PMC:7200337 / 21316-28807 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7200337","sourcedb":"PMC","sourceid":"7200337","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7200337","text":"Innate Lymphoid Cells\nInnate lymphoid cells (ILCs) are innate immune effector cells that lack the expression of rearranged antigen receptors (T cell receptor [TCR], B cell receptor [BCR]). The ILC family is divided into two main groups: the cytotoxic natural killer (NK) cells and the non-cytotoxic helper ILCs, which include ILC1, ILC2, and ILC3 (Vivier et al., 2018). Conventional NK cells include CD56brightCD16− NK cells and CD56dimCD16+ cells, which are specialized in cytokine production or cytotoxicity, respectively.\n\nNK Cells Are Decreased in the Peripheral Blood of COVID-19 patients\nMultiple studies have reported reduced numbers of NK cells in the peripheral blood of COVID-19 patients, which is associated with severity of the disease (Song et al., 2020, Wang et al., 2020f, Yu et al., 2020, Zheng et al., 2020b). A recent scRNA-seq analysis revealed a transcriptomic signature for NK cells that was equally represented in lungs from patients and healthy donors (Liao et al., 2020). The majority of lung NK cells are non-resident (Gasteiger et al., 2015, Marquardt et al., 2017), and CXCR3 has been shown to mediate NK cell infiltration upon influenza infection (Carlin et al., 2018). In vitro, CXCR3 ligands (CXCL9-11) are increased in SARS-CoV-2-infected human lung tissue (Chu et al., 2020), and CXCR3-ligand-producing monocytes are expanded in the lungs of COVID-19 patients (Liao et al., 2020). This suggests that the CXCR3 pathway might facilitate NK cell recruitment from the peripheral blood to the lungs in COVID-19 patients (Figure 2).\n\nNK Cell Activation Pathways in Antiviral Immunity\nNK cells express inhibitory and activating receptors that regulate their cytotoxicity. They are therefore able to induce the lysis of virus-infected cells that upregulate virus-derived proteins, as well as stress-inducible ligands, which are then recognized by NK-cell-activating receptors, such as NKp46 (Cerwenka and Lanier, 2001, Draghi et al., 2007, Duev-Cohen et al., 2016, Glasner et al., 2012). Future studies should investigate the expression of NK receptor ligands on SARS-CoV-2-infected cells in order to better understand the mechanisms underlying NK cell activation in COVID-19 disease. Further, secretion of IgG1 and IgG3 antibodies during SARS-CoV-2 infection (Amanat et al., 2020) may induce CD56dim CD16+ NK cell activation through Fc receptor recognition of antibodies either bound to surface antigens expressed on infected cells or to extracellular virions as immune complexes (Figure 2). This interaction might trigger both cytokine production by NK cells and lysis of infected cells through antibody-mediated cellular cytotoxicity (ADCC), as shown in influenza infection (Von Holle and Moody, 2019). Emerging data highlight the capacity for NK-mediated ADCC in response to naturally isolated SARS-CoV-1 anti-S IgG that crossreacts with SARS-CoV-2 S glycoprotein when transfected into Chinese hamster ovary (CHO) cells (Pinto et al., 2020). These findings suggest that triggering NK cell activation may not only contribute to the resolution of infection, but also contribute to the cytokine storm in ARDS.