Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
ABSTRACT Estrogen, a major female sex steroid hormone, has been shown to promote the selection of mucoid Pseudomonas aeruginosa in the airways of patients with chronic respiratory diseases, including cystic fibrosis. This results in long-term persistence, poorer clinical outcomes, and limited therap...
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American Society for Microbiology
2020
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oai:doaj.org-article:a70f533655e045bc87d30e38bc6cedeb2021-11-15T16:19:08ZSex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>10.1128/mBio.01774-202150-7511https://doaj.org/article/a70f533655e045bc87d30e38bc6cedeb2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01774-20https://doaj.org/toc/2150-7511ABSTRACT Estrogen, a major female sex steroid hormone, has been shown to promote the selection of mucoid Pseudomonas aeruginosa in the airways of patients with chronic respiratory diseases, including cystic fibrosis. This results in long-term persistence, poorer clinical outcomes, and limited therapeutic options. In this study, we demonstrate that at physiological concentrations, sex steroids, including testosterone and estriol, induce membrane stress responses in P. aeruginosa. This is characterized by increased virulence and consequent inflammation and release of proinflammatory outer membrane vesicles promoting in vivo persistence of the bacteria. The steroid-induced P. aeruginosa response correlates with the molecular polarity of the hormones and membrane fluidic properties of the bacteria. This novel mechanism of interaction between sex steroids and P. aeruginosa explicates the reported increased disease severity observed in females with cystic fibrosis and provides evidence for the therapeutic potential of the modulation of sex steroids to achieve better clinical outcomes in patients with hormone-responsive strains. IMPORTANCE Molecular mechanisms by which sex steroids interact with P. aeruginosa to modulate its virulence have yet to be reported. Our work provides the first characterization of a steroid-induced membrane stress mechanism promoting P. aeruginosa virulence, which includes the release of proinflammatory outer membrane vesicles, resulting in inflammation, host tissue damage, and reduced bacterial clearance. We further demonstrate that at nanomolar (physiological) concentrations, male and female sex steroids promote virulence in clinical strains of P. aeruginosa based on their dynamic membrane fluidic properties. This work provides, for the first-time, mechanistic insight to better understand and predict the P. aeruginosa related response to sex steroids and explain the interindividual patient variability observed in respiratory diseases such as cystic fibrosis that are complicated by gender differences and chronic P. aeruginosa infection.Celine VidaillacValerie Fei Lee YongMarie-Stephanie AschtgenJing QuShuowei YangGuangfu XuZi Jing SengAlexandra C. BrownMd Khadem AliTavleen K. JaggiJagadish SankaranYong Hwee FooFrancesco RighettiAnu Maashaa NedumaranMicheál Mac AogáinDan RoizmanJean-Alexandre RichardThomas R. RogersMasanori ToyofukuDahai LuoEdmund LohThorsten WohlandBertrand CzarnyJay C. HorvatPhilip M. HansbroLiang YangLiang LiStaffan NormarkBirgitta Henriques-NormarkSanjay H. ChotirmallAmerican Society for MicrobiologyarticlehormonessteroidsPseudomonas aeruginosamembrane stressgenderMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020) |
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DOAJ |
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| topic |
hormones steroids Pseudomonas aeruginosa membrane stress gender Microbiology QR1-502 |
| spellingShingle |
hormones steroids Pseudomonas aeruginosa membrane stress gender Microbiology QR1-502 Celine Vidaillac Valerie Fei Lee Yong Marie-Stephanie Aschtgen Jing Qu Shuowei Yang Guangfu Xu Zi Jing Seng Alexandra C. Brown Md Khadem Ali Tavleen K. Jaggi Jagadish Sankaran Yong Hwee Foo Francesco Righetti Anu Maashaa Nedumaran Micheál Mac Aogáin Dan Roizman Jean-Alexandre Richard Thomas R. Rogers Masanori Toyofuku Dahai Luo Edmund Loh Thorsten Wohland Bertrand Czarny Jay C. Horvat Philip M. Hansbro Liang Yang Liang Li Staffan Normark Birgitta Henriques-Normark Sanjay H. Chotirmall Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| description |
ABSTRACT Estrogen, a major female sex steroid hormone, has been shown to promote the selection of mucoid Pseudomonas aeruginosa in the airways of patients with chronic respiratory diseases, including cystic fibrosis. This results in long-term persistence, poorer clinical outcomes, and limited therapeutic options. In this study, we demonstrate that at physiological concentrations, sex steroids, including testosterone and estriol, induce membrane stress responses in P. aeruginosa. This is characterized by increased virulence and consequent inflammation and release of proinflammatory outer membrane vesicles promoting in vivo persistence of the bacteria. The steroid-induced P. aeruginosa response correlates with the molecular polarity of the hormones and membrane fluidic properties of the bacteria. This novel mechanism of interaction between sex steroids and P. aeruginosa explicates the reported increased disease severity observed in females with cystic fibrosis and provides evidence for the therapeutic potential of the modulation of sex steroids to achieve better clinical outcomes in patients with hormone-responsive strains. IMPORTANCE Molecular mechanisms by which sex steroids interact with P. aeruginosa to modulate its virulence have yet to be reported. Our work provides the first characterization of a steroid-induced membrane stress mechanism promoting P. aeruginosa virulence, which includes the release of proinflammatory outer membrane vesicles, resulting in inflammation, host tissue damage, and reduced bacterial clearance. We further demonstrate that at nanomolar (physiological) concentrations, male and female sex steroids promote virulence in clinical strains of P. aeruginosa based on their dynamic membrane fluidic properties. This work provides, for the first-time, mechanistic insight to better understand and predict the P. aeruginosa related response to sex steroids and explain the interindividual patient variability observed in respiratory diseases such as cystic fibrosis that are complicated by gender differences and chronic P. aeruginosa infection. |
| format |
article |
| author |
Celine Vidaillac Valerie Fei Lee Yong Marie-Stephanie Aschtgen Jing Qu Shuowei Yang Guangfu Xu Zi Jing Seng Alexandra C. Brown Md Khadem Ali Tavleen K. Jaggi Jagadish Sankaran Yong Hwee Foo Francesco Righetti Anu Maashaa Nedumaran Micheál Mac Aogáin Dan Roizman Jean-Alexandre Richard Thomas R. Rogers Masanori Toyofuku Dahai Luo Edmund Loh Thorsten Wohland Bertrand Czarny Jay C. Horvat Philip M. Hansbro Liang Yang Liang Li Staffan Normark Birgitta Henriques-Normark Sanjay H. Chotirmall |
| author_facet |
Celine Vidaillac Valerie Fei Lee Yong Marie-Stephanie Aschtgen Jing Qu Shuowei Yang Guangfu Xu Zi Jing Seng Alexandra C. Brown Md Khadem Ali Tavleen K. Jaggi Jagadish Sankaran Yong Hwee Foo Francesco Righetti Anu Maashaa Nedumaran Micheál Mac Aogáin Dan Roizman Jean-Alexandre Richard Thomas R. Rogers Masanori Toyofuku Dahai Luo Edmund Loh Thorsten Wohland Bertrand Czarny Jay C. Horvat Philip M. Hansbro Liang Yang Liang Li Staffan Normark Birgitta Henriques-Normark Sanjay H. Chotirmall |
| author_sort |
Celine Vidaillac |
| title |
Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_short |
Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_full |
Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_fullStr |
Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_full_unstemmed |
Sex Steroids Induce Membrane Stress Responses and Virulence Properties in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_sort |
sex steroids induce membrane stress responses and virulence properties in <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/a70f533655e045bc87d30e38bc6cedeb |
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