Skip to main content
PMC home page
Clinical Microbiology Reviews logoLink to Clinical Microbiology Reviews
. 1993 Apr;6(2):137–149. doi: 10.1128/cmr.6.2.137

Role of iron in regulation of virulence genes.

C M Litwin 1, S B Calderwood 1
PMCID: PMC358274  PMID: 8472246

Abstract

The abilities of bacterial pathogens to adapt to the environment within the host are essential to their virulence. Microorganisms have adapted to the iron limitation present in mammalian hosts by evolving diverse mechanisms for the assimilation of iron sufficient for growth. In addition, many bacterial pathogens have used the low concentration of iron present in the host as an important signal to enhance the expression of a wide variety of bacterial toxins and other virulence determinants. The molecular basis of coordinate regulation by iron has been most thoroughly studied in Escherichia coli. In this organism, coordinate regulation of gene expression by iron depends on the regulatory gene, fur. Regulation of gene expression by iron in a number of pathogenic organisms is coordinated by proteins homologous to the Fur protein of E. coli. Additional regulatory proteins may be superimposed on the Fur repressor to provide the fine-tuning necessary for the precise regulation of individual virulence genes in response to iron and other environmental signals. Studies of the mechanisms of regulation of iron acquisition systems and virulence determinants by iron should lead to a better understanding of the adaptive response of bacteria to the low-iron environment of the host and its importance in virulence.

Full text

PDF

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Actis L. A., Fish W., Crosa J. H., Kellerman K., Ellenberger S. R., Hauser F. M., Sanders-Loehr J. Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775(pJM1). J Bacteriol. 1986 Jul;167(1):57–65. doi: 10.1128/jb.167.1.57-65.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Actis L. A., Potter S. A., Crosa J. H. Iron-regulated outer membrane protein OM2 of Vibrio anguillarum is encoded by virulence plasmid pJM1. J Bacteriol. 1985 Feb;161(2):736–742. doi: 10.1128/jb.161.2.736-742.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Actis L. A., Tolmasky M. E., Farrell D. H., Crosa J. H. Genetic and molecular characterization of essential components of the Vibrio anguillarum plasmid-mediated iron-transport system. J Biol Chem. 1988 Feb 25;263(6):2853–2860. [PubMed] [Google Scholar]
  4. Aisen P., Leibman A. Lactoferrin and transferrin: a comparative study. Biochim Biophys Acta. 1972 Feb 29;257(2):314–323. doi: 10.1016/0005-2795(72)90283-8. [DOI] [PubMed] [Google Scholar]
  5. Bagg A., Neilands J. B. Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry. 1987 Aug 25;26(17):5471–5477. doi: 10.1021/bi00391a039. [DOI] [PubMed] [Google Scholar]
  6. Bagg A., Neilands J. B. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev. 1987 Dec;51(4):509–518. doi: 10.1128/mr.51.4.509-518.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barry D. M., Reeve A. W. Increased incidence of gram-negative neonatal sepsis with intramuscula iron administration. Pediatrics. 1977 Dec;60(6):908–912. [PubMed] [Google Scholar]
  8. Becroft D. M., Dix M. R., Farmer K. Intramuscular iron-dextran and susceptibility of neonates to bacterial infections. In vitro studies. Arch Dis Child. 1977 Oct;52(10):778–781. doi: 10.1136/adc.52.10.778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Berish S. A., Kapczynski D. R., Morse S. A. Nucleotide sequence of the Fbp gene from Neisseria meningitidis. Nucleic Acids Res. 1990 Aug 11;18(15):4596–4596. doi: 10.1093/nar/18.15.4596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Berish S. A., Mietzner T. A., Mayer L. W., Genco C. A., Holloway B. P., Morse S. A. Molecular cloning and characterization of the structural gene for the major iron-regulated protein expressed by Neisseria gonorrhoeae. J Exp Med. 1990 May 1;171(5):1535–1546. doi: 10.1084/jem.171.5.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Beutler B., Cerami A. Cachectin: more than a tumor necrosis factor. N Engl J Med. 1987 Feb 12;316(7):379–385. doi: 10.1056/NEJM198702123160705. [DOI] [PubMed] [Google Scholar]
  12. Bindereif A., Neilands J. B. Promoter mapping and transcriptional regulation of the iron assimilation system of plasmid ColV-K30 in Escherichia coli K-12. J Bacteriol. 1985 Jun;162(3):1039–1046. doi: 10.1128/jb.162.3.1039-1046.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bjorn M. J., Iglewski B. H., Ives S. K., Sadoff J. C., Vasil M. L. Effect of iron on yields of exotoxin A in cultures of Pseudomonas aeruginosa PA-103. Infect Immun. 1978 Mar;19(3):785–791. doi: 10.1128/iai.19.3.785-791.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bjorn M. J., Sokol P. A., Iglewski B. H. Influence of iron on yields of extracellular products in Pseudomonas aeruginosa cultures. J Bacteriol. 1979 Apr;138(1):193–200. doi: 10.1128/jb.138.1.193-200.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Blake P. A., Merson M. H., Weaver R. E., Hollis D. G., Heublein P. C. Disease caused by a marine Vibrio. Clinical characteristics and epidemiology. N Engl J Med. 1979 Jan 4;300(1):1–5. doi: 10.1056/NEJM197901043000101. [DOI] [PubMed] [Google Scholar]
