PubMed] [Google Scholar]
  22. Tuomanen E., Hengstler B., Zak O., Tomasz A. Induction of meningeal inflammation by diverse bacterial cell walls. Eur J Clin Microbiol. 1986 Dec;5(6):682–684. doi: 10.1007/BF02013304. [DOI] [PubMed] [Google Scholar]
  23. Tuomanen E., Lindquist S., Sande S., Galleni M., Light K., Gage D., Normark S. Coordinate regulation of beta-lactamase induction and peptidoglycan composition by the amp operon. Science. 1991 Jan 11;251(4990):201–204. doi: 10.1126/science.1987637. [DOI] [PubMed] [Google Scholar]

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