Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19
Peter A. Szabo, Pranay Dogra, Joshua I. Gray, Steven B. Wells, Thomas J. Connors, Stuart P. Weisberg, Izabela Krupska, Rei Matsumoto, Maya M.L. Poon, Emma Idzikowski, Sinead E. Morris, Chloé Pasin, Andrew J. Yates, Amy Ku, Michael Chait, Julia Davis-Porada, Xinzheng V. Guo, Jing Zhou, Matthew Steinle, Sean Mackay, Anjali Saqi, Matthew R. Baldwin, Peter A. Sims, Donna L. Farber
Abstract
Immune response dynamics in coronavirus disease 2019 (COVID-19) and their severe manifestations have largely been studied in circulation. Here, we examined the relationship between immune processes in the respiratory tract and circulation through longitudinal phenotypic, transcriptomic, and cytokine profiling of paired airway and blood samples from patients with severe COVID-19 relative to heathy controls. In COVID-19 airways, T cells exhibited activated, tissue-resident, and protective profiles; higher T cell frequencies correlated with survival and younger age. Myeloid cells in COVID-19 airways featured hyperinflammatory signatures, and higher frequencies of these cells correlated with mortality and older age. In COVID-19 blood, aberrant CD163+ monocytes predominated over conventional monocytes, and were found in corresponding airway samples and in damaged alveoli. High levels of myeloid chemoattractants in airways suggest recruitment of these cells through a CCL2-CCR2 chemokine axis. Our findings provide insights into immune processes driving COVID-19 lung pathology with therapeutic implications for targeting inflammation in the respiratory tract.
Datasets
1. 49 years old male - Fresh PBMCs (2 days post-intubation)
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Preview
2. 49 years old male - Airway Wash (2 days post-intubation)
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3. 49 years old male - Fresh PBMCs (3 days post-intubation)
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4. 66 years old female - Fresh PBMCs (2 days post-intubation)
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5. 66 years old female - Airway Wash (2 days post-intubation)
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6. 74 years old female - Airway Wash (3 days post-intubation)
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Preview
7. 66 years old female - Fresh PBMCs (4 days post-intubation)
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8. 74 years old female - Fresh PBMCs (3 days post-intubation)
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9. 74 years old female - Fresh PBMCs (4 days post-intubation)
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Preview
10. 74 years old female - Fresh PBMCs (7 days post-intubation)
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Preview
11. 66 years old female - Fresh PBMCs (3 days post-intubation)
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Preview
12. 74 years old female - Fresh PBMCs (8 days post-intubation)
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Preview
13. 74 years old female - Airway Wash (1 day post-intubation)
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Preview
14. 49 years old male - Fresh PBMCs (1 day post-intubation)
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Preview
15. 66 years old female - Airway Wash (7 days post-intubation)
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Preview
16. 82 years old female - Fresh PBMCs (1 day post-intubation)
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development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
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development_stage
COV0274232 cells
Tcell/NK3580 cells
myeloid269 cells
Bcell261 cells
unknown69 cells
multiplet36 cells
plasma16 cells
platelet1 cells
EFO:00099224232 cells
CL:00008143580 cells