  16. Blanton K. J., Biswas G. D., Tsai J., Adams J., Dyer D. W., Davis S. M., Koch G. G., Sen P. K., Sparling P. F. Genetic evidence that Neisseria gonorrhoeae produces specific receptors for transferrin and lactoferrin. J Bacteriol. 1990 Sep;172(9):5225–5235. doi: 10.1128/jb.172.9.5225-5235.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Blumentals I. I., Skaja A. K., Kelly R. M., Clem T. R., Shiloach J. Effect of culturing conditions on the production of exotoxin A by Pseudomonas aeruginosa. Ann N Y Acad Sci. 1987;506:663–668. doi: 10.1111/j.1749-6632.1987.tb23864.x. [DOI] [PubMed] [Google Scholar]
  18. Boyd J., Murphy J. R. Analysis of the diphtheria tox promoter by site-directed mutagenesis. J Bacteriol. 1988 Dec;170(12):5949–5952. doi: 10.1128/jb.170.12.5949-5952.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Boyd J., Oza M. N., Murphy J. R. Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5968–5972. doi: 10.1073/pnas.87.15.5968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Brener D., DeVoe I. W., Holbein B. E. Increased virulence of Neisseria meningitidis after in vitro iron-limited growth at low pH. Infect Immun. 1981 Jul;33(1):59–66. doi: 10.1128/iai.33.1.59-66.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Brooks H. J., O'Grady F., McSherry M. A., Cattell W. R. Uropathogenic properties of Escherichia coli in recurrent urinary-tract infection. J Med Microbiol. 1980 Feb;13(1):57–68. doi: 10.1099/00222615-13-1-57. [DOI] [PubMed] [Google Scholar]
  22. Buck G. A., Cross R. E., Wong T. P., Loera J., Groman N. DNA relationships among some tox-bearing corynebacteriophages. Infect Immun. 1985 Sep;49(3):679–684. doi: 10.1128/iai.49.3.679-684.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Bullen J. J., Leigh L. C., Rogers H. J. The effect of iron compounds on the virulence of Escherichia coli for guinea-pigs. Immunology. 1968 Oct;15(4):581–588. [PMC free article] [PubMed] [Google Scholar]
  24. Bullen J. J., Rogers H. J., Griffiths E. Role of iron in bacterial infection. Curr Top Microbiol Immunol. 1978;80:1–35. doi: 10.1007/978-3-642-66956-9_1. [DOI] [PubMed] [Google Scholar]
  25. Calderwood S. B., Auclair F., Donohue-Rolfe A., Keusch G. T., Mekalanos J. J. Nucleotide sequence of the Shiga-like toxin genes of Escherichia coli. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4364–4368. doi: 10.1073/pnas.84.13.4364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Calderwood S. B., Mekalanos J. J. Confirmation of the Fur operator site by insertion of a synthetic oligonucleotide into an operon fusion plasmid. J Bacteriol. 1988 Feb;170(2):1015–1017. doi: 10.1128/jb.170.2.1015-1017.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Calderwood S. B., Mekalanos J. J. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J Bacteriol. 1987 Oct;169(10):4759–4764. doi: 10.1128/jb.169.10.4759-4764.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Carniel E., Antoine J. C., Guiyoule A., Guiso N., Mollaret H. H. Purification, location, and immunological characterization of the iron-regulated high-molecular-weight proteins of the highly pathogenic yersiniae. Infect Immun. 1989 Feb;57(2):540–545. doi: 10.1128/iai.57.2.540-545.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Carniel E., Guiyoule A., Guilvout I., Mercereau-Puijalon O. Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia. Mol Microbiol. 1992 Feb;6(3):379–388. doi: 10.1111/j.1365-2958.1992.tb01481.x. [DOI] [PubMed] [Google Scholar]
  30. Carniel E., Mazigh D., Mollaret H. H. Expression of iron-regulated proteins in Yersinia species and their relation to virulence. Infect Immun. 1987 Jan;55(1):277–280. doi: 10.1128/iai.55.1.277-280.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Carniel E., Mercereau-Puijalon O., Bonnefoy S. The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect Immun. 1989 Apr;57(4):1211–1217. doi: 10.1128/iai.57.4.1211-1217.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Collier R. J. Effect of diphtheria toxin on protein synthesis: inactivation of one of the transfer factors. J Mol Biol. 1967 Apr 14;25(1):83–98. doi: 10.1016/0022-2836(67)90280-x. [DOI] [PubMed] [Google Scholar]
