The legacy of maternal SARS-CoV-2 infection on the immunology of the neonate.
Adult
Antibodies, Viral
/ immunology
COVID-19
/ diagnosis
Cytokines
/ blood
Female
Humans
Immunity, Innate
/ immunology
Immunoglobulin G
/ immunology
Infant, Newborn
Infant, Newborn, Diseases
/ diagnosis
Infectious Disease Transmission, Vertical
Killer Cells, Natural
/ immunology
Pregnancy
Pregnancy Complications, Infectious
/ immunology
Receptors, Antigen, T-Cell, gamma-delta
/ immunology
SARS-CoV-2
/ immunology
T-Lymphocytes
/ immunology
T-Lymphocytes, Regulatory
/ immunology
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
27
05
2021
accepted:
14
09
2021
pubmed:
8
10
2021
medline:
21
12
2021
entrez:
7
10
2021
Statut:
ppublish
Résumé
Despite extensive studies into severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the effect of maternal infection on the neonate is unclear. To investigate this, we characterized the immunology of neonates born to mothers with confirmed SARS-CoV-2 infection during pregnancy. Here we show that maternal SARS-CoV-2 infection affects the neonatal immune system. Despite similar proportions of B cells, CD4
Identifiants
pubmed: 34616036
doi: 10.1038/s41590-021-01049-2
pii: 10.1038/s41590-021-01049-2
doi:
Substances chimiques
Antibodies, Viral
0
Cytokines
0
Immunoglobulin G
0
Receptors, Antigen, T-Cell, gamma-delta
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1490-1502Subventions
Organisme : Action Medical Research (AMR)
ID : GN2790
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/N013700/1
Organisme : Tommy's
ID : Charity No. 1060508
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Sutton, D., Fuchs, K., D’Alton, M. & Goffman, D. Universal screening for SARS-CoV-2 in women admitted for delivery. N. Engl. J. Med. 382, 2163–2164 (2020).
pubmed: 32283004
doi: 10.1056/NEJMc2009316
Allotey, J. et al. Clinical manifestations, risk factors, and maternal and perinatal outcomes of coronavirus disease 2019 in pregnancy: living systematic review and meta-analysis. BMJ 370, m3320 (2020).
pubmed: 32873575
doi: 10.1136/bmj.m3320
Kadiwar, S. et al. Were pregnant women more affected by COVID-19 in the second wave of the pandemic? Lancet 397, 1539–1540 (2021).
pubmed: 33864751
pmcid: 8046416
doi: 10.1016/S0140-6736(21)00716-9
Martinez-Perez, O. et al. The association between SARS-CoV-2 infection and preterm delivery: a prospective study with a multivariable analysis. BMC Pregnancy Childbirth 21, 273 (2021).
pubmed: 33794829
pmcid: 8016158
doi: 10.1186/s12884-021-03742-4
Gale, C. et al. Characteristics and outcomes of neonatal SARS-CoV-2 infection in the UK: a prospective national cohort study using active surveillance. Lancet Child Adolesc. Health 5, 113–121 (2021).
pubmed: 33181124
doi: 10.1016/S2352-4642(20)30342-4
Salvatore, C. M. et al. Neonatal management and outcomes during the COVID-19 pandemic: an observation cohort study. Lancet Child Adolesc. Health 4, 721–727 (2020).
pubmed: 32711687
pmcid: 7377726
doi: 10.1016/S2352-4642(20)30235-2
Vivanti, A. J. et al. Transplacental transmission of SARS-CoV-2 infection. Nat. Commun. 11, 3572 (2020).
pubmed: 32665677
pmcid: 7360599
doi: 10.1038/s41467-020-17436-6
Fenizia, C. et al. Analysis of SARS-CoV-2 vertical transmission during pregnancy. Nat. Commun. 11, 5128 (2020).
pubmed: 33046695
pmcid: 7552412
doi: 10.1038/s41467-020-18933-4
Dong, L. et al. Possible vertical transmission of SARS-CoV-2 from an infected mother to her newborn. JAMA 323, 1846–1848 (2020).
pubmed: 32215581
pmcid: 7099527
Chen, G. et al. Immune response to COVID-19 during pregnancy. Front. Immunol. 12, 675476 (2021).
pubmed: 34012458
pmcid: 8126657
doi: 10.3389/fimmu.2021.675476
Kamdar, S. et al. Perinatal inflammation influences but does not arrest rapid immune development in preterm babies. Nat. Commun. 11, 1284 (2020).
pubmed: 32152273
pmcid: 7062833
doi: 10.1038/s41467-020-14923-8
Gabriel, B. et al. Analysis of the TCR repertoire in HIV-exposed but uninfected infants. Sci. Rep. 9, 11954 (2019).
pubmed: 31420576
pmcid: 6697688
doi: 10.1038/s41598-019-48434-4
Babik, J. M., Cohan, D., Monto, A., Hartigan-O’Connor, D. J. & McCune, J. M. The human fetal immune response to hepatitis C virus exposure in utero. J. Infect. Dis. 203, 196–206 (2011).
