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Chapter 2 : Regulation of Bacterial Toxin Synthesis by Iron

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Regulation of Bacterial Toxin Synthesis by Iron, Page 1 of 2

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Abstract:

Iron availability is one of the regulators of catalase and superoxide dismutase gene expression, and the oxidative stress-response regulators OxyR and SoxRS influence expression of the iron regulator gene in . The discussion of three iron-regulated toxins, diphtheria toxin, Shiga toxin, and exotoxin A, in this chapter illustrates the similarities and differences in the control mechanisms using bacterial toxin regulation. exotoxin A has the most complex regulation of the three; regulation by an iron-binding repressor is one step in a cascade of positive and negative regulators that act in concert to control toxin expression. The functions of some of these iron-regulated promoter (irp) genes have not been determined as yet. Like for diphtheria toxin, iron was shown to be the component of media that reduced production of the Shiga toxin. The mutation resulted in loss of repression in high iron. Studies were done with the cloned toxin genes, and the construct lacked phage sequences that could influence regulation. Thus, the effect of iron and Fur, independent of potential prophage regulators, was determined in the studies. The Shiga toxin gene appears to have identical iron regulation as . Repression of toxin synthesis by iron is observed in a number of unrelated pathogens. In each case, an iron-binding repressor protein provides the link between elevated iron levels in the environment and repression of toxin synthesis.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2

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Mobile Genetic Elements
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Figures

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Figure 1

Bacterial growth and toxin production as a function of iron concentration of the medium. The solid line indicates the total amount of toxin in the culture, and the dashed line indicates the final cell density as the concentration of iron increases.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 2
Figure 2

Regulation of diphtheria toxin gene () expression. The line indicates bacterial DNA, and the open box indicates prophage sequences. The prophage is drawn in the opposite orientation so that the gene is shown 5' to 3'. The sequence below the promoter and operator region is the DtxR-binding site.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 3
Figure 3

Comparison of DtxR-binding sites of selected promoters. The sequences for DtxR binding to (heme oxygenase), and (an iron-regulated promoter) are shown for comparison. The consensus sequence derived from these and other iron-regulated promoters is shown below, with arrows indicating the inverted repeat. Bold type indicates the two bases shown to be critical for DtxR binding to the promoter.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 4
Figure 4

Organization of the Shiga toxin genes in and . Portions of the lambdoid phages encoding Stx1 (StxI; ) and Stx2 (StxII; ) are shown. The organization of the same region of λ is shown for comparison. The dashed lines indicate that the distances are not drawn to scale. Highly homologous genes are indicated by the same hatching. Solid boxes are insertion sequences.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 5
Figure 5

Comparison of the Fur boxes of iron-regulated promoters of , , and . The DNA sequence of the known or predicted Fur binding sites in the promoters for , Shiga toxin gene, the aerobactin siderophore operon (), , and the and genes. The consensus binding site for Fur in gram-negative bacteria is shown. The longer arrows indicate the palindrome, and the shorter arrows and bold letters indicate the core repeat units.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 6
Figure 6

Regulation of Shiga toxin gene () expression. The sequence below the promoter and operator region is the Fur-binding site or Fur box.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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Image of Figure 7
Figure 7

Model of iron regulation of exotoxin A synthesis. Genes and gene products that regulate expression of are shown. Solid arrows indicate positive regulation by the indicated protein. Open arrow indicates negative regulation.

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2
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References

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1. Calderwood, S. B.,, and J. J. Mekalanos. 1987. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J. Bacteriol. 169:47594764.
2. Escolar, L.,, J. Pérez-Martín,, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:62236229.
3. Frank, D. W.,, D. G. Storey,, M. S. Hindahl,, and B. H. Iglewski. 1989. Differential regulation by iron of regA and toxA transcript accumulation in Pseudomonas aeruginosa. J. Bacteriol. 171:53045313.
4. Hantke, K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4:172177.
5. McDonough, M. A.,, and J. R. Butterton. 1999. Spontaneous tandem amplification and deletion of the Shiga toxin operon in Shigella dysenteriae 1. Mol. Microbiol. 34: 10581069.
6. Murphy, J. R.,, A. M. Pappenheimer, Jr.,, and S. Tayart de Borms. 1974. Synthesis of diphtheria tox-gene products in Escherichia coli extracts. Proc. Natl. Acad. Sci. USA 71: 1115.
7. Pappenheimer, A. M., Jr.,, and S. J. Johnson. 1936. Studies in diphtheria toxin production. I: the effect of iron and copper. Br. J. Exp. Pathol. 17:335341.
8. Qiu, X.,, C. L. Verlinde,, S. Zhang,, M. P. Schmitt,, R. K. Holmes,, and W. G. Hol. 1995. Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors. Structure 3:87100.
9. Sung, L. M.,, M. P. Jackson,, A. D. O’Brien,, and R. K. Holmes. 1990. Transcription of the Shiga-like toxin type II variant operons of Escherichia coli. J. Bacteriol. 172:63866395.
10. Vasil, M. L.,, and U. A. Ochsner. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol. Microbiol. 34:399413.
11. White, A.,, X. Ding,, J. C. van der Spek,, J. R. Murphy,, and D. Ringe. 1998. Structure of the metal-ion-activated diphtheria toxin repressor/tox operator complex. Nature 394:502506.

Tables

Generic image for table
Table 1

Toxins and other secreted virulence proteins whose synthesis is negatively regulated by iron

Citation: Payne S. 2003. Regulation of Bacterial Toxin Synthesis by Iron, p 25-38. In Burns D, Barbieri J, Iglewski B, Rappuoli R (ed), Bacterial Protein Toxins. ASM Press, Washington, DC. doi: 10.1128/9781555817893.ch2

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