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. 1993 May 1;291(Pt 3):895–900. doi: 10.1042/bj2910895

Formylmethionyl-leucylphenylalanine and the SOS operon in Escherichia coli: a model of host-bacterial interactions.

M F Broom 1, R M Sherriff 1, D M Ferry 1, V S Chadwick 1
PMCID: PMC1132453  PMID: 8489516

Abstract

To determine the biological significance of the existence of highly specific receptors for the bacterial chemotactic peptide formylmethionyl-leucylphenylalanine (fMet-Leu-Phe) on neutrophil leucocytes, we investigated the role of this peptide in bacterial metabolism. The UmuD protein of the Escherichia coli SOS operon was identified as having an N-terminal fMet-Leu-Phe sequence and a recombinant E. coli with the umuD gene on plasmid pSB13 was shown to be an over-producer of both UmuD and fMet-Leu-Phe. Activation of SOS genes in conventional wild-type E. coli (K12) by u.v. light or hydrogen peroxide increased fMet-Leu-Phe production up to 4-fold. A RecA- strain, incapable of SOS activation, was a low basal producer of fMet-Leu-Phe and showed no increased production with u.v. light or oxidant stress. We propose that host phagocytes respond to fMet-Leu-Phe and closely related peptides because they are generated by bacteria under oxidant stress. Increased fMet-Leu-Phe production may signal to the host a change in the organism's biological status from commensal to pathogen because of the invasion into tissues exposing bacteria to high pO2 levels and oxidant stress.

