{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T16:56:32Z","timestamp":1788281792015,"version":"build-2803163510"},"update-to":[{"DOI":"10.1371\/journal.ppat.1011990","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,2,20]],"date-time":"2024-02-20T00:00:00Z","timestamp":1708387200000}}],"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2024,2,7]],"date-time":"2024-02-07T00:00:00Z","timestamp":1707264000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["1D71TW012265-01"],"award-info":[{"award-number":["1D71TW012265-01"]}]},{"name":"NIH","award":["1U01AI131566-01"],"award-info":[{"award-number":["1U01AI131566-01"]}]},{"name":"NIH","award":["HD065987"],"award-info":[{"award-number":["HD065987"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Hofbauer cells (HBCs) and cytotrophoblasts (CTBs) are major cell populations in placenta. The indirect impact of maternal SARS-CoV-2 disease on these cells that are not directly infected has not been extensively studied. Herein, we profiled gene expression in HBCs and CTBs isolated from placentae of recovered pregnant subjects infected with SARS-CoV-2 during all trimesters of pregnancy, placentae from subjects with active infection, SARS-CoV-2 vaccinated subjects, and those who were unexposed to the virus.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>Placentae were collected within 4 h post-delivery and membrane-free tissues were enzymatically digested for the isolation of HBCs and CTBs. RNA extracted from HBCs and CTBs were sequenced using 150bp paired-end reads. Differentially expressed genes (DEGs) were identified by DESeq2 package in R and enriched in GO Biological Processes, KEGG Pathway, Reactome Gene Sets, Hallmark Gene Sets, and Canonical Pathways. Protein-protein interactions among the DEGs were modelled using STRING and BioGrid.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>Pregnant subjects (n = 30) were recruited and categorized into six groups: infected with SARS-CoV-2 in i) the first (1T, n = 4), ii) second (2T, n = 5), iii) third (3T, n = 5) trimester, iv) tested positive at delivery (Delivery, n = 5), v) never infected (Control, n = 6), and vi) fully mRNA-vaccinated by delivery (Vaccinated, n = 5). Compared to the Control group, gene expression analysis showed that HBCs from infected subjects had significantly altered gene expression profiles, with the 2T group having the highest number of DEGs (1,696), followed by 3T and 1T groups (1,656 and 958 DEGs, respectively). These DEGs were enriched for pathways involved in immune regulation for host defense, including production of cytokines, chemokines, antimicrobial proteins, ribosomal assembly, neutrophil degranulation inflammation, morphogenesis, and cell migration\/adhesion. Protein-protein interaction analysis mapped these DEGs with oxidative phosphorylation, translation, extracellular matrix organization, and type I interferon signaling. Only 95, 23, and 8 DEGs were identified in CTBs of 1T, 2T, and 3T groups, respectively. Similarly, 11 and 3 DEGs were identified in CTBs and HBCs of vaccinated subjects, respectively. Reassuringly, mRNA vaccination did not induce an inflammatory response in placental cells.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>Our studies demonstrate a significant impact of indirect SARS-CoV-2 infection on gene expression of inner mesenchymal HBCs, with limited effect on lining CTB cells isolated from pregnant subjects infected and recovered from SARS-CoV-2. The pathways associated with these DEGs identify potential targets for therapeutic intervention.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.ppat.1011990","type":"journal-article","created":{"date-parts":[[2024,2,7]],"date-time":"2024-02-07T18:41:34Z","timestamp":1707331294000},"page":"e1011990","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Maternal SARS-CoV-2 infection in pregnancy disrupts gene expression in Hofbauer cells with limited impact on cytotrophoblasts"],"prefix":"10.1371","volume":"20","author":[{"given":"Elizabeth Ann L.","family":"Enninga","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huy Quang","family":"Quach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin Sung","family":"Jang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Cristina Miranda","family":"de Araujo Correia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaroslav","family":"Fedyshyn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bohdana","family":"Fedyshyn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maureen","family":"Lemens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dawn","family":"Littlefield","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Supriya","family":"Behl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elise","family":"Sintim-Aboagye","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria