SARS-CoV-2 infection elucidates features of pregnancy-specific immunity
Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and...
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| Published in | Cell reports (Cambridge) Vol. 43; no. 11; p. 114933 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
26.11.2024
Elsevier |
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| Online Access | Get full text |
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| Abstract | Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8+ T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection.
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•COVID-19 is associated with altered T cell responses in pregnant patients•Identified altered cytokine and chemokine levels in pregnant patients with COVID-19•scRNA-seq analyses reveal decreased ISG responses in pregnant patients with COVID-19•Severe/critical illness and maternal obesity are associated with additional immune dysfunction
Oh et al. perform a comprehensive immune survey of COVID-19 in pregnant and non-pregnant women, identifying pregnancy-specific alterations in immune responses. These include altered T cell responses, monocyte function, chemokines and cytokines, and gut microbial composition. This work provides insights into how pregnancy shapes antiviral immunity. |
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| AbstractList | Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8
T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection. Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8+ T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection. [Display omitted] •COVID-19 is associated with altered T cell responses in pregnant patients•Identified altered cytokine and chemokine levels in pregnant patients with COVID-19•scRNA-seq analyses reveal decreased ISG responses in pregnant patients with COVID-19•Severe/critical illness and maternal obesity are associated with additional immune dysfunction Oh et al. perform a comprehensive immune survey of COVID-19 in pregnant and non-pregnant women, identifying pregnancy-specific alterations in immune responses. These include altered T cell responses, monocyte function, chemokines and cytokines, and gut microbial composition. This work provides insights into how pregnancy shapes antiviral immunity. Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8+ T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection.Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8+ T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection. Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8 + T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection. Oh et al. perform a comprehensive immune survey of COVID-19 in pregnant and non-pregnant women, identifying pregnancy-specific alterations in immune responses. These include altered T cell responses, monocyte function, chemokines and cytokines, and gut microbial composition. This work provides insights into how pregnancy shapes antiviral immunity. Pregnancy is a risk factor for increased severity of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and other respiratory infections, but the mechanisms underlying this risk are poorly understood. To gain insight into the role of pregnancy in modulating immune responses at baseline and upon SARS-CoV-2 infection, we collected peripheral blood mononuclear cells and plasma from 226 women, including 152 pregnant individuals and 74 non-pregnant women. We find that SARS-CoV-2 infection is associated with altered T cell responses in pregnant women, including a clonal expansion of CD4-expressing CD8+ T cells, diminished interferon responses, and profound suppression of monocyte function. We also identify shifts in cytokine and chemokine levels in the sera of pregnant individuals, including a robust increase of interleukin-27, known to drive T cell exhaustion. Our findings reveal nuanced pregnancy-associated immune responses, which may contribute to the increased susceptibility of pregnant individuals to viral respiratory infection. |
| ArticleNumber | 114933 |
| Author | Filbin, Michael R. Shook, Lydia L. Goldberg, Marcia B. Perlis, Roy H. Sen, Pritha Arnold, Benjamin Y. Edlow, Andrea G. Lyall, Amanda Gilbert, Emily Kim, Joon Normand, Rachelly Slowikowski, Kamil Yu, Xu G. Demidkin, Stepan Gray, Kathryn J. Fasano, Alessio Huh, Jun R. Akinwunmi, Babatunde Tirard, Alice Drew, David A. Choi, Gloria B. Oh, Dong Sun Hacohen, Nir Villani, Alexandra-Chloé Pasternak, Ofer Lu, Guangqing Kim, Eunha Nguyen, Long H. Jasset, Olyvia Tantivit, Jessica Chan, Andrew T. Li, Jonathan Z. Yonker, Lael |
| AuthorAffiliation | 13 Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA 23 Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA 02114, USA 14 Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA 7 Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA 25 Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA 9 Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA 8 Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA 18 Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA 30 Senior author 19 Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA 2 BK21 Graduate Progra |
