Pathogenic T-cells and inflammatory monocytes incite inflammatory storms in severe COVID-19 patients
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Abstract
Pathogenic human coronavirus infections, such as severe acute respiratory syndrome CoV (SARS-CoV) and Middle East respiratory syndrome CoV (MERS-CoV), cause high morbidity and mortality [1,2]. Recently, a severe pneumonia-associated respiratory syndrome caused by a new coronavirus (SARS-CoV-2) was reported in December 2019 in the city of Wuhan, Hubei province, China [3–5], which was also named as pneumonia-associated respiratory syndrome (PARS) [6] and can cause coronavirus disease 2019 (COVID-19) to seriously endanger human health. Up to 24 February 2020, at least 77 779 cases had been reported, with 2666 fatal cases according to the report from China CDC. However, the immune mechanism that potentially orchestrates acute mortality from COVID-19 patients is still unknown. Here, we show that, after the SARS-CoV-2 infection, CD4+ T lymphocytes are rapidly activated to become pathogenic T helper (Th) 1 cells and generate GM-CSF, etc. The cytokine environment induces inflammatory CD14+CD16+ monocytes with a high expression of IL-6 and accelerates the inflammation. Given that a large number of inflammatory-cell infiltrations have been observed in lungs from severe COVID-19 patients [7,8], these aberrant pathogenic Th1 cells and inflammatory monocytes may enter the pulmonary circulation in huge numbers and play an immune-damaging role causing lung functional disability and quick mortality. Our results demonstrate that excessive non-effective host-immune responses by pathogenic T-cells and inflammatory monocytes may be associated with severe lung pathology. Thus, we suggest that monoclonal antibodies targeting GM-CSF or interleukin 6 may be effective in blocking inflammatory storms and, therefore, be a promising treatment for severe COVID-19 patients. Coronavirus, including SARS and MERS, has caused two large-scale pandemics in the last two decades [1,2]. Although viral evasion of host-immune responses and virus-induced cytopathic effects are believed to be critical in disease severity, studies from humans who died of SARS and animal models have suggested that an excessive and aberrant host-cytokine storm results in an exuberant immunopathology and lethal disease [9–11]. Inflammatory cytokine storm refers to the immune system gone awry and an excessive inflammatory response flaring out of control. Cytokine storms are associated with a wide variety of infectious and non-infectious diseases including graft-versus-host disease, autoimmune disease, severe virus infection, multiple organ dysfunction syndromes and chimeric antigen receptor (CAR) T-cell therapy [12,13]. It has been reported that, following SARS-CoV infection, dysregulated cytokine/chemokine responses and higher virus titers cause an inflammatory cytokine storm with lung immunopathological injury [12,14]. Such inflammation associated with the cytokine storm may begin at one local site but spread farther throughout the body via the systemic circulation [12,14]. Similarly, patients infected with SARS-CoV-2 who have been reported recently have had increased plasma concentrations of inflammation-related cytokines, including interleukins (IL) 2, 7 and 10, granulocyte-colony-stimulating factor (G-CSF), interferon-γ-inducible protein 10 (IP10), monocyte chemoattractant protein 1 (MCP1), macrophage inflammatory protein 1 alpha (MIP1A) and tumour necrosis factor α (TNF-α), especially in moribund patients [15]. Importantly, COVID-19 patients have developed characteristic pulmonary ground glass changes on imaging and peripheral lymphocytes decreasing [14,16,17]. More importantly, a large number of inflammatory immune-cell infiltrations were also found in a COVID-19 patient with pulmonary pathology [7,8]. These phenomena suggest that severe pulmonary inflammation and cytokine storm also exist in SARS-CoV-2 infection. At present, symptomatic treatments with organ support to moribund patients are the mainstays of clinical management [17]. It is urgent to identify the immunopathology mechanism to delay the pulmonary immune injury. In patients infected with SARS-CoV, it has been reported that the severity of pulmonary immune injury correlated with extensive infiltration of neutrophils and macrophages in the lungs [18,19], accompanied by increased numbers of neutrophils and monocytes and lower CD8+ and CD4+ T-cell counts in the peripheral blood samples [20–22]. To identify the immune characteristics of patients infected with SARS-CoV-2, peripheral blood samples from patients with severe pneumonia were collected for immune analysis. Consistently with previous clinical-characteristics reports [23], these hospitalized patients with confirmed SARS-CoV-2 infection involved in the First Affiliated Hospital of University of Science and Technology of China commonly have fever symptoms. Patients in intensive care units (ICUs) have significantly decreased concentrations of haemoglobin and albumin, but increased concentrations of C-reactive protein, alanine aminotransferase, asparta
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SARS-CoV-2 infection elicits a Th1 CD4+ T cell response, with IFNγ and IL-2 as the main cytokines produced and some TNFα as well.
“SARS-CoV-2 infection elicits a Th1 CD4+ T cell response, with IFNγ and IL-2 being the primary cytokines produced by these cells and some TNFα production as well112,126-129.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [112]
HLA-DR expression on monocytes from severe COVID-19 patients is lower than on monocytes from mild patients.
“HLA-DR expression on monocytes from severe COVID-19 patients is also reduced relative to those from mild patients109,110,112,122.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [112]
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Monocytes and Macrophages in COVID-19
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Immunosenescence, aging and successful aging
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- Authors
- Zhou, Y., Fu, B., Zheng, X., Wang, D., Zhao, C., Qi, Y., Sun, R., Tian, Z., Xu, X., & Wei, H.
- Affiliations
- University of Science and Technology of China (CN)
- Corresponding author
- Xu, Xiaoling
- Wei, Haiming
- ORCID
- Venue
- National Science Review
- Publisher
- Oxford University Press (OUP)
- Published
- 2020-03-13
- Volume
- 7
- Issue
- 6
- Pages
- 998-1002
- ISSN
- 2053-714X (ISSN-L)
- 2095-5138
- PMC
- PMC7108005
- OpenAlex
- W3011230498
- Cited by
- 1,295
- References
- 36
- Citations by year
- 2026: 14 · 2025: 48 · 2024: 78 · 2023: 131 · 2022: 201 · 2021: 392 · 2020: 431
- FWCI
- 37.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- National Science Review (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- China National Center for Biotechnology Development (2020YFC0843800)
- Natural Science Foundation of China (81788101, 81922028)
- Youth Innovation Promotion Association of Chinese Academy of Sciences (2019442)
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Keywords
- COVID-19 pandemic, SARS-CoV-2, CD4+ T cells, inflammatory monocytes, CD14+CD16+ monocytes, interleukin-6, GM-CSF, cytokine storm, lung inflammation, immunopathology, monoclonal antibodies, IL-6 inhibition, severe pneumonia
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