Swimming Impedes Intestinal Microbiota and Lipid Metabolites of Tumorigenesis in Colitis-Associated Cancer

Weiyi Wang; Ying Xu; Xiaofeng Wang; Yimin Chu; Haiqin Zhang; Lu Zhou; Haijin Zhu; Ji Li; Rong Kuai; Fengli Zhou; Daming Yang; Haixia Peng

doi:10.3389/fonc.2022.929092

Swimming Impedes Intestinal Microbiota and Lipid Metabolites of Tumorigenesis in Colitis-Associated Cancer

Front Oncol. 2022 Jul 1:12:929092. doi: 10.3389/fonc.2022.929092. eCollection 2022.

Authors

Weiyi Wang¹, Ying Xu¹, Xiaofeng Wang¹, Yimin Chu¹, Haiqin Zhang¹, Lu Zhou¹, Haijin Zhu¹, Ji Li¹, Rong Kuai¹, Fengli Zhou¹, Daming Yang¹, Haixia Peng¹

Affiliation

¹ Department of Endoscopy, Shanghai Tong Ren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Abstract

Background: Accumulating data support that regular physical activity potentially inhibits chronic colitis, a risk factor for colitis-associated cancer (CAC). However, possible effects of physical activity on CAC and the underlying mechanisms remain poorly understood.

Methods: A pretreatment of swimming on azoxymethane/dextran sodium sulfate (AOM/DSS)-induced CAC mice was implemented to determine its protective effect. Inflammation and tumorigenesis were assessed using colorectums from C57BL/6 mice. In order to determine how swimming alters colonic lipid metabolism and gene expression, a comparative analysis was conducted. Meanwhile, alterations in intestinal microbiota and short-chain fatty acids (SCFAs) were detected and analyzed. Finally, an integration analysis of colonic lipid metabolism with gene expression and intestinal microbiota was performed respectively.

Result: Swimming pretreatment relieved bowel inflammation and minimized tumor formation. We demonstrated that prostaglandin E2 (PGE2)/PGE2 receptor 2 subtype (EP2) signaling as a potential regulatory target for swimming induces colonic lipid metabolites. Swimming-induced genera, Erysipelatoclostridium, Parabacteroides, Bacteroides, and Rikenellaceae_RC9_gut_group, induced intestinal SCFAs and affected the function of colonic lipid metabolites enriched in glycerophospholipid metabolism and choline metabolism in cancer.

Conclusion: According to our experiments, swimming pretreatment can protect mice from CAC by intervention in the possible link between colonic lipid metabolites and PGE2/EP2 signaling. Further, swimming-induced genera and probiotics promoted glycerophospholipid metabolism and choline metabolism in cancer, the major constituents of colonic lipid metabolites, and increased SCFAs, which were also important mechanisms for the anti-inflammatory and anti-tumorigenic effects of swimming.

Keywords: chronic inflammation; colonic lipid metabolites; colorectal cancer; intestinal microbiota; physical activity; swimming; tumorigenesis.