\n\nImpairment of NK Cell Function in SARS-CoV-2 Infection\nEx vivo NK cells from peripheral blood of COVID-19 patients have reduced intracellular expression of CD107a, Ksp37, granzyme B, and granulysin, suggesting an impaired cytotoxicity, as well as an impaired production of chemokines, IFN-ɣ, and TNF-α (Wilk et al., 2020, Zheng et al., 2020b). Several pathways may contribute to the dysregulation of NK cells. While influenza virus infects NK cells and induces apoptosis (Mao et al., 2009), lung NK cells do not express the entry receptor for SARS-CoV-2, ACE2, and are therefore unlikely to be directly infected by SARS-CoV-2 (Travaglini et al., 2020). The majority of NK cells found in human lung display a mature CD16+KIR+CD56dim phenotype and are able to induce cell cytotoxicity in response to loss of human leukocyte antigen (HLA) class I or through Fc receptor signaling, although to a lower extent than their peripheral blood counterpart (Marquardt et al., 2017). Killer-immunoglobulin receptors (KIRs) are acquired during NK cell development alongside CD16 (FcRγIIIA) and are essential for NK cell licensing and subsequent capacity for cytolytic function (Sivori et al., 2019). Frequencies of NK cells expressing CD16 and/or KIRs are decreased in the blood following SARS-CoV-2 and SARS-CoV-1 infection, respectively (Xia et al., 2004, Wang et al., 2020d). Collectively, the data suggest either an impaired maturation of the NK compartment or migration of the mature, circulating NK cells into the lungs or other peripheral tissues of SARS-CoV-2-infected patients.\nThe immune checkpoint NKG2A is increased on NK cells and CD8 T cells from COVID-19 patients (Zheng et al., 2020b). NKG2A inhibits cell cytotoxicity by binding the non-classical HLA-E molecule (Braud et al., 1998, Brooks et al., 1997), and this interaction is strongly correlated with poor control of HIV-1 infection (Ramsuran et al., 2018). Genes encoding the inhibitory receptors LAG3 and TIM3 are also upregulated in NK cells from COVID-19 patients (Wilk et al., 2020, Hadjadj et al., 2020). Thus, increased immune checkpoints on NK cells might contribute to viral escape. Additionally, COVID-19 patients have higher plasma concentrations of IL-6 (Huang et al., 2020b), which significantly correlate with lower NK cell numbers (Wang et al., 2020d, Wang et al., 2020f). In vitro stimulation by IL-6 and soluble IL-6 receptor has previously revealed impaired cytolytic functions (perforin and granzyme B production) by healthy donor NK cells, which can be restored following addition of tocilizumab (IL-6R blockade) (Cifaldi et al., 2015). TNF-α is also upregulated in the plasma of COVID-19 patients (Huang et al., 2020b), and ligand-receptor interaction analysis of peripheral blood scRNA-seq data suggests that monocyte-secreted TNF-α might bind to its receptors on NK cells (Guo et al., 2020). TNF-α is known to contribute to NK cell differentiation (Lee et al., 2009), which includes downregulation of NKp46 (Ivagnès et al., 2017), though no effect of TNF-α or IL-6 on NK cell-mediated ADCC has been reported so far. Collectively, these data suggest that crosstalk with monocytes might impair NK cell recognition and killing of SARS-CoV-2-infected cells, and antibodies targeting IL-6 and TNF-signaling may benefit enhanced NK cell functions in COVID-19 patients (Figure 2).\n\nRelevance for Helper ILCs in SARS-CoV-2 Infection\nNo studies, to date, have reported ILC1, ILC2, or ILC3 functions in SARS-CoV-2 infection. All three subsets are present in healthy lung (De Grove et al., 2016, Yudanin et al., 2019). ILC2s are essential for the improvement of lung function following influenza infection in mice through amphiregulin-mediated restoration of the airway epithelium and oxygen saturation (Monticelli et al., 2011). However, ILC2s also produce IL-13, contributing to the recruitment of macrophages to the lung and influenza-induced airway hyperreactivity (Chang et al., 2011). Indeed, ILCs are involved in the polarization of alveolar macrophages, either toward a M1-like phenotype (ILC1 and ILC3) or a M2-like phenotype (ILC2) (Kim et al., 2019). Given the increased IL-13 concentrations (Huang et al., 2020b) and the dysregulation of the macrophage compartment observed in COVID-19 patients, the role played by ILCs in SARS-CoV-2 infection warrants further 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