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Longitudinal single-cell epitope and RNA-sequencing reveals the immunological impact of type 1 interferon autoantibodies in critical COVID-19

van der Wijst, M. G. P.; Vazquez, S. E.; Hartoularos, G. C.; Bastard, P.; Grant, T.; Bueno, R.; Lee, D. S.; Greenland, J. R.; Sun, Y.; Perez, R.; Ogorodnikov, A.; Ward, A.; Mann, S. A.; Lynch, K. L.; Yun, C.; Havlir, D. V.; Chamie, G.; Marquez, C.; Greenhouse, B.; Lionakis, M. S.; Norris, P. J.; Dumont, L. J.; Kelly, K.; Zhang, P.; Zhang, Q.; Gervais, A.; Le Voyer, T.; Whatley, A.; Si, Y.; Byrne, A.; Combes, A. J.; Arkal, A.; Song, Y. S.; Fragiadakis, G. K.; UCSF COMET consortium, ; Kangelaris, K.; Calfee, C. S.; Erle, D. J.; Hendrickson, C.; Krummel, M. F.; Woodruff, P. G.; Langelier, C. R.;

2021-03-10 immunology
10.1101/2021.03.09.434529 bioRxiv
Show abstract

Type I interferon (IFN-I) neutralizing autoantibodies have been found in some critical COVID-19 patients; however, their prevalence and longitudinal dynamics across the disease severity scale, and functional effects on circulating leukocytes remain unknown. Here, in 284 COVID-19 patients, we found IFN-I autoantibodies in 19% of critical, 6% of severe and none of the moderate cases. Longitudinal profiling of over 600,000 peripheral blood mononuclear cells using multiplexed single-cell epitope and transcriptome sequencing from 54 COVID-19 patients, 15 non-COVID-19 patients and 11 non-hospitalized healthy controls, revealed a lack of IFN-I stimulated gene (ISG-I) response in myeloid cells from critical cases, including those producing anti-IFN-I autoantibodies. Moreover, surface protein analysis showed an inverse correlation of the inhibitory receptor LAIR-1 with ISG-I expression response early in the disease course. This aberrant ISG-I response in critical patients with and without IFN-I autoantibodies, supports a unifying model for disease pathogenesis involving ISG-I suppression via convergent mechanisms.

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