Host Peptidic Hormones Affecting Bacterial Biofilm Formation and Virulence

Lesouhaitier, Olivier; Clamens, Thomas; Rosay, Thibaut; Desriac, Florie; Louis, Mélissande; Rodrigues, Sophie; Ганнесен, А. В.; Плакунов, В. К.; Bouffartigues, Emeline; Tahrioui, Ali; Bazire, Alexis; Dufour, Alain; Cornélis, Pierre; Chevalier, Sylvie; Feuilloley, Marc

doi:10.1159/000493926

Cited by 37 publications

(37 citation statements)

References 119 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The first studies were performed using Escherichia coli as a model, but it has now been demonstrated that many Gram-negative and Gram-positive bacteria can respond to catecholamines (5, 6). The concept of microbial endocrinology was later broadened to a large variety of eukaryotic communication molecules, ranging from cytokines to neuropeptides (7).…”

Section: Introductionmentioning

confidence: 99%

Acne and Stress: Impact of Catecholamines on Cutibacterium acnes

et al. 2019

View full text Add to dashboard Cite

Cutibacterium acnes (former Propionibacterium acnes ), is a bacterium characterized by high genomic variability, consisting of four subtypes and six major ribotypes. Skin is the largest neuroendocrine organ of the human body and many cutaneous hormones and neurohormones can modulate b acterial physiology. Here, we investigated the effect of catecholamines, i.e., epinephrine and norepinephrine, on two representative strains of C. acnes , of which the genome has been fully sequenced, identified as RT4 acneic and RT6 non-acneic strains. Epinephrine and norepinephrine (10 −6 M) had no impact on the growth of C. acnes but epinephrine increased RT4 and RT6 biofilm formation, as measured by crystal violet staining, whereas norepinephrine was only active on the RT4 strain. We obtained the same results by confocal microscopy with the RT4 strain, whereas there was no effect of either catecholamine on the RT6 strain. However, this strain was also sensitive to catecholamines, as shown by MATs tests, as epinephrine and norepinephrine affected its surface polarity. Flow cytometry studies revealed that epinephrine and norepinephrine are unable to induce major changes of bacterial surface properties and membrane integrity. Exposure of sebocytes to control or catecholamine-treated bacteria showed epinephrine and norepinephrine to have no effect on the cytotoxic or inflammatory potential of either C. acnes strains but to stimulate their effect on sebocyte lipid synthesis. Uriage thermal spring water was previously shown to inhibit biofilm production by C. acnes . We thus tested its effect after exposure of the bacteria to epinephrine and norepinephrine. The effect of the thermal water on the response of C. acnes to catecholamines depended on the surface on which the biofilm was grown. Finally, an in-silico study revealed the presence of a protein in the genome of C. acnes that shows homology with the catecholamine receptor of Escherichia coli and eukaryotes. This study suggests that C. acnes may play a role as a relay between stress mediators (catecholamines) and acne.

show abstract

Section: Introductionmentioning

confidence: 99%

Acne and Stress: Impact of Catecholamines on Cutibacterium acnes

et al. 2019

View full text Add to dashboard Cite

show abstract

“…3,4 In many bacterial species, biofilm formation responds to a variety of environmental cues including nutritional availability, host-derived signals or, in some cases, to nonlethal concentrations of antibiotics. 5–8 The process of biofilm development is coordinated by molecular pathways involving second-messenger signaling, cell-to-cell quorum sensing (QS) signaling, two-component systems and small noncoding RNAs (sRNAs). 6 Interestingly, antibiotics at levels below the minimal inhibitory concentration (referred to hereafter as sub-MIC) have the ability to trigger the alteration of multiple physiological processes including biofilm formation, virulence, and gene expression, which can lead to bacterial genetic and phenotypic resistance.…”

Section: Introductionmentioning

confidence: 99%

Extracellular DNA release, quorum sensing, and PrrF1/F2 small RNAs are key players in Pseudomonas aeruginosa tobramycin-enhanced biofilm formation

