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Fusobacterium nucleatum Aggravates the Progression of Colitis by Regulating M1 Macrophage Polarization via AKT2

Le Liu¹, Liping Liang¹, Huifen Liang¹

¹Guangdong Provincial Key Laboratory of Gastroenterology, State Key Laboratory of Organ Failure Research, Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, China.

Frontiers in Immunology

|June 29, 2019

Abstract:

Disordered intestinal flora and discordant immune response are associated with the development of ulcerative colitis (UC). Recent work has described the ability of macrophages to undergo repolarization toward a proinflammatory M1 or anti-inflammatory M2 phenotype in response to particular bacterium-derived signals. Fusobacterium nucleatum (F. nucleatum, Fn) is a species of intestinal commensal bacteria with potential pathogenicity, but its association with UC and how it may contribute to progression of UC is largely unknown. In this study, we provide new evidence that F. nucleatum accumulated heavily in the intestine of UC patients and was accompanied by the secretion of IFN-γ and the skewing of M1 macrophages. Mechanistically, our data showed that F. nucleatum aggravated dextran sodium sulfate (DSS)-induced colitis in the production of Th1-related cytokines IFN-γ through the AKT2 signaling pathway in vitro and in vivo. To further confirm the disease-relevance of these shifts in macrophage repolarization in response to F. nucleatum, stimulated bone marrow-derived macrophages (BMDMs) were transferred into recipient mice with DSS colitis. This transfer resulted in increased disease activity and inflammatory cytokine production. Taken together, we show clearly that F. nucleatum can promote the progression of UC via proinflammatory M1 macrophage skewing, and targeting F. nucleatum or AKT2 signaling may be a viable means of blocking development of UC.

Insights

Fusobacterium nucleatum accumulation in the gut promotes ulcerative colitis (UC) by driving M1 macrophage polarization and IFN-γ production. Targeting this bacterium or AKT2 signaling may offer new UC treatments.

Area of Science:

Gastroenterology and Immunology
Microbiome Research
Inflammatory Bowel Disease Pathogenesis

Background:

Ulcerative colitis (UC) is linked to gut dysbiosis and immune dysregulation.
Macrophages can polarize into pro-inflammatory (M1) or anti-inflammatory (M2) phenotypes.
The role of Fusobacterium nucleatum (F. nucleatum) in UC progression is unclear.

Purpose of the Study:

To investigate the association of F. nucleatum with UC.
To elucidate the mechanisms by which F. nucleatum influences intestinal inflammation and macrophage polarization in UC.

Main Methods:

Quantification of F. nucleatum in UC patient intestines.
In vitro and in vivo studies using dextran sodium sulfate (DSS)-induced colitis models.
Analysis of cytokine production (IFN-γ) and macrophage polarization.
Investigation of the AKT2 signaling pathway.
Adoptive transfer of F. nucleatum-stimulated bone marrow-derived macrophages (BMDMs) in mice.

Main Results:

F. nucleatum was significantly elevated in UC patients' intestines.
F. nucleatum promoted Th1 cytokine IFN-γ production and M1 macrophage skewing in DSS-induced colitis.
The AKT2 signaling pathway mediated F. nucleatum-induced IFN-γ production.
Transfer of F. nucleatum-stimulated BMDMs exacerbated colitis severity and inflammation in recipient mice.

Conclusions:

F. nucleatum promotes UC progression by inducing proinflammatory M1 macrophage polarization.
Targeting F. nucleatum or the AKT2 signaling pathway presents potential therapeutic strategies for UC.

Read full analysis

Keywords:

Fusobacterium nucleatum M1 macrophage gut microbiota mucosal barrier ulcerative colitis

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