Impact of smoking on gut microbiota and short-chain fatty acids in human and mice: Implications for COPD
We aimed to elucidate the dynamic changes in short-chain fatty acids (SCFA) produced by the gut microbiota following smoking exposure and their role in chronic obstructive pulmonary disease (COPD) pathogenesis. SCFA concentrations were measured in human plasma, comparing non-smokers (n = 6) and smokers (n = 12). Using a mouse COPD model induced by cigarette smoke exposure or elastase-induced emphysema, we modulated SCFA levels through dietary interventions and antibiotics to evaluate their effects on inflammation and alveolar destruction. Human smokers showed lower plasma SCFA concentrations than non-smokers, with plasma propionic acid positively correlating with forced expiratory volume in 1 s/forced vital capacity. Three-month smoking-exposed mice demonstrated altered gut microbiota and significantly reduced fecal SCFA concentrations compared to air-exposed controls. In these mice, a high-fiber diet increased fecal SCFAs and mitigated inflammation and alveolar destruction, while antibiotics decreased fecal SCFAs and exacerbated disease features. However, in the elastase-induced model, fecal SCFA concentration remained unchanged, and high-fiber diet or antibiotic interventions had no significant effect. These findings suggest that smoking exposure alters gut microbiota and SCFA production through its systemic effects. The anti-inflammatory properties of SCFAs may play a role in COPD pathogenesis, highlighting their potential as therapeutic targets.
Authors
- Junki Miyamoto (ORCID: https://orcid.org/0000-0002-6994-1787)
- Ikuo Kimura (ORCID: https://orcid.org/0000-0001-8778-145X)
- Shinichi Okuzumi
- Yuri Haneishi
- Hiroki Kabata (ORCID: https://orcid.org/0000-0001-8853-6149)
- Takanori Asakura (ORCID: https://orcid.org/0000-0003-3122-6937)
- Jun Miyata (ORCID: https://orcid.org/0000-0002-3189-1702)
- Koichi Fukunaga (ORCID: https://orcid.org/0000-0001-7460-1990)
- Koichiro Asano (ORCID: https://orcid.org/0000-0002-9044-3061)
- Junichiro Irie (ORCID: https://orcid.org/0000-0003-2662-4121)
- Hidetoshi Nakamura (ORCID: https://orcid.org/0000-0001-7434-9764)
- Shotaro Chubachi (ORCID: https://orcid.org/0000-0002-5046-3762)
- Takashi Shimada (ORCID: https://orcid.org/0000-0001-7182-7003)
- Tetsuya Arai
- Kaori Sakurai (ORCID: https://orcid.org/0000-0002-1565-781X)
- Shiro Otake
- Hideto Izuka
Institutions
- Tokai University (JP)
- Keio University (JP)
- Kyoto University (JP)
- Kitasato Institute Hospital (JP)
- Kitasato University (JP)
- Saitama Medical University (JP)
- Tokyo University of Agriculture and Technology (JP)
Publication Details
- Journal
- Mucosal Immunology
- Published
- 2024-12-13
- DOI
- https://doi.org/10.1016/j.mucimm.2024.12.006
- Citations
- 14
- Primary Topic
- Gut microbiota and health
- Type
- article
- Field-Weighted Citation Impact
- 3.27
Funders
- Novartis Foundation
- Keio University
- Secom Science and Technology Foundation
- Tokyo University of Agriculture
- Tokyo University of Agriculture and Technology
- NOVARTIS Foundation (Japan) for the Promotion of Science