Tahrioui

Duchesne

Bouffartigues

et al. 2019

npj Biofilms Microbiomes

Self Cite

View full text Add to dashboard Cite

Biofilms are structured microbial communities that are the leading cause of numerous chronic infections which are difficult to eradicate. Within the lungs of individuals with cystic fibrosis (CF), Pseudomonas aeruginosa causes persistent biofilm infection that is commonly treated with aminoglycoside antibiotics such as tobramycin. However, sublethal concentrations of this aminoglycoside were previously shown to increase biofilm formation by P. aeruginosa , but the underlying adaptive mechanisms still remain elusive. Herein, we combined confocal laser scanning microscope analyses, proteomics profiling, gene expression assays and phenotypic studies to unravel P. aeruginosa potential adaptive mechanisms in response to tobramycin exposure during biofilm growth. Under this condition, we show that the modified biofilm architecture is related at least in part to increased extracellular DNA (eDNA) release, most likely as a result of biofilm cell death. Furthermore, the activity of quorum sensing (QS) systems was increased, leading to higher production of QS signaling molecules. We also demonstrate upon tobramycin exposure an increase in expression of the PrrF small regulatory RNAs, as well as expression of iron uptake systems. Remarkably, biofilm biovolumes and eDNA relative abundances in pqs and prrF mutant strains decrease in the presence of tobramycin. Overall, our findings offer experimental evidences for a potential adaptive mechanism linking PrrF sRNAs, QS signaling, biofilm cell death, eDNA release, and tobramycin-enhanced biofilm formation in P. aeruginosa . These specific adaptive mechanisms should be considered to improve treatment strategies against P. aeruginosa biofilm establishment in CF patients’ lungs.

show abstract

“…Those catecholamines (adrenaline and noradrenaline) are able to regulate a number of processes in bacteria such as toxin synthesis, growth, and pili synthesis (Hughes and Sperandio, 2008). Near neurotransmitters, peptidic hormones are also able to modulate bacterial physiology (Lesouhaitier et al, 2018). In this way, one of the most abundant neuropeptides of skin – substance P, which is released by skin nerve endings and diffuses in sweat and skin – exerts a central role in expressing virulence in cutaneous strains of S. aureus and Staphylococcus epidermidis (Feuilloley, 2018 for review).…”

Section: Introductionmentioning

confidence: 99%

Regulation of Monospecies and Mixed Biofilms Formation of Skin Staphylococcus aureus and Cutibacterium acnes by Human Natriuretic Peptides

et al. 2018

Self Cite

View full text Add to dashboard Cite

Staphylococcus aureus and Cutibacterium acnes are common representatives of the human skin microbiome. However, when these bacteria are organized in biofilm, they could be involved in several skin disorders such as acne or psoriasis. They inhabit in hollows of hair follicles and skin glands, where they form biofilms. There, they are continuously exposed to human hormones, including human natriuretic peptides (NUPs). We first observed that the atrial natriuretic peptide (ANP) and the C-type natriuretic peptide (CNP) have a strong effect S. aureus and C. acnes biofilm formation on the skin. These effects are significantly dependent on the aero-anaerobic conditions and temperature. We also show that both ANP and CNP increased competitive advantages of C. acnes toward S. aureus in mixed biofilm. Because of their temperature-dependent effects, NUPs appear to act as a thermostat, allowing the skin to modulate bacterial development in normal and inflammatory conditions. This is an important step toward understanding how human neuroendocrine systems can regulate the cutaneous microbial community and should be important for applications in fundamental sciences, medicine, dermatology, and cosmetology.

show abstract

Host Peptidic Hormones Affecting Bacterial Biofilm Formation and Virulence

Cited by 37 publications

References 119 publications

Acne and Stress: Impact of Catecholamines on Cutibacterium acnes

Acne and Stress: Impact of Catecholamines on Cutibacterium acnes

Extracellular DNA release, quorum sensing, and PrrF1/F2 small RNAs are key players in Pseudomonas aeruginosa tobramycin-enhanced biofilm formation

Regulation of Monospecies and Mixed Biofilms Formation of Skin Staphylococcus aureus and Cutibacterium acnes by Human Natriuretic Peptides

Contact Info

Product

Resources

About