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Cited by 476

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Transmigrating Neutrophils Shape the Mucosal Microenvironment through Localized Oxygen Depletion to Influence Resolution of Inflammation

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Campbell, Eric L., Bruyninckx, Walter J., Kelly, Caleb J., Glover, Louise E., McNamee, Eóin N., Bowers, Brittelle E., Bayless, Amanda J., Scully, Melanie, Saeedi, Bejan J., Golden-Mason, Lucy, Ehrentraut, Stefan F., Curtis, Valerie F., Burgess, Adrianne, Garvey, John F., Sorensen, Amber, Nemenoff, Raphael, Jedlicka, Paul, Taylor, Cormac T., Kominsky, Douglas J., Colgan, Sean P.·2014·Immunity
DOI 10.1016/j.immuni.2013.11.020
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Abstract

SUMMARY Acute intestinal inflammation involves early accumulation of neutrophils (PMN) followed by either resolution or progression to chronic inflammation. Based on recent evidence mucosal metabolism influences disease outcomes, we hypothesized that transmigrating PMN influence the transcriptional profile of the surrounding mucosa. Microarray studies revealed a cohort of hypoxia-responsive genes regulated by PMN-epithelial crosstalk. Transmigrating PMN rapidly depleted microenvironmental O2 sufficiently to stabilize intestinal epithelial cell hypoxia-inducible factor (HIF). Utilizing HIF reporter mice in an acute colitis model, we investigated the relative contribution of PMN and the respiratory burst to “inflammatory hypoxia” in vivo. CGD mice, lacking a respiratory burst, developed accentuated colitis compared to control, with exaggerated PMN infiltration and diminished inflammatory hypoxia. Finally, pharmacological HIF stabilization within the mucosa protected CGD mice from severe colitis. In conclusion, transcriptional imprinting by infiltrating neutrophils modulates the host response to inflammation, via localized O2 depletion, resulting in microenvironmental hypoxia and effective inflammatory resolution.

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Show all 10 references

Research works printed but not linked: 32

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Metadata

Authors
Campbell, E. L., Bruyninckx, W. J., Kelly, C. J., Glover, L. E., McNamee, E. N., Bowers, B. E., Bayless, A. J., Scully, M., Saeedi, B. J., Golden-Mason, L., Ehrentraut, S. F., Curtis, V. F., Burgess, A., Garvey, J. F., Sorensen, A., Nemenoff, R., Jedlicka, P., Taylor, C. T., Kominsky, D. J., & Colgan, S. P.
Venue
Immunity
Publisher
Elsevier BV
Published
2014-01
Volume
40
Issue
1
Pages
66-77
ISSN
1074-7613 (ISSN-L)
DOI
10.1016/j.immuni.2013.11.020
OpenAlex
W2067659428
Cited by
476
References
10
FWCI
18.67
Type
journal article
Language
en
Open access
bronze
Licence

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CoChat. (2026). Citation check: Transmigrating Neutrophils Shape the Mucosal Microenvironment through Localized Oxygen Depletion to Influence Resolution of Inflammation. https://app.cochat.ai/papers/10.1016/j.immuni.2013.11.020
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Campbell, E. L., Bruyninckx, W. J., Kelly, C. J., Glover, L. E., McNamee, E. N., Bowers, B. E., Bayless, A. J., Scully, M., Saeedi, B. J., Golden-Mason, L., Ehrentraut, S. F., Curtis, V. F., Burgess, A., Garvey, J. F., Sorensen, A., Nemenoff, R., Jedlicka, P., Taylor, C. T., Kominsky, D. J., & Colgan, S. P. (2014). Transmigrating Neutrophils Shape the Mucosal Microenvironment through Localized Oxygen Depletion to Influence Resolution of Inflammation. Immunity. https://doi.org/10.1016/j.immuni.2013.11.020

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Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.