pubmed: 21288819
pmcid: 3071071
doi: 10.1093/infdis/jiq044
Gomez de Aguero, M. et al. The maternal microbiota drives early postnatal innate immune development. Science 351, 1296–1302 (2016).
pubmed: 26989247
doi: 10.1126/science.aad2571
Torow, N. & Hornef, M. W. The neonatal window of opportunity: setting the stage for life-long host-microbial interaction and immune homeostasis. J. Immunol. 198, 557–563 (2017).
pubmed: 28069750
doi: 10.4049/jimmunol.1601253
Liu, P. et al. The immunologic status of newborns born to SARS-CoV-2-infected mothers in Wuhan, China. J. Allergy Clin. Immunol. 146, 101–109 (2020).
pubmed: 32437740
pmcid: 7211641
doi: 10.1016/j.jaci.2020.04.038
Garcia-Flores, V. et al. Maternal–fetal immune responses in pregnant women infected with SARS-CoV-2. Preprint at https://doi.org/10.21203/rs.3.rs-362886/v1 (2021).
Pickering, S. et al. Comparative assessment of multiple COVID-19 serological technologies supports continued evaluation of point-of-care lateral flow assays in hospital and community healthcare settings. PLoS Pathog. 16, e1008817 (2020).
pubmed: 32970782
pmcid: 7514033
doi: 10.1371/journal.ppat.1008817
Lu-Culligan, A. et al. Maternal respiratory SARS-CoV-2 infection in pregnancy is associated with a robust inflammatory response at the maternal-fetal interface. Med (NY) 2, 591–610 (2021).
Laing, A. G. et al. A dynamic COVID-19 immune signature includes associations with poor prognosis. Nat. Med. 26, 1623–1635 (2020).
pubmed: 32807934
doi: 10.1038/s41591-020-1038-6
Arunachalam, P. S. et al. Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans. Science 369, 1210–1220 (2020).
pubmed: 32788292
pmcid: 7665312
doi: 10.1126/science.abc6261
Tornblom, S. A. et al. mRNA expression and localization of bNOS, eNOS and iNOS in human cervix at preterm and term labour. Reprod. Biol. Endocrinol. 3, 33 (2005).
pubmed: 16092967
pmcid: 1188074
doi: 10.1186/1477-7827-3-33
Flannery, D. D. et al. Assessment of maternal and neonatal cord blood SARS-CoV-2 antibodies and placental transfer ratios. JAMA Pediatr. 175, 594–600 (2021).
pubmed: 33512440
doi: 10.1001/jamapediatrics.2021.0038
Martinez, D. R. et al. Fc characteristics mediate selective placental transfer of IgG in HIV-infected women. Cell 178, 190–201 (2019).
pubmed: 31204101
pmcid: 6727200
doi: 10.1016/j.cell.2019.05.046
Goncalves, G. et al. Transplacental transfer of measles and total IgG. Epidemiol. Infect. 122, 273–279 (1999).
pubmed: 10355792
pmcid: 2809616
doi: 10.1017/S0950268899002046
Edlow, A. G. et al. Assessment of maternal and neonatal SARS-CoV-2 viral load, transplacental antibody transfer, and placental pathology in pregnancies during the COVID-19 pandemic. JAMA Netw. Open 3, e2030455 (2020).
pubmed: 33351086
pmcid: 7756241
doi: 10.1001/jamanetworkopen.2020.30455
Atyeo, C. et al. Compromised SARS-CoV-2-specific placental antibody transfer. Cell 184, 628–642 (2021).
pubmed: 33476549
pmcid: 7755577
doi: 10.1016/j.cell.2020.12.027
Bordt, E. A. et al. Sexually dimorphic placental responses to maternal SARS-CoV-2 infection. Preprint at https://doi.org/10.1101/2021.03.29.437516 (2021).
Beharier, O. et al. Efficient maternal to neonatal transfer of antibodies against SARS-CoV-2 and BNT162b2 mRNA COVID-19 vaccine. J. Clin. Invest. 131, e150319 (2021).
pmcid: 8245182
doi: 10.1172/JCI150319
Gleditsch, D. D. et al. Maternal inflammation modulates infant immune response patterns to viral lung challenge in a murine model. Pediatr. Res. 76, 33–40 (2014).
pubmed: 24727945
doi: 10.1038/pr.2014.57
Apostol, A. C., Jensen, K. D. C. & Beaudin, A. E. Training the fetal immune system through maternal inflammation—a layered hygiene hypothesis. Front. Immunol. 11, 123 (2020).
pubmed: 32117273
pmcid: 7026678
doi: 10.3389/fimmu.2020.00123
Bilbo, S. D. & Schwarz, J. M. Early-life programming of later-life brain and behavior: a critical role for the immune system. Front. Behav. Neurosci. 3, 14 (2009).
pubmed: 19738918
pmcid: 2737431
doi: 10.3389/neuro.08.014.2009
Acquah, J. K., Dahal, R. & Sloan, F. A. 1918 influenza pandemic: in utero exposure in the United States and long-term impact on hospitalizations. Am. J. Public Health 107, 1477–1483 (2017).