  33. Cornelissen C. N., Biswas G. D., Tsai J., Paruchuri D. K., Thompson S. A., Sparling P. F. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J Bacteriol. 1992 Sep;174(18):5788–5797. doi: 10.1128/jb.174.18.5788-5797.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Crosa J. H. A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system. Nature. 1980 Apr 10;284(5756):566–568. doi: 10.1038/284566a0. [DOI] [PubMed] [Google Scholar]
  36. Crosa J. H., Hodges L. L., Schiewe M. H. Curing of a plasmid is correlated with an attenuation of virulence in the marine fish pathogen Vibrio anguillarum. Infect Immun. 1980 Mar;27(3):897–902. doi: 10.1128/iai.27.3.897-902.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. De Grandis S., Ginsberg J., Toone M., Climie S., Friesen J., Brunton J. Nucleotide sequence and promoter mapping of the Escherichia coli Shiga-like toxin operon of bacteriophage H-19B. J Bacteriol. 1987 Sep;169(9):4313–4319. doi: 10.1128/jb.169.9.4313-4319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. DeBoy J. M., 2nd, Wachsmuth I. K., Davis B. R. Hemolytic activity in enterotoxigenic and non-enterotoxigenic strains of Escherichia coli. J Clin Microbiol. 1980 Aug;12(2):193–198. doi: 10.1128/jcm.12.2.193-198.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Dinarello C. A. Interleukin-1 and the pathogenesis of the acute-phase response. N Engl J Med. 1984 Nov 29;311(22):1413–1418. doi: 10.1056/NEJM198411293112205. [DOI] [PubMed] [Google Scholar]
  40. Donohue-Rolfe A., Keusch G. T., Edson C., Thorley-Lawson D., Jacewicz M. Pathogenesis of Shigella diarrhea. IX. Simplified high yield purification of Shigella toxin and characterization of subunit composition and function by the use of subunit-specific monoclonal and polyclonal antibodies. J Exp Med. 1984 Dec 1;160(6):1767–1781. doi: 10.1084/jem.160.6.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Dyer D. W., West E. P., Sparling P. F. Effects of serum carrier proteins on the growth of pathogenic neisseriae with heme-bound iron. Infect Immun. 1987 Sep;55(9):2171–2175. doi: 10.1128/iai.55.9.2171-2175.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Eaton J. W., Brandt P., Mahoney J. R., Lee J. T., Jr Haptoglobin: a natural bacteriostat. Science. 1982 Feb 5;215(4533):691–693. doi: 10.1126/science.7036344. [DOI] [PubMed] [Google Scholar]
  43. Eiklid K., Olsnes S. Animal toxicity of Shigella dysenteriae cytotoxin: evidence that the neurotoxic, enterotoxic, and cytotoxic activities are due to one toxin. J Immunol. 1983 Jan;130(1):380–384. [PubMed] [Google Scholar]
  44. Endo Y., Mitsui K., Motizuki M., Tsurugi K. The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28 S ribosomal RNA caused by the toxins. J Biol Chem. 1987 Apr 25;262(12):5908–5912. [PubMed] [Google Scholar]
  45. Endo Y., Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem. 1987 Jun 15;262(17):8128–8130. [PubMed] [Google Scholar]
  46. Endo Y., Tsurugi K., Yutsudo T., Takeda Y., Ogasawara T., Igarashi K. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem. 1988 Jan 15;171(1-2):45–50. doi: 10.1111/j.1432-1033.1988.tb13756.x. [DOI] [PubMed] [Google Scholar]
  47. Ernst J. F., Bennett R. L., Rothfield L. I. Constitutive expression of the iron-enterochelin and ferrichrome uptake systems in a mutant strain of Salmonella typhimurium. J Bacteriol. 1978 Sep;135(3):928–934. doi: 10.1128/jb.135.3.928-934.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Farrell D. H., Mikesell P., Actis L. A., Crosa J. H. A regulatory gene, angR, of the iron uptake system of Vibrio anguillarum: similarity with phage P22 cro and regulation by iron. Gene. 1990 Jan 31;86(1):45–51. doi: 10.1016/0378-1119(90)90112-5. [DOI] [PubMed] [Google Scholar]
  49. Field L. H., Headley V. L., Payne S. M., Berry L. J. Influence of iron on growth, morphology, outer membrane protein composition, and synthesis of siderophores in Campylobacter jejuni. Infect Immun. 1986 Oct;54(1):126–132. doi: 10.1128/iai.54.1.126-132.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Finkelstein R. A., Yancey R. J. Effect of siderophores on virulence of Neisseria gonorrhoeae. Infect Immun. 1981 May;32(2):609–613. doi: 10.1128/iai.32.2.609-613.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ford A., Hayhoe P. V. An investigation of alternatives to hog gastric mucin as virulence-enhancing agents in the cholera vaccine potency assay. J Biol Stand. 1976;4(4):353–366. doi: 10.1016/s0092-1157(76)80020-0. [DOI] [PubMed] [Google Scholar]