CL:0000763269 cells
CL:0000236261 cells
unknown105 cells
CL:000078616 cells
CL:00002331 cells
HsapDv:00002084232 cells
MONDO:01000964232 cells
unknown4232 cells
NCBITaxon:96064232 cells
PATO:00003834232 cells
UBERON:00001784232 cells
cell4232 cells
tissue4232 cells
mature NK T cell3580 cells
myeloid cell269 cells
B cell261 cells
unknown105 cells
plasma cell16 cells
platelet1 cells
10x 3' v34232 cells
COVID-194232 cells
Homo sapiens4232 cells
female4232 cells
blood4232 cells
unknown4232 cells
82-year-old human stage4232 cells
Preview
17. 74 years old female - Airway Wash (4 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0264147 cells
myeloid2070 cells
Tcell/NK1221 cells
Bcell498 cells
platelet204 cells
epithelial80 cells
multiplet47 cells
mast20 cells
unknown3 cells
RBC2 cells
neutrophil1 cells
ionocyte1 cells
EFO:00099224147 cells
CL:00007632070 cells
CL:00008141221 cells
CL:0000236498 cells
CL:0000233204 cells
CL:000006680 cells
unknown50 cells
CL:000009720 cells
CL:00002322 cells
CL:00050061 cells
CL:00007751 cells
HsapDv:00001684147 cells
MONDO:01000964147 cells
unknown4147 cells
NCBITaxon:96064147 cells
PATO:00003834147 cells
UBERON:00010054147 cells
cell4147 cells
tissue4147 cells
myeloid cell2070 cells
mature NK T cell1221 cells
B cell498 cells
platelet204 cells
epithelial cell80 cells
unknown50 cells
mast cell20 cells
erythrocyte2 cells
neutrophil1 cells
ionocyte1 cells
10x 3' v34147 cells
COVID-194147 cells
Homo sapiens4147 cells
female4147 cells
respiratory airway4147 cells
unknown4147 cells
74-year-old human stage4147 cells
Preview
18. 66 years old female - Fresh PBMCs (7 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0283726 cells
Tcell/NK1859 cells
myeloid924 cells
plasma565 cells
Bcell124 cells
multiplet96 cells
unknown81 cells
platelet64 cells
dendritic12 cells
neutrophil1 cells
EFO:00099223726 cells
CL:00008141859 cells
CL:0000763924 cells
CL:0000786565 cells
unknown177 cells
CL:0000236124 cells
CL:000023364 cells
CL:000045112 cells
CL:00007751 cells
HsapDv:00001603726 cells
MONDO:01000963726 cells
unknown3726 cells
NCBITaxon:96063726 cells
PATO:00003833726 cells
UBERON:00001783726 cells
cell3726 cells
tissue3726 cells
mature NK T cell1859 cells
myeloid cell924 cells
plasma cell565 cells
unknown177 cells
B cell124 cells
platelet64 cells
dendritic cell12 cells
neutrophil1 cells
10x 3' v33726 cells
COVID-193726 cells
Homo sapiens3726 cells
female3726 cells
blood3726 cells
unknown3726 cells
66-year-old human stage3726 cells
Preview
19. 66 years old female - Airway Wash (3 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0283434 cells
myeloid2421 cells
neutrophil427 cells
multiplet335 cells
Tcell/NK166 cells
epithelial43 cells
Bcell30 cells
RBC9 cells
unknown3 cells
EFO:00099223434 cells
CL:00007632421 cells
CL:0000775427 cells
unknown338 cells
CL:0000814166 cells
CL:000006643 cells
CL:000023630 cells
CL:00002329 cells
HsapDv:00001603434 cells
MONDO:01000963434 cells
unknown3434 cells
NCBITaxon:96063434 cells
PATO:00003833434 cells
UBERON:00010053434 cells
cell3434 cells
tissue3434 cells
myeloid cell2421 cells
neutrophil427 cells
unknown338 cells
mature NK T cell166 cells
epithelial cell43 cells
B cell30 cells
erythrocyte9 cells
10x 3' v33434 cells
COVID-193434 cells
Homo sapiens3434 cells
female3434 cells
respiratory airway3434 cells
unknown3434 cells
66-year-old human stage3434 cells
Preview
20. 74 years old female - Airway Wash (6 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0262834 cells
neutrophil1250 cells
epithelial982 cells
myeloid503 cells
Tcell/NK75 cells
multiplet16 cells
unknown3 cells
Bcell3 cells
ionocyte2 cells
EFO:00099222834 cells
CL:00007751250 cells
CL:0000066982 cells
CL:0000763503 cells
CL:000081475 cells
unknown19 cells
CL:00002363 cells
CL:00050062 cells
HsapDv:00001682834 cells
MONDO:01000962834 cells
unknown2834 cells
