Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection
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Abstract
The relationship of SARS-CoV-2 pulmonary infection and severity of disease is not fully understood. Here we show analysis of autopsy specimens from 24 patients who succumbed to SARS-CoV-2 infection using a combination of different RNA and protein analytical platforms to characterize inter-patient and intra-patient heterogeneity of pulmonary virus infection. There is a spectrum of high and low virus cases associated with duration of disease. High viral cases have high activation of interferon pathway genes and a predominant M1-like macrophage infiltrate. Low viral cases are more heterogeneous likely reflecting inherent patient differences in the evolution of host response, but there is consistent indication of pulmonary epithelial cell recovery based on napsin A immunohistochemistry and RNA expression of surfactant and mucin genes. Using a digital spatial profiling platform, we find the virus corresponds to distinct spatial expression of interferon response genes demonstrating the intra-pulmonary heterogeneity of SARS-CoV-2 infection.
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SARS-CoV-2 mRNA is detectable in many but not all VIS-positive samples, suggesting that VIS can persist after the initial infection.
“SARS-CoV-2 mRNA was detectable by in situ hybridization in many but not all VIS-positive samples, suggesting that VIS may persist beyond the initial infection28,61,62”
From COVID-19 and cellular senescence (2023) · cites this paper as [61]
Lungs from patients with severe COVID-19 show much higher infiltration by CD86+ macrophages and stronger SASP-reminiscent cytokine expression than controls.
“lungs from patients with severe COVID-19 exhibited much higher levels of infiltration by CD86+ macrophages and much stronger SASP-reminiscent cytokine expression compared to lungs from patients who died without notable signs of a respiratory infection and who were not infected with SARS-CoV-2 (refs.28,61).”
From COVID-19 and cellular senescence (2023) · cites this paper as [61]
In COVID-19, ARDS appears as diffuse alveolar damage on autopsy and is linked to lung immune cell infiltration, cytokine storm and tissue damage.
“During COVID-19, ARDS manifests as a diffuse alveolar damage pattern seen on autopsies of COVID-19 patients, and is linked to a combination of lung immune cell infiltration, cytokine storm, and tissue damage from secreted proteases, reactive oxygen species (ROS), and viral killing 49,50.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [50]
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- Authors
- Desai, N., Neyaz, A., Szabolcs, A., Shih, A. R., Chen, J. H., Thapar, V., Nieman, L. T., Solovyov, A., Mehta, A., Lieb, D. J., Kulkarni, A. S., Jaicks, C., Xu, K. H., Raabe, M. J., Pinto, C. J., Juric, D., Chebib, I., Colvin, R. B., Kim, A. Y., Monroe, R., Warren, S. E., Danaher, P., Reeves, J. W., Gong, J., Rueckert, E. H., Greenbaum, B. D., Hacohen, N., Lagana, S. M., Rivera, M. N., Sholl, L. M., Stone, J. R., Ting, D. T., & Deshpande, V.
- Affiliations
- Massachusetts General Hospital (US)
- Memorial Sloan Kettering Cancer Center (US)
- Broad Institute (US)
- Advanced Cell Diagnostics (United States) (US)
- Nanostring Technologies (United States) (US)
- Columbia University Irving Medical Center (US)
- Brigham and Women's Hospital (US)
- Harvard University (US)
- Corresponding author
- Stone, James R.
- Ting, David T.
- Deshpande, Vikram
- ORCID
- Desai, Niyati
- Neyaz, Azfar
- Szabolcs, Annamaria
- Shih, Angela R.
- Chen, Jonathan H.
- Thapar, Vishal
- Nieman, Linda T.
- Solovyov, Alexander
- Mehta, Arnav
- Lieb, David J.
- Kulkarni, Anupriya S.
- Jaicks, Christopher
- Xu, Katherine H.
- Raabe, Michael J.
- Juric, Dejan
- Chebib, Ivan
- Colvin, Robert B.
- Kim, Arthur Y.
- Warren, Sarah E.
- Danaher, Patrick
- Reeves, Jason W.
- Gong, Jingjing
- Greenbaum, Benjamin D.
- Hacohen, Nir
- Lagana, Stephen M.
- Rivera, Miguel N.
- Sholl, Lynette M.
- Stone, James R.
- Ting, David T.
- Deshpande, Vikram
- Venue
- Nature Communications
- Published
- 2020-12-09
- Volume
- 11
- Issue
- 1
- Pages
- 6319-6319
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7725958
- OpenAlex
- W3112860625
- Cited by
- 245
- References
- 51
- Citations by year
- 2026: 17 · 2025: 9 · 2024: 27 · 2023: 45 · 2022: 70 · 2021: 70 · 2020: 7
- FWCI
- 6.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- medRxiv (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Health & Human Services | NIH | National Cancer Institute (R01CA240924, 7R01AI081848-04)
- ACD/Biotechne, The MGH Research Scholars Program, The Pershing Square Sohn Prize—Mark Foundation Fellow, The V Foundation, SU2C-Lustgarten
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Keywords
- SARS-CoV-2, COVID-19 pandemic, pulmonary infection, interferon pathway, M1 macrophages, spatial transcriptomics, digital spatial profiling, Napsin A, mucin genes, disease severity, autopsy specimens
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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