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Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection

Author

Listed:
  • Niyati Desai

    (Massachusetts General Hospital Cancer Center)

  • Azfar Neyaz

    (Massachusetts General Hospital Cancer Center)

  • Annamaria Szabolcs

    (Massachusetts General Hospital Cancer Center)

  • Angela R. Shih

    (Massachusetts General Hospital)

  • Jonathan H. Chen

    (Massachusetts General Hospital Cancer Center
    Massachusetts General Hospital)

  • Vishal Thapar

    (Massachusetts General Hospital Cancer Center)

  • Linda T. Nieman

    (Massachusetts General Hospital Cancer Center)

  • Alexander Solovyov

    (Memorial Sloan Kettering Cancer Center)

  • Arnav Mehta

    (Massachusetts General Hospital Cancer Center
    The Broad Institute)

  • David J. Lieb

    (The Broad Institute)

  • Anupriya S. Kulkarni

    (Massachusetts General Hospital Cancer Center)

  • Christopher Jaicks

    (Massachusetts General Hospital Cancer Center)

  • Katherine H. Xu

    (Massachusetts General Hospital Cancer Center)

  • Michael J. Raabe

    (Massachusetts General Hospital Cancer Center)

  • Christopher J. Pinto

    (Massachusetts General Hospital Cancer Center)

  • Dejan Juric

    (Massachusetts General Hospital Cancer Center)

  • Ivan Chebib

    (Massachusetts General Hospital)

  • Robert B. Colvin

    (Massachusetts General Hospital)

  • Arthur Y. Kim

    (Massachusetts General Hospital)

  • Robert Monroe

    (Advanced Cell Diagnostics, a Bio-Techne Brand)

  • Sarah E. Warren

    (NanoString Inc.)

  • Patrick Danaher

    (NanoString Inc.)

  • Jason W. Reeves

    (NanoString Inc.)

  • Jingjing Gong

    (NanoString Inc.)

  • Erroll H. Rueckert

    (NanoString Inc.)

  • Benjamin D. Greenbaum

    (Memorial Sloan Kettering Cancer Center)

  • Nir Hacohen

    (Massachusetts General Hospital Cancer Center
    The Broad Institute
    Massachusetts General Hospital)

  • Stephen M. Lagana

    (Columbia University Irving Medical Center)

  • Miguel N. Rivera

    (Massachusetts General Hospital Cancer Center
    Massachusetts General Hospital
    The Broad Institute)

  • Lynette M. Sholl

    (Brigham and Woman’s Hospital)

  • James R. Stone

    (Massachusetts General Hospital)

  • David T. Ting

    (Massachusetts General Hospital Cancer Center
    Massachusetts General Hospital)

  • Vikram Deshpande

    (Massachusetts General Hospital Cancer Center
    Massachusetts General Hospital)

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.

Suggested Citation

  • Niyati Desai & Azfar Neyaz & Annamaria Szabolcs & Angela R. Shih & Jonathan H. Chen & Vishal Thapar & Linda T. Nieman & Alexander Solovyov & Arnav Mehta & David J. Lieb & Anupriya S. Kulkarni & Christ, 2020. "Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-20139-7
    DOI: 10.1038/s41467-020-20139-7
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    Cited by:

    1. Emily E. Bendall & Amy P. Callear & Amy Getz & Kendra Goforth & Drew Edwards & Arnold S. Monto & Emily T. Martin & Adam S. Lauring, 2023. "Rapid transmission and tight bottlenecks constrain the evolution of highly transmissible SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    2. Matthew J. Cummings & Barnabas Bakamutumaho & Julius J. Lutwama & Nicholas Owor & Xiaoyu Che & Maider Astorkia & Thomas S. Postler & John Kayiwa & Jocelyn Kiconco & Moses Muwanga & Christopher Nsereko, 2024. "COVID-19 immune signatures in Uganda persist in HIV co-infection and diverge by pandemic phase," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Jolien Van Cleemput & Willem van Snippenberg & Laurens Lambrechts & Amélie Dendooven & Valentino D’Onofrio & Liesbeth Couck & Wim Trypsteen & Jan Vanrusselt & Sebastiaan Theuns & Nick Vereecke & Thier, 2021. "Organ-specific genome diversity of replication-competent SARS-CoV-2," Nature Communications, Nature, vol. 12(1), pages 1-11, December.

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