NCBITaxon:96062834 cells
PATO:00003832834 cells
UBERON:00010052834 cells
cell2834 cells
tissue2834 cells
neutrophil1250 cells
epithelial cell982 cells
myeloid cell503 cells
mature NK T cell75 cells
unknown19 cells
B cell3 cells
ionocyte2 cells
10x 3' v32834 cells
COVID-192834 cells
Homo sapiens2834 cells
female2834 cells
respiratory airway2834 cells
unknown2834 cells
74-year-old human stage2834 cells
Preview
21. 66 years old female - Airway Wash (4 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0282598 cells
myeloid2388 cells
neutrophil123 cells
Tcell/NK44 cells
multiplet18 cells
epithelial12 cells
Bcell7 cells
unknown4 cells
RBC2 cells
EFO:00099222598 cells
CL:00007632388 cells
CL:0000775123 cells
CL:000081444 cells
unknown22 cells
CL:000006612 cells
CL:00002367 cells
CL:00002322 cells
HsapDv:00001602598 cells
MONDO:01000962598 cells
unknown2598 cells
NCBITaxon:96062598 cells
PATO:00003832598 cells
UBERON:00010052598 cells
cell2598 cells
tissue2598 cells
myeloid cell2388 cells
neutrophil123 cells
mature NK T cell44 cells
unknown22 cells
epithelial cell12 cells
B cell7 cells
erythrocyte2 cells
10x 3' v32598 cells
COVID-192598 cells
Homo sapiens2598 cells
female2598 cells
respiratory airway2598 cells
unknown2598 cells
66-year-old human stage2598 cells
Preview
22. 49 years old male - Airway Wash (1 day post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0222489 cells
myeloid1407 cells
epithelial571 cells
Tcell/NK233 cells
neutrophil145 cells
mast105 cells
Bcell13 cells
multiplet10 cells
unknown3 cells
ionocyte2 cells
EFO:00099222489 cells
CL:00007631407 cells
CL:0000066571 cells
CL:0000814233 cells
CL:0000775145 cells
CL:0000097105 cells
unknown13 cells
CL:000023613 cells
CL:00050062 cells
HsapDv:00001432489 cells
MONDO:01000962489 cells
unknown2489 cells
NCBITaxon:96062489 cells
PATO:00003842489 cells
UBERON:00010052489 cells
cell2489 cells
tissue2489 cells
myeloid cell1407 cells
epithelial cell571 cells
mature NK T cell233 cells
neutrophil145 cells
mast cell105 cells
unknown13 cells
B cell13 cells
ionocyte2 cells
10x 3' v32489 cells
COVID-192489 cells
Homo sapiens2489 cells
male2489 cells
respiratory airway2489 cells
unknown2489 cells
49-year-old human stage2489 cells
Preview
23. 49 years old male - Airway Wash (3 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0222487 cells
myeloid1083 cells
epithelial479 cells
Tcell/NK439 cells
multiplet357 cells
unknown95 cells
Bcell14 cells
mast11 cells
neutrophil4 cells
RBC4 cells
ionocyte1 cells
EFO:00099222487 cells
CL:00007631083 cells
CL:0000066479 cells
unknown452 cells
CL:0000814439 cells
CL:000023614 cells
CL:000009711 cells
CL:00007754 cells
CL:00002324 cells
CL:00050061 cells
HsapDv:00001432487 cells
MONDO:01000962487 cells
unknown2487 cells
NCBITaxon:96062487 cells
PATO:00003842487 cells
UBERON:00010052487 cells
cell2487 cells
tissue2487 cells
myeloid cell1083 cells
epithelial cell479 cells
unknown452 cells
mature NK T cell439 cells
B cell14 cells
mast cell11 cells
neutrophil4 cells
erythrocyte4 cells
ionocyte1 cells
10x 3' v32487 cells
COVID-192487 cells
Homo sapiens2487 cells
male2487 cells
respiratory airway2487 cells
unknown2487 cells
49-year-old human stage2487 cells
Preview
24. 74 years old female - Airway Wash (8 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0262065 cells
myeloid1405 cells
Tcell/NK349 cells
epithelial207 cells
multiplet41 cells
neutrophil29 cells
mast11 cells
platelet8 cells
Bcell7 cells
unknown4 cells
RBC4 cells
EFO:00099222065 cells
CL:00007631405 cells
CL:0000814349 cells
CL:0000066207 cells
unknown45 cells
CL:000077529 cells
CL:000009711 cells
CL:00002338 cells
CL:00002367 cells
CL:00002324 cells
HsapDv:00001682065 cells
MONDO:01000962065 cells
unknown2065 cells
NCBITaxon:96062065 cells
PATO:00003832065 cells
UBERON:00010052065 cells
cell2065 cells
tissue2065 cells