C.","family":"Mejia Plazas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria C.","family":"Cardenas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shree","family":"Chakraborty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoko","family":"Yamaoka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hideki","family":"Ebihara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akhilesh","family":"Pandey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hu","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew D.","family":"Badley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erica L.","family":"Johnson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew P.","family":"Norgan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Regan N.","family":"Theiler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2191-5771","authenticated-orcid":true,"given":"Rana","family":"Chakraborty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,2,7]]},"reference":[{"issue":"8","key":"ppat.1011990.ref001","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1056\/NEJMoa2001017","article-title":"A Novel Coronavirus from Patients with Pneumonia in China, 2019","volume":"382","author":"N Zhu","year":"2020","journal-title":"N Engl J Med"},{"issue":"6","key":"ppat.1011990.ref002","doi-asserted-by":"crossref","DOI":"10.1172\/JCI145427","article-title":"Severe SARS-CoV-2 placenta infection can impact neonatal outcome in the absence of vertical transmission","volume":"131","author":"FM Cribi\u00f9","year":"2021","journal-title":"The Journal of Clinical Investigation"},{"issue":"9","key":"ppat.1011990.ref003","doi-asserted-by":"crossref","first-page":"4947","DOI":"10.1172\/JCI139569","article-title":"SARS\u2013CoV-2 infection of the placenta","volume":"130","author":"H Hosier","year":"2020","journal-title":"The Journal of clinical investigation"},{"key":"ppat.1011990.ref004","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.placenta.2020.07.022","article-title":"Placental barrier against COVID-19","volume":"99","author":"S Komine-Aizawa","year":"2020","journal-title":"Placenta"},{"issue":"1","key":"ppat.1011990.ref005","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1159\/000511324","article-title":"Placental pathology findings during and after SARS-CoV-2 infection: features of villitis and malperfusion","volume":"88","author":"T Menter","year":"2021","journal-title":"Pathobiology"},{"issue":"6","key":"ppat.1011990.ref006","doi-asserted-by":"crossref","first-page":"994","DOI":"10.1111\/his.14215","article-title":"Third-trimester placentas of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-positive women: histomorphology, including viral immunohistochemistry and in-situ hybridization","volume":"77","author":"MC Smithgall","year":"2020","journal-title":"Histopathology"},{"issue":"10","key":"ppat.1011990.ref007","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/S2352-4642(20)30235-2","article-title":"Neonatal management and outcomes during the COVID-19 pandemic: an observation cohort study","volume":"4","author":"CM Salvatore","year":"2020","journal-title":"Lancet Child Adolesc Health"},{"issue":"5","key":"ppat.1011990.ref008","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1093\/jpids\/piaa109","article-title":"A Possible Case of Vertical Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in a Newborn With Positive Placental In Situ Hybridization of SARS-CoV-2 RNA","volume":"9","author":"I Alamar","year":"2020","journal-title":"J Pediatric Infect Dis Soc"},{"issue":"18","key":"ppat.1011990.ref009","first-page":"1846","article-title":"Possible Vertical Transmission of SARS-CoV-2 From an Infected Mother to Her Newborn","volume":"323","author":"L Dong","year":"2020","journal-title":"Jama"},{"key":"ppat.1011990.ref010","doi-asserted-by":"crossref","first-page":"102951","DOI":"10.1016\/j.ebiom.2020.102951","article-title":"SARS-CoV2 vertical transmission with adverse effects on the newborn revealed through integrated immunohistochemical, electron microscopy and molecular analyses of Placenta","volume":"59","author":"F Facchetti","year":"2020","journal-title":"EBioMedicine"},{"issue":"1","key":"ppat.1011990.ref011","doi-asserted-by":"crossref","first-page":"5128","DOI":"10.1038\/s41467-020-18933-4","article-title":"Analysis of SARS-CoV-2 vertical transmission