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The Dynamic Changes in Cytokine Responses in COVID-19

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The Dynamic Changes in Cytokine Responses in COVID-19 meeting report SARS-COV-2 The dynamic changes in cytokine responses in COVID-19: a snapshot of the current state of knowledge “The role of cytokines in COVID-19” online symposium was presented on 18 June 2020 by the NIH/FDA Immunology and Cytokine Interest Groups and was purposed to discuss our rapidly changing understanding of COVID-19-related cytokine responses in diferent stages of infection, including the etiologies, downstream consequences and possible mitigation strategies. The recording is available at https://nci.rev.vbrick.com/ sharevideo/03106730-66cc-47ba-870b-f6e6274a998a. he symposium was opened by address that underscored the broad variety serum cytokine concentrations with disease Anthony Fauci, Director of the of clinical presentations of COVID-19, outcome. Her data showed that IL-6, IL-8 TNational Institute of Allergy and thus highlighting the central role of the and TNF, and to a lesser extent, IL-1β, were Infectious Diseases at the US National immune response in this disease. She also elevated at the time of hospitalization, and Institutes of Health (NIAID, NIH), and remarked on the apparent geographic their concentrations correlated with disease Janet Woodcock, Director of the Center clusters of disease manifestations and the outcome and mortality, even after correcting of Drug Evaluation and Research, Food need to better understand possible factors for age, ethnicity, race and comorbidities, and Drug Administration (CDER, FDA) in host–pathogen interactions beyond those suggesting that they could be used to and currently leading the therapeutics health conditions already identified, such identify patients at risk of severe disease2. component of Operation Warp Speed. as prior innate immune experience and The proinflammatory cytokines Fauci briefly reviewed the current subtle differences in ACE2 expression in remained elevated throughout the disease status of the coronavirus disease 2019 the populations. Lastly, she discussed the course unless patients were treated with (COVID-19) pandemic, noting that complexity of the data emerging from the steroids or remdesivir, which reduced the worldwide incidence had grown to multiple clinical trials that are targeting the level of circulating IL-6. She also 8 million cases and more than 300,000 the inflammatory process underlying the stressed that IL-6 and TNF are regulated deaths, with >120,000 fatalities in the USA disease, emphasizing the importance of independently and thus could be targeted alone (incidence on June 18 2020). The establishing clinically relevant biomarkers to in parallel in patients with severe disease. causative virus, the severe acute respiratory guide the therapeutic course. Merad then described early results from syndrome coronavirus 2 (SARS-CoV-2), deep-profiling longitudinal studies using is a single-stranded RNA virus that uses Cytokine response and disease severity whole-blood proteomics that identified 23 angiotensin-converting enzyme 2 (ACE2) The first scientific session of the meeting clusters of cytokines that are differentially as a cellular receptor. The atomic-level focused on the changing cytokine response expressed in patients with mild disease, conformation of the prefusion spike protein over the course of COVID-19 and was severe disease without end organ damage of the virus was recently described by opened by Miriam Merad (Mount Sinai and severe disease with end organ damage. NIAID Vaccine Research Center scientists School of Medicine). Merad first reminded In this broader assessment, patients with and colleagues1. He also underscored us that the infection is asymptomatic severe disease had increased IL-6 and other the role of cytokines in the pathogenesis in 80% of adults and most children, but proinflammatory cytokines, while those of the different clinical presentations of 20% of patients require hospitalization with moderate disease had a pattern that COVID-19, ranging from asymptomatic to in the intensive care unit (ICU). The suggested T cell priming. Lastly, Merad pneumonia, neurological disorders, acute mortality rate for patients in the ICU is suggested that the pattern of cytokine respiratory distress syndrome (ARDS), 25%, with most deaths attributed to severe response in children with multisystem cardiomyopathies, sepsis, hypercoagulability, inflammation and embolic complications. inflammatory syndrome partly resembled multiorgan failure and death, as well as In agreement with Woodcock’s remarks that of adults with severe disease, as they had the multisystem inflammatory syndrome on the importance of biomarkers to better increased expression of proinflammatory seen in children. Also, the benefit of target therapeutic