myeloid cell1405 cells
mature NK T cell349 cells
epithelial cell207 cells
unknown45 cells
neutrophil29 cells
mast cell11 cells
platelet8 cells
B cell7 cells
erythrocyte4 cells
10x 3' v32065 cells
COVID-192065 cells
Homo sapiens2065 cells
female2065 cells
respiratory airway2065 cells
unknown2065 cells
74-year-old human stage2065 cells
Preview
25. 74 years old female - Airway Wash (5 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0261324 cells
myeloid965 cells
Tcell/NK136 cells
epithelial94 cells
unknown57 cells
neutrophil31 cells
multiplet28 cells
mast11 cells
plasma1 cells
Bcell1 cells
EFO:00099221324 cells
CL:0000763965 cells
CL:0000814136 cells
CL:000006694 cells
unknown85 cells
CL:000077531 cells
CL:000009711 cells
CL:00007861 cells
CL:00002361 cells
HsapDv:00001681324 cells
MONDO:01000961324 cells
unknown1324 cells
NCBITaxon:96061324 cells
PATO:00003831324 cells
UBERON:00010051324 cells
cell1324 cells
tissue1324 cells
myeloid cell965 cells
mature NK T cell136 cells
epithelial cell94 cells
unknown85 cells
neutrophil31 cells
mast cell11 cells
plasma cell1 cells
B cell1 cells
10x 3' v31324 cells
COVID-191324 cells
Homo sapiens1324 cells
female1324 cells
respiratory airway1324 cells
unknown1324 cells
74-year-old human stage1324 cells
Preview
26. 82 years old female - Airway Wash (1 day post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV0271074 cells
epithelial358 cells
myeloid353 cells
Tcell/NK239 cells
neutrophil50 cells
Bcell22 cells
RBC21 cells
multiplet15 cells
unknown14 cells
mast2 cells
EFO:00099221074 cells
CL:0000066358 cells
CL:0000763353 cells
CL:0000814239 cells
CL:000077550 cells
unknown29 cells
CL:000023622 cells
CL:000023221 cells
CL:00000972 cells
HsapDv:00002081074 cells
MONDO:01000961074 cells
unknown1074 cells
NCBITaxon:96061074 cells
PATO:00003831074 cells
UBERON:00010051074 cells
cell1074 cells
tissue1074 cells
epithelial cell358 cells
myeloid cell353 cells
mature NK T cell239 cells
neutrophil50 cells
unknown29 cells
B cell22 cells
erythrocyte21 cells
mast cell2 cells
10x 3' v31074 cells
COVID-191074 cells
Homo sapiens1074 cells
female1074 cells
respiratory airway1074 cells
unknown1074 cells
82-year-old human stage1074 cells
Preview
27. 74 years old female - Airway Wash (7 days post-intubation)
Metadata
donor_id
author_cell_type
assay_ontology_term_id
cell_type_ontology_term_id
development_stage_ontology_term_id
disease_ontology_term_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sex_ontology_term_id
tissue_ontology_term_id
suspension_type
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
COV026810 cells
epithelial449 cells
myeloid228 cells
Tcell/NK67 cells
neutrophil30 cells
multiplet29 cells
Bcell4 cells
unknown1 cells
ionocyte1 cells
RBC1 cells
EFO:0009922810 cells
CL:0000066449 cells
CL:0000763228 cells
CL:000081467 cells
unknown30 cells
CL:000077530 cells
CL:00002364 cells
CL:00050061 cells
CL:00002321 cells
HsapDv:0000168810 cells
MONDO:0100096810 cells
unknown810 cells
NCBITaxon:9606810 cells
PATO:0000383810 cells
UBERON:0001005810 cells
cell810 cells
tissue810 cells
epithelial cell449 cells
myeloid cell228 cells
mature NK T cell67 cells
unknown30 cells
neutrophil30 cells
B cell4 cells
ionocyte1 cells
erythrocyte1 cells
10x 3' v3810 cells
COVID-19810 cells
Homo sapiens810 cells
female810 cells
respiratory airway810 cells
unknown810 cells
74-year-old human stage810 cells
Preview
Analyze this study
Source data
https://cellxgene.cziscience.com/collections/29f92179-ca10-4309-a32b-d383d80347c1
Alias names
PMID33765436, PMC7951561
Cite this study
Szabo, P.A., Dogra, P., Gray, J.I., Wells, S.B., Connors, T.J., Weisberg, S.P., Krupska, I., Matsumoto, R., Poon, M.M., Idzikowski, E. and Morris, S.E., 2021. Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19. Immunity, 54(4), pp.797-814. https://doi.org/10.1016/j.immuni.2021.03.005