  52. Fourel G., Phalipon A., Kaczorek M. Evidence for direct regulation of diphtheria toxin gene transcription by an Fe2+-dependent DNA-binding repressor, DtoxR, in Corynebacterium diphtheriae. Infect Immun. 1989 Oct;57(10):3221–3225. doi: 10.1128/iai.57.10.3221-3225.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Frank D. W., Iglewski B. H. Kinetics of toxA and regA mRNA accumulation in Pseudomonas aeruginosa. J Bacteriol. 1988 Oct;170(10):4477–4483. doi: 10.1128/jb.170.10.4477-4483.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Frank D. W., Storey D. G., Hindahl M. S., Iglewski B. H. Differential regulation by iron of regA and toxA transcript accumulation in Pseudomonas aeruginosa. J Bacteriol. 1989 Oct;171(10):5304–5313. doi: 10.1128/jb.171.10.5304-5313.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Frost G. E., Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta. 1973 Nov 30;330(1):90–101. doi: 10.1016/0005-2736(73)90287-3. [DOI] [PubMed] [Google Scholar]
  56. Genco C. A., Chen C. Y., Arko R. J., Kapczynski D. R., Morse S. A. Isolation and characterization of a mutant of Neisseria gonorrhoeae that is defective in the uptake of iron from transferrin and haemoglobin and is avirulent in mouse subcutaneous chambers. J Gen Microbiol. 1991 Jun;137(6):1313–1321. doi: 10.1099/00221287-137-6-1313. [DOI] [PubMed] [Google Scholar]
  57. Gladstone G. P., Walton E. Effect of iron on the bactericidal proteins from rabbit polymorphonuclear leukocytes. Nature. 1970 Aug 22;227(5260):849–851. doi: 10.1038/227849a0. [DOI] [PubMed] [Google Scholar]
  58. Goldberg M. B., Boyko S. A., Butterton J. R., Stoebner J. A., Payne S. M., Calderwood S. B. Characterization of a Vibrio cholerae virulence factor homologous to the family of TonB-dependent proteins. Mol Microbiol. 1992 Aug;6(16):2407–2418. doi: 10.1111/j.1365-2958.1992.tb01415.x. [DOI] [PubMed] [Google Scholar]
  59. Goldberg M. B., Boyko S. A., Calderwood S. B. Positive transcriptional regulation of an iron-regulated virulence gene in Vibrio cholerae. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1125–1129. doi: 10.1073/pnas.88.4.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Goldberg M. B., Boyko S. A., Calderwood S. B. Transcriptional regulation by iron of a Vibrio cholerae virulence gene and homology of the gene to the Escherichia coli fur system. J Bacteriol. 1990 Dec;172(12):6863–6870. doi: 10.1128/jb.172.12.6863-6870.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Goldberg M. B., DiRita V. J., Calderwood S. B. Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis. Infect Immun. 1990 Jan;58(1):55–60. doi: 10.1128/iai.58.1.55-60.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Grant C. C., Vasil M. L. Analysis of transcription of the exotoxin A gene of Pseudomonas aeruginosa. J Bacteriol. 1986 Dec;168(3):1112–1119. doi: 10.1128/jb.168.3.1112-1119.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Griffiths E., Stevenson P., Ray A. Antigenic and molecular heterogeneity of the transferrin-binding protein of Neisseria meningitidis. FEMS Microbiol Lett. 1990 May;57(1-2):31–36. doi: 10.1016/0378-1097(90)90408-i. [DOI] [PubMed] [Google Scholar]
  64. Hantke K. Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol Gen Genet. 1984;197(2):337–341. doi: 10.1007/BF00330982. [DOI] [PubMed] [Google Scholar]
  65. Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182(2):288–292. doi: 10.1007/BF00269672. [DOI] [PubMed] [Google Scholar]
  66. Hart R. C., Kadis S., Chapman W. L., Jr Nutritional iron status and susceptibility to Proteus mirabilis pyelonephritis in the rat. Can J Microbiol. 1982 Jun;28(6):713–717. doi: 10.1139/m82-108. [DOI] [PubMed] [Google Scholar]
  67. Helms S. D., Oliver J. D., Travis J. C. Role of heme compounds and haptoglobin in Vibrio vulnificus pathogenicity. Infect Immun. 1984 Aug;45(2):345–349. doi: 10.1128/iai.45.2.345-349.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Henikoff S., Haughn G. W., Calvo J. M., Wallace J. C. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. doi: 10.1073/pnas.85.18.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Hindahl M. S., Frank D. W., Iglewski B. H. Molecular studies of a positive regulator of toxin A synthesis in Pseudomonas aeruginosa. Antibiot Chemother (1971) 1987;39:279–289. doi: 10.1159/000414353. [DOI] [PubMed] [Google Scholar]
  70. Holbein B. E. Enhancement of Neisseria meningitidis infection in mice by addition of iron bound to transferrin. Infect Immun. 1981 Oct;34(1):120–125. doi: 10.1128/iai.34.1.120-125.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Holbein B. E. Iron-controlled infection with Neisseria meningitidis in mice. Infect Immun. 1980 Sep;29(3):886–891. doi: 10.1128/iai.29.3.886-891.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Honjo T., Nishizuka Y., Kato I., Hayaishi O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J Biol Chem. 1971 Jul 10;246(13):4251–4260. [PubMed] [Google Scholar]
  73. Iglewski B. H., Kabat D. NAD-dependent inhibition of protein synthesis by Pseudomonas aeruginosa toxin,. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2284–2288. doi: 10.1073/pnas.72.6.2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Johnson W. M., Lior H., Bezanson G. S. Cytotoxic Escherichia coli O157:H7 associated with haemorrhagic colitis in Canada. Lancet. 1983 Jan 1;1(8314-5):76–76. doi: 10.1016/s0140-6736(83)91616-1. [DOI] [PubMed] [Google Scholar]