pubmed: 28727536
pmcid: 5551642
doi: 10.2105/AJPH.2017.303887
Lu, W. et al. Early immune responses and prognostic factors in children with COVID-19: a single-center retrospective analysis. BMC Pediatr. 21, 181 (2021).
pubmed: 33865340
pmcid: 8052550
doi: 10.1186/s12887-021-02561-y
Sherer, M. L. et al. Pregnancy alters interleukin-1 beta expression and antiviral antibody responses during severe acute respiratory syndrome coronavirus 2 infection. Am. J. Obstet. Gynecol. 225, 301.e1–301.e14 (2021).
doi: 10.1016/j.ajog.2021.03.028
Lohman-Payne, B. et al. HIV-exposed uninfected infants: elevated cord blood interleukin 8 (IL-8) is significantly associated with maternal HIV infection and systemic IL-8 in a Kenyan cohort. Clin. Transl. Med 7, 26 (2018).
pubmed: 30198049
pmcid: 6129453
doi: 10.1186/s40169-018-0206-5
Reuschel, E. et al. Perinatal gram-positive bacteria exposure elicits distinct cytokine responses in vitro. Int. J. Mol. Sci. 22, 332 (2020).
pmcid: 7795300
doi: 10.3390/ijms22010332
Jouan, Y. et al. Phenotypical and functional alteration of unconventional T cells in severe COVID-19 patients. J. Exp. Med. 217, e20200872 (2020).
pubmed: 32886755
pmcid: 7472174
doi: 10.1084/jem.20200872
Kuri-Cervantes, L. et al. Comprehensive mapping of immune perturbations associated with severe COVID-19. Sci. Immunol. 5, eabd7114 (2020).
pubmed: 32669287
pmcid: 7402634
doi: 10.1126/sciimmunol.abd7114
Gibbons, D. et al. Interleukin-8 (CXCL8) production is a signatory T cell effector function of human newborn infants. Nat. Med. 20, 1206–1210 (2014).
pubmed: 25242415
doi: 10.1038/nm.3670
White, G. P., Watt, P. M., Holt, B. J. & Holt, P. G. Differential patterns of methylation of the IFN-γ promoter at CpG and non-CpG sites underlie differences in IFN-γ gene expression between human neonatal and adult CD45RO
pubmed: 11884451
doi: 10.4049/jimmunol.168.6.2820
Tang, W. Y. et al. Maternal exposure to polycyclic aromatic hydrocarbons and 5′-CpG methylation of interferon-γ in cord white blood cells. Environ. Health Perspect. 120, 1195–1200 (2012).
pubmed: 22562770
pmcid: 3440069
doi: 10.1289/ehp.1103744
van Esch, B. et al. The impact of milk and its components on epigenetic programming of immune function in early life and beyond: implications for allergy and asthma. Front Immunol. 11, 2141 (2020).
pubmed: 33193294
pmcid: 7641638
doi: 10.3389/fimmu.2020.02141
Hong, M. et al. Trained immunity in newborn infants of HBV-infected mothers. Nat. Commun. 6, 6588 (2015).
pubmed: 25807344
doi: 10.1038/ncomms7588
Garcia-Knight, M. A. et al. Altered memory T cell responses to Bacillus Calmette-Guerin and tetanus toxoid vaccination and altered cytokine responses to polyclonal stimulation in HIV-exposed uninfected Kenyan infants. PLoS ONE 10, e0143043 (2015).
pubmed: 26569505
pmcid: 4646342
doi: 10.1371/journal.pone.0143043
Mishra, A. et al. Microbial exposure during early human development primes fetal immune cells. Cell 184, 3394–3409 (2021).
pubmed: 34077752
pmcid: 8240556
doi: 10.1016/j.cell.2021.04.039
Fajnzylber, J. et al. SARS-CoV-2 viral load is associated with increased disease severity and mortality. Nat. Commun. 11, 5493 (2020).
pubmed: 33127906
pmcid: 7603483
doi: 10.1038/s41467-020-19057-5
Kappanayil, M. et al. Multisystem inflammatory syndrome in a neonate, temporally associated with prenatal exposure to SARS-CoV-2: a case report. Lancet Child Adolesc. Health 5, 304–308 (2021).
pubmed: 33675696
pmcid: 7929789
doi: 10.1016/S2352-4642(21)00055-9
Seow, J. et al. Longitudinal observation and decline of neutralizing antibody responses in the three months following SARS-CoV-2 infection in humans. Nat. Microbiol. 5, 1598–1607 (2020).
pubmed: 33106674
pmcid: 7610833
doi: 10.1038/s41564-020-00813-8
Monin, L. et al. Safety and immunogenicity of one versus two doses of the COVID-19 vaccine BNT162b2 for patients with cancer: interim analysis of a prospective observational study. Lancet Oncol. 22, 765–778 (2021).
pubmed: 33930323
pmcid: 8078907
doi: 10.1016/S1470-2045(21)00213-8