during pregnancy","volume":"11","author":"C Fenizia","year":"2020","journal-title":"Nat Commun"},{"issue":"3","key":"ppat.1011990.ref012","doi-asserted-by":"crossref","first-page":"510","DOI":"10.3201\/eid2803.211735","article-title":"Detection of SARS-CoV-2 in Neonatal Autopsy Tissues and Placenta","volume":"28","author":"S Reagan-Steiner","year":"2022","journal-title":"Emerg Infect Dis"},{"issue":"1","key":"ppat.1011990.ref013","doi-asserted-by":"crossref","first-page":"3572","DOI":"10.1038\/s41467-020-17436-6","article-title":"Transplacental transmission of SARS-CoV-2 infection","volume":"11","author":"AJ Vivanti","year":"2020","journal-title":"Nat Commun"},{"key":"ppat.1011990.ref014","article-title":"Vertical Transmission of SARS-CoV-2-Specific Antibodies and Cytokine Profiles in Pregnancy","author":"JM Monroe","year":"2023","journal-title":"J Infect 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State","volume":"223","author":"EM Lokken","year":"2020","journal-title":"Am J Obstet Gynecol"},{"issue":"38","key":"ppat.1011990.ref021","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.15585\/mmwr.mm6938e2","article-title":"SARS-CoV-2 Infection Among Hospitalized Pregnant Women: Reasons for Admission and Pregnancy Characteristics\u2014Eight U.S. Health Care Centers, March 1-May 30, 2020","volume":"69","author":"L Panagiotakopoulos","year":"2020","journal-title":"MMWR Morb Mortal Wkly Rep"},{"issue":"8","key":"ppat.1011990.ref022","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1001\/jamapediatrics.2021.1050","article-title":"Maternal and Neonatal Morbidity and Mortality Among Pregnant Women With and Without COVID-19 Infection: The INTERCOVID Multinational Cohort Study","volume":"175","author":"J Villar","year":"2021","journal-title":"JAMA Pediatr"},{"issue":"44","key":"ppat.1011990.ref023","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.15585\/mmwr.mm6944e2","article-title":"Birth and Infant Outcomes Following Laboratory-Confirmed SARS-CoV-2 Infection in Pregnancy\u2014SET-NET, 16 Jurisdictions, March 29-October 14, 2020","volume":"69","author":"KR Woodworth","year":"2020","journal-title":"MMWR Morb Mortal Wkly Rep"},{"key":"ppat.1011990.ref024","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/978-3-319-54090-0_3","article-title":"Hofbauer Cells: Placental Macrophages of Fetal Origin","volume":"62","author":"L Reyes","year":"2017","journal-title":"Results Probl Cell Differ"},{"issue":"5","key":"ppat.1011990.ref025","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/j.chom.2017.04.007","article-title":"Microbial Vertical Transmission during Human Pregnancy","volume":"21","author":"N Arora","year":"2017","journal-title":"Cell Host Microbe"},{"issue":"4","key":"ppat.1011990.ref026","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1086\/422330","article-title":"Viral and bacterial pathogens at the maternal-fetal interface","volume":"190","author":"S McDonagh","year":"2004","journal-title":"J Infect Dis"},{"issue":"19","key":"ppat.1011990.ref027","doi-asserted-by":"crossref","DOI":"10.1172\/jci.insight.172658","article-title":"Mild\/asymptomatic COVID-19 in unvaccinated pregnant mothers impairs neonatal immune responses","volume":"8","author":"BM Doratt","year":"2023","journal-title":"JCI Insight"},{"issue":"2","key":"ppat.1011990.ref028","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41579-021-00610-y","article-title":"Infections at the maternal-fetal interface: an overview of pathogenesis and defence","volume":"20","author":"CJ Megli","year":"2022","journal-title":"Nat Rev Microbiol"},{"issue":"12","key":"ppat.1011990.ref029","doi-asserted-by":"crossref","first-page":"100456","DOI":"10.1016\/j.xcrm.2021.100456","article-title":"SARS-CoV-2 can infect and propagate in human placenta explants","volume":"2","author":"A Fahmi","year":"2021","journal-title":"Cell Reports Medicine"},{"issue":"11","key":"ppat.1011990.ref030","doi-asserted-by":"crossref","first-page":"2092","DOI":"10.1038\/s41379-020-0639-4","article-title":"SARS-CoV-2 can infect the placenta and is not associated with specific placental histopathology: a series of 19 placentas from COVID-19-positive mothers","volume":"33","author":"JL Hecht","year":"2020","journal-title":"Mod Pathol"},{"issue":"5","key":"ppat.1011990.ref031","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/j.medj.2021.04.016","article-title":"Maternal respiratory SARS-CoV-2 infection in pregnancy is associated with a robust inflammatory response at the maternal-fetal interface","volume":"2","author":"A