  75. Kaczorek M., Zettlmeissl G., Delpeyroux F., Streeck R. E. Diphtheria toxin promoter function in Corynebacterium diphtheriae and Escherichia coli. Nucleic Acids Res. 1985 May 10;13(9):3147–3159. doi: 10.1093/nar/13.9.3147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Kanei C., Uchida T., Yoneda M. Isolation from corynebacterium diphtheriae C7(beta) of bacterial mutants that produce toxin in medium with excess iron. Infect Immun. 1977 Oct;18(1):203–209. doi: 10.1128/iai.18.1.203-209.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Karmali M. A., Petric M., Lim C., Fleming P. C., Arbus G. S., Lior H. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis. 1985 May;151(5):775–782. doi: 10.1093/infdis/151.5.775. [DOI] [PubMed] [Google Scholar]
  78. Keown P., Descamps-Latscha B. In vitro suppression of cell-mediated immunity by ferroproteins and ferric salts. Cell Immunol. 1983 Sep;80(2):257–266. doi: 10.1016/0008-8749(83)90114-4. [DOI] [PubMed] [Google Scholar]
  79. Lawlor K. M., Daskaleros P. A., Robinson R. E., Payne S. M. Virulence of iron transport mutants of Shigella flexneri and utilization of host iron compounds. Infect Immun. 1987 Mar;55(3):594–599. doi: 10.1128/iai.55.3.594-599.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Lawlor K. M., Payne S. M. Aerobactin genes in Shigella spp. J Bacteriol. 1984 Oct;160(1):266–272. doi: 10.1128/jb.160.1.266-272.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Leffell M. S., Spitznagel J. K. Fate of human lactoferrin and myeloperoxidase in phagocytizing human neutrophils: effects of immunoglobulin G subclasses and immune complexes coated on latex beads. Infect Immun. 1975 Oct;12(4):813–820. doi: 10.1128/iai.12.4.813-820.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Leong D., Murphy J. R. Characterization of the diphtheria tox transcript in Corynebacterium diphtheriae and Escherichia coli. J Bacteriol. 1985 Sep;163(3):1114–1119. doi: 10.1128/jb.163.3.1114-1119.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Linggood M. A., Ingram P. L. The role of alpha haemolysin in the virulence of Escherichia coli for mice. J Med Microbiol. 1982 Feb;15(1):23–30. doi: 10.1099/00222615-15-1-23. [DOI] [PubMed] [Google Scholar]
  84. Litwin C. M., Boyko S. A., Calderwood S. B. Cloning, sequencing, and transcriptional regulation of the Vibrio cholerae fur gene. J Bacteriol. 1992 Mar;174(6):1897–1903. doi: 10.1128/jb.174.6.1897-1903.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Liu P. V. Exotoxins of Pseudomonas aeruginosa. I. Factors that influence the production of exotoxin A. J Infect Dis. 1973 Oct;128(4):506–513. doi: 10.1093/infdis/128.4.506. [DOI] [PubMed] [Google Scholar]
  86. Lory S. Effect of iron on accumulation of exotoxin A-specific mRNA in Pseudomonas aeruginosa. J Bacteriol. 1986 Dec;168(3):1451–1456. doi: 10.1128/jb.168.3.1451-1456.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Marolda C. L., Valvano M. A., Lawlor K. M., Payne S. M., Crosa J. H. Flanking and internal regions of chromosomal genes mediating aerobactin iron uptake systems in enteroinvasive Escherichia coli and Shigella flexneri. J Gen Microbiol. 1987 Aug;133(8):2269–2278. doi: 10.1099/00221287-133-8-2269. [DOI] [PubMed] [Google Scholar]
  88. McDougall S., Neilands J. B. Plasmid- and chromosome-coded aerobactin synthesis in enteric bacteria: insertion sequences flank operon in plasmid-mediated systems. J Bacteriol. 1984 Jul;159(1):300–305. doi: 10.1128/jb.159.1.300-305.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. McKenna W. R., Mickelsen P. A., Sparling P. F., Dyer D. W. Iron uptake from lactoferrin and transferrin by Neisseria gonorrhoeae. Infect Immun. 1988 Apr;56(4):785–791. doi: 10.1128/iai.56.4.785-791.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Melby K., Slørdahl S., Gutteberg T. J., Nordbø S. A. Septicaemia due to Yersinia enterocolitica after oral overdoses of iron. Br Med J (Clin Res Ed) 1982 Aug 14;285(6340):467–468. doi: 10.1136/bmj.285.6340.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Mickelsen P. A., Blackman E., Sparling P. F. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from lactoferrin. Infect Immun. 1982 Mar;35(3):915–920. doi: 10.1128/iai.35.3.915-920.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Mickelsen P. A., Sparling P. F. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds. Infect Immun. 1981 Aug;33(2):555–564. doi: 10.1128/iai.33.2.555-564.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Middlebrook J. L., Dorland R. B. Response of cultured mammalian cells to the exotoxins of Pseudomonas aeruginosa and Corynebacterium diphtheriae: differential cytotoxicity. Can J Microbiol. 1977 Feb;23(2):183–189. doi: 10.1139/m77-026. [DOI] [PubMed] [Google Scholar]
