☆ 4.7 Review

Respiratory and systemic monocytes, dendritic cells, and myeloid-derived suppressor cells in COVID-19: Implications for disease severity

JOURNAL OF INTERNAL MEDICINE (2023)

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Immuno-proteomic profiling reveals aberrant immune cell regulation in the airways of individuals with ongoing post-COVID-19 respiratory disease

Bavithra Vijayakumar et al.

Summary: Patients with persistent lung disease after COVID-19 discharge exhibit abnormal immune-proteomic profiles in the airways, characterized by elevated levels of proteins associated with cell death, tissue repair, and epithelial injury. The severity of airway dysfunction correlates with increased cytotoxic lymphocyte counts, while more extensive lung abnormalities are associated with elevated B cell numbers and altered monocyte subsets. Long-term follow-up indicates that these abnormalities resolve over time.

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Article Immunology

Maturation signatures of conventional dendritic cell subtypes in COVID-19 suggest direct viral sensing

Laura Marongiu et al.

Summary: Growing evidence suggests that in COVID-19, conventional dendritic cells (cDCs) may undergo aberrant maturation that affects T-cell activation negatively while effective T-cell responses can limit disease severity. Studies indicate that infection-induced gene signatures of cDC2 subtypes are associated with disease severity, showing increased inflammation and decreased antigen presentation capacity.

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Article Multidisciplinary Sciences

Inflammasome activation in infected macrophages drives COVID-19 pathology

Esen Sefik et al.

Summary: This study demonstrates that lung-resident human macrophages play a critical role in the development of lung inflammation caused by SARS-CoV-2 infection. Macrophages activate inflammasomes, release inflammatory cytokines, and undergo pyroptosis in response to infection, contributing to the hyperinflammatory state in the lungs. Inhibition of the NLRP3 inflammasome pathway reverses chronic lung pathology, indicating the importance of inflammasome activation in lung inflammation.

NATURE (2022)

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Article Multidisciplinary Sciences

FcγR-mediated SARS-CoV-2 infection of monocytes activates inflammation

Caroline Junqueira et al.

Summary: This study suggests that SARS-CoV-2 infection in monocytes and macrophages, mediated by antibody uptake, triggers inflammatory cell death and systemic inflammation, which prevents the production of infectious virus but contributes to COVID-19 pathogenesis.

NATURE (2022)

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Article Critical Care Medicine

Tissue-Specific Immunopathology in Fatal COVID-19

David A. Dorward et al.

Summary: In fatal COVID-19 cases, abnormal immune responses were found primarily in the lung and reticuloendothelial system, which were not clearly associated with the virus. Tissue-specific immunopathology in COVID-19 implicates a significant role of immune-mediated, virus-independent mechanisms in severe disease.

AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE (2021)

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Article Cell Biology

Discriminating mild from critical COVID-19 by innate and adaptive immune single-cell profiling of bronchoalveolar lavages

Els Wauters et al.

Summary: Single-cell deep-immune profiling revealed that specific T cells in mild COVID-19 patients exhibit active expansion and function, while in critical COVID-19 they remain more naive. Furthermore, the monocyte-to-macrophage trajectories show enrichment of chronic hyperinflammatory monocytes and depletion of anti-inflammatory alveolar macrophages in critical COVID-19.

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Article Biochemistry & Molecular Biology

SARS-CoV-2 infection triggers profibrotic macrophage responses and lung fibrosis

Daniel Wendisch et al.

Summary: Analysis of pulmonary immune responses and lung pathology in patients with COVID-19 ARDS revealed an accumulation of profibrotic macrophages and similarities with macrophage populations in idiopathic pulmonary fibrosis. Exposure to SARS-CoV-2 induced a profibrotic phenotype in human monocytes, suggesting a mechanistic link between the virus and fibroproliferative ARDS.

CELL (2021)

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Monocytes in sarcoidosis are potent tumour necrosis factor producers and predict disease outcome

Rico Lepzien et al.

Summary: The study found an increase in pulmonary monocyte-derived cells in sarcoidosis patients, which was associated with the development of chronic disease. Highly inflammatory cells were observed in the blood and BAL of sarcoidosis patients. The frequency of BAL monocytes/monocyte-derived cells producing TNF without exogenous stimulation at diagnosis increased in patients who developed progressive disease.

