Neutrophil ageing is regulated by the microbiome
Open accessAbstract
Blood polymorphonuclear neutrophils provide immune protection against pathogens, but may also promote tissue injury in inflammatory diseases. Although neutrophils are generally considered to be a relatively homogeneous population, evidence for heterogeneity is emerging. Under steady-state conditions, neutrophil heterogeneity may arise from ageing and replenishment by newly released neutrophils from the bone marrow. Aged neutrophils upregulate CXCR4, a receptor allowing their clearance in the bone marrow, with feedback inhibition of neutrophil production via the IL-17/G-CSF axis, and rhythmic modulation of the haematopoietic stem-cell niche. The aged subset also expresses low levels of L-selectin. Previous studies have suggested that in vitro-aged neutrophils exhibit impaired migration and reduced pro-inflammatory properties. Here, using in vivo ageing analyses in mice, we show that neutrophil pro-inflammatory activity correlates positively with their ageing whilst in circulation. Aged neutrophils represent an overly active subset exhibiting enhanced αMβ2 integrin activation and neutrophil extracellular trap formation under inflammatory conditions. Neutrophil ageing is driven by the microbiota via Toll-like receptor and myeloid differentiation factor 88-mediated signalling pathways. Depletion of the microbiota significantly reduces the number of circulating aged neutrophils and dramatically improves the pathogenesis and inflammation-related organ damage in models of sickle-cell disease or endotoxin-induced septic shock. These results identify a role for the microbiota in regulating a disease-promoting neutrophil subset.
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The relation between gut bacterial burden and systemic injury in shock has been reported consistently across species, types of shock, and decades of rigorous inquiry.
“This relation has been reported consistently across species (mice,90,93 rats,94 rabbits,89 and dogs87), types of shock (haemorrhage,87 sepsis,89 and ischaemia–reperfusion90), and decades of rigorous inquiry.”
From The microbiome and critical illness (2016) · cites this paper as [93]
When the bacterial burden of the gut is minimised, either by pretreatment with enteric antibiotics or by use of germ-free animals, the inflammation and injury sustained by distal organs in shock is lessened.
“When the bacterial burden of the gut is minimised, either by pretreatment with enteric antibiotics or by use of germ-free animals, the inflammation and injury sustained by distal organs in shock is lessened.”
From The microbiome and critical illness (2016) · cites this paper as [93]
During severe systemic illness such as sepsis or haemorrhagic shock, the bacterial content of the gut determines the severity of systemic injury.
“During severe systemic illness, such as sepsis or haemorrhagic shock, the bacterial content of the gut determines the severity of systemic injury”
From The microbiome and critical illness (2016) · cites this paper as [93]
These features of bacterial pneumonia correlate tightly with multiple indices of host inflammation, including alveolar neutrophilia and high alveolar concentrations of catecholamines and TNF-α.
“These features correlate tightly with multiple indices of host inflammation, including alveolar neutrophilia93 and high alveolar concentrations of catecholamines50 and TNF-α.”
From The microbiome and critical illness (2016) · cites this paper as [93]
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- Authors
- Zhang, D., Chen, G., Manwani, D., Mortha, A., Xu, C., Faith, J. J., Burk, R. D., Kunisaki, Y., Jang, J.-E., Scheiermann, C., Merad, M., & Frenette, P. S.
- Affiliations
- Albert Einstein College of Medicine (US)
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Frenette, Paul S.
- ORCID
- Venue
- Nature
- Published
- 2015-09
- Volume
- 525
- Issue
- 7570
- Pages
- 528-532
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4712631
- OpenAlex
- W2112671019
- Cited by
- 839
- References
- 34
- Citations by year
- 2026: 73 · 2025: 74 · 2024: 68 · 2023: 77 · 2022: 108 · 2021: 102 · 2020: 89 · 2019: 80 · 2018: 57 · 2017: 52 · 2016: 53 · 2015: 5
- FWCI
- 31.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- Memorial Sloan-Kettering Cancer Center
- Japan Society for the Promotion of Science (15K15364, 15H04859)
- National Heart, Lung, and Blood Institute (R01HL116340, R01HL069438)
- National Cancer Institute (R01CA173861, R01CA190400, R01CA154947)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK041296, R01DK056638)
- Topics
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- gut microbiota, sickle cell disease, vascular occlusion, Toll-like receptor signaling, MyD88, inflammation, septic shock, neutrophil heterogeneity, neutrophil extracellular traps, L-selectin, CXCR4
- MeSH terms
- Anemia, Sickle Cell, Animals, Disease Models, Animal, Erythrocytes, Abnormal, Inflammation, Male, Neutrophils, Shock, Septic, Signal Transduction, Macrophage-1 Antigen, Cellular Senescence, Toll-Like Receptors, Mice, Myeloid Differentiation Factor 88, Microbiota
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