  94. Miller J. F., Mekalanos J. J., Falkow S. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science. 1989 Feb 17;243(4893):916–922. doi: 10.1126/science.2537530. [DOI] [PubMed] [Google Scholar]
  95. Minshew B. H., Jorgensen J., Counts G. W., Falkow S. Association of hemolysin production, hemagglutination of human erythrocytes, and virulence for chicken embryos of extraintestinal Escherichia coli isolates. Infect Immun. 1978 Apr;20(1):50–54. doi: 10.1128/iai.20.1.50-54.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Morse S. A., Chen C. Y., LeFaou A., Mietzner T. A. A potential role for the major iron-regulated protein expressed by pathogenic Neisseria species. Rev Infect Dis. 1988 Jul-Aug;10 (Suppl 2):S306–S310. doi: 10.1093/cid/10.supplement_2.s306. [DOI] [PubMed] [Google Scholar]
  97. Muller D., Edwards M. L., Smith D. W. Changes in iron and transferrin levels and body temperature in experimental airborne legionellosis. J Infect Dis. 1983 Feb;147(2):302–307. doi: 10.1093/infdis/147.2.302. [DOI] [PubMed] [Google Scholar]
  98. Murphy J. R., Skiver J., McBride G. Isolation and partial characterization of a corynebacteriophage beta, tox operator constitutive-like mutant lysogen of Corynebacterium diphtheriae. J Virol. 1976 Apr;18(1):235–244. doi: 10.1128/jvi.18.1.235-244.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Neilands J. B. Microbial envelope proteins related to iron. Annu Rev Microbiol. 1982;36:285–309. doi: 10.1146/annurev.mi.36.100182.001441. [DOI] [PubMed] [Google Scholar]
  100. 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]
  101. O'Brien A. D., LaVeck G. D. Purification and characterization of a Shigella dysenteriae 1-like toxin produced by Escherichia coli. Infect Immun. 1983 May;40(2):675–683. doi: 10.1128/iai.40.2.675-683.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. O'Brien A. D., LaVeck G. D., Thompson M. R., Formal S. B. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J Infect Dis. 1982 Dec;146(6):763–769. doi: 10.1093/infdis/146.6.763. [DOI] [PubMed] [Google Scholar]
  103. O'Brien A. D., Newland J. W., Miller S. F., Holmes R. K., Smith H. W., Formal S. B. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science. 1984 Nov 9;226(4675):694–696. doi: 10.1126/science.6387911. [DOI] [PubMed] [Google Scholar]
  104. Olsnes S., Reisbig R., Eiklid K. Subunit structure of Shigella cytotoxin. J Biol Chem. 1981 Aug 25;256(16):8732–8738. [PubMed] [Google Scholar]
  105. Opal S. M., Cross A. S., Gemski P., Lyhte L. W. Aerobactin and alpha-hemolysin as virulence determinants in Escherichia coli isolated from human blood, urine, and stool. J Infect Dis. 1990 Apr;161(4):794–796. doi: 10.1093/infdis/161.4.794. [DOI] [PubMed] [Google Scholar]
  106. Padda J. S., Schryvers A. B. N-linked oligosaccharides of human transferrin are not required for binding to bacterial transferrin receptors. Infect Immun. 1990 Sep;58(9):2972–2976. doi: 10.1128/iai.58.9.2972-2976.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Payne S. M., Finkelstein R. A. Pathogenesis and immunology of experimental gonococcal infection: role of iron in virulence. Infect Immun. 1975 Dec;12(6):1313–1318. doi: 10.1128/iai.12.6.1313-1318.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Perry R. D., Brubaker R. R. Accumulation of iron by yersiniae. J Bacteriol. 1979 Mar;137(3):1290–1298. doi: 10.1128/jb.137.3.1290-1298.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Prince R. W., Storey D. G., Vasil A. I., Vasil M. L. Regulation of toxA and regA by the Escherichia coli fur gene and identification of a Fur homologue in Pseudomonas aeruginosa PA103 and PA01. Mol Microbiol. 1991 Nov;5(11):2823–2831. doi: 10.1111/j.1365-2958.1991.tb01991.x. [DOI] [PubMed] [Google Scholar]
  110. Puschmann M., Ganzoni A. M. Increased resistance of iron-deficient mice to salmonella infection. Infect Immun. 1977 Sep;17(3):663–664. doi: 10.1128/iai.17.3.663-664.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Reisbig R., Olsnes S., Eiklid K. The cytotoxic activity of Shigella toxin. Evidence for catalytic inactivation of the 60 S ribosomal subunit. J Biol Chem. 1981 Aug 25;256(16):8739–8744. [PubMed] [Google Scholar]
  112. Robins-Browne R. M., Prpic J. K. Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar;47(3):774–779. doi: 10.1128/iai.47.3.774-779.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Russell L. M., Cryz S. J., Jr, Holmes R. K. Genetic and biochemical evidence for a siderophore-dependent iron transport system in Corynebacterium diphtheriae. Infect Immun. 1984 Jul;45(1):143–149. doi: 10.1128/iai.45.1.143-149.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. SMITH H. W. The haemolysins of Escherichia coli. J Pathol Bacteriol. 1963 Jan;85:197–211. doi: 10.1002/path.1700850119. [DOI] [PubMed] [Google Scholar]