Lu-Culligan","year":"2021","journal-title":"Med"},{"key":"ppat.1011990.ref032","doi-asserted-by":"crossref","first-page":"957224","DOI":"10.3389\/fimmu.2022.957224","article-title":"SARS-CoV-2 modulates virus receptor expression in placenta and can induce trophoblast fusion, inflammation and endothelial permeability","volume":"13","author":"C Agostinis","year":"2022","journal-title":"Front Immunol"},{"issue":"1","key":"ppat.1011990.ref033","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1093\/ajcp\/aqaa089","article-title":"Placental Pathology in COVID-19","volume":"154","author":"ED Shanes","year":"2020","journal-title":"Am J Clin Pathol"},{"issue":"4","key":"ppat.1011990.ref034","doi-asserted-by":"crossref","first-page":"382.e1","DOI":"10.1016\/j.ajog.2020.10.020","article-title":"Coronavirus disease 2019 infection and placental histopathology in women delivering at term","volume":"224","author":"ET Patberg","year":"2021","journal-title":"Am J Obstet Gynecol"},{"key":"ppat.1011990.ref035","article-title":"INFECTIONS IN PREGNANCY WITH COVID-19 AND OTHER RESPIRATORY RNA VIRUS DISEASES ARE RARELY, IF EVER, TRANSMITTED TO THE FETUS: EXPERIENCES WITH CORONAVIRUSES, HPIV, hMPV RSV, AND INFLUENZA","author":"DA Schwartz","year":"2020","journal-title":"Arch Pathol Lab Med"},{"issue":"31","key":"ppat.1011990.ref036","doi-asserted-by":"crossref","DOI":"10.1126\/sciimmunol.aat6114","article-title":"Immune responses at the maternal-fetal interface","volume":"4","author":"SE Ander","year":"2019","journal-title":"Sci Immunol"},{"key":"ppat.1011990.ref037","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1146\/annurev-immunol-032712-100003","article-title":"Immunology of the maternal-fetal interface","volume":"31","author":"A. Erlebacher","year":"2013","journal-title":"Annu Rev Immunol"},{"issue":"7731","key":"ppat.1011990.ref038","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1038\/s41586-018-0698-6","article-title":"Single-cell reconstruction of the early maternal-fetal interface in humans","volume":"563","author":"R Vento-Tormo","year":"2018","journal-title":"Nature"},{"issue":"11","key":"ppat.1011990.ref039","doi-asserted-by":"crossref","DOI":"10.3390\/v12111308","article-title":"Placental Pathology of COVID-19 with and without Fetal and Neonatal Infection: Trophoblast Necrosis and Chronic Histiocytic Intervillositis as Risk Factors for Transplacental Transmission of SARS-CoV-2","volume":"12","author":"DA Schwartz","year":"2020","journal-title":"Viruses"},{"issue":"11","key":"ppat.1011990.ref040","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.5858\/arpa.2021-0296-SA","article-title":"Hofbauer Cells and COVID-19 in Pregnancy","volume":"145","author":"DA Schwartz","year":"2021","journal-title":"Arch Pathol Lab Med"},{"issue":"11","key":"ppat.1011990.ref041","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.5858\/arpa.2021-0246-SA","article-title":"Defining Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Placentitis","volume":"145","author":"JC Watkins","year":"2021","journal-title":"Arch Pathol Lab Med"},{"issue":"5","key":"ppat.1011990.ref042","doi-asserted-by":"crossref","first-page":"517","DOI":"10.5858\/arpa.2020-0771-SA","article-title":"Chronic Histiocytic Intervillositis With Trophoblast Necrosis Is a Risk Factor Associated With Placental Infection From Coronavirus Disease 2019 (COVID-19) and Intrauterine Maternal-Fetal Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Transmission in Live-Born and Stillborn Infants","volume":"145","author":"DA Schwartz","year":"2021","journal-title":"Arch Pathol Lab 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Israel","year":"2021","journal-title":"Vaccines"},{"issue":"3","key":"ppat.1011990.ref046","doi-asserted-by":"crossref","first-page":"e13373","DOI":"10.1111\/aji.13373","article-title":"Chronic histiocytic intervillositis: A breakdown in immune tolerance comparable to allograft rejection?","volume":"85","author":"CA Brady","year":"2021","journal-title":"Am J Reprod Immunol"},{"issue":"5","key":"ppat.1011990.ref047","doi-asserted-by":"crossref","first-page":"104223","DOI":"10.1016\/j.isci.2022.104223","article-title":"Inflammatory responses in the placenta upon SARS-CoV-2 infection late in pregnancy","volume":"25","author":"LB Argueta","year":"2022","journal-title":"iScience"},{"issue":"6","key":"ppat.1011990.ref048","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1159\/000497416","article-title":"The Elusive Role of Placental Macrophages: The Hofbauer Cell","volume":"11","author":"MZ Zulu","year":"2019","journal-title":"J Innate 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