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Distinct developmental pathways from blood monocytes generate human lung macrophage diversity

Elza Evren et al.

Summary: This study investigates the development of lung macrophages from human hematopoiesis using a humanized mouse model. The results show that different types of blood monocytes generate macrophages in distinct anatomical niches in the lung. Additionally, single-cell RNA sequencing reveals intermediate differentiation stages in human lung macrophage development.

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SARS-CoV-2-Induced ARDS Associates with MDSC Expansion, Lymphocyte Dysfunction, and Arginine Shortage

Florian Reizine et al.

Summary: The study revealed that ARDS patients with COVID-19 had increased MDSC and decreased CD8(pos) effector memory cell compared to patients with moderate COVID-19 pneumonia. The expansion of COVID-19-related MDSC was directly correlated to lymphopenia and enhanced arginase activity. T cell proliferative capacity in vitro was significantly reduced among COVID-19 patients but could be restored through arginine supplementation.

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Severe Acute Respiratory Syndrome Coronavirus 2-Induced Immune Activation and Death of Monocyte-Derived Human Macrophages and Dendritic Cells

Jian Zheng et al.

Summary: Studies have shown that SARS-CoV-2 infection of immature macrophages and dendritic cells leads to failed replication but induces the production of various antiviral and proinflammatory cytokines, ultimately causing cell death mediated by interferon. Activation and death of macrophages are not enhanced even when exposed to low levels of convalescent plasma.

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Circuits between infected macrophages and T cells in SARS-CoV-2 pneumonia

Rogan A. Grant et al.

Summary: The study found that patients infected with SARS-CoV-2 have enriched T cells and monocytes in the alveolar space, suggesting that the virus infects alveolar macrophages and induces T cell production of interferon-, leading to inflammation and persistent alveolitis.

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Article Immunology

Untuned antiviral immunity in COVID-19 revealed by temporal type I/III interferon patterns and flu comparison

Ioanna-Evdokia Galani et al.

Summary: Andreakos and colleagues conducted a study comparing patients with COVID-19 and influenza, finding that COVID-19 patients exhibited a dysregulated interferon response with diminished and delayed interferon production compared to flu patients. In COVID-19 patients, pro-inflammatory cytokines were produced before interferons and persisted longer, leading to worsened clinical outcomes.

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Major alterations in the mononuclear phagocyte landscape associated with COVID-19 severity

Egle Kvedaraite et al.

Summary: This study found that COVID-19 patients experience a redistribution of monocyte subsets towards intermediate monocytes and a general decrease in circulating dendritic cells. Severe disease is associated with the appearance of monocytic myeloid-derived suppressor cell-like cells and a higher frequency of pre-DC2. The phenotypic alterations in mononuclear phagocytes are cell-lineage-specific and linked to the response against SARS-CoV-2 or COVID-19 severity.

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Longitudinal Analysis of Inflammatory Response to SARS-CoV-2 in the Upper Respiratory Tract Reveals an Association with Viral Load, Independent of Symptoms

Diem-Lan Vu et al.

Summary: The study found that levels of certain cytokines in the nasal cavity of SARS-CoV-2-infected patients can remain elevated for up to 3 weeks, and some patients had S1-specific IgA present in their nasal cavity. In this mild cohort, anosmia was not associated with locally produced cytokines.

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An immune-based biomarker signature is associated with mortality in COVID-19 patients

Michael S. Abers et al.

Summary: Immune and inflammatory responses are important factors contributing to disease severity in COVID-19. This study identified specific immune-based biomarkers associated with mortality in COVID-19 patients, with some biomarkers consistently higher in those who died compared to those who recovered, suggesting their potential for early prediction of disease outcome.

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Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19

Peter A. Szabo et al.

Summary: This study investigated the immune responses in the respiratory tract and blood of severe COVID-19 patients, revealing that T cells in the airways showed protective profiles while myeloid cells exhibited hyperinflammatory signatures. These findings provide important insights for understanding and treating COVID-19 lung pathology.

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SARS-CoV-2 induces human plasmacytoid predendritic cell diversification via UNC93B and IRAK4

Fanny Onodi et al.

Summary: Studies have shown that human pDCs can be efficiently activated by SARS-CoV-2 particles and may contribute to type I IFN-dependent immunity against SARS-CoV-2 infection.