  115. Salinas P. C., Tolmasky M. E., Crosa J. H. Regulation of the iron uptake system in Vibrio anguillarum: evidence for a cooperative effect between two transcriptional activators. Proc Natl Acad Sci U S A. 1989 May;86(10):3529–3533. doi: 10.1073/pnas.86.10.3529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Saxena S. K., O'Brien A. D., Ackerman E. J. Shiga toxin, Shiga-like toxin II variant, and ricin are all single-site RNA N-glycosidases of 28 S RNA when microinjected into Xenopus oocytes. J Biol Chem. 1989 Jan 5;264(1):596–601. [PubMed] [Google Scholar]
  117. Schmitt M. P., Holmes R. K. Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene dtxR in C. diphtheriae C7 strains. Infect Immun. 1991 Jun;59(6):1899–1904. doi: 10.1128/iai.59.6.1899-1904.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Schryvers A. B., Morris L. J. Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol Microbiol. 1988 Mar;2(2):281–288. doi: 10.1111/j.1365-2958.1988.tb00029.x. [DOI] [PubMed] [Google Scholar]
  119. Schäffer S., Hantke K., Braun V. Nucleotide sequence of the iron regulatory gene fur. Mol Gen Genet. 1985;200(1):110–113. doi: 10.1007/BF00383321. [DOI] [PubMed] [Google Scholar]
  120. Sokol P. A., Cox C. D., Iglewski B. H. Pseudomonas aeruginosa mutants altered in their sensitivity to the effect of iron on toxin A or elastase yields. J Bacteriol. 1982 Aug;151(2):783–787. doi: 10.1128/jb.151.2.783-787.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Staggs T. M., Perry R. D. Fur regulation in Yersinia species. Mol Microbiol. 1992 Sep;6(17):2507–2516. doi: 10.1111/j.1365-2958.1992.tb01427.x. [DOI] [PubMed] [Google Scholar]
  122. Staggs T. M., Perry R. D. Identification and cloning of a fur regulatory gene in Yersinia pestis. J Bacteriol. 1991 Jan;173(2):417–425. doi: 10.1128/jb.173.2.417-425.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Stoebner J. A., Payne S. M. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect Immun. 1988 Nov;56(11):2891–2895. doi: 10.1128/iai.56.11.2891-2895.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Storey D. G., Raivio T. L., Frank D. W., Wick M. J., Kaye S., Iglewski B. H. Effect of regB on expression from the P1 and P2 promoters of the Pseudomonas aeruginosa regAB operon. J Bacteriol. 1991 Oct;173(19):6088–6094. doi: 10.1128/jb.173.19.6088-6094.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Strockbine N. A., Jackson M. P., Sung L. M., Holmes R. K., O'Brien A. D. Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1. J Bacteriol. 1988 Mar;170(3):1116–1122. doi: 10.1128/jb.170.3.1116-1122.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Strockbine N. A., Marques L. R., Newland J. W., Smith H. W., Holmes R. K., O'Brien A. D. Two toxin-converting phages from Escherichia coli O157:H7 strain 933 encode antigenically distinct toxins with similar biologic activities. Infect Immun. 1986 Jul;53(1):135–140. doi: 10.1128/iai.53.1.135-140.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Stull T. L. Protein sources of heme for Haemophilus influenzae. Infect Immun. 1987 Jan;55(1):148–153. doi: 10.1128/iai.55.1.148-153.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Sung L. M., Jackson M. P., O'Brien A. D., Holmes R. K. Transcription of the Shiga-like toxin type II and Shiga-like toxin type II variant operons of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6386–6395. doi: 10.1128/jb.172.11.6386-6395.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Tai S. P., Holmes R. K. Iron regulation of the cloned diphtheria toxin promoter in Escherichia coli. Infect Immun. 1988 Sep;56(9):2430–2436. doi: 10.1128/iai.56.9.2430-2436.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Tai S. P., Krafft A. E., Nootheti P., Holmes R. K. Coordinate regulation of siderophore and diphtheria toxin production by iron in Corynebacterium diphtheriae. Microb Pathog. 1990 Oct;9(4):267–273. doi: 10.1016/0882-4010(90)90015-i. [DOI] [PubMed] [Google Scholar]
  131. Tolmasky M. E., Salinas P. C., Actis L. A., Crosa J. H. Increased production of the siderophore anguibactin mediated by pJM1-like plasmids in Vibrio anguillarum. Infect Immun. 1988 Jun;56(6):1608–1614. doi: 10.1128/iai.56.6.1608-1614.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Tullus K., Jacobson S. H., Katouli M., Brauner A. Relative importance of eight virulence characteristics of pyelonephritogenic Escherichia coli strains assessed by multivariate statistical analysis. J Urol. 1991 Oct;146(4):1153–1155. doi: 10.1016/s0022-5347(17)38029-1. [DOI] [PubMed] [Google Scholar]
