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Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates

Invasive bacterial infections during pregnancy are a major risk factor for preterm birth, stillbirth, and fetal injury. Group B streptococci (GBS) are Gram-positive bacteria that asymptomatically colonize the lower genital tract but infect the amniotic fluid and induce preterm birth or stillbirth. E...

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Autores principales: Coleman, Michelle, Armistead, Blair, Orvis, Austyn, Quach, Phoenicia, Brokaw, Alyssa, Gendrin, Claire, Sharma, Kavita, Ogle, Jason, Merillat, Sean, Dacanay, Matthew, Wu, Tsung-Yen, Munson, Jeff, Baldessari, Audrey, Vornhagen, Jay, Furuta, Anna, Nguyen, Shayla, Adams Waldorf, Kristina M., Rajagopal, Lakshmi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545101/
https://www.ncbi.nlm.nih.gov/pubmed/33402537
http://dx.doi.org/10.1128/mBio.03115-20
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author Coleman, Michelle
Armistead, Blair
Orvis, Austyn
Quach, Phoenicia
Brokaw, Alyssa
Gendrin, Claire
Sharma, Kavita
Ogle, Jason
Merillat, Sean
Dacanay, Matthew
Wu, Tsung-Yen
Munson, Jeff
Baldessari, Audrey
Vornhagen, Jay
Furuta, Anna
Nguyen, Shayla
Adams Waldorf, Kristina M.
Rajagopal, Lakshmi
author_facet Coleman, Michelle
Armistead, Blair
Orvis, Austyn
Quach, Phoenicia
Brokaw, Alyssa
Gendrin, Claire
Sharma, Kavita
Ogle, Jason
Merillat, Sean
Dacanay, Matthew
Wu, Tsung-Yen
Munson, Jeff
Baldessari, Audrey
Vornhagen, Jay
Furuta, Anna
Nguyen, Shayla
Adams Waldorf, Kristina M.
Rajagopal, Lakshmi
author_sort Coleman, Michelle
collection PubMed
description Invasive bacterial infections during pregnancy are a major risk factor for preterm birth, stillbirth, and fetal injury. Group B streptococci (GBS) are Gram-positive bacteria that asymptomatically colonize the lower genital tract but infect the amniotic fluid and induce preterm birth or stillbirth. Experimental models that closely emulate human pregnancy are pivotal for the development of successful strategies to prevent these adverse pregnancy outcomes. Using a unique nonhuman primate model that mimics human pregnancy and informs temporal events surrounding amniotic cavity invasion and preterm labor, we show that the animals inoculated with hyaluronidase (HylB)-expressing GBS consistently exhibited microbial invasion into the amniotic cavity, fetal bacteremia, and preterm labor. Although delayed cytokine responses were observed at the maternal-fetal interface, increased prostaglandin and matrix metalloproteinase levels in these animals likely mediated preterm labor. HylB-proficient GBS dampened reactive oxygen species production and exhibited increased resistance to neutrophils compared to an isogenic mutant. Together, these findings demonstrate how a bacterial enzyme promotes GBS amniotic cavity invasion and preterm labor in a model that closely resembles human pregnancy.
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spelling pubmed-85451012021-10-27 Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates Coleman, Michelle Armistead, Blair Orvis, Austyn Quach, Phoenicia Brokaw, Alyssa Gendrin, Claire Sharma, Kavita Ogle, Jason Merillat, Sean Dacanay, Matthew Wu, Tsung-Yen Munson, Jeff Baldessari, Audrey Vornhagen, Jay Furuta, Anna Nguyen, Shayla Adams Waldorf, Kristina M. Rajagopal, Lakshmi mBio Research Article Invasive bacterial infections during pregnancy are a major risk factor for preterm birth, stillbirth, and fetal injury. Group B streptococci (GBS) are Gram-positive bacteria that asymptomatically colonize the lower genital tract but infect the amniotic fluid and induce preterm birth or stillbirth. Experimental models that closely emulate human pregnancy are pivotal for the development of successful strategies to prevent these adverse pregnancy outcomes. Using a unique nonhuman primate model that mimics human pregnancy and informs temporal events surrounding amniotic cavity invasion and preterm labor, we show that the animals inoculated with hyaluronidase (HylB)-expressing GBS consistently exhibited microbial invasion into the amniotic cavity, fetal bacteremia, and preterm labor. Although delayed cytokine responses were observed at the maternal-fetal interface, increased prostaglandin and matrix metalloproteinase levels in these animals likely mediated preterm labor. HylB-proficient GBS dampened reactive oxygen species production and exhibited increased resistance to neutrophils compared to an isogenic mutant. Together, these findings demonstrate how a bacterial enzyme promotes GBS amniotic cavity invasion and preterm labor in a model that closely resembles human pregnancy. American Society for Microbiology 2021-01-05 /pmc/articles/PMC8545101/ /pubmed/33402537 http://dx.doi.org/10.1128/mBio.03115-20 Text en Copyright © 2021 Coleman 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
Coleman, Michelle
Armistead, Blair
Orvis, Austyn
Quach, Phoenicia
Brokaw, Alyssa
Gendrin, Claire
Sharma, Kavita
Ogle, Jason
Merillat, Sean
Dacanay, Matthew
Wu, Tsung-Yen
Munson, Jeff
Baldessari, Audrey
Vornhagen, Jay
Furuta, Anna
Nguyen, Shayla
Adams Waldorf, Kristina M.
Rajagopal, Lakshmi
Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title_full Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title_fullStr Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title_full_unstemmed Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title_short Hyaluronidase Impairs Neutrophil Function and Promotes Group B Streptococcus Invasion and Preterm Labor in Nonhuman Primates
title_sort hyaluronidase impairs neutrophil function and promotes group b streptococcus invasion and preterm labor in nonhuman primates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545101/
https://www.ncbi.nlm.nih.gov/pubmed/33402537
http://dx.doi.org/10.1128/mBio.03115-20
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