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. 1997 Jul;65(7):2778–2785. doi: 10.1128/iai.65.7.2778-2785.1997

Utilization of iron-catecholamine complexes involving ferric reductase activity in Listeria monocytogenes.

V Coulanges 1, P Andre 1, O Ziegler 1, L Buchheit 1, D J Vidon 1
PMCID: PMC175392  PMID: 9199450

Abstract

Listeria monocytogenes is a ubiquitous potentially pathogenic organism requiring iron for growth and virulence. Although it does not produce siderophores, L. monocytogenes is able to obtain iron by using either exogenous siderophores produced by various microorganisms or natural catechol compounds widespread in the environment. In the presence of tropolone, an iron-chelating agent, growth of L. monocytogenes is completely inhibited. However, the growth inhibition can be relieved by the addition of dopamine or norepinephrine under their different isomeric forms, while the catecholamine derivatives 4-hydroxy-3-methoxyphenylglycol and normetanephrine did not relieve the inhibitory effect of tropolone. Preincubation of L. monocytogenes with chlorpromazine and yohimbine did not antagonize the growth-promoting effect of catecholamines in iron-complexed medium. In addition, norepinephrine stimulated the growth-promoting effect induced by human transferrin in iron-limited medium. Furthermore, dopamine and norepinephrine allowed 55Fe uptake by iron-deprived bacterial cells. The uptake of iron was energy dependent, as indicated by inhibition of 55Fe uptake at 0 degrees C as well as by preincubating the bacteria with KCN. Inhibition of 55Fe uptake by L. monocytogenes was also observed in the presence of Pt(II). Moreover, when assessed by a whole-cell ferric reductase assay, reductase activity of L. monocytogenes was inhibited by Pt(II). These data demonstrate that dopamine and norepinephrine can function as siderophore-like compounds in L. monocytogenes owing to their ortho-diphenol function and that catecholamine-mediated iron acquisition does not involve specific catecholamine receptors but acts through a cell-bound ferrireductase activity.