| AuthorAffiliation_xml | – name: 7 Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA – name: 2 BK21 Graduate Program, Department of Biomedical Sciences and Department of Neuroscience, Korea University College of Medicine, Seoul 02841, Republic of Korea – name: 8 Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA – name: 25 Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 24 Division of Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital, Boston, MA 02114, USA – name: 29 Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 22 Division of Infectious Diseases, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 14 Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA – name: 19 Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA – name: 30 Senior author – name: 32 Lead contact – name: 3 Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA – name: 15 Department of Medicine, Harvard Medical School, Boston, MA 02115, USA – name: 9 Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 18 Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA – name: 28 Transplant, Oncology, and Immunocompromised Host Group, Division of Infectious Diseases, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 21 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA – name: 10 Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA – name: 12 Department of Microbiology, Harvard Medical School, Boston, MA 02115, USA – name: 6 Harvard Medical School, Boston, MA 02115, USA – name: 26 Department of Obstetrics & Gynecology, University of Washington, Seattle, WA 98195, USA – name: 4 Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA – name: 23 Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA 02114, USA – name: 17 Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – name: 5 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – name: 11 Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02114, USA – name: 31 These authors contributed equally – name: 16 Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – name: 20 Infectious Disease Division, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 27 The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – name: 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA – name: 13 Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA |
| Author_xml | – sequence: 1 givenname: Dong Sun surname: Oh fullname: Oh, Dong Sun organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA – sequence: 2 givenname: Eunha surname: Kim fullname: Kim, Eunha organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA – sequence: 3 givenname: Rachelly surname: Normand fullname: Normand, Rachelly organization: Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA – sequence: 4 givenname: Guangqing surname: Lu fullname: Lu, Guangqing organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA – sequence: 5 givenname: Lydia L. surname: Shook fullname: Shook, Lydia L. organization: Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA – 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| Keywords | COVID-19 CP: Immunology SARS-CoV-2 pregnancy maternal immune activation single-cell RNA-seq immune cells cytokines T cells immune responses |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS A.G.E. and J.R.H. conceptualized the study. A.G.E. supervised all the clinical aspects of the study, metadata generation, and results interpretation. J.R.H. supervised immune analyses. A.-C.V. managed and supervised scRNA-seq data generation and analyses. D.S.O., E.K., G.L., G.B.C., A.G.E., and J.R.H. designed experiments. D.S.O., E.K., G.L., R.N., A.L., and O.P. analyzed data. MGH COVID Collection & Processing Team, P.S., J.T., A.T., and B.Y.A., collected, processed, and generated samples and/or data from the MGH acute COVID-19 non-pregnant cohort, which was overseen by X.G.Y. and J.Z.L. L.L.S., O.J., S.D., E.G., J.K., and B.A. enrolled, collected, processed, and generated samples and phenotypic data from the MGB COVID-19 Pregnancy Biorepository, which was supervised by A.G.E. and K.J.G., and to which L.Y. and A.F. also contributed personnel support and resources. M.B.G., M.R.F, and N.H. oversaw the MGH acute COVID cohort. P.S., J.T., A.T., and B.Y.A. performed the single-cell multiomics experiments for the COVID-19 pregnancy cohort. R.N. performed single-cell data analysis. R.N., P.S., and A.-C.V. performed single-cell data analysis interpretation. D.A.D. and L.H.N. performed metagenomic sequencing and analysis, supervised by A.T.C. D.S.O., E.K., G.L., R.N., P.S., A.-C.V., A.G.E., and J.R.H. wrote the manuscript. All authors read or provided comments on the manuscript. |
| ORCID | 0000-0002-1540-6244 0000-0003-2915-5949 |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.1016/j.celrep.2024.114933 |
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| PublicationCentury | 2000 |
| PublicationDate | 2024-11-26 |
| PublicationDateYYYYMMDD | 2024-11-26 |
| PublicationDate_xml | – month: 11 year: 2024 text: 2024-11-26 day: 26 |
| PublicationDecade | 2020 |
| PublicationPlace | United States |
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| PublicationTitle | Cell reports (Cambridge) |
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| PublicationYear | 2024 |
| Publisher | Elsevier Inc Elsevier |
| Publisher_xml | – name: Elsevier Inc – name: Elsevier |
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| Title | SARS-CoV-2 infection elucidates features of pregnancy-specific immunity |
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