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[Preprint]. 2020 Aug 7:2020.08.05.238188. [Version 2] doi: 10.1101/2020.08.05.238188

Alveolitis in severe SARS-CoV-2 pneumonia is driven by self-sustaining circuits between infected alveolar macrophages and T cells

Rogan A Grant, Luisa Morales-Nebreda, Nikolay S Markov, Suchitra Swaminathan, Estefany R Guzman, Darryl A Abbott, Helen K Donnelly, Alvaro Donayre, Isaac A Goldberg, Zasu M Klug, Nicole Borkowski, Ziyan Lu, Hermon Kihshen, Yuliya Politanska, Lango Sichizya, Mengjia Kang, Ali Shilatifard, Chao Qi, A Christine Argento, Jacqueline M Kruser, Elizabeth S Malsin, Chiagozie O Pickens, Sean Smith, James M Walter, Anna E Pawlowski, Daniel Schneider, Prasanth Nannapaneni, Hiam Abdala-Valencia, Ankit Bharat, Cara J Gottardi, GR Scott Budinger, Alexander V Misharin, Benjamin D Singer, Richard G Wunderink; for The NU SCRIPT Study Investigators
PMCID: PMC8132268  PMID: 34013276

Abstract

Some patients infected with Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) develop severe pneumonia and the acute respiratory distress syndrome (ARDS) [1]. Distinct clinical features in these patients have led to speculation that the immune response to virus in the SARS-CoV-2-infected alveolus differs from other types of pneumonia [2]. We collected bronchoalveolar lavage fluid samples from 86 patients with SARS-CoV-2-induced respiratory failure and 252 patients with known or suspected pneumonia from other pathogens and subjected them to flow cytometry and bulk transcriptomic profiling. We performed single cell RNA-Seq in 5 bronchoalveolar lavage fluid samples collected from patients with severe COVID-19 within 48 hours of intubation. In the majority of patients with SARS-CoV-2 infection at the onset of mechanical ventilation, the alveolar space is persistently enriched in alveolar macrophages and T cells without neutrophilia. Bulk and single cell transcriptomic profiling suggest SARS-CoV-2 infects alveolar macrophages that respond by recruiting T cells. These T cells release interferon-gamma to induce inflammatory cytokine release from alveolar macrophages and further promote T cell recruitment. Our results suggest SARS-CoV-2 causes a slowly unfolding, spatially-limited alveolitis in which alveolar macrophages harboring SARS-CoV-2 transcripts and T cells form a positive feedback loop that drives progressive alveolar inflammation.

This manuscript is accompanied by an online resource: https://www.nupulmonary.org/covid-19/

One sentence summary

SARS-CoV-2-infected alveolar macrophages form positive feedback loops with T cells in patients with severe COVID-19.

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