<named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism
ABSTRACT Streptococcus agalactiae, or group B Streptococcus (GBS), is a common perinatal pathogen. GBS colonization of the vaginal mucosa during pregnancy is a risk factor for invasive infection of the fetal membranes (chorioamnionitis) and its consequences such as membrane rupture, preterm labor, s...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02084-18 |
| _version_ | 1819199663075491840 |
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| author | Ryan S. Doster Jessica A. Sutton Lisa M. Rogers David M. Aronoff Jennifer A. Gaddy |
| author_facet | Ryan S. Doster Jessica A. Sutton Lisa M. Rogers David M. Aronoff Jennifer A. Gaddy |
| author_sort | Ryan S. Doster |
| collection | DOAJ |
| description | ABSTRACT Streptococcus agalactiae, or group B Streptococcus (GBS), is a common perinatal pathogen. GBS colonization of the vaginal mucosa during pregnancy is a risk factor for invasive infection of the fetal membranes (chorioamnionitis) and its consequences such as membrane rupture, preterm labor, stillbirth, and neonatal sepsis. Placental macrophages, or Hofbauer cells, are fetally derived macrophages present within placental and fetal membrane tissues that perform vital functions for fetal and placental development, including supporting angiogenesis, tissue remodeling, and regulation of maternal-fetal tolerance. Although placental macrophages as tissue-resident innate phagocytes are likely to engage invasive bacteria such as GBS, there is limited information regarding how these cells respond to bacterial infection. Here, we demonstrate in vitro that placental macrophages release macrophage extracellular traps (METs) in response to bacterial infection. Placental macrophage METs contain proteins, including histones, myeloperoxidase, and neutrophil elastase similar to neutrophil extracellular traps, and are capable of killing GBS cells. MET release from these cells occurs by a process that depends on the production of reactive oxygen species. Placental macrophage METs also contain matrix metalloproteases that are released in response to GBS and could contribute to fetal membrane weakening during infection. MET structures were identified within human fetal membrane tissues infected ex vivo, suggesting that placental macrophages release METs in response to bacterial infection during chorioamnionitis. IMPORTANCE Streptococcus agalactiae, also known as group B Streptococcus (GBS), is a common pathogen during pregnancy where infection can result in chorioamnionitis, preterm premature rupture of membranes (PPROM), preterm labor, stillbirth, and neonatal sepsis. Mechanisms by which GBS infection results in adverse pregnancy outcomes are still incompletely understood. This study evaluated interactions between GBS and placental macrophages. The data demonstrate that in response to infection, placental macrophages release extracellular traps capable of killing GBS. Additionally, this work establishes that proteins associated with extracellular trap fibers include several matrix metalloproteinases that have been associated with chorioamnionitis. In the context of pregnancy, placental macrophage responses to bacterial infection might have beneficial and adverse consequences, including protective effects against bacterial invasion, but they may also release important mediators of membrane breakdown that could contribute to membrane rupture or preterm labor. |
| first_indexed | 2024-12-23T03:19:55Z |
| format | Article |
| id | doaj.art-5bf2d5cce90b459b92809d352647c769 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-23T03:19:55Z |
| publishDate | 2018-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-5bf2d5cce90b459b92809d352647c7692022-12-21T18:02:02ZengAmerican Society for MicrobiologymBio2150-75112018-12-019610.1128/mBio.02084-18<named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent MechanismRyan S. Doster0Jessica A. Sutton1Lisa M. Rogers2David M. Aronoff3Jennifer A. Gaddy4Division of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USADepartment of Microbiology and Immunology, Meharry Medical College, Nashville, Tennessee, USADivision of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USADivision of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USADivision of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USAABSTRACT Streptococcus agalactiae, or group B Streptococcus (GBS), is a common perinatal pathogen. GBS colonization of the vaginal mucosa during pregnancy is a risk factor for invasive infection of the fetal membranes (chorioamnionitis) and its consequences such as membrane rupture, preterm labor, stillbirth, and neonatal sepsis. Placental macrophages, or Hofbauer cells, are fetally derived macrophages present within placental and fetal membrane tissues that perform vital functions for fetal and placental development, including supporting angiogenesis, tissue remodeling, and regulation of maternal-fetal tolerance. Although placental macrophages as tissue-resident innate phagocytes are likely to engage invasive bacteria such as GBS, there is limited information regarding how these cells respond to bacterial infection. Here, we demonstrate in vitro that placental macrophages release macrophage extracellular traps (METs) in response to bacterial infection. Placental macrophage METs contain proteins, including histones, myeloperoxidase, and neutrophil elastase similar to neutrophil extracellular traps, and are capable of killing GBS cells. MET release from these cells occurs by a process that depends on the production of reactive oxygen species. Placental macrophage METs also contain matrix metalloproteases that are released in response to GBS and could contribute to fetal membrane weakening during infection. MET structures were identified within human fetal membrane tissues infected ex vivo, suggesting that placental macrophages release METs in response to bacterial infection during chorioamnionitis. IMPORTANCE Streptococcus agalactiae, also known as group B Streptococcus (GBS), is a common pathogen during pregnancy where infection can result in chorioamnionitis, preterm premature rupture of membranes (PPROM), preterm labor, stillbirth, and neonatal sepsis. Mechanisms by which GBS infection results in adverse pregnancy outcomes are still incompletely understood. This study evaluated interactions between GBS and placental macrophages. The data demonstrate that in response to infection, placental macrophages release extracellular traps capable of killing GBS. Additionally, this work establishes that proteins associated with extracellular trap fibers include several matrix metalloproteinases that have been associated with chorioamnionitis. In the context of pregnancy, placental macrophage responses to bacterial infection might have beneficial and adverse consequences, including protective effects against bacterial invasion, but they may also release important mediators of membrane breakdown that could contribute to membrane rupture or preterm labor.https://journals.asm.org/doi/10.1128/mBio.02084-18Streptococcus agalactiaeextracellular trapsgroup B Streptococcusmacrophagesmatrix metalloproteinase |
| spellingShingle | Ryan S. Doster Jessica A. Sutton Lisa M. Rogers David M. Aronoff Jennifer A. Gaddy <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism mBio Streptococcus agalactiae extracellular traps group B Streptococcus macrophages matrix metalloproteinase |
| title | <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism |
| title_full | <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism |
| title_fullStr | <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism |
| title_full_unstemmed | <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism |
| title_short | <named-content content-type="genus-species">Streptococcus agalactiae</named-content> Induces Placental Macrophages To Release Extracellular Traps Loaded with Tissue Remodeling Enzymes via an Oxidative Burst-Dependent Mechanism |
| title_sort | named content content type genus species streptococcus agalactiae named content induces placental macrophages to release extracellular traps loaded with tissue remodeling enzymes via an oxidative burst dependent mechanism |
| topic | Streptococcus agalactiae extracellular traps group B Streptococcus macrophages matrix metalloproteinase |
| url | https://journals.asm.org/doi/10.1128/mBio.02084-18 |
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