  133. Uchida T., Gill D. M., Pappenheimer A. M., Jr Mutation in the structural gene for diphtheria toxin carried by temperate phage . Nat New Biol. 1971 Sep 1;233(35):8–11. doi: 10.1038/newbio233008a0. [DOI] [PubMed] [Google Scholar]
  134. VAN HEYNINGEN W. E., GLADSTONE G. P. The neurotoxin of Shigella shigae. III. The effect of iron on production of the toxin. Br J Exp Pathol. 1953 Apr;34(2):221–229. [PMC free article] [PubMed] [Google Scholar]
  135. Valvano M. A., Crosa J. H. Aerobactin iron transport genes commonly encoded by certain ColV plasmids occur in the chromosome of a human invasive strain of Escherichia coli K1. Infect Immun. 1984 Oct;46(1):159–167. doi: 10.1128/iai.46.1.159-167.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Van Snick J. L., Masson P. L., Heremans J. F. The involvement of lactoferrin in the hyposideremia of acute inflammation. J Exp Med. 1974 Oct 1;140(4):1068–1084. doi: 10.1084/jem.140.4.1068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Waalwijk C., MacLaren D. M., de Graaff J. In vivo function of hemolysin in the nephropathogenicity of Escherichia coli. Infect Immun. 1983 Oct;42(1):245–249. doi: 10.1128/iai.42.1.245-249.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. Walter M. A., Potter S. A., Crosa J. H. Iron uptake system medicated by Vibrio anguillarum plasmid pJM1. J Bacteriol. 1983 Nov;156(2):880–887. doi: 10.1128/jb.156.2.880-887.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. Ward C. G., Hammond J. S., Bullen J. J. Effect of iron compounds on antibacterial function of human polymorphs and plasma. Infect Immun. 1986 Mar;51(3):723–730. doi: 10.1128/iai.51.3.723-730.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Warner P. J., Williams P. H., Bindereif A., Neilands J. B. ColV plasmid-specific aerobactin synthesis by invasive strains of Escherichia coli. Infect Immun. 1981 Aug;33(2):540–545. doi: 10.1128/iai.33.2.540-545.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  141. Weinberg E. D. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. doi: 10.1152/physrev.1984.64.1.65. [DOI] [PubMed] [Google Scholar]
  142. Welkos S. L., Holmes R. K. Regulation of toxinogenesis in Corynebacterium diphtheriae. I. Mutations in bacteriophage beta that alter the effects of iron on toxin production. J Virol. 1981 Mar;37(3):936–945. doi: 10.1128/jvi.37.3.936-945.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. West S. E., Sparling P. F. Response of Neisseria gonorrhoeae to iron limitation: alterations in expression of membrane proteins without apparent siderophore production. Infect Immun. 1985 Feb;47(2):388–394. doi: 10.1128/iai.47.2.388-394.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Williams P. H. Novel iron uptake system specified by ColV plasmids: an important component in the virulence of invasive strains of Escherichia coli. Infect Immun. 1979 Dec;26(3):925–932. doi: 10.1128/iai.26.3.925-932.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Williams P. H., Warner P. J. ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infect Immun. 1980 Aug;29(2):411–416. doi: 10.1128/iai.29.2.411-416.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Wochner R. D., Spilberg I., Iio A., Liem H. H., Muller-Eberhard U. Hemopexin metabolism in sickle-cell disease, porphyrias and control subjects--effects of heme injection. N Engl J Med. 1974 Apr 11;290(15):822–826. doi: 10.1056/NEJM197404112901503. [DOI] [PubMed] [Google Scholar]
  147. Woods D. E., Iglewski B. H. Toxins of Pseudomonas aeruginosa: new perspectives. Rev Infect Dis. 1983 Sep-Oct;5 (Suppl 4):S715–S722. doi: 10.1093/clinids/5.supplement_4.s715. [DOI] [PubMed] [Google Scholar]
  148. Wright A. C., Simpson L. M., Oliver J. D. Role of iron in the pathogenesis of Vibrio vulnificus infections. Infect Immun. 1981 Nov;34(2):503–507. doi: 10.1128/iai.34.2.503-507.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Wright D. G., Gallin J. I. Secretory responses of human neutrophils: exocytosis of specific (secondary) granules by human neutrophils during adherence in vitro and during exudation in vivo. J Immunol. 1979 Jul;123(1):285–294. [PubMed] [Google Scholar]
  150. Yancey R. J., Finkelstein R. A. Assmilation of iron by pathogenic Neisseria spp. Infect Immun. 1981 May;32(2):592–599. doi: 10.1128/iai.32.2.592-599.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. de Lorenzo V., Neilands J. B. Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coli. J Bacteriol. 1986 Jul;167(1):350–355. doi: 10.1128/jb.167.1.350-355.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. de Lorenzo V., Wee S., Herrero M., Neilands J. B. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol. 1987 Jun;169(6):2624–2630. doi: 10.1128/jb.169.6.2624-2630.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Clinical Microbiology Reviews are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES