Immune Profile of the Normal Maternal-Fetal Interface in Rhesus Macaques and Its Alteration Following Zika Virus Infection

The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the fetus against vertical transmission of maternal pathogens. To better understand host immune determinants of congenital infection at the mater...

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Published inFrontiers in immunology Vol. 12; p. 719810
Main Authors Moström, Matilda J., Scheef, Elizabeth A., Sprehe, Lesli M., Szeltner, Dawn, Tran, Dollnovan, Hennebold, Jon D., Roberts, Victoria H. J., Maness, Nicholas J., Fahlberg, Marissa, Kaur, Amitinder
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 29.07.2021
Subjects
Animals
decidua
Decidua - immunology
Decidua - metabolism
decidual T cells
Disease Susceptibility
dNK
Female
fetal-maternal immunity
gammadelta T cells
Host-Pathogen Interactions - immunology
Immunohistochemistry
Immunology
Immunophenotyping
Killer Cells, Natural - immunology
Killer Cells, Natural - metabolism
Leukocyte Count
Macaca mulatta
Maternal-Fetal Exchange - immunology
Monkey Diseases - etiology
Monkey Diseases - metabolism
Monkey Diseases - pathology
Monkey Diseases - transmission
Pregnancy
T-Lymphocyte Subsets - immunology
T-Lymphocyte Subsets - metabolism
Zika
Zika Virus - immunology
Zika Virus Infection - veterinary
dNK
decidual T cells
gammadelta T cells
decidua
Treg
congenital viral infection
fetal-maternal immunity
Zika
Online AccessGet full text
ISSN1664-3224
1664-3224
DOI10.3389/fimmu.2021.719810

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Abstract The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the fetus against vertical transmission of maternal pathogens. To better understand host immune determinants of congenital infection at the maternal-fetal tissue interface, we performed a comparative analysis of innate and adaptive immune cell subsets in the peripheral blood and decidua of healthy rhesus macaque pregnancies across all trimesters of gestation and determined changes after Zika virus (ZIKV) infection. Using one 28-color and one 18-color polychromatic flow cytometry panel we simultaneously analyzed the frequency, phenotype, activation status and trafficking properties of αβ T, γδ T, iNKT, regulatory T (Treg), NK cells, B lymphocytes, monocytes, macrophages, and dendritic cells (DC). Decidual leukocytes showed a striking enrichment of activated effector memory and tissue-resident memory CD4+ and CD8+ T lymphocytes, CD4+ Tregs, CD56+ NK cells, CD14+CD16+ monocytes, CD206+ tissue-resident macrophages, and a paucity of B lymphocytes when compared to peripheral blood. t-distributed stochastic neighbor embedding (tSNE) revealed unique populations of decidual NK, T, DC and monocyte/macrophage subsets. Principal component analysis showed distinct spatial localization of decidual and circulating leukocytes contributed by NK and CD8+ T lymphocytes, and separation of decidua based on gestational age contributed by memory CD4+ and CD8+ T lymphocytes. Decidua from 10 ZIKV-infected dams obtained 16-56 days post infection at third (n=9) or second (n=1) trimester showed a significant reduction in frequency of activated, CXCR3+, and/or Granzyme B+ memory CD4+ and CD8+ T lymphocytes and γδ T compared to normal decidua. These data suggest that ZIKV induces local immunosuppression with reduced immune recruitment and impaired cytotoxicity. Our study adds to the immune characterization of the maternal-fetal interface in a translational nonhuman primate model of congenital infection and provides novel insight in to putative mechanisms of vertical transmission.
AbstractList The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the fetus against vertical transmission of maternal pathogens. To better understand host immune determinants of congenital infection at the maternal-fetal tissue interface, we performed a comparative analysis of innate and adaptive immune cell subsets in the peripheral blood and decidua of healthy rhesus macaque pregnancies across all trimesters of gestation and determined changes after Zika virus (ZIKV) infection. Using one 28-color and one 18-color polychromatic flow cytometry panel we simultaneously analyzed the frequency, phenotype, activation status and trafficking properties of αβ T, γδ T, iNKT, regulatory T (Treg), NK cells, B lymphocytes, monocytes, macrophages, and dendritic cells (DC). Decidual leukocytes showed a striking enrichment of activated effector memory and tissue-resident memory CD4+ and CD8+ T lymphocytes, CD4+ Tregs, CD56+ NK cells, CD14+CD16+ monocytes, CD206+ tissue-resident macrophages, and a paucity of B lymphocytes when compared to peripheral blood. t-distributed stochastic neighbor embedding (tSNE) revealed unique populations of decidual NK, T, DC and monocyte/macrophage subsets. Principal component analysis showed distinct spatial localization of decidual and circulating leukocytes contributed by NK and CD8+ T lymphocytes, and separation of decidua based on gestational age contributed by memory CD4+ and CD8+ T lymphocytes. Decidua from 10 ZIKV-infected dams obtained 16-56 days post infection at third (n=9) or second (n=1) trimester showed a significant reduction in frequency of activated, CXCR3+, and/or Granzyme B+ memory CD4+ and CD8+ T lymphocytes and γδ T compared to normal decidua. These data suggest that ZIKV induces local immunosuppression with reduced immune recruitment and impaired cytotoxicity. Our study adds to the immune characterization of the maternal-fetal interface in a translational nonhuman primate model of congenital infection and provides novel insight in to putative mechanisms of vertical transmission.
The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the fetus against vertical transmission of maternal pathogens. To better understand host immune determinants of congenital infection at the maternal-fetal tissue interface, we performed a comparative analysis of innate and adaptive immune cell subsets in the peripheral blood and decidua of healthy rhesus macaque pregnancies across all trimesters of gestation and determined changes after Zika virus (ZIKV) infection. Using one 28-color and one 18-color polychromatic flow cytometry panel we simultaneously analyzed the frequency, phenotype, activation status and trafficking properties of αβ T, γδ T, iNKT, regulatory T (Treg), NK cells, B lymphocytes, monocytes, macrophages, and dendritic cells (DC). Decidual leukocytes showed a striking enrichment of activated effector memory and tissue-resident memory CD4+ and CD8+ T lymphocytes, CD4+ Tregs, CD56+ NK cells, CD14+CD16+ monocytes, CD206+ tissue-resident macrophages, and a paucity of B lymphocytes when compared to peripheral blood. t-distributed stochastic neighbor embedding (tSNE) revealed unique populations of decidual NK, T, DC and monocyte/macrophage subsets. Principal component analysis showed distinct spatial localization of decidual and circulating leukocytes contributed by NK and CD8+ T lymphocytes, and separation of decidua based on gestational age contributed by memory CD4+ and CD8+ T lymphocytes. Decidua from 10 ZIKV-infected dams obtained 16-56 days post infection at third (n=9) or second (n=1) trimester showed a significant reduction in frequency of activated, CXCR3+, and/or Granzyme B+ memory CD4+ and CD8+ T lymphocytes and γδ T compared to normal decidua. These data suggest that ZIKV induces local immunosuppression with reduced immune recruitment and impaired cytotoxicity. Our study adds to the immune characterization of the maternal-fetal interface in a translational nonhuman primate model of congenital infection and provides novel insight in to putative mechanisms of vertical transmission.The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the fetus against vertical transmission of maternal pathogens. To better understand host immune determinants of congenital infection at the maternal-fetal tissue interface, we performed a comparative analysis of innate and adaptive immune cell subsets in the peripheral blood and decidua of healthy rhesus macaque pregnancies across all trimesters of gestation and determined changes after Zika virus (ZIKV) infection. Using one 28-color and one 18-color polychromatic flow cytometry panel we simultaneously analyzed the frequency, phenotype, activation status and trafficking properties of αβ T, γδ T, iNKT, regulatory T (Treg), NK cells, B lymphocytes, monocytes, macrophages, and dendritic cells (DC). Decidual leukocytes showed a striking enrichment of activated effector memory and tissue-resident memory CD4+ and CD8+ T lymphocytes, CD4+ Tregs, CD56+ NK cells, CD14+CD16+ monocytes, CD206+ tissue-resident macrophages, and a paucity of B lymphocytes when compared to peripheral blood. t-distributed stochastic neighbor embedding (tSNE) revealed unique populations of decidual NK, T, DC and monocyte/macrophage subsets. Principal component analysis showed distinct spatial localization of decidual and circulating leukocytes contributed by NK and CD8+ T lymphocytes, and separation of decidua based on gestational age contributed by memory CD4+ and CD8+ T lymphocytes. Decidua from 10 ZIKV-infected dams obtained 16-56 days post infection at third (n=9) or second (n=1) trimester showed a significant reduction in frequency of activated, CXCR3+, and/or Granzyme B+ memory CD4+ and CD8+ T lymphocytes and γδ T compared to normal decidua. These data suggest that ZIKV induces local immunosuppression with reduced immune recruitment and impaired cytotoxicity. Our study adds to the immune characterization of the maternal-fetal interface in a translational nonhuman primate model of congenital infection and provides novel insight in to putative mechanisms of vertical transmission.
Author Tran, Dollnovan
Roberts, Victoria H. J.
Szeltner, Dawn
Maness, Nicholas J.
Moström, Matilda J.
Sprehe, Lesli M.
Scheef, Elizabeth A.
Hennebold, Jon D.
Kaur, Amitinder
Fahlberg, Marissa
AuthorAffiliation 3 Division of Reproductive and Developmental Sciences, Oregon National Primate Research Center , Beaverton, OR , United States
4 Division of Microbiology, Tulane National Primate Research Center , Covington, LA , United States
1 Division of Immunology, Tulane National Primate Research Center , Covington, LA , United States
2 Department of Microbiology and Immunology, Tulane School of Medicine , New Orleans, LA , United States
AuthorAffiliation_xml – name: 2 Department of Microbiology and Immunology, Tulane School of Medicine , New Orleans, LA , United States
– name: 1 Division of Immunology, Tulane National Primate Research Center , Covington, LA , United States
– name: 3 Division of Reproductive and Developmental Sciences, Oregon National Primate Research Center , Beaverton, OR , United States
– name: 4 Division of Microbiology, Tulane National Primate Research Center , Covington, LA , United States
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Copyright Copyright © 2021 Moström, Scheef, Sprehe, Szeltner, Tran, Hennebold, Roberts, Maness, Fahlberg and Kaur.
Copyright © 2021 Moström, Scheef, Sprehe, Szeltner, Tran, Hennebold, Roberts, Maness, Fahlberg and Kaur 2021 Moström, Scheef, Sprehe, Szeltner, Tran, Hennebold, Roberts, Maness, Fahlberg and Kaur
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Keywords dNK
decidual T cells
gammadelta T cells
decidua
Treg
congenital viral infection
fetal-maternal immunity
Zika
Language English
License Copyright © 2021 Moström, Scheef, Sprehe, Szeltner, Tran, Hennebold, Roberts, Maness, Fahlberg and Kaur.
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Reviewed by: Lucia De Noronha, Pontifical Catholic University of Parana, Brazil; Abhay P. S. Rathore, Duke University, United States
This article was submitted to Viral Immunology, a section of the journal Frontiers in Immunology
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Snippet The maternal decidua is an immunologically complex environment that balances maintenance of immune tolerance to fetal paternal antigens with protection of the...
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SubjectTerms Animals
decidua
Decidua - immunology
Decidua - metabolism
decidual T cells
Disease Susceptibility
dNK
Female
fetal-maternal immunity
gammadelta T cells
Host-Pathogen Interactions - immunology
Immunohistochemistry
Immunology
Immunophenotyping
Killer Cells, Natural - immunology
Killer Cells, Natural - metabolism
Leukocyte Count
Macaca mulatta
Maternal-Fetal Exchange - immunology
Monkey Diseases - etiology
Monkey Diseases - metabolism
Monkey Diseases - pathology
Monkey Diseases - transmission
Pregnancy
T-Lymphocyte Subsets - immunology
T-Lymphocyte Subsets - metabolism
Zika
Zika Virus - immunology
Zika Virus Infection - veterinary
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Title Immune Profile of the Normal Maternal-Fetal Interface in Rhesus Macaques and Its Alteration Following Zika Virus Infection
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