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Metabolic programs define dysfunctional immune responses in severe COVID-19 patients

Elizabeth A. Thompson et al.

Summary: The study identifies a unique population of T cells expressing increased VDAC1 in severe and recovered COVID-19 patients, associated with mitochondrial dysfunction and apoptosis. Additionally, specific metabolic phenotypes of myeloid-derived suppressor cells in COVID-19 patients can distinguish between severe and mild disease. These findings offer insight into dysfunctional immune response in COVID-19 patients and potential for developing personalized therapeutic approaches.

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Impaired function and delayed regeneration of dendritic cells in COVID-19

Elena Winheim et al.

Summary: COVID-19 patients exhibit reduced numbers and impaired function of DCs in the blood, correlated with disease severity and potential consequences for disease management and susceptibility to secondary infections.

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Defining the Innate Immune Responses for SARS-CoV-2-Human Macrophage Interactions

Mai M. Abdelmoaty et al.

Summary: Following SARS-CoV-2 infection, the host mounts a robust innate immune response characterized by a pro-inflammatory storm, leading to end-organ tissue damage.

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Functional monocytic myeloid-derived suppressor cells increase in blood but not airways and predict COVID-19 severity

Sara Falck-Jones et al.

Summary: The frequency of M-MDSCs is elevated in the blood of patients with COVID-19, suppressing T cells and strongly associated with disease severity.

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Recruitment of dendritic cell progenitors to foci of influenza A virus infection sustains immunity

Mar Cabeza-Cabrerizo et al.

Summary: Protection from respiratory viruses like influenza A virus (IAV) requires T cell-mediated immune responses initiated by conventional dendritic cells (cDCs) in the respiratory tract. Reinforcing the resident lung cDC network by cDC progenitors is necessary for effective induction of T cell responses against IAV in mice. Chemokines produced during IAV infection recruit pre-cDCs from blood, directing them to infection sites to increase cDC numbers and amplify T cell responses.

SCIENCE IMMUNOLOGY (2021)

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Article Medicine, Research & Experimental

Airway antibodies emerge according to COVID-19 severity and wane rapidly but reappear after SARS-CoV-2 vaccination

Alberto Cagigi et al.

Summary: The study found that systemic and airway antibody responses were correlated with the severity of COVID-19 disease, with systemic IgG levels lasting longer but IgG and IgA in the airways declining within 3 months. After vaccination, antibody levels significantly increased, especially IgG, and airway antibody levels were significantly elevated in previously infected individuals after receiving a booster dose of the vaccine.

JCI INSIGHT (2021)

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Article Multidisciplinary Sciences

A molecular single-cell lung atlas of lethal COVID-19

Johannes C. Melms et al.

Summary: Single-nucleus RNA sequencing of lung tissues from individuals who died of COVID-19 revealed a highly inflamed lung environment with impaired T cell responses and failed transition of alveolar type 2 cells. Additionally, expansion of pathological fibroblasts contributing to rapidly ensuing pulmonary fibrosis in COVID-19 was identified as a unique feature compared to other causes of pneumonia.

NATURE (2021)

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SARS-CoV-2 induces double-stranded RNA-mediated innate immune responses in respiratory epithelial-derived cells and cardiomyocytes

Yize Li et al.

Summary: Coronaviruses, including SARS-CoV-2, are skilled at evading host antiviral pathways but the extent to which SARS-CoV-2 activates or antagonizes these pathways is relatively unknown. SARS-CoV-2 infects various cell types without strong activation of IFN or OAS-RNase L, while PKR activation is evident. Unlike other coronaviruses, SARS-CoV-2 does not effectively inhibit host defense pathways, but shows a generally weak IFN signaling response, contributing to its unique pathogenesis.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2021)

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The COVID-19 puzzle: deciphering pathophysiology and phenotypes of a new disease entity

Marcin F. Osuchowski et al.

Summary: The zoonotic SARS-CoV-2 virus causing COVID-19 has devastating consequences worldwide, affecting primarily the respiratory system but also leading to long-term complications. Understanding the pathophysiology and immune response of COVID-19 is crucial for optimizing patient care and treatment strategies.