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Selected References

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  1. Battista J. R., Donnelly C. E., Ohta T., Walker G. C. The SOS response and induced mutagenesis. Prog Clin Biol Res. 1990;340A:169–178. [PubMed] [Google Scholar]
  2. Bornside G. H., Cherry G. W., Myers M. B. Intracolonic oxygen tension and in vivo bactericidal effect of hyperbaric oxygen on rat colonic flora. Aerosp Med. 1973 Nov;44(11):1282–1286. [PubMed] [Google Scholar]
  3. Broom M. F., Mellor D. M., Chadwick V. S. Purification and amino acid sequencing of naturally occurring N-formyl-methionyl oligopeptides from Escherichia coli. Experientia. 1989 Dec 1;45(11-12):1097–1099. doi: 10.1007/BF01950167. [DOI] [PubMed] [Google Scholar]
  4. Burckhardt S. E., Woodgate R., Scheuermann R. H., Echols H. UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1811–1815. doi: 10.1073/pnas.85.6.1811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chadwick V. S., Mellor D. M., Myers D. B., Selden A. C., Keshavarzian A., Broom M. F., Hobson C. H. Production of peptides inducing chemotaxis and lysosomal enzyme release in human neutrophils by intestinal bacteria in vitro and in vivo. Scand J Gastroenterol. 1988 Jan;23(1):121–128. doi: 10.3109/00365528809093861. [DOI] [PubMed] [Google Scholar]
  6. Chadwick V. S., Schlup M. M., Ferry D. M., Chang A. R., Butt T. J. Measurements of unsaturated vitamin B12-binding capacity and myeloperoxidase as indices of severity of acute inflammation in serial colonoscopy biopsy specimens from patients with inflammatory bowel disease. Scand J Gastroenterol. 1990 Dec;25(12):1196–1204. doi: 10.3109/00365529008998554. [DOI] [PubMed] [Google Scholar]
  7. Elledge S. J., Walker G. C. Proteins required for ultraviolet light and chemical mutagenesis. Identification of the products of the umuC locus of Escherichia coli. J Mol Biol. 1983 Feb 25;164(2):175–192. doi: 10.1016/0022-2836(83)90074-8. [DOI] [PubMed] [Google Scholar]
  8. Freer R. J., Day A. R., Muthukumaraswamy N., Pinon D., Wu A., Showell H. J., Becker E. L. Formyl peptide chemoattractants: a model of the receptor on rabbit neutrophils. Biochemistry. 1982 Jan 19;21(2):257–263. doi: 10.1021/bi00531a009. [DOI] [PubMed] [Google Scholar]
  9. Gardner J. P., Melnick D. A., Malech H. L. Characterization of the formyl peptide chemotactic receptor appearing at the phagocytic cell surface after exposure to phorbol myristate acetate. J Immunol. 1986 Feb 15;136(4):1400–1405. [PubMed] [Google Scholar]
  10. Goerlich O., Quillardet P., Hofnung M. Induction of the SOS response by hydrogen peroxide in various Escherichia coli mutants with altered protection against oxidative DNA damage. J Bacteriol. 1989 Nov;171(11):6141–6147. doi: 10.1128/jb.171.11.6141-6147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hobson C. H., Roberts E. C., Broom M. F., Mellor D. M., Sherriff R. M., Chadwick V. S. Radio-immunoassay for formyl methionyl leucyl phenylalanine. I. Development and application to assessment of chemotactic peptide production by enteric bacteria. J Gastroenterol Hepatol. 1990 Jan-Feb;5(1):32–37. doi: 10.1111/j.1440-1746.1990.tb01765.x. [DOI] [PubMed] [Google Scholar]
  12. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  13. Leonard E. J., Noer K., Skeel A. Analysis of human monocyte chemoattractant binding by flow cytometry. J Leukoc Biol. 1985 Sep;38(3):403–413. doi: 10.1002/jlb.38.3.403. [DOI] [PubMed] [Google Scholar]
  14. Lu C., Echols H. RecA protein and SOS. Correlation of mutagenesis phenotype with binding of mutant RecA proteins to duplex DNA and LexA cleavage. J Mol Biol. 1987 Aug 5;196(3):497–504. doi: 10.1016/0022-2836(87)90027-1. [DOI] [PubMed] [Google Scholar]
  15. Marasco W. A., Becker K. M., Feltner D. E., Brown C. S., Ward P. A., Nairn R. Covalent affinity labeling, detergent solubilization, and fluid-phase characterization of the rabbit neutrophil formyl peptide chemotaxis receptor. Biochemistry. 1985 Apr 23;24(9):2227–2236. doi: 10.1021/bi00330a017. [DOI] [PubMed] [Google Scholar]
  16. Marasco W. A., Phan S. H., Krutzsch H., Showell H. J., Feltner D. E., Nairn R., Becker E. L., Ward P. A. Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J Biol Chem. 1984 May 10;259(9):5430–5439. [PubMed] [Google Scholar]
  17. McCord J. M., Keele B. B., Jr, Fridovich I. An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc Natl Acad Sci U S A. 1971 May;68(5):1024–1027. doi: 10.1073/pnas.68.5.1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moody C. S., Hassan H. M. Mutagenicity of oxygen free radicals. Proc Natl Acad Sci U S A. 1982 May;79(9):2855–2859. doi: 10.1073/pnas.79.9.2855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Perry K. L., Elledge S. J., Mitchell B. B., Marsh L., Walker G. C. umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4331–4335. doi: 10.1073/pnas.82.13.4331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rotrosen D., Malech H. L., Gallin J. I. Formyl peptide leukocyte chemoattractant uptake and release by cultured human umbilical vein endothelial cells. J Immunol. 1987 Nov 1;139(9):3034–3040. [PubMed] [Google Scholar]
  21. Sassanfar M., Roberts J. W. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol. 1990 Mar 5;212(1):79–96. doi: 10.1016/0022-2836(90)90306-7. [DOI] [PubMed] [Google Scholar]
  22. Schiffmann E., Showell H. V., Corcoran B. A., Ward P. A., Smith E., Becker E. L. The isolation and partial characterization of neutrophil chemotactic factors from Escherichia coli. J Immunol. 1975 Jun;114(6):1831–1837. [PubMed] [Google Scholar]
  23. Shinagawa H., Iwasaki H., Kato T., Nakata A. RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1806–1810. doi: 10.1073/pnas.85.6.1806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sidman K. E., George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1988 Mar 11;16(5):1869–1871. doi: 10.1093/nar/16.5.1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tennenberg S. D., Zemlan F. P., Solomkin J. S. Characterization of N-formyl-methionyl-leucyl-phenylalanine receptors on human neutrophils. Effects of isolation and temperature on receptor expression and functional activity. J Immunol. 1988 Dec 1;141(11):3937–3944. [PubMed] [Google Scholar]
  26. Williams L. T., Snyderman R., Pike M. C., Lefkowitz R. J. Specific receptor sites for chemotactic peptides on human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1204–1208. doi: 10.1073/pnas.74.3.1204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Woodgate R., Ennis D. G. Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol Gen Genet. 1991 Sep;229(1):10–16. doi: 10.1007/BF00264207. [DOI] [PubMed] [Google Scholar]

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