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Selected References

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  1. Adams T. J., Vartivarian S., Cowart R. E. Iron acquisition systems of Listeria monocytogenes. Infect Immun. 1990 Aug;58(8):2715–2718. doi: 10.1128/iai.58.8.2715-2718.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aisen P., Listowsky I. Iron transport and storage proteins. Annu Rev Biochem. 1980;49:357–393. doi: 10.1146/annurev.bi.49.070180.002041. [DOI] [PubMed] [Google Scholar]
  3. Barchini E., Cowart R. E. Extracellular iron reductase activity produced by Listeria monocytogenes. Arch Microbiol. 1996 Jul;166(1):51–57. doi: 10.1007/s002030050354. [DOI] [PubMed] [Google Scholar]
  4. Barghouthi S., Young R., Olson M. O., Arceneaux J. E., Clem L. W., Byers B. R. Amonabactin, a novel tryptophan- or phenylalanine-containing phenolate siderophore in Aeromonas hydrophila. J Bacteriol. 1989 Apr;171(4):1811–1816. doi: 10.1128/jb.171.4.1811-1816.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benedict C. R., Grahame-Smith D. G. Plasma noradrenaline and adrenaline concentrations and dopamine-beta-hydroxylase activity in patients with shock due to septicaemia, trauma and haemorrhage. Q J Med. 1978 Jan;47(185):1–20. [PubMed] [Google Scholar]
  6. Cossart P., Mengaud J. Listeria monocytogenes. A model system for the molecular study of intracellular parasitism. Mol Biol Med. 1989 Oct;6(5):463–474. [PubMed] [Google Scholar]
  7. Coulanges V., André P., Vidon D. J. Esculetin antagonizes iron-chelating agents and increases the virulence of Listeria monocytogenes. Res Microbiol. 1996 Nov-Dec;147(9):677–685. doi: 10.1016/s0923-2508(97)85115-7. [DOI] [PubMed] [Google Scholar]
  8. Cowart R. E., Foster B. G. Differential effects of iron on the growth of Listeria monocytogenes: minimum requirements and mechanism of acquisition. J Infect Dis. 1985 Apr;151(4):721–730. doi: 10.1093/infdis/151.4.721. [DOI] [PubMed] [Google Scholar]
  9. Dailey H. A., Jr, Lascelles J. Reduction of iron and synthesis of protoheme by Spirillum itersonii and other organisms. J Bacteriol. 1977 Feb;129(2):815–820. doi: 10.1128/jb.129.2.815-820.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dancis A., Klausner R. D., Hinnebusch A. G., Barriocanal J. G. Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2294–2301. doi: 10.1128/mcb.10.5.2294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deneer H. G., Boychuk I. Reduction of ferric iron by Listeria monocytogenes and other species of Listeria. Can J Microbiol. 1993 May;39(5):480–485. doi: 10.1139/m93-068. [DOI] [PubMed] [Google Scholar]
  12. Deneer H. G., Healey V., Boychuk I. Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp. Microbiology. 1995 Aug;141(Pt 8):1985–1992. doi: 10.1099/13500872-141-8-1985. [DOI] [PubMed] [Google Scholar]
  13. Dix D. R., Bridgham J. T., Broderius M. A., Byersdorfer C. A., Eide D. J. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J Biol Chem. 1994 Oct 21;269(42):26092–26099. [PubMed] [Google Scholar]
  14. Ecker D. J., Emery T. Iron uptake from ferrichrome A and iron citrate in Ustilago sphaerogena. J Bacteriol. 1983 Aug;155(2):616–622. doi: 10.1128/jb.155.2.616-622.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Eide D., Davis-Kaplan S., Jordan I., Sipe D., Kaplan J. Regulation of iron uptake in Saccharomyces cerevisiae. The ferrireductase and Fe(II) transporter are regulated independently. J Biol Chem. 1992 Oct 15;267(29):20774–20781. [PubMed] [Google Scholar]
  16. Evans S. L., Arceneaux J. E., Byers B. R., Martin M. E., Aranha H. Ferrous iron transport in Streptococcus mutans. J Bacteriol. 1986 Dec;168(3):1096–1099. doi: 10.1128/jb.168.3.1096-1099.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Farber J. M., Peterkin P. I. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev. 1991 Sep;55(3):476–511. doi: 10.1128/mr.55.3.476-511.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Genco C. A., Desai P. J. Iron acquisition in the pathogenic Neisseria. Trends Microbiol. 1996 May;4(5):179–184. doi: 10.1016/0966-842x(96)10029-9. [DOI] [PubMed] [Google Scholar]
  19. Goulet V., Jacquet C., Vaillant V., Rebière I., Mouret E., Lorente C., Maillot E., Staïner F., Rocourt J. Listeriosis from consumption of raw-milk cheese. Lancet. 1995 Jun 17;345(8964):1581–1582. doi: 10.1016/s0140-6736(95)91135-9. [DOI] [PubMed] [Google Scholar]
  20. Grossman T. H., Tuckman M., Ellestad S., Osburne M. S. Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes. J Bacteriol. 1993 Oct;175(19):6203–6211. doi: 10.1128/jb.175.19.6203-6211.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hartford T., O'Brien S., Andrew P. W., Jones D., Roberts I. S. Utilization of transferrin-bound iron by Listeria monocytogenes. FEMS Microbiol Lett. 1993 Apr 15;108(3):311–318. doi: 10.1111/j.1574-6968.1993.tb06121.x. [DOI] [PubMed] [Google Scholar]
