Mechanism and impact of catecholamine conversion by Vibrio cholerae

Toulouse, Charlotte; Schmucker, Sonja; Metesch, Kristina; Pfannstiel, Jens; Michel, Bernd; Starke, Ines; Möller, Heiko M.; Stefanski, Volker; Steuber, Julia

doi:10.1016/j.bbabio.2019.04.003

Cited by 8 publications

(11 citation statements)

References 65 publications

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“…Based on own previous studies, AC was a promising candidate for the observed immunosuppression by S. Typhimurium. These experiments demonstrated that AC was formed during bacterial culture of V. cholerae (29,41) upon ADR addition, and AC treatment of the human monocytic cell line THP-1 caused a hampered TNF-α production (41). Also, it is already known that AC can bind to ARs (39), which are present on all immune cells (4).…”

Section: Discussionmentioning

confidence: 93%

“…Because AC can also have a direct effect on bacteria, like in V. cholerae ( 41 ), we assumed that its effect on PBMCs might possibly be mediated indirectly, by modulating the behavior of S. Typhimurium upon sensing. In addition to the treatment of Salmonella cultures with NA or ADR, we thus also cultured S. Typhimurium with 2 × 10 –5 M AC for 8 h at 37°C before centrifugation and microfiltration.…”

Section: Resultsmentioning

confidence: 99%

“…A boost of AC formation by superoxide-producing bacteria might cause immunomodulation as it was shown that AC can bind to β-ARs (39), which can be found on most immune cells (40). Indeed, it was demonstrated in Vibrio cholerae O395N1 that the bacterial Na + -translocating NADH:quinone oxidoreductase (NQR) promoted the oxidation of ADR to AC by superoxide production (41). AC supported the pathogenicity of V. cholerae by stimulating its growth even stronger than ADR and in addition exerted immunomodulating effects by inhibiting tumor necrosis factor α (TNF-α) production in a human monocytic cell line (41).…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, it was demonstrated in Vibrio cholerae O395N1 that the bacterial Na + -translocating NADH:quinone oxidoreductase (NQR) promoted the oxidation of ADR to AC by superoxide production (41). AC supported the pathogenicity of V. cholerae by stimulating its growth even stronger than ADR and in addition exerted immunomodulating effects by inhibiting tumor necrosis factor α (TNF-α) production in a human monocytic cell line (41). It can be hypothesized that V. cholerae is not the only gut pathogen capable of this reaction, and the promotion of AC formation may be a strategy also used by other bacteria to manipulate host immune functionality.…”

Section: Introductionmentioning

confidence: 99%

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Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro

et al. 2020

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In stressful situations, catecholamines modulate mammalian immune function, and in addition, they can be sensed by many bacteria. Catecholamine sensing was also found in the zoonotic gut pathogen Salmonella Typhimurium, probably contributing to the stress-induced increased risk of salmonellosis. Virulence traits such as proliferation and invasiveness are promoted upon bacterial catecholamine sensing, but it is unknown whether S. Typhimurium may also inhibit mammalian immune function in stressful situations. We thus investigated whether supernatants from S. Typhimurium grown in the presence of catecholamines modulate porcine mitogen-induced lymphocyte proliferation. Lymphocyte proliferation was reduced by supernatants from catecholamine-exposed Salmonella in a dose-dependent manner. We further examined whether adrenaline oxidation to adrenochrome, which is promoted by bacteria, could be responsible for the observed effect, but this molecule either enhanced lymphocyte functionality or had no effect. We could thereby exclude adrenochrome as a potential immunomodulating agent produced by S. Typhimurium. This study is the first to demonstrate that bacteria grown in the presence of catecholamine stress hormones alter their growth environment, probably by producing immunomodulating substances, in a way that host immune response is suppressed. These findings add a new dimension to interkingdom signaling and provide novel clues to explain the increased susceptibility of a stressed host to Salmonella infection.

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Section: Discussionmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro

et al. 2020

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“…These molecules modulate the growth and virulence of the pathogen. Adrenaline transformed by V. cholerae to adrenochrome during the process of its respiration not only stimulates the growth of the pathogen, but also elicits specific responses in immune cells (Toulouse et al, 2019 ). In the host, adrenochrome inhibited lipopolysaccharide activates formation of TNF-α by THP-1 monocytes.…”

Section: Host Responsementioning

confidence: 99%

Virulence Regulation and Innate Host Response in the Pathogenicity of Vibrio cholerae

Ramamurthy

Nandy

Mukhopadhyay

et al. 2020

Front. Cell. Infect. Microbiol.

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The human pathogen Vibrio cholerae is the causative agent of severe diarrheal disease known as cholera. Of the more than 200 "O" serogroups of this pathogen, O1 and O139 cause cholera outbreaks and epidemics. The rest of the serogroups, collectively known as non-O1/non-O139 cause sporadic moderate or mild diarrhea and also systemic infections. Pathogenic V. cholerae circulates between nutrient-rich human gut and nutrient-deprived aquatic environment. As an autochthonous bacterium in the environment and as a human pathogen, V. cholerae maintains its survival and proliferation in these two niches. Growth in the gastrointestinal tract involves expression of several genes that provide bacterial resistance against host factors. An intricate regulatory program involving extracellular signaling inputs is also controlling this function. On the other hand, the ability to store carbon as glycogen facilitates bacterial fitness in the aquatic environment. To initiate the infection, V. cholerae must colonize the small intestine after successfully passing through the acid barrier in the stomach and survive in the presence of bile and antimicrobial peptides in the intestinal lumen and mucus, respectively. In V. cholerae, virulence is a multilocus phenomenon with a large functionally associated network. More than 200 proteins have been identified that are functionally linked to the virulence-associated genes of the pathogen. Several of these genes have a role to play in virulence and/or in functions that have importance in the human host or the environment. A total of 524 genes are differentially expressed in classical and El Tor strains, the two biotypes of V. cholerae serogroup O1. Within the host, many immune and biological factors are able to induce genes that are responsible for survival, colonization, and virulence. The innate host immune response to V. cholerae infection includes activation of several immune protein complexes, receptor-mediated signaling pathways, and other bactericidal proteins. This article presents an overview of regulation of important virulence factors in V. cholerae and host response in the context of pathogenesis.

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Eukaryotic catecholamine hormones influence the chemotactic control of Vibrio campbellii by binding to the coupling protein CheW

Muñoz

Hoyer

Schumacher

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Significance Host-emitted stress hormones significantly influence the growth and behavior of various bacterial species; however, their cellular targets have so far remained elusive. Here, we used customized probes and quantitative proteomics to identify the target of epinephrine and the α-adrenoceptor agonist phenylephrine in live cells of the aquatic pathogen Vibrio campbellii . Consequently, we have discovered the coupling protein CheW, which is in the center of the chemotaxis signaling network, as a target of both molecules. We not only demonstrate direct ligand binding to CheW but also elucidate how this affects chemotactic control. These findings are pivotal for further research on hormone-specific effects on bacterial behavior.

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Mechanism and impact of catecholamine conversion by Vibrio cholerae

Cited by 8 publications

References 65 publications

Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro

Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro

Virulence Regulation and Innate Host Response in the Pathogenicity of Vibrio cholerae

Eukaryotic catecholamine hormones influence the chemotactic control of Vibrio campbellii by binding to the coupling protein CheW

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