Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection

Summary: While severe coronavirus 2019 (COVID-19) is associated with immune activation at the maternal-fetal interface, responses to asymptomatic/mild severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection during pregnancy remain unknown. Here, we assess immunological adaptations in...

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Main Authors: Suhas Sureshchandra, Michael Z. Zulu, Brianna M. Doratt, Allen Jankeel, Delia Tifrea, Robert Edwards, Monica Rincon, Nicole E. Marshall, Ilhem Messaoudi
Format: Article
Language:English
Published: Elsevier 2022-06-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124722007203
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author Suhas Sureshchandra
Michael Z. Zulu
Brianna M. Doratt
Allen Jankeel
Delia Tifrea
Robert Edwards
Monica Rincon
Nicole E. Marshall
Ilhem Messaoudi
author_facet Suhas Sureshchandra
Michael Z. Zulu
Brianna M. Doratt
Allen Jankeel
Delia Tifrea
Robert Edwards
Monica Rincon
Nicole E. Marshall
Ilhem Messaoudi
author_sort Suhas Sureshchandra
collection DOAJ
description Summary: While severe coronavirus 2019 (COVID-19) is associated with immune activation at the maternal-fetal interface, responses to asymptomatic/mild severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection during pregnancy remain unknown. Here, we assess immunological adaptations in blood and term decidua in response to asymptomatic/mild disease in pregnant women. We report attenuated antigen presentation and type I interferon (IFN) signaling pathways, loss of tissue-resident decidual macrophages, and upregulated cytokine/chemokine signaling in monocyte-derived decidual macrophages. Furthermore, we describe increased frequencies of activated tissue-resident T cells and decreased abundance of regulatory T cells with infection while frequencies of cytotoxic CD4/CD8 T cells are increased in the blood. In contrast to decidual macrophages, type I IFN signaling is higher in decidual T cells. Finally, infection leads to a narrowing of T cell receptor diversity in both blood and decidua. Collectively, these observations indicate that asymptomatic/mild COVID-19 during pregnancy results in remodeling of the immunological landscape of the maternal-fetal interface, with a potential for long-term adverse outcomes for the offspring.
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spelling doaj.art-d5555b8dc8e64730963623c27f78b0512022-12-22T03:30:03ZengElsevierCell Reports2211-12472022-06-013911110938Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infectionSuhas Sureshchandra0Michael Z. Zulu1Brianna M. Doratt2Allen Jankeel3Delia Tifrea4Robert Edwards5Monica Rincon6Nicole E. Marshall7Ilhem Messaoudi8Department of Molecular Biology and Biochemistry, School of Biological Sciences, University of California, Irvine, CA 92697, USA; Institute for Immunology, University of California, Irvine, CA 92697, USADepartment of Molecular Biology and Biochemistry, School of Biological Sciences, University of California, Irvine, CA 92697, USA; Institute for Immunology, University of California, Irvine, CA 92697, USADepartment of Molecular Biology and Biochemistry, School of Biological Sciences, University of California, Irvine, CA 92697, USA; Institute for Immunology, University of California, Irvine, CA 92697, USA; Department of Microbiology, Immunology, and Molecular Genetics, College of Medicine, University of Kentucky, Lexington, KY 40536, USADepartment of Molecular Biology and Biochemistry, School of Biological Sciences, University of California, Irvine, CA 92697, USADepartment of Pathology and Laboratory Medicine, School of Medicine, University of California, Irvine, CA 92697, USADepartment of Pathology and Laboratory Medicine, School of Medicine, University of California, Irvine, CA 92697, USAMaternal-Fetal Medicine, Oregon Health and Sciences University, Portland, OR 97239, USAMaternal-Fetal Medicine, Oregon Health and Sciences University, Portland, OR 97239, USADepartment of Molecular Biology and Biochemistry, School of Biological Sciences, University of California, Irvine, CA 92697, USA; Institute for Immunology, University of California, Irvine, CA 92697, USA; Department of Microbiology, Immunology, and Molecular Genetics, College of Medicine, University of Kentucky, Lexington, KY 40536, USA; Corresponding authorSummary: While severe coronavirus 2019 (COVID-19) is associated with immune activation at the maternal-fetal interface, responses to asymptomatic/mild severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection during pregnancy remain unknown. Here, we assess immunological adaptations in blood and term decidua in response to asymptomatic/mild disease in pregnant women. We report attenuated antigen presentation and type I interferon (IFN) signaling pathways, loss of tissue-resident decidual macrophages, and upregulated cytokine/chemokine signaling in monocyte-derived decidual macrophages. Furthermore, we describe increased frequencies of activated tissue-resident T cells and decreased abundance of regulatory T cells with infection while frequencies of cytotoxic CD4/CD8 T cells are increased in the blood. In contrast to decidual macrophages, type I IFN signaling is higher in decidual T cells. Finally, infection leads to a narrowing of T cell receptor diversity in both blood and decidua. Collectively, these observations indicate that asymptomatic/mild COVID-19 during pregnancy results in remodeling of the immunological landscape of the maternal-fetal interface, with a potential for long-term adverse outcomes for the offspring.http://www.sciencedirect.com/science/article/pii/S2211124722007203CP: ImmunologyCP: Microbiology
spellingShingle Suhas Sureshchandra
Michael Z. Zulu
Brianna M. Doratt
Allen Jankeel
Delia Tifrea
Robert Edwards
Monica Rincon
Nicole E. Marshall
Ilhem Messaoudi
Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
Cell Reports
CP: Immunology
CP: Microbiology
title Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
title_full Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
title_fullStr Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
title_full_unstemmed Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
title_short Single-cell RNA sequencing reveals immunological rewiring at the maternal-fetal interface following asymptomatic/mild SARS-CoV-2 infection
title_sort single cell rna sequencing reveals immunological rewiring at the maternal fetal interface following asymptomatic mild sars cov 2 infection
topic CP: Immunology
CP: Microbiology
url http://www.sciencedirect.com/science/article/pii/S2211124722007203
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