. 2024 Nov 26;43(11):114933.

doi: 10.1016/j.celrep.2024.114933. Epub 2024 Nov 5.

SARS-CoV-2 infection elucidates features of pregnancy-specific immunity

Dong Sun Oh¹, Eunha Kim², Rachelly Normand³, Guangqing Lu¹, Lydia L Shook⁴, Amanda Lyall⁵, Olyvia Jasset⁶, Stepan Demidkin⁶, Emily Gilbert⁶, Joon Kim⁶, Babatunde Akinwunmi⁶, Jessica Tantivit⁷, Alice Tirard⁷, Benjamin Y Arnold⁷, Kamil Slowikowski³; MGH COVID-19 Collection & Processing Team; Marcia B Goldberg⁸, Michael R Filbin⁹, Nir Hacohen¹⁰, Long H Nguyen¹¹, Andrew T Chan¹², Xu G Yu¹³, Jonathan Z Li¹⁴, Lael Yonker¹⁵, Alessio Fasano¹⁶, Roy H Perlis¹⁷, Ofer Pasternak¹⁸, Kathryn J Gray¹⁹, Gloria B Choi²⁰, David A Drew¹⁷, Pritha Sen²¹, Alexandra-Chloé Villani²², Andrea G Edlow²³, Jun R Huh²⁴

Affiliations

¹ Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA.
² Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA; BK21 Graduate Program, Department of Biomedical Sciences and Department of Neuroscience, Korea University College of Medicine, Seoul 02841, Republic of Korea.
³ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA.
⁴ Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
⁵ Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
⁶ Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
⁷ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
⁸ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Department of Microbiology, Harvard Medical School, Boston, MA 02115, USA; Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
⁹ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
¹⁰ Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Medicine, Harvard Medical School, Boston, MA 02115, USA.
¹¹ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹² Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA; Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹³ Infectious Disease Division, Brigham and Women's Hospital, Boston, MA 02115, USA; Ragon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA.
¹⁴ Division of Infectious Diseases, Brigham and Women's Hospital, Boston, MA 02115, USA.
¹⁵ Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA 02114, USA.
¹⁶ Division of Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital, Boston, MA 02114, USA.
¹⁷ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
¹⁸ Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
¹⁹ Department of Obstetrics & Gynecology, University of Washington, Seattle, WA 98195, USA.
²⁰ The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
²¹ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA; Transplant, Oncology, and Immunocompromised Host Group, Division of Infectious Diseases, Brigham and Women's Hospital, Boston, MA 02115, USA; Dana-Farber Cancer Institute, Boston, MA 02215, USA.
²² Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA. Electronic address: avillani@mgh.harvard.edu.
²³ Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA. Electronic address: aedlow@mgh.harvard.edu.
²⁴ Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA. Electronic address: jun_huh@hms.harvard.edu.

PMID: 39504241
PMCID: PMC11724703
DOI: 10.1016/j.celrep.2024.114933

SARS-CoV-2 infection elucidates features of pregnancy-specific immunity

Dong Sun Oh et al. Cell Rep. 2024.

. 2024 Nov 26;43(11):114933.

doi: 10.1016/j.celrep.2024.114933. Epub 2024 Nov 5.

Authors

Affiliations

¹ Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA.
² Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA; BK21 Graduate Program, Department of Biomedical Sciences and Department of Neuroscience, Korea University College of Medicine, Seoul 02841, Republic of Korea.
³ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA.
⁴ Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
⁵ Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
⁶ Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
⁷ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
⁸ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Department of Microbiology, Harvard Medical School, Boston, MA 02115, USA; Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
⁹ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
¹⁰ Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Medicine, Harvard Medical School, Boston, MA 02115, USA.
¹¹ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹² Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Harvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA; Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹³ Infectious Disease Division, Brigham and Women's Hospital, Boston, MA 02115, USA; Ragon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA.
¹⁴ Division of Infectious Diseases, Brigham and Women's Hospital, Boston, MA 02115, USA.
¹⁵ Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA 02114, USA.
¹⁶ Division of Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital, Boston, MA 02114, USA.
¹⁷ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
¹⁸ Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
¹⁹ Department of Obstetrics & Gynecology, University of Washington, Seattle, WA 98195, USA.
²⁰ The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
²¹ Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA; Transplant, Oncology, and Immunocompromised Host Group, Division of Infectious Diseases, Brigham and Women's Hospital, Boston, MA 02115, USA; Dana-Farber Cancer Institute, Boston, MA 02215, USA.
²² Center for Immunology and Inflammatory Diseases, Department of Medicine, Massachusetts General Hospital, Boston, MA 02129, USA; Krantz Family Center for Cancer Research, Massachusetts General Hospital, Boston, MA 02114, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Harvard Medical School, Boston, MA 02115, USA. Electronic address: avillani@mgh.harvard.edu.
²³ Department of Obstetrics, Gynecology and Reproductive Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA 02114, USA. Electronic address: aedlow@mgh.harvard.edu.
²⁴ Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA. Electronic address: jun_huh@hms.harvard.edu.