LANCET RESPIRATORY MEDICINE (2021)

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Article Immunology

Human plasmacytoid dendritic cells mount a distinct antiviral response to virus-infected cells

Tae Jin Yun et al.

Summary: Plasmacytoid dendritic cells (pDCs) can recognize live infected cells and produce a unique antiviral immune response, including high amounts of interferons, prolonged and efficient responses to CMV-infected cells, and activation of natural killer cells. Patients with CMV viremia show activated pDCs and increased circulating IFN-I and IFN-III.

SCIENCE IMMUNOLOGY (2021)

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Impaired local intrinsic immunity to SARS-CoV-2 infection in severe COVID-19

Carly G. K. Ziegler et al.

Summary: Our study reveals the diverse responses of cells in the nasopharyngeal epithelium to SARS-CoV-2 infection, with different gene expression profiles observed in mild, moderate, and severe cases of COVID-19. The identification of specific cell types and associated genes highlights the complexity of the host response to viral infection, and suggests that impaired nasal epithelial anti-viral immunity may contribute to the development of severe COVID-19.

CELL (2021)

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Dendritic cell deficiencies persist seven months after SARS-CoV-2 infection

Alberto Perez-Gomez et al.

Summary: SARS-CoV-2 infection causes abnormal immune response, affecting the quantity and function of dendritic cells, with some markers remaining altered during acute phase and follow-up.

CELLULAR & MOLECULAR IMMUNOLOGY (2021)

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Plasma from patients with bacterial sepsis or severe COVID-19 induces suppressive myeloid cell production from hematopoietic progenitors in vitro

Miguel Reyes et al.

Summary: The study found an expanded CD14(+) monocyte state, MS1, in patients with bacterial sepsis and severe COVID-19, with the gene expression program of MS1 correlating with sepsis severity and being up-regulated in monocytes from severe COVID-19 patients. In vitro induction of MS1 cells from healthy bone marrow HSPCs showed that plasma from sepsis or COVID-19 patients could induce myelopoiesis and expression of the MS1 gene program. The study also demonstrated that systemic cytokines such as IL-6 and IL-10 played a role in inducing myelopoiesis during severe bacterial or SARS-CoV-2 infection.

SCIENCE TRANSLATIONAL MEDICINE (2021)

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Monocyte-driven atypical cytokine storm and aberrant neutrophil activation as key mediators of COVID-19 disease severity

L. Vanderbeke et al.

Summary: Research indicates that COVID-19 severity is driven by a hyperinflammatory response rather than direct viral damage, with classical monocytes playing a key role in driving the hypercytokinemia. Disease severity correlates with a reduction in T-lymphocytes, particularly affecting CD8+ cells, and neutrophils contribute to tissue damage through amplification of cytokine levels. The findings suggest a myeloid-driven immunopathology in COVID-19.

NATURE COMMUNICATIONS (2021)

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Differential plasmacytoid dendritic cell phenotype and type I Interferon response in asymptomatic and severe COVID-19 infection

Martina Severa et al.

Summary: The study highlights the crucial role of pDC/type I IFN axis in defending against SARS-CoV-2 infection in COVID-19 patients, suggesting that a deeper understanding may aid in the development of new drug strategies and host-directed therapies. Moreover, the findings indicate that critically ill patients exhibit impaired type I IFN response and high levels of inflammatory cytokines and chemokines, leading to multi-organ failure.

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X-linked recessive TLR7 deficiency in ∼1% of men under 60 years old with life-threatening COVID-19

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Summary: A study revealed that rare X-linked TLR7 variants were found in 16 unrelated male individuals with critical COVID-19 pneumonia out of a cohort of 1202 male patients. No such variants were detected in 331 asymptomatic or mildly infected male individuals.

SCIENCE IMMUNOLOGY (2021)

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Dendritic Cells and Monocytes with Distinct Inflammatory Responses Reside in Lung Mucosa of Healthy Humans

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Minimal Differentiation of Classical Monocytes as They Survey Steady-State Tissues and Transport Antigen to Lymph Nodes

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Immunosuppressive CD14+HLA-DRlow/- monocytes in B-cell non-Hodgkin lymphoma

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Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets

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HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment

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Review Cell Biology

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Different roles for human lung dendritic cell subsets in pulmonary immune defense mechanisms

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Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2

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Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract

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In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma

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In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens

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