A type 2 immune circuit and arachidonic acid metabolism role in anti-nematode infection: evidence from transcriptome and targeted metabolome data in goat
W.X. Chen,
Q.X. Yