Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know

In humans, the hemochorial placenta is a unique temporary organ that forms during pregnancy to support fetal development, gaseous exchange, delivery of nutrition, removal of waste products, and provides immune protection, while maintaining tolerance to the HLA-haploidentical fetus. In this review, w...

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Main Authors: James H. Girsch, Maria C. Mejia Plazas, Amanda Olivier, Mohamed Farah, Dawn Littlefield, Supriya Behl, Sohan Punia, Reona Sakemura, Jack R. Hemsath, Andrew Norgan, Elizabeth A. L. Enninga, Erica L. Johnson, Rana Chakraborty
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Virology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fviro.2022.833106/full
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author James H. Girsch
James H. Girsch
Maria C. Mejia Plazas
Amanda Olivier
Mohamed Farah
Dawn Littlefield
Supriya Behl
Sohan Punia
Reona Sakemura
Jack R. Hemsath
Andrew Norgan
Elizabeth A. L. Enninga
Elizabeth A. L. Enninga
Erica L. Johnson
Rana Chakraborty
Rana Chakraborty
Rana Chakraborty
author_facet James H. Girsch
James H. Girsch
Maria C. Mejia Plazas
Amanda Olivier
Mohamed Farah
Dawn Littlefield
Supriya Behl
Sohan Punia
Reona Sakemura
Jack R. Hemsath
Andrew Norgan
Elizabeth A. L. Enninga
Elizabeth A. L. Enninga
Erica L. Johnson
Rana Chakraborty
Rana Chakraborty
Rana Chakraborty
author_sort James H. Girsch
collection DOAJ
description In humans, the hemochorial placenta is a unique temporary organ that forms during pregnancy to support fetal development, gaseous exchange, delivery of nutrition, removal of waste products, and provides immune protection, while maintaining tolerance to the HLA-haploidentical fetus. In this review, we characterize decidual and placental immunity during maternal viral (co)-infection with HIV-1, human cytomegalovirus (HCMV), and Zika virus. We discuss placental immunology, clinical presentation, and epidemiology, before characterizing host susceptibility and cellular tropism, and how the three viruses gain access into specific placental target cells. We describe current knowledge on host-viral interactions with decidual and stromal human placental macrophages or Hofbauer cells, trophoblasts including extra villous trophoblasts, T cells, and decidual natural killer (dNK) cells. These clinically significant viral infections elicit both innate and adaptive immune responses to control replication. However, the three viruses either during mono- or co-infection (HIV-1 and HCMV) escape detection to initiate placental inflammation associated with viral transmission to the developing fetus. Aside from congenital or perinatal infection, other adverse pregnancy outcomes include preterm labor and spontaneous abortion. In addition, maternal HIV-1 and HCMV co-infection are associated with impaired fetal and infant immunity in postnatal life and poor clinical outcomes during childhood in exposed infants, even in the absence of vertical transmission of HIV-1. Given the rapidly expanding numbers of HIV-1-exposed uninfected infants and children globally, further research is urgently needed on neonatal immune programming during maternal mono-and co-infection. This review therefore includes sections on current knowledge gaps that may prompt future research directions. These gaps reflect an emerging but poorly characterized field. Their significance and potential investigation is underscored by the fact that although viral infections result in adverse consequences in both mother and developing fetus/newborn, antiviral and immunomodulatory therapies can improve clinical outcomes in the dyad.
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spelling doaj.art-9808515080ff4732be16966cb58d4e6f2022-12-21T23:55:51ZengFrontiers Media S.A.Frontiers in Virology2673-818X2022-03-01210.3389/fviro.2022.833106833106Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to KnowJames H. Girsch0James H. Girsch1Maria C. Mejia Plazas2Amanda Olivier3Mohamed Farah4Dawn Littlefield5Supriya Behl6Sohan Punia7Reona Sakemura8Jack R. Hemsath9Andrew Norgan10Elizabeth A. L. Enninga11Elizabeth A. L. Enninga12Erica L. Johnson13Rana Chakraborty14Rana Chakraborty15Rana Chakraborty16Department of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesMayo Clinic Graduate School of Biomedical Science, Rochester, MN, United StatesDepartment of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Microbiology, Biochemistry, and Immunology, Morehouse School of Medicine, Atlanta, GA, United StatesDepartment of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Pediatric Research, Mayo Clinic, Rochester, MN, United StatesDepartment of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Hematology Research, Mayo Clinic, Rochester, MN, United StatesDepartment of Infectious Diseases Research, Mayo Clinic, Rochester, MN, United StatesDepartment of Laboratory Medicine and Pathology, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Immunology, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Obstetrics and Gynecology, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Microbiology, Biochemistry, and Immunology, Morehouse School of Medicine, Atlanta, GA, United StatesDepartment of Pediatric and Adolescent Medicine, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Immunology, Mayo Clinic College of Medicine, Rochester, MN, United StatesDepartment of Obstetrics and Gynecology, Mayo Clinic College of Medicine, Rochester, MN, United StatesIn humans, the hemochorial placenta is a unique temporary organ that forms during pregnancy to support fetal development, gaseous exchange, delivery of nutrition, removal of waste products, and provides immune protection, while maintaining tolerance to the HLA-haploidentical fetus. In this review, we characterize decidual and placental immunity during maternal viral (co)-infection with HIV-1, human cytomegalovirus (HCMV), and Zika virus. We discuss placental immunology, clinical presentation, and epidemiology, before characterizing host susceptibility and cellular tropism, and how the three viruses gain access into specific placental target cells. We describe current knowledge on host-viral interactions with decidual and stromal human placental macrophages or Hofbauer cells, trophoblasts including extra villous trophoblasts, T cells, and decidual natural killer (dNK) cells. These clinically significant viral infections elicit both innate and adaptive immune responses to control replication. However, the three viruses either during mono- or co-infection (HIV-1 and HCMV) escape detection to initiate placental inflammation associated with viral transmission to the developing fetus. Aside from congenital or perinatal infection, other adverse pregnancy outcomes include preterm labor and spontaneous abortion. In addition, maternal HIV-1 and HCMV co-infection are associated with impaired fetal and infant immunity in postnatal life and poor clinical outcomes during childhood in exposed infants, even in the absence of vertical transmission of HIV-1. Given the rapidly expanding numbers of HIV-1-exposed uninfected infants and children globally, further research is urgently needed on neonatal immune programming during maternal mono-and co-infection. This review therefore includes sections on current knowledge gaps that may prompt future research directions. These gaps reflect an emerging but poorly characterized field. Their significance and potential investigation is underscored by the fact that although viral infections result in adverse consequences in both mother and developing fetus/newborn, antiviral and immunomodulatory therapies can improve clinical outcomes in the dyad.https://www.frontiersin.org/articles/10.3389/fviro.2022.833106/fullplacentaHIV-1human cytomegalovirusZikavertical transmissioncytotrophoblast
spellingShingle James H. Girsch
James H. Girsch
Maria C. Mejia Plazas
Amanda Olivier
Mohamed Farah
Dawn Littlefield
Supriya Behl
Sohan Punia
Reona Sakemura
Jack R. Hemsath
Andrew Norgan
Elizabeth A. L. Enninga
Elizabeth A. L. Enninga
Erica L. Johnson
Rana Chakraborty
Rana Chakraborty
Rana Chakraborty
Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
Frontiers in Virology
placenta
HIV-1
human cytomegalovirus
Zika
vertical transmission
cytotrophoblast
title Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
title_full Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
title_fullStr Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
title_full_unstemmed Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
title_short Host-Viral Interactions at the Maternal-Fetal Interface. What We Know and What We Need to Know
title_sort host viral interactions at the maternal fetal interface what we know and what we need to know
topic placenta
HIV-1
human cytomegalovirus
Zika
vertical transmission
cytotrophoblast
url https://www.frontiersin.org/articles/10.3389/fviro.2022.833106/full
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