Regulatory and Structural Differences in the Cu,Zn-Superoxide Dismutases of Salmonella enterica and Their Significance for Virulence

Ammendola, Serena; Pasquali, Paolo; Pacello, Francesca; Rotilio, Giuseppe; Castor, Margaret; Libby, Stephen J.; Figueroa‐Bossi, Nara; Bossi, Lionello; Fang, Ferric C.; Battistoni, Andrea

doi:10.1074/jbc.m710499200

Cited by 56 publications

(94 citation statements)

References 68 publications

(116 reference statements)

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“…This hypothesis was supported by the role of SodC in other bacteria. Hfq is required for the optimal production of SodC during stationary phase in B. abortus (30), and SodC-defective strains of B. abortus (30) or S. enterica (2) are affected in virulence. Nevertheless, this is not true in all bacteria, since the lack of SodC in Haemophilus ducreyi has no consequence on the virulence (13).…”

Section: Discussionmentioning

confidence: 99%

Proteomic Alterations Explain Phenotypic Changes in Sinorhizobium meliloti Lacking the RNA Chaperone Hfq

et al. 2010

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The ubiquitous bacterial RNA-binding protein Hfq is involved in stress resistance and pathogenicity. In Sinorhizobium meliloti, Hfq is essential for the establishment of symbiosis with Medicago sativa and for nitrogen fixation. A proteomic analysis identifies 55 proteins with significantly affected expression in the hfq mutant; most of them are involved in cell metabolism or stress resistance. Important determinants of oxidative stress resistance, such as CysK, Gsh, Bfr, SodC, KatB, KatC, and a putative peroxiredoxine (SMc00072), are downregulated in the hfq mutant. The hfq mutant is affected for H 2 O 2 , menadione, and heat stress resistance. Part of these defects could result from the reductions of rpoE1, rpoE2, rpoE3, and rpoE4 expression levels in the hfq mutant. Some proteins required for efficient symbiosis are reduced in the hfq mutant, contributing to the drastic defect in nodulation observed in this mutant.Gene expression in bacteria is regulated by a wide diversity of mechanisms, including alternative sigma factors, transcriptional regulatory proteins, attenuation mechanisms (including riboswitches) (15), and translational and posttranslational regulations (37). The interplay of central regulatory proteins and alternative sigma factors allows the creation of complex regulatory networks modulating transcription (4).Compared to transcription regulation, the mechanisms affecting the regulation of translation are less understood. Studies dedicated to translation regulation have increased over the past few years (55,76,77). An important development has been the recognition of small regulatory RNAs (sRNAs) that have emerged as crucial actors of translation regulation. In enterobacteria, most sRNAs require Hfq to complex with their targets. Hfq is an RNA chaperone necessary for the pairing of sRNAs with mRNAs (40). Furthermore, Hfq affects translation efficiency by allowing the polyadenylation of specific mRNAs (44). Thus, Hfq is a central actor in translation regulation (72). Hfq is also able to affect transcription, directly by coupling with RNA polymerase (67) or indirectly via its action on sRNAs modulating translation of sigma factors (19,32,69).Due to its central role, hfq inactivation results in a pleiotropic phenotype in enterobacteria and Brucella abortus, including growth defects, stress susceptibility, and altered pathogenicity (56,65,76). Our accompanying study shows that loss of hfq impairs the ability of Sinorhizobium meliloti to establish a nitrogen-fixing symbiosis with its legume host, Medicago sativa. S. meliloti faces numerous stresses during the course of invading the developing root nodules and colonizing the plant cells (21,22,35,46,62). Bacterial abilities to resist and adapt to these stresses are of crucial importance for the symbiosis. Oxidative stress has been the most intensively investigated stress that S. meliloti must withstand and appears as a key factor for bacterium-plant cell interaction. To cope with oxidative stress, S. meliloti cells posses a detoxification system involvi...

