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Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli

Staphylococcus aureus is a human pathogen with many infections originating on mucosal surfaces. One common group of S. aureus is the USA200 (CC30) clonal group, which produces toxic shock syndrome toxin-1 (TSST-1). Many USA200 infections occur on mucosal surfaces, particularly in the vagina and gast...

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Autores principales: Schlievert, Patrick M., Gaitán, Adriana V., Kilgore, Samuel H., Roe, Amy L., Maukonen, Johanna, Lehtoranta, Liisa, Leung, Donald Y. M., Marsman, Daniel S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434015/
https://www.ncbi.nlm.nih.gov/pubmed/37404182
http://dx.doi.org/10.1128/spectrum.01735-23
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author Schlievert, Patrick M.
Gaitán, Adriana V.
Kilgore, Samuel H.
Roe, Amy L.
Maukonen, Johanna
Lehtoranta, Liisa
Leung, Donald Y. M.
Marsman, Daniel S.
author_facet Schlievert, Patrick M.
Gaitán, Adriana V.
Kilgore, Samuel H.
Roe, Amy L.
Maukonen, Johanna
Lehtoranta, Liisa
Leung, Donald Y. M.
Marsman, Daniel S.
author_sort Schlievert, Patrick M.
collection PubMed
description Staphylococcus aureus is a human pathogen with many infections originating on mucosal surfaces. One common group of S. aureus is the USA200 (CC30) clonal group, which produces toxic shock syndrome toxin-1 (TSST-1). Many USA200 infections occur on mucosal surfaces, particularly in the vagina and gastrointestinal tract. This allows these organisms to cause cases of menstrual TSS and enterocolitis. The current study examined the ability of two lactobacilli, Lactobacillus acidophilus strain LA-14 and Lacticaseibacillus rhamnosus strain HN001, for their ability to inhibit the growth of TSST-1 positive S. aureus, the production of TSST-1, and the ability of TSST-1 to induce pro-inflammatory chemokines from human vaginal epithelial cells (HVECs). In competition growth experiments, L. rhamnosus did not affect the growth of TSS S. aureus but did inhibit the production of TSST-1; this effect was partially due to acidification of the growth medium. L. acidophilus was both bactericidal and prevented the production of TSST-1 by S. aureus. This effect appeared to be partially due to acidification of the growth medium, production of H(2)O(2), and production of other antibacterial molecules. When both organisms were incubated with S. aureus, the effect of L. acidophilus LA-14 dominated. In in vitro experiments with HVECs, neither lactobacillus induced significant production of the chemokine interleukin-8, whereas TSST-1 did induce production of the chemokine. When the lactobacilli were incubated with HVECs in the presence of TSST-1, the lactobacilli reduced chemokine production. These data suggest that these two bacteria in probiotics could reduce the incidence of menstrual and enterocolitis-associated TSS. IMPORTANCE Toxic shock syndrome (TSS) Staphylococcus aureus commonly colonize mucosal surfaces, giving them the ability to cause TSS through the action of TSS toxin-1 (TSST-1). This study examined the ability of two probiotic lactobacilli to inhibit S. aureus growth and TSST-1 production, and the reduction of pro-inflammatory chemokine production by TSST-1. Lacticaseibacillus rhamnosus strain HN001 inhibited TSST-1 production due to acid production but did not affect S. aureus growth. Lactobacillus acidophilus strain LA-14 was bactericidal against S. aureus, partially due to acid and H(2)O(2) production, and consequently also inhibited TSST-1 production. Neither lactobacillus induced the production of pro-inflammatory chemokines by human vaginal epithelial cells, and both inhibited chemokine production by TSST-1. These data suggest that the two probiotics could reduce the incidence of mucosa-associated TSS, including menstrual TSS and cases originating as enterocolitis.
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spelling pubmed-104340152023-08-18 Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli Schlievert, Patrick M. Gaitán, Adriana V. Kilgore, Samuel H. Roe, Amy L. Maukonen, Johanna Lehtoranta, Liisa Leung, Donald Y. M. Marsman, Daniel S. Microbiol Spectr Research Article Staphylococcus aureus is a human pathogen with many infections originating on mucosal surfaces. One common group of S. aureus is the USA200 (CC30) clonal group, which produces toxic shock syndrome toxin-1 (TSST-1). Many USA200 infections occur on mucosal surfaces, particularly in the vagina and gastrointestinal tract. This allows these organisms to cause cases of menstrual TSS and enterocolitis. The current study examined the ability of two lactobacilli, Lactobacillus acidophilus strain LA-14 and Lacticaseibacillus rhamnosus strain HN001, for their ability to inhibit the growth of TSST-1 positive S. aureus, the production of TSST-1, and the ability of TSST-1 to induce pro-inflammatory chemokines from human vaginal epithelial cells (HVECs). In competition growth experiments, L. rhamnosus did not affect the growth of TSS S. aureus but did inhibit the production of TSST-1; this effect was partially due to acidification of the growth medium. L. acidophilus was both bactericidal and prevented the production of TSST-1 by S. aureus. This effect appeared to be partially due to acidification of the growth medium, production of H(2)O(2), and production of other antibacterial molecules. When both organisms were incubated with S. aureus, the effect of L. acidophilus LA-14 dominated. In in vitro experiments with HVECs, neither lactobacillus induced significant production of the chemokine interleukin-8, whereas TSST-1 did induce production of the chemokine. When the lactobacilli were incubated with HVECs in the presence of TSST-1, the lactobacilli reduced chemokine production. These data suggest that these two bacteria in probiotics could reduce the incidence of menstrual and enterocolitis-associated TSS. IMPORTANCE Toxic shock syndrome (TSS) Staphylococcus aureus commonly colonize mucosal surfaces, giving them the ability to cause TSS through the action of TSS toxin-1 (TSST-1). This study examined the ability of two probiotic lactobacilli to inhibit S. aureus growth and TSST-1 production, and the reduction of pro-inflammatory chemokine production by TSST-1. Lacticaseibacillus rhamnosus strain HN001 inhibited TSST-1 production due to acid production but did not affect S. aureus growth. Lactobacillus acidophilus strain LA-14 was bactericidal against S. aureus, partially due to acid and H(2)O(2) production, and consequently also inhibited TSST-1 production. Neither lactobacillus induced the production of pro-inflammatory chemokines by human vaginal epithelial cells, and both inhibited chemokine production by TSST-1. These data suggest that the two probiotics could reduce the incidence of mucosa-associated TSS, including menstrual TSS and cases originating as enterocolitis. American Society for Microbiology 2023-07-05 /pmc/articles/PMC10434015/ /pubmed/37404182 http://dx.doi.org/10.1128/spectrum.01735-23 Text en Copyright © 2023 Schlievert et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Schlievert, Patrick M.
Gaitán, Adriana V.
Kilgore, Samuel H.
Roe, Amy L.
Maukonen, Johanna
Lehtoranta, Liisa
Leung, Donald Y. M.
Marsman, Daniel S.
Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title_full Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title_fullStr Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title_full_unstemmed Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title_short Inhibition of Toxic Shock Syndrome-Associated Staphylococcus aureus by Probiotic Lactobacilli
title_sort inhibition of toxic shock syndrome-associated staphylococcus aureus by probiotic lactobacilli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434015/
https://www.ncbi.nlm.nih.gov/pubmed/37404182
http://dx.doi.org/10.1128/spectrum.01735-23
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