Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma
Background: Increased blood/sputum neutrophil counts are related to poor clinical outcomes of severe asthma (SA), where we hypothesized that classical monocytes (CMs)/CM-derived macrophages (Mφ) are involved. We aimed to elucidate the mechanisms of how CMs/Mφ induce the activation of neutrophils/inn...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-01-01
|
| Series: | Allergology International |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1323893023000680 |
| _version_ | 1797365616590454784 |
|---|---|
| author | Quang Luu Quoc Thi Bich Tra Cao Ji-Young Moon Jae-Hyuk Jang Yoo Seob Shin Youngwoo Choi Min Sook Ryu Hae-Sim Park |
| author_facet | Quang Luu Quoc Thi Bich Tra Cao Ji-Young Moon Jae-Hyuk Jang Yoo Seob Shin Youngwoo Choi Min Sook Ryu Hae-Sim Park |
| author_sort | Quang Luu Quoc |
| collection | DOAJ |
| description | Background: Increased blood/sputum neutrophil counts are related to poor clinical outcomes of severe asthma (SA), where we hypothesized that classical monocytes (CMs)/CM-derived macrophages (Mφ) are involved. We aimed to elucidate the mechanisms of how CMs/Mφ induce the activation of neutrophils/innate lymphoid cells (ILCs) in SA. Methods: Serum levels of monocyte chemoattractant protein-1 (MCP-1) and soluble suppression of tumorigenicity 2 (sST2) were measured from 39 patients with SA and 98 those with nonsevere asthma (NSA). CMs/Mφ were isolated from patients with SA (n = 19) and those with NSA (n = 18) and treated with LPS/interferon-gamma. Monocyte/M1Mφ extracellular traps (MoETs/M1ETs) were evaluated by western blotting, immunofluorescence, and PicoGreen assay. The effects of MoETs/M1ETs on neutrophils, airway epithelial cells (AECs), ILC1, and ILC3 were assessed in vitro and in vivo. Results: The SA group had significantly higher CM counts with increased migration as well as higher levels of serum MCP-1/sST2 than the NSA group. Moreover, the SA group had significantly greater production of MoETs/M1ETs (from CMs/M1Mφ) than the NSA group. The levels of MoETs/M1ETs were positively correlated with blood neutrophils and serum levels of MCP-1/sST2, but negatively correlated with FEV1%. In vitro/in vivo studies demonstrated that MoETs/M1ETs could activate AECs, neutrophils, ILC1, and ILC3 by increased migration as well as proinflammatory cytokine production. Conclusions: CM/Mφ-derived MoETs/M1ETs could contribute to asthma severity by enhancing neutrophilic airway inflammation in SA, where modulating CMs/Mφ may be a potential therapeutic option. |
| first_indexed | 2024-03-08T16:52:28Z |
| format | Article |
| id | doaj.art-e5f1877010c34ad1a515f77e382f4ccf |
| institution | Directory Open Access Journal |
| issn | 1323-8930 |
| language | English |
| last_indexed | 2024-03-08T16:52:28Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Allergology International |
| spelling | doaj.art-e5f1877010c34ad1a515f77e382f4ccf2024-01-05T04:23:36ZengElsevierAllergology International1323-89302024-01-017318193Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthmaQuang Luu Quoc0Thi Bich Tra Cao1Ji-Young Moon2Jae-Hyuk Jang3Yoo Seob Shin4Youngwoo Choi5Min Sook Ryu6Hae-Sim Park7Department of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South Korea; Department of Biomedical Sciences, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South Korea; Department of Biomedical Sciences, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South KoreaDepartment of Allergy and Clinical Immunology, Ajou University School of Medicine, Suwon, South Korea; Department of Biomedical Sciences, Ajou University School of Medicine, Suwon, South Korea; Corresponding author. Department of Allergy and Clinical Immunology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South Korea. Worldcup-ro 164, Yeoungtong-gu, Suwon-si, South Korea.Background: Increased blood/sputum neutrophil counts are related to poor clinical outcomes of severe asthma (SA), where we hypothesized that classical monocytes (CMs)/CM-derived macrophages (Mφ) are involved. We aimed to elucidate the mechanisms of how CMs/Mφ induce the activation of neutrophils/innate lymphoid cells (ILCs) in SA. Methods: Serum levels of monocyte chemoattractant protein-1 (MCP-1) and soluble suppression of tumorigenicity 2 (sST2) were measured from 39 patients with SA and 98 those with nonsevere asthma (NSA). CMs/Mφ were isolated from patients with SA (n = 19) and those with NSA (n = 18) and treated with LPS/interferon-gamma. Monocyte/M1Mφ extracellular traps (MoETs/M1ETs) were evaluated by western blotting, immunofluorescence, and PicoGreen assay. The effects of MoETs/M1ETs on neutrophils, airway epithelial cells (AECs), ILC1, and ILC3 were assessed in vitro and in vivo. Results: The SA group had significantly higher CM counts with increased migration as well as higher levels of serum MCP-1/sST2 than the NSA group. Moreover, the SA group had significantly greater production of MoETs/M1ETs (from CMs/M1Mφ) than the NSA group. The levels of MoETs/M1ETs were positively correlated with blood neutrophils and serum levels of MCP-1/sST2, but negatively correlated with FEV1%. In vitro/in vivo studies demonstrated that MoETs/M1ETs could activate AECs, neutrophils, ILC1, and ILC3 by increased migration as well as proinflammatory cytokine production. Conclusions: CM/Mφ-derived MoETs/M1ETs could contribute to asthma severity by enhancing neutrophilic airway inflammation in SA, where modulating CMs/Mφ may be a potential therapeutic option.http://www.sciencedirect.com/science/article/pii/S1323893023000680AsthmaMacrophagesMonocytesNeutrophilsSevere asthma |
| spellingShingle | Quang Luu Quoc Thi Bich Tra Cao Ji-Young Moon Jae-Hyuk Jang Yoo Seob Shin Youngwoo Choi Min Sook Ryu Hae-Sim Park Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma Allergology International Asthma Macrophages Monocytes Neutrophils Severe asthma |
| title | Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| title_full | Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| title_fullStr | Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| title_full_unstemmed | Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| title_short | Contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| title_sort | contribution of monocyte and macrophage extracellular traps to neutrophilic airway inflammation in severe asthma |
| topic | Asthma Macrophages Monocytes Neutrophils Severe asthma |
| url | http://www.sciencedirect.com/science/article/pii/S1323893023000680 |
| work_keys_str_mv | AT quangluuquoc contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT thibichtracao contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT jiyoungmoon contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT jaehyukjang contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT yooseobshin contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT youngwoochoi contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT minsookryu contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma AT haesimpark contributionofmonocyteandmacrophageextracellulartrapstoneutrophilicairwayinflammationinsevereasthma |