PMID: 39504241
PMCID: PMC11724703
DOI: 10.1016/j.celrep.2024.114933

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.

Keywords: COVID-19; CP: Immunology; SARS-CoV-2; T cells; cytokines; immune cells; immune responses; maternal immune activation; pregnancy; single-cell RNA-seq.

PubMed Disclaimer

Conflict of interest statement

Declaration of interests A.-C.V. has a financial interest in 10X Genomics. The company designs and manufactures gene-sequencing technology for use in research, and such technology is being used in this research. A.-C.V.’s interests were reviewed by The Massachusetts General Hospital and Mass General Brigham in accordance with their institutional policies. J.R.H. consults for CJ CheilJedang and Interon Laboratories. A.G.E. consults for Mirvie, Inc. outside of this work and receives research funding from Merck Pharmaceuticals outside of this work. K.J.G. has served as a consultant for BillionToOne, Aetion, Roche, and Janssen Global Services outside of this work.

Figures

**Figure 1.. Comparative T cell analyses of pregnant versus non-pregnant patients with COVID-19**
(A) A schematic of the analyses performed in this paper: non-pregnant versus pregnant women with or without COVID-19. (B) CD25⁺ FOXP3⁺-expressing CD4⁺ T cell frequencies in PBMCs. (C and D) Left panels show CM (CD45RO⁺ CCR7⁺) and right panels show EM (CD45RO⁺ CCR7⁻) frequencies in CD4⁺ T cells (CD19⁻ CD3⁺ CD4⁺) (C) and CD8⁺ (CD19⁻ CD3⁺ CD8⁺) T cells (D) in PBMCs. (E and F) Frequencies of CD8⁺ T cells expressing (E) PD-1 and Tim-3 and (F) IL-2 and TNF-α. Healthy (non-pregnant, n = 19; pregnant, n = 34), severe/critical COVID-19 (non-pregnant, n = 9; pregnant, n = 15), or convalescent COVID-19 (non-pregnant, n = 18; pregnant, n = 22). Data are shown as the mean ± SEM. *p < 0.05, **p < 0.01, ***p < 0.001.

**Figure 2.. Pregnancy enhances monocyte function**
(A) Representative fluorescence-activated cell sorting (FACS) plots and quantifications of classical monocytes (CD14⁺), intermediate monocytes (CD14⁺CD16⁺), and non-classical monocytes (CD16⁺) as analyzed by flow cytometry from PBMCs. (B) Mean fluorescence intensities (MFIs) of HLA-DR expression in classical, intermediate, and alternative monocytes. (C) Frequencies of Ki67, a proliferation marker, expressed in classical, intermediate, and alternative monocytes. (D and E) A heatmap presenting monocyte-secreted cytokines upon 1 ng/mL LPS stimulation (D) and representative cytokine levels in the supernatant as quantified by cytometric bead array analyses (E). Healthy (non-pregnant, n = 19; pregnant, n = 34), severe/critical COVID-19 (non-pregnant, n = 9; pregnant, n = 15), or convalescent COVID-19 (non-pregnant, n = 18; pregnant, n = 22). Data are shown as the mean ± SEM. *p < 0.05, **p < 0.01, ***p < 0.001.

