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Article

Lung Spatial Profiling Reveals a T Cell Signature in COPD Patients with Fatal SARS-CoV-2 Infection

by
Chen Xi Yang
1,2,
Michael Tomchaney
3,
Manuel F. Landecho
4,
Borja R. Zamacona
4,
Marta Marin Oto
4,
Javier Zulueta
5,
Joshua Malo
6,
Steve Knoper
6,
Marco Contoli
7,
Alberto Papi
7,
Dragoş M. Vasilescu
1,8,
Maor Sauler
9,
Christof Straub
10,
Cheryl Tan
10,
Fernando D. Martinez
3,
Deepta Bhattacharya
11,
Ivan O. Rosas
12,
Farrah Kheradmand
12,
Tillie-Louise Hackett
1,2,† and
Francesca Polverino
12,*,†
1
Centre for Heart and Lung Innovation, St. Paul’s Hospital, Vancouver, BC V6T 1Z4, Canada
2
Department of Anesthesiology, Pharmacology and Therapeutics, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
3
Asthma and Airway Disease Research Center, College of Medicine, University of Arizona College of Medicine, Tucson, AZ 85719, USA
4
Department of Internal Medicine, Clinica Universidad de Navarra, 31008 Pamplona, Spain
5
Mount-Sinai Hospital, New York, NY 10029, USA
6
Department of Surgery, University of Arizona, Tucson, AZ 85719, USA
7
Pulmonary Division, University of Ferrara, 44121 Ferrara, Italy
8
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
9
Department of Medicine, Yale University, New Haven, CT 06520, USA
10
Nanostring Technologies, Seattle, WA 98109, USA
11
Department of Immunobiology, University of Arizona, Tucson, AZ 85719, USA
12
Department of Medicine and Center for Translational Research, Baylor College of Medicine, Houston, TX 77030, USA
 
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*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Cells 2022, 11(12), 1864; https://doi.org/10.3390/cells11121864
Submission received: 1 May 2022 / Revised: 1 June 2022 / Accepted: 3 June 2022 / Published: 7 June 2022
(This article belongs to the Topic Proteins in Health and Diseases: New Knowledge and Practical Applications)
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Abstract

People with pre-existing lung diseases such as chronic obstructive pulmonary disease (COPD) are more likely to get very sick from SARS-CoV-2 disease 2019 (COVID-19). Still, an interrogation of the immune response to COVID-19 infection, spatially throughout the lung structure, is lacking in patients with COPD. For this study, we characterized the immune microenvironment of the lung parenchyma, airways, and vessels of never- and ever-smokers with or without COPD, all of whom died of COVID-19, using spatial transcriptomic and proteomic profiling. The parenchyma, airways, and vessels of COPD patients, compared to control lungs had (1) significant enrichment for lung-resident CD45RO+ memory CD4+ T cells; (2) downregulation of genes associated with T cell antigen priming and memory T cell differentiation; and (3) higher expression of proteins associated with SARS-CoV-2 entry and primary receptor ubiquitously across the ROIs and in particular the lung parenchyma, despite similar SARS-CoV-2 structural gene expression levels. In conclusion, the lung parenchyma, airways, and vessels of COPD patients have increased T-lymphocytes with a blunted memory CD4 T cell response and a more invasive SARS-CoV-2 infection pattern and may underlie the higher death toll observed with COVID-19.
Keywords: COVID-19; chronic obstructive pulmonary disease (COPD); T cells COVID-19; chronic obstructive pulmonary disease (COPD); T cells

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MDPI and ACS Style

Yang, C.X.; Tomchaney, M.; Landecho, M.F.; Zamacona, B.R.; Marin Oto, M.; Zulueta, J.; Malo, J.; Knoper, S.; Contoli, M.; Papi, A.; et al. Lung Spatial Profiling Reveals a T Cell Signature in COPD Patients with Fatal SARS-CoV-2 Infection. Cells 2022, 11, 1864. https://doi.org/10.3390/cells11121864

AMA Style

Yang CX, Tomchaney M, Landecho MF, Zamacona BR, Marin Oto M, Zulueta J, Malo J, Knoper S, Contoli M, Papi A, et al. Lung Spatial Profiling Reveals a T Cell Signature in COPD Patients with Fatal SARS-CoV-2 Infection. Cells. 2022; 11(12):1864. https://doi.org/10.3390/cells11121864

Chicago/Turabian Style

Yang, Chen Xi, Michael Tomchaney, Manuel F. Landecho, Borja R. Zamacona, Marta Marin Oto, Javier Zulueta, Joshua Malo, Steve Knoper, Marco Contoli, Alberto Papi, and et al. 2022. "Lung Spatial Profiling Reveals a T Cell Signature in COPD Patients with Fatal SARS-CoV-2 Infection" Cells 11, no. 12: 1864. https://doi.org/10.3390/cells11121864

APA Style

Yang, C. X., Tomchaney, M., Landecho, M. F., Zamacona, B. R., Marin Oto, M., Zulueta, J., Malo, J., Knoper, S., Contoli, M., Papi, A., Vasilescu, D. M., Sauler, M., Straub, C., Tan, C., Martinez, F. D., Bhattacharya, D., Rosas, I. O., Kheradmand, F., Hackett, T.-L., & Polverino, F. (2022). Lung Spatial Profiling Reveals a T Cell Signature in COPD Patients with Fatal SARS-CoV-2 Infection. Cells, 11(12), 1864. https://doi.org/10.3390/cells11121864

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