Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells

<b>Objectives:</b> In the present study, we aimed to clarify the mechanisms by which periodontal pathogens, particularly <i>Prevotella intermedia</i>, induce severe neutrophilic inflammation. In addition, we aimed to test the efficacy of macrolides, which has not been resolve...

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Main Authors: Naoki Iwanaga, Ayaka Ota, Hiroki Ashizawa, Yuya Ito, Tatsuro Hirayama, Masataka Yoshida, Kazuaki Takeda, Shotaro Ide, Masato Tashiro, Naoki Hosogaya, Noriho Sakamoto, Takahiro Takazono, Kosuke Kosai, Mariko Naito, Yoshimasa Tanaka, Kazuhiro Yatera, Koichi Izumikawa, Katsunori Yanagihara, Hiroshi Mukae
Format: Article
Language:English
Published: MDPI AG 2024-09-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/13/9/909
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author Naoki Iwanaga
Ayaka Ota
Hiroki Ashizawa
Yuya Ito
Tatsuro Hirayama
Masataka Yoshida
Kazuaki Takeda
Shotaro Ide
Masato Tashiro
Naoki Hosogaya
Noriho Sakamoto
Takahiro Takazono
Kosuke Kosai
Mariko Naito
Yoshimasa Tanaka
Kazuhiro Yatera
Koichi Izumikawa
Katsunori Yanagihara
Hiroshi Mukae
author_facet Naoki Iwanaga
Ayaka Ota
Hiroki Ashizawa
Yuya Ito
Tatsuro Hirayama
Masataka Yoshida
Kazuaki Takeda
Shotaro Ide
Masato Tashiro
Naoki Hosogaya
Noriho Sakamoto
Takahiro Takazono
Kosuke Kosai
Mariko Naito
Yoshimasa Tanaka
Kazuhiro Yatera
Koichi Izumikawa
Katsunori Yanagihara
Hiroshi Mukae
author_sort Naoki Iwanaga
collection DOAJ
description <b>Objectives:</b> In the present study, we aimed to clarify the mechanisms by which periodontal pathogens, particularly <i>Prevotella intermedia</i>, induce severe neutrophilic inflammation. In addition, we aimed to test the efficacy of macrolides, which has not been resolved in the neutrophilic inflammation induced by <i>P. intermedia</i>. <b>Methods:</b> NCl-H292 human airway epithelial cells were pre-incubated with clarithromycin for 2 h before incubation with <i>P. intermedia</i> supernatants. Then, C-X-C motif chemokine ligand 8 (<i>CXCL8</i>) transcription and interleukin (IL)-8 production were measured. To elucidate the signaling pathway, mitogen-activated protein kinase inhibitors were added to the cell culture, and the cells were subjected to Western blotting. <b>Results:</b><i>P. intermedia</i> supernatants promoted <i>CXCL8</i> transcription and IL-8 production, and the reactions were significantly suppressed by clarithromycin pretreatment. Only trametinib, the selective mitogen-activated extracellular signal-regulated kinase inhibitor, downregulated <i>CXCL8</i> transcription and IL-8 production. Furthermore, Western blotting revealed that stimulation with <i>P. intermedia</i> supernatants specifically induces extracellular signal-regulated kinases (ERK) 1/2 phosphorylation, which is suppressed by clarithromycin pretreatment. Notably, the interference analysis revealed that ERK3 might be dispensable for IL-8 production under the stimulation of <i>P. intermedia</i> supernatants. <b>Conclusions:</b> Our results provide new insight into the mechanism underlying <i>P. intermedia</i>-induced production of IL-8 from human airway epithelial cells. Furthermore, macrolides might have therapeutic potential in regulating periodontal pathogen-induced neutrophilic inflammation in the lungs.
