NK Cell–Monocyte Cross-talk Underlies NK Cell Activation in Severe COVID-19
NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell–cell interactions in modula...
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| Published in | The Journal of immunology (1950) Vol. 212; no. 11; pp. 1693 - 1705 |
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| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
AAI
01.06.2024
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0022-1767 1550-6606 1550-6606 |
| DOI | 10.4049/jimmunol.2300731 |
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| Abstract | NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell–cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell–cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16− NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19. |
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| AbstractList | NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell-cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell-cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16- NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19.NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell-cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell-cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16- NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19. scRNA-seq analysis predicts interactions between NK cells and monocytes in COVID-19. Monocytes from COVID-19 donors induce activation and proliferation in healthy NK cells. CD56 bright NK cells are activated by monocyte-derived soluble proinflammatory factors. NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell–cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell–cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19 + or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56 bright CD16 − NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19. NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell-cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell-cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16- NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19. NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell–cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell–cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16− NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19. |
| Author | Yang, Otto O Tobin, Nicole H Aldrovandi, Grace M Wilk, Aaron J Ferbas, Kathie G Blish, Catherine A Lee, Madeline J Vales Torres, Xariana Fulcher, Jennifer A Barnard, Trisha R Rimoin, Anne W de los Rios Kobara, Izumi |
| AuthorAffiliation | Division of Infectious Diseases, Department of Pediatrics, David Geffen School of Medicine at UCLA, Los Angeles, CA Division of Infectious Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA Stanford Medical Scientist Training Program, Stanford University School of Medicine, Palo Alto, CA Chan Zuckerberg Biohub, San Francisco, CA Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles, Los Angeles, CA Department of Medicine, Stanford University School of Medicine, Palo Alto, CA Stanford Immunology Program, Stanford University School of Medicine, Palo Alto, CA |
| AuthorAffiliation_xml | – name: Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles, Los Angeles, CA – name: Stanford Immunology Program, Stanford University School of Medicine, Palo Alto, CA – name: Division of Infectious Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA – name: Division of Infectious Diseases, Department of Pediatrics, David Geffen School of Medicine at UCLA, Los Angeles, CA – name: Department of Medicine, Stanford University School of Medicine, Palo Alto, CA – name: Chan Zuckerberg Biohub, San Francisco, CA – name: Stanford Medical Scientist Training Program, Stanford University School of Medicine, Palo Alto, CA |
| Author_xml | – sequence: 1 givenname: Madeline J orcidid: 0000-0001-5039-6806 surname: Lee fullname: Lee, Madeline J – sequence: 2 givenname: Izumi orcidid: 0000-0002-6479-110X surname: de los Rios Kobara fullname: de los Rios Kobara, Izumi – sequence: 3 givenname: Trisha R orcidid: 0009-0000-3820-1375 surname: Barnard fullname: Barnard, Trisha R – sequence: 4 givenname: Xariana surname: Vales Torres fullname: Vales Torres, Xariana – sequence: 5 givenname: Nicole H orcidid: 0000-0001-6904-6128 surname: Tobin fullname: Tobin, Nicole H – sequence: 6 givenname: Kathie G orcidid: 0009-0005-8861-2240 surname: Ferbas fullname: Ferbas, Kathie G – sequence: 7 givenname: Anne W surname: Rimoin fullname: Rimoin, Anne W – sequence: 8 givenname: Otto O orcidid: 0000-0003-1970-8992 surname: Yang fullname: Yang, Otto O – sequence: 9 givenname: Grace M orcidid: 0000-0003-1604-9637 surname: Aldrovandi fullname: Aldrovandi, Grace M – sequence: 10 givenname: Aaron J orcidid: 0000-0003-1430-5852 surname: Wilk fullname: Wilk, Aaron J – sequence: 11 givenname: Jennifer A orcidid: 0000-0001-9895-8636 surname: Fulcher fullname: Fulcher, Jennifer A – sequence: 12 givenname: Catherine A orcidid: 0000-0001-6946-7627 surname: Blish fullname: Blish, Catherine A |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38578283$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3390_app142311048 |
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| Copyright | Copyright © 2024 by The American Association of Immunologists, Inc. Copyright © 2024 The Authors. Copyright © 2024 The Authors 2024 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 M.J.L. and C.A.B. conceived the project and designed the experiments. M.J.L., I.D.L.R.K., T.R.B., and X.V.T performed the experiments. M.J.L. performed statistical analyses and generated figures. N.H.T., K.G.F., A.W.R., O.O.Y., G.M.A., and J.F. processed and stored patient samples used in this study. A.J.W and J.A.F. provided intellectual input. M.J.L. and C.A.B. wrote the manuscript. All authors reviewed and revised the manuscript. |
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| Snippet | NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have... scRNA-seq analysis predicts interactions between NK cells and monocytes in COVID-19. Monocytes from COVID-19 donors induce activation and proliferation in... |
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| Title | NK Cell–Monocyte Cross-talk Underlies NK Cell Activation in Severe COVID-19 |
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