**Figure 3.. Changes in CD8⁺ T cell clonal expansion and cell subset abundances in pregnant patients with COVID-19**
(A) Uniform manifold approximation and projection (UMAP) embedding of 50,140 CD8⁺ T and NK cells and their clustering to 13 cell subsets (left). Expression of main marker genes, scaled mean log (counts per million, CPM) (right). (B) A boxplot illustrating the abundance of CD8⁺ T cell subsets out of all CD8⁺ T and NK cells. (C) Frequency of TCR clones projected on CD8⁺ T and NK cell UMAP and split by condition (SEV, severe; ASX, asymptomatic; CTRL, control). (D) A boxplot illustrating the percentage of expanded clones out of total expanded clones per cell subset in pregnant versus non-pregnant COVID-19 patients. (E) Gene and protein expression that characterize cell subset CD8T_3_cytotoxic_CD4; hex bin plots with log(CPM). (F) TCR clones with specificity to SARS-CoV-2 projected onto CD8⁺ T and NK UMAPs. (G) Percentage of TCR clones with specificity to SARS-CoV-2 epitopes out of total cells in each cell subset (x axis) and number of cells with SARS-CoV-2 specificity (annotation at the end of the bars). *p < 0.05, **p < 0.01, ***p < 0.001.

**Figure 4.. ISGs are downregulated in pregnant patients with COVID-19**
(A) UMAP embedding of 50,140 CD8⁺ T and NK cells and their clustering to 13 cell subsets. (B) A boxplot illustrating the expression signature of 91 ISGs across CD8⁺ T cell subsets in pregnant versus non-pregnant COVID-19 patients. (C) UMAP embedding of 66,719 mononuclear phagocyte (MNP) cells and their clustering to eight cell subsets. (D) A boxplot illustrating the expression signature of 91 ISGs across MNP cell subsets in pregnant versus non-pregnant COVID-19 patients. (E) UMAP embedding of 29,960 CD4⁺ T cells and their clustering to eight cell subsets. (F) A boxplot illustrating the expression signature of 91 ISGs across CD4 T cell subsets in pregnant versus non-pregnant COVID-19 patients. (G) UMAP embedding of 19,168 B and plasma cells and their clustering to nine cell subsets. (H) A boxplot illustrating the expression signature of 91 ISGs across B cell subsets in pregnant versus non-pregnant COVID-19 patients. (I) A boxplot illustrating the B_3_naive_ISG cell subset abundances in pregnant versus non-pregnant COVID-19 patients. NonPreg_COVID includes non-pregnant patients with asymptomatic and severe COVID-19; Preg_COVID includes pregnant patients with asymptomatic and severe COVID-19. *p < 0.05, ***p < 0.001.

**Figure 5.. Comparative analyses of plasma cytokines, chemokines, and growth factors of pregnant versus non-pregnant control and COVID-19 patients**
Concentrations of cytokines, chemokines, and growth factors in pregnant and non-pregnant women who were healthy (non-pregnant, n = 17; pregnant, n = 21) or who had mild (non-pregnant, n = 12; pregnant, n = 21), moderate (non-pregnant, n = 9; pregnant, n = 6), or severe/critical (non-pregnant, n = 10; pregnant, n = 11) COVID-19. Data are shown as the mean ± SEM. *p < 0.05, **p < 0.01, ***p < 0.001.

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Update of

SARS-CoV-2 infection elucidates unique features of pregnancy-specific immunity.
Oh DS, Kim E, Lu G, Normand R, Shook LL, Lyall A, Jasset O, Demidkin S, Gilbert E, Kim J, Akinwunmi B, Tantivit J, Tirard A, Arnold BY, Slowikowski K; MGH COVID-19 Collection & Processing Team; Goldberg MB, Filbin MR, Hacohen N, Nguyen LH, Chan AT, Yu XG, Li JZ, Yonker L, Fasano A, Perlis RH, Pasternak O, Gray KJ, Choi GB, Drew DA, Sen P, Villani AC, Edlow AG, Huh JR. Oh DS, et al. medRxiv [Preprint]. 2024 Feb 7:2024.02.05.24301794. doi: 10.1101/2024.02.05.24301794. medRxiv. 2024. Update in: Cell Rep. 2024 Nov 26;43(11):114933. doi: 10.1016/j.celrep.2024.114933. PMID: 38370801 Free PMC article. Updated. Preprint.

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SARS-CoV-2 infection elucidates features of pregnancy-specific immunity

Affiliations

SARS-CoV-2 infection elucidates features of pregnancy-specific immunity

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

Update of

References

Publication types

MeSH terms

Substances

Associated data

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Molecular Biology Databases

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