Schistosoma japonicum Infection Leads to the Reprogramming of Glucose and Lipid Metabolism in the Colon of Mice

Xiaoying Yang; Weimin Ding; Xinyu Qian; Pengfei Jiang; Qingqing Chen; Xin Zhang; Yang Lu; Jiacheng Wu; Fenfen Sun; Zhihua Pan; Xiangyang Li; Wei Pan

doi:10.3389/fvets.2021.645807

Schistosoma japonicum Infection Leads to the Reprogramming of Glucose and Lipid Metabolism in the Colon of Mice

Front Vet Sci. 2021 Mar 10:8:645807. doi: 10.3389/fvets.2021.645807. eCollection 2021.

Authors

Xiaoying Yang^{1

2}, Weimin Ding^{1

2

3}, Xinyu Qian^{1

2

4}, Pengfei Jiang^{1

2}, Qingqing Chen^{1

2

4}, Xin Zhang^{1

2

4}, Yang Lu^{1

2

4}, Jiacheng Wu^{1

2

5}, Fenfen Sun^{1

2}, Zhihua Pan², Xiangyang Li^{1

2}, Wei Pan^{1

2}

Affiliations

¹ Jiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, China.
² National Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, China.
³ School of Life Sciences, Xuzhou Medical University, Xuzhou, China.
⁴ The First Clinical Medical College, Xuzhou Medical University, Xuzhou, China.
⁵ The Second Clinical Medical College, Xuzhou Medical University, Xuzhou, China.

Abstract

The deposition of Schistosoma japonicum (S. japonicum) eggs commonly induces inflammation, fibrosis, hyperplasia, ulceration, and polyposis in the colon, which poses a serious threat to human health. However, the underlying mechanism is largely neglected. Recently, the disorder of glucose and lipid metabolism was reported to participate in the liver fibrosis induced by the parasite, which provides a novel clue for studying the underlying mechanism of the intestinal pathology of the disease. This study focused on the metabolic reprogramming profiles of glucose and lipid in the colon of mice infected by S. japonicum. We found that S. japonicum infection shortened the colonic length, impaired intestinal integrity, induced egg-granuloma formation, and increased colonic inflammation. The expression of key enzymes involved in the pathways regulating glucose and lipid metabolism was upregulated in the colon of infected mice. Conversely, phosphatase and tensin homolog deleted on chromosome ten (PTEN) and its downstream signaling targets were significantly inhibited after infection. In line with these results, in vitro stimulation with soluble egg antigens (SEA) downregulated the expression of PTEN in CT-26 cells and induced metabolic alterations similar to that observed under in vivo results. Moreover, PTEN over-expression prevented the reprogramming of glucose and lipid metabolism induced by SEA in CT-26 cells. Overall, the present study showed that S. japonicum infection induces the reprogramming of glucose and lipid metabolism in the colon of mice, and PTEN may play a vital role in mediating this metabolic reprogramming. These findings provide a novel insight into the pathogenicity of S. japonicum in hosts.

Keywords: PTEN; Schistosoma japonicum; colon; glucose and lipid metabolism; soluble egg antigens.