efforts, Merad described cytokines; however, they also had a variety dexamethasone treatment in severe COVID- studies using high-dimensional profiling to of autoantibodies, including some classical 19 cases requiring ventilation was discussed, identify early markers that predict disease autoantibodies, but also autoantibodies which is consistent with the central roles severity. In one study, her group selected directed to cardiac and endothelial of inflammation and a cytokine storm in a platform that monitors interleukin (IL)- antigens that might explain the disease causing serious pathology. Fauci ended 6, IL-8, IL-1β and tumor necrosis factor manifestations. Importantly, the cytokine his talk by calling attention to the multiple (TNF), which are well-established targets patterns that were present at the time of initiatives undertaken and supported by for anti-inflammatory therapeutics. They hospitalization in children as well as adults the NIAID to address the COVID-19 tested over 1,500 patients on the day of were maintained throughout the disease outbreak. Woodcock followed with an hospitalization and then correlated the course unless modified by treatment with 1146 NATURE IMMUNOLOGY | VOL 21 | OctoBER 2020 | 1146–1151 | www.nature.com/natureimmunology meeting report steroids, remdesivir or immunomodulatory therapy and could be correlated with disease outcome, suggesting that they can be used to guide the therapeutic approach. John Tsang (NIAID, NIH) then spoke of Capillary the application of a systems immunology analysis of COVID-19. He described Alveolus studies employing cellular indexing of Pneumocyte type I transcriptomes and epitopes by sequencing Macrophage (CITE-seq), a single-cell analysis method B2 LMWK that combines highly multiplexed surface Tissue protein marker detection with transcriptome kallikrein profiling. The Tsang lab and collaborators SARS-CoV-2 ACE2 B1 Lys-bradykinin evaluated peripheral blood mononuclear IL-1 B1 Bradykinin cells (PBMCs) from a longitudinal cohort TNF of hospitalized patients with COVID-19 Leakage des-Arg9-BK Plasma ACE2 kallikrein from Brescia, Italy, taken at the height of Lys-des-Arg9-BK the outbreak in that region. The patients Plasma HMWK evaluated in this first experiment included Tissue kallikrein 13 severe or critical patients and 5 age- and sex-matched healthy controls. Two LMWK observations in particular emerged that differed from findings reported by other investigators. First, whereas previous studies suggested that the virus disrupted the type I Fig. 1 | Alveolus during severe COVID-19 hyperinflammation. ACE2 downregulation by SARS-CoV-2 interferon (IFN) signaling pathway, fueling is followed by the loss of neutralizing capacity of Lys-[des-Arg9]-bradykinin (BK) in the lung, leading speculation that the lack of an early type I to plasma leakage. Subsequently, plasma leakage results in more B1R ligands (des-Arg9-BK) and B2R (and III) IFN response permits rapid viral ligands (bradykinin), enhancing vascular permeability and angioedema. CPM, carboxypeptidase M; spread and induces hyperinflammatory CPN, carboxypeptidase N; HMWK, high-molecular-weight kininogen; LMWK, low-molecular-weight responses, this study identified a clear type kininogen. Figure reproduced with permission from ref. 4, eLife Sciences Publications. I IFN signature across major immune cell subsets in patients with COVID-19. These findings suggest that a careful evaluation of disease, with an initial focus on IL-1 biology patients with severe disease, which is of clear the patient populations scrutinized across and autoinflammation and a subsequent interest from a therapeutic standpoint. In the different studies should be performed, as the focus on the kallikrein–kinin system. IL-6 last part of his talk, van de Veerdonk focused timelines for the induction of such responses upregulation was prominent in patients on the reduced amounts of serpin family may differ according to disease stage and with severe disease, which van de Veerdonk A member 12 (SERPINA12) and DPP4 may be further influenced by genetic proposed was a manifestation of the (CD26) in patients in the ICU versus those and environmental factors. Furthermore, strong induction of an autoinflammatory not in the ICU. Since these factors suppress thus far, Tsang has found no evidence loop via IL-1β and the IL-1 receptor (IL- inflammation mediated by kallikreins of T cell exhaustion, as the expanded 1R). He proposed that, following SARS and it is expected that there is positive, CD8+ T cell clones were found to have CoV-2 binding to pathogen recognition coordinated stimulation of the kallikrein– decreased PD-1 expression in comparison receptors, pro-IL-1β is induced, processed kinin system from increases in IL-1 and with the non-expanded cells in patients. to IL-1β by activated inflammasomes and IL-6 as well as from activated
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