  22. Huschka H., Naegeli H. U., Leuenberger-Ryf H., Keller-Schierlein W., Winkelmann G. Evidence for a common siderophore transport system but different siderophore receptors in Neurospora crassa. J Bacteriol. 1985 May;162(2):715–721. doi: 10.1128/jb.162.2.715-721.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Huyer M., Page W. J. Ferric reductase activity in Azotobacter vinelandii and its inhibition by Zn2+. J Bacteriol. 1989 Jul;171(7):4031–4037. doi: 10.1128/jb.171.7.4031-4037.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jalal M. A., Mocharla R., Barnes C. L., Hossain M. B., Powell D. R., Eng-Wilmot D. L., Grayson S. L., Benson B. A., van der Helm D. Extracellular siderophores from Aspergillus ochraceous. J Bacteriol. 1984 May;158(2):683–688. doi: 10.1128/jb.158.2.683-688.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Johnson W., Varner L., Poch M. Acquisition of iron by Legionella pneumophila: role of iron reductase. Infect Immun. 1991 Jul;59(7):2376–2381. doi: 10.1128/iai.59.7.2376-2381.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jones S. B., Westfall M. V., Sayeed M. M. Plasma catecholamines during E. coli bacteremia in conscious rats. Am J Physiol. 1988 Mar;254(3 Pt 2):R470–R477. doi: 10.1152/ajpregu.1988.254.3.R470. [DOI] [PubMed] [Google Scholar]
  27. Lenard J., VanDeroef R. A novel bacteristatic action of bovine and porcine serum that is reversed by norepinephrine. Life Sci. 1995;57(5):443–447. doi: 10.1016/0024-3205(95)00277-d. [DOI] [PubMed] [Google Scholar]
  28. Lesuisse E., Raguzzi F., Crichton R. R. Iron uptake by the yeast Saccharomyces cerevisiae: involvement of a reduction step. J Gen Microbiol. 1987 Nov;133(11):3229–3236. doi: 10.1099/00221287-133-11-3229. [DOI] [PubMed] [Google Scholar]
  29. Lodge J. S., Gaines C. G., Arceneaux J. E., Byers B. R. Ferrisiderophore reductase activity in Agrobacterium tumefaciens. J Bacteriol. 1982 Feb;149(2):771–774. doi: 10.1128/jb.149.2.771-774.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lyte M., Arulanandam B. P., Frank C. D. Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. J Lab Clin Med. 1996 Oct;128(4):392–398. doi: 10.1016/s0022-2143(96)80011-4. [DOI] [PubMed] [Google Scholar]
  31. Lyte M., Ernst S. Alpha and beta adrenergic receptor involvement in catecholamine-induced growth of gram-negative bacteria. Biochem Biophys Res Commun. 1993 Jan 29;190(2):447–452. doi: 10.1006/bbrc.1993.1068. [DOI] [PubMed] [Google Scholar]
  32. Lyte M., Ernst S. Catecholamine induced growth of gram negative bacteria. Life Sci. 1992;50(3):203–212. doi: 10.1016/0024-3205(92)90273-r. [DOI] [PubMed] [Google Scholar]
  33. Meyer J. M., Hohnadel D., Hallé F. Cepabactin from Pseudomonas cepacia, a new type of siderophore. J Gen Microbiol. 1989 Jun;135(6):1479–1487. doi: 10.1099/00221287-135-6-1479. [DOI] [PubMed] [Google Scholar]
  34. Morrissey J. A., Williams P. H., Cashmore A. M. Candida albicans has a cell-associated ferric-reductase activity which is regulated in response to levels of iron and copper. Microbiology. 1996 Mar;142(Pt 3):485–492. doi: 10.1099/13500872-142-3-485. [DOI] [PubMed] [Google Scholar]
  35. Neilands J. B. Microbial iron compounds. Annu Rev Biochem. 1981;50:715–731. doi: 10.1146/annurev.bi.50.070181.003435. [DOI] [PubMed] [Google Scholar]
  36. Polacheck I., Platt Y., Aronovitch J. Catecholamines and virulence of Cryptococcus neoformans. Infect Immun. 1990 Sep;58(9):2919–2922. doi: 10.1128/iai.58.9.2919-2922.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Premaratne R. J., Lin W. J., Johnson E. A. Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol. 1991 Oct;57(10):3046–3048. doi: 10.1128/aem.57.10.3046-3048.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Reeves M. W., Pine L., Neilands J. B., Balows A. Absence of siderophore activity in Legionella species grown in iron-deficient media. J Bacteriol. 1983 Apr;154(1):324–329. doi: 10.1128/jb.154.1.324-329.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Simon N., Coulanges V., Andre P., Vidon D. J. Utilization of exogenous siderophores and natural catechols by Listeria monocytogenes. Appl Environ Microbiol. 1995 Apr;61(4):1643–1645. doi: 10.1128/aem.61.4.1643-1645.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sword C. P. Mechanisms of pathogenesis in Listeria monocytogenes infection. I. Influence of iron. J Bacteriol. 1966 Sep;92(3):536–542. doi: 10.1128/jb.92.3.536-542.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]

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