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Section: Discussionmentioning

confidence: 99%

Proteomic Alterations Explain Phenotypic Changes in Sinorhizobium meliloti Lacking the RNA Chaperone Hfq

et al. 2010

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“…Production of ROS is part of this response, as evidenced for D. melanogaster (7)(8)(9), and the detoxification of ROS is known to be part of virulence mechanisms. SODs, for instance, are used as immune-suppressive toxins by a large number of pathogens, including eukaryotic protozoan parasites (21)(22)(23)(24)(25)(26).…”

Section: Discussionmentioning

confidence: 99%

“…This is quite surprising as a well known virulence strategy employed by numerous bacterial and fungal pathogens, including pathogens of insects as well as protozoan parasites, is the detoxification of reactive species by antioxidant enzymes, mainly superoxide dismutases (SODs) (21)(22)(23)(24)(25)(26). SODs are one of the most important cellular enzymatic defenses against the detrimental ROS generated by the aerobic metabolism.…”

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confidence: 99%

Extracellular Superoxide Dismutase in Insects

Colinet

Cazes

Belghazi³

et al. 2011

Journal of Biological Chemistry

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Background: Endoparasitoid wasps inject venom proteins at oviposition to alter host immunity. Results: The venom of Leptopilina boulardi, but not of a related species, contains an active extracellular SOD. Recombinant SODs inhibit the Drosophila host phenoloxidase activity. Conclusion: An extracellular SOD is secreted and active in an insect fluid. Significance: SODs may be used as immune suppressive virulence factors by parasitoid wasps.

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“…SodCI is reported to have a 2.7-fold higher specific activity than that of SodCII (2). These two enzymes also differ in their affinities for Cu and Zn (2).…”

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confidence: 99%

Protecting against Antimicrobial Effectors in the Phagosome Allows SodCII To Contribute to Virulence in Salmonella enterica Serovar Typhimurium

Kim¹,

Richards

Slauch

2010

J Bacteriol

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Salmonella enterica serovar Typhimurium replicates in macrophages, where it is subjected to antimicrobial substances, including superoxide, antimicrobial peptides, and proteases. The bacterium produces two periplasmic superoxide dismutases, SodCI and SodCII. Although both are expressed during infection, only SodCI contributes to virulence in the mouse by combating phagocytic superoxide. The differential contribution to virulence is at least partially due to inherent differences in the SodCI and SodCII proteins that are independent of enzymatic activity. SodCII is protease sensitive, and like other periplasmic proteins, it is released by osmotic shock. In contrast, SodCI is protease resistant and is retained within the periplasm after osmotic shock, a phenomenon that we term "tethering." We hypothesize that in the macrophage, antimicrobial peptides transiently disrupt the outer membrane. SodCII is released and/or phagocytic proteases gain access to the periplasm, and SodCII is degraded. SodCI is tethered within the periplasm and is protease resistant, thereby remaining to combat superoxide. Here we test aspects of this model. SodCII was released by the antimicrobial peptide polymyxin B or a mouse macrophage antimicrobial peptide (CRAMP), while SodCI remained tethered within the periplasm. A Salmonella pmrA constitutive mutant no longer released SodCII in vitro. Moreover, in the constitutive pmrA background, SodCII could contribute to survival of Salmonella during infection. SodCII also provided a virulence benefit in mice genetically defective in production of CRAMP. Thus, consistent with our model, protecting the outer membrane against antimicrobial peptides allows SodCII to contribute to virulence in vivo. These data also suggest direct in vivo cooperative interactions between macrophage antimicrobial effectors.

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Regulatory and Structural Differences in the Cu,Zn-Superoxide Dismutases of Salmonella enterica and Their Significance for Virulence

Cited by 56 publications

References 68 publications

Proteomic Alterations Explain Phenotypic Changes in Sinorhizobium meliloti Lacking the RNA Chaperone Hfq

Proteomic Alterations Explain Phenotypic Changes in Sinorhizobium meliloti Lacking the RNA Chaperone Hfq

Extracellular Superoxide Dismutase in Insects

Protecting against Antimicrobial Effectors in the Phagosome Allows SodCII To Contribute to Virulence in Salmonella enterica Serovar Typhimurium

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