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spelling doaj-art-a3b2725af27243d4a7def22c9111aa132025-08-20T01:55:57ZengMDPI AGAntibiotics2079-63822024-09-0113990910.3390/antibiotics13090909Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial CellsNaoki Iwanaga0Ayaka Ota1Hiroki Ashizawa2Yuya Ito3Tatsuro Hirayama4Masataka Yoshida5Kazuaki Takeda6Shotaro Ide7Masato Tashiro8Naoki Hosogaya9Noriho Sakamoto10Takahiro Takazono11Kosuke Kosai12Mariko Naito13Yoshimasa Tanaka14Kazuhiro Yatera15Koichi Izumikawa16Katsunori Yanagihara17Hiroshi Mukae18Department of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Pharmacotherapeutics, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Pharmacotherapeutics, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Infectious Diseases Experts Training Center, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Infectious Diseases, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Laboratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Microbiology and Oral Infection, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8501, JapanCenter for Medical Innovation, Nagasaki University, Nagasaki 852-8588, JapanDepartment of Respiratory Medicine, University of Occupational and Environmental Health, Kitakyushu 807-8555, JapanDepartment of Infectious Diseases, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8501, JapanDepartment of Laboratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, JapanDepartment of Respiratory Medicine, Nagasaki University Hospital, Nagasaki 852-8501, Japan<b>Objectives:</b> In the present study, we aimed to clarify the mechanisms by which periodontal pathogens, particularly <i>Prevotella intermedia</i>, induce severe neutrophilic inflammation. In addition, we aimed to test the efficacy of macrolides, which has not been resolved in the neutrophilic inflammation induced by <i>P. intermedia</i>. <b>Methods:</b> NCl-H292 human airway epithelial cells were pre-incubated with clarithromycin for 2 h before incubation with <i>P. intermedia</i> supernatants. Then, C-X-C motif chemokine ligand 8 (<i>CXCL8</i>) transcription and interleukin (IL)-8 production were measured. To elucidate the signaling pathway, mitogen-activated protein kinase inhibitors were added to the cell culture, and the cells were subjected to Western blotting. <b>Results:</b><i>P. intermedia</i> supernatants promoted <i>CXCL8</i> transcription and IL-8 production, and the reactions were significantly suppressed by clarithromycin pretreatment. Only trametinib, the selective mitogen-activated extracellular signal-regulated kinase inhibitor, downregulated <i>CXCL8</i> transcription and IL-8 production. Furthermore, Western blotting revealed that stimulation with <i>P. intermedia</i> supernatants specifically induces extracellular signal-regulated kinases (ERK) 1/2 phosphorylation, which is suppressed by clarithromycin pretreatment. Notably, the interference analysis revealed that ERK3 might be dispensable for IL-8 production under the stimulation of <i>P. intermedia</i> supernatants. <b>Conclusions:</b> Our results provide new insight into the mechanism underlying <i>P. intermedia</i>-induced production of IL-8 from human airway epithelial cells. Furthermore, macrolides might have therapeutic potential in regulating periodontal pathogen-induced neutrophilic inflammation in the lungs.https://www.mdpi.com/2079-6382/13/9/909<i>Prevotella intermedia</i>clarithromycinhuman airway epithelial cells
spellingShingle Naoki Iwanaga
Ayaka Ota
Hiroki Ashizawa
Yuya Ito
Tatsuro Hirayama
Masataka Yoshida
Kazuaki Takeda
Shotaro Ide
Masato Tashiro
Naoki Hosogaya
Noriho Sakamoto
Takahiro Takazono
Kosuke Kosai
Mariko Naito
Yoshimasa Tanaka
Kazuhiro Yatera
Koichi Izumikawa
Katsunori Yanagihara
Hiroshi Mukae
Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
Antibiotics
<i>Prevotella intermedia</i>
clarithromycin
human airway epithelial cells
title Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
title_full Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
title_fullStr Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
title_full_unstemmed Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
title_short Clarithromycin Modulates Neutrophilic Inflammation Induced by <i>Prevotella intermedia</i> in Human Airway Epithelial Cells
title_sort clarithromycin modulates neutrophilic inflammation induced by i prevotella intermedia i in human airway epithelial cells
topic <i>Prevotella intermedia</i>
clarithromycin
human airway epithelial cells
url https://www.mdpi.com/2079-6382/13/9/909
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