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Multi-omic spatial profiling reveals the unique virus-driven immune landscape of COVID-19 placentitis

Pugh, M.; Fennel, E.; Leahy, C. I.; Perry, T.; Hargitai, B.; Marton, T.; Hunter, K. J.; Halford, G.; Yilmaz, H. O.; Stamataki, Z.; Reynolds, G.; Hill, H. J.; Willcox, B. E.; Steven, N. M.; Thornton, C. A.; Dojcinov, S.; Culhane, A.; Murray, P. G.; Taylor, G. S.

2022-11-14 immunology
10.1101/2022.11.14.516398 bioRxiv
Show abstract

COVID-19 placentitis, a rare complication of maternal SARS-CoV-2 infection, only shows detectable virus in the placenta of a subset of cases. We provide a deep multi-omic spatial characterisation of placentitis from obstetrically complicated maternal COVID-19 infection. We found that SARS-CoV-2 infected placentas have a distinct transcriptional and immunopathological signature. This signature overlaps with virus-negative cases supporting a common viral aetiology. An inverse correlation between viral load and disease duration suggests viral clearance over time. Quantitative spatial analyses revealed a unique microenvironment surrounding virus-infected trophoblasts characterised by PDL1-expressing macrophages, T-cell exclusion, and interferon blunting. In contrast to uninfected mothers, ACE2 was localised to the maternal side of the placental trophoblast layer of almost all mothers with placental SARS-CoV-2 infection, which may explain variable susceptibility to placental infection. Our results demonstrate a pivotal role for direct placental SARS-CoV-2 infection in driving the unique immunopathology of COVID-19 placentitis. Graphical Abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

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