Bordetella Adenylate Cyclase-Hemolysin Toxins
Abstract
:1. Introduction
2. Bordetella pertussis Adenylate Cyclase-Hemolysin Toxin
2.1. Structure
2.2. Regulation of Expression
2.3. Biological Activities
2.4. Role As a Toxin
- (i)
- Bp AC-Hly is able to induce apoptosis of macrophages in vitro and in vivo [36,37]. Apoptotic death of bronchopulmonary cells in vivo was observed exclusively following intranasal infection with bacteria re-isolated from the lungs of infected mice and not with B. pertussis collected after in vitro subculture [24]. Depletion of ATP, as a result of adenylate cyclase activity, might be sufficient for macrophage cytotoxicity, but an unconventional calcium influx mediated by the translocating AC domain may also contribute to cytotoxic effects [38,39]. Bp AC-Hly-deficient mutants were shown to be more efficiently phagocytosed by human neutrophils [40], stressing the importance of Bp AC-Hly in targeting phagocytic cells for B. pertussis pathogenesis. However, neutrophil depletion did not enhance infection by Bp AC-Hly-deficient B. pertussis mutants in naive mice, but in neutrophil-depleted immune (previously infected) mice; the Bp AC-Hly-deficient mutants are as virulent as the parental strain, indicating that the toxin is important in neutrophil inhibition only in the presence of opsonizing antibodies [41].
- (ii)
- B. pertussis, as well as Bp AC-Hly, are not cytotoxic for human tracheal epithelial cells [42]. However, we observed induction of IL-6 production by Bp AC-Hly in human tracheal epithelial cells in vitro [43], which enhances recruitment of neutrophils during infection. This observation correlates with our in vivo experiments using the murine respiratory model [24,44].
- (iii)
- Bp AC-Hly production, as well as that of PRN (probably indirectly via its interaction with AC-Hly), inhibits invasion of B. pertussis in human tracheal cells, whereas FHA favors this process [42]. It is possible that B. pertussis could have evolved anti-invasive mechanisms such as production of AC-Hly to avoid destruction within tracheal epithelial cells. Martin et al., using B. pertussis recombinant AC-Hly, showed that the toxin promotes bacterial internalization into non-phagocytic cells. They hypothesize that this internalization favors the persistence of the bacteria in the host. However, they didn’t (a) use human tracheal cells, (b) verify the survival of the bacteria inside the cells, and (c) discuss the fact that B. pertussis was not shown to induce persistent or chronic infection in humans, even in immuno-suppressed patients in contrast to some other Bordetella species [45]. Further experiments are, therefore, required to investigate these issues.
- (iv)
- While the action of Bp AC-Hly appears to first inhibit bactericidal functions of host innate immunity, such as neutrophils and macrophages, the toxin is likely to have effects on adaptive immunity as well. Bp AC-Hly might mediate an escape strategy for the bacterium, since it reduces Th1 immunity and increases Th17 responses thought to be responsible for enhanced lung inflammation [24,37,44,46,47,48,49].
2.5. Immunogenicity
2.6. Role as a Protective Antigen
3. Bordetella parapertussis and B. bronchiseptica Adenylate Cyclase-Hemolysin Toxins
3.1. Structure
3.2. Regulation of Expression
3.3. Biological Activities
3.4. Role As a Protective Antigen
4. Conclusions
- (i)
- Can genetically inactivated Bp AC-Hly produced by B. pertussis be used? A B. pertussis mutant carrying double mutations in the cyaA gene could be used [82]. This double mutant produces a toxoid devoid of both adenylate cyclase and pore-forming activities that may be a suitable antigen for inclusion in a next generation of acellular pertussis vaccines [82]. However, it is well known that the amount of AC-Hly produced by B. pertussis is very low. Moreover, Bp AC-Hly is a hydrophobic protein that aggregates or is degraded during purification and needs urea to be solubilized [14,83];
- (ii)
- Can the genetically detoxified r-Bp AC-Hly, produced by E. coli K-12, be used? It has been demonstrated that large-scale production of detoxified r-Bp AC-Hly is now possible and clinical cGMP batches have been produced and tested as safe in Phase I clinical trials of T-cell vaccines developed for cancer immunotherapy [83]. However, it was previously shown that the protective activity of Bp AC-Hly and r-Bp AC-Hly were different. This was hypothesized to be due to the different PTM of both proteins [17]. However, we recently showed that this might not be the case [18]. We favor the hypothesis that the difference might be due to the interactions with FHA, PRN and LPS for the final conformation of Bp AC-Hly [19,20,70,71]. Additional investigations are, therefore, requested to test the detoxified r-Bp AC-Hly as an antigen;
- (iii)
- Can the recombinant monomeric polypeptide which has been recently isolated [14] be used? First, it is necessary to demonstrate that a detoxified monomer induces a protective immunity. Moreover, the production of a high amount of monomeric polypeptide remains to be solved;
- (iv)
- Can the C-terminal fragment of the toxin produced by E. coli K-12 (and bearing the PTM) be used? It needs to be confirmed that this recombinant fragment, which induces the synthesis of neutralizing antibodies, also induces a protective immunity, at least in the murine model [58,59]. In fact, we showed, using several different fragments of the r-Bp AC-Hly, that there is no correlation between induction of the neutralizing antibody and induction of a protective immunity [52];
- (v)
- Can Outer Membrane Vesicule (OMV) produced by B. pertussis be used? Bacterial OMV naturally contain bacterial surface antigens. The composition of the pertussis OMV was characterized as containing >200 protein components, including the virulence factors PT, PRN, FHA, FIM and AC-Hly. [84,85]. The production of Bp OMV has been developed: (a) the interactions between virulence factors and LPS are preserved; (b) they are immunogenic; (c) they induce an immunity close to that induced after natural infection; (d) they are less reactogenic than pertussis whole-cell vaccines; and (e) induce a protective immunity [84,85]. Furthermore, they contain more antigens than pertussis acellular vaccines and so are less susceptible to inducing the phenomenon of “antigenic sin” [53]. Detoxified Bp OMV can be developed. However, this development will also need further research;
- (vi)
- Can a mixture of B. pertussis and B. parapertussis OMVs be used? As shown in France, the circulation of B. parapertussis has been slowly increasing for a decade [86]. The increase can be due either to the use of pertussis acellular vaccine or to the evolution of the Bordetella species [1,87]. The circulation of B. parapertussis has also now been detected in the USA, a country using an acellular pertussis vaccine, but also in Pakistan, a country using a whole-cell pertussis vaccine [3,88]. This means that it could be advantageous to use a vaccine containing both detoxified Bp OMV and Bpp OMV, although it has been shown that Bpp OMV might induce protection against B. pertussis and B. parapertussis infection [84].
Acknowledgments
Conflicts of Interest
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Guiso, N. Bordetella Adenylate Cyclase-Hemolysin Toxins. Toxins 2017, 9, 277. https://doi.org/10.3390/toxins9090277
Guiso N. Bordetella Adenylate Cyclase-Hemolysin Toxins. Toxins. 2017; 9(9):277. https://doi.org/10.3390/toxins9090277
Chicago/Turabian StyleGuiso, Nicole. 2017. "Bordetella Adenylate Cyclase-Hemolysin Toxins" Toxins 9, no. 9: 277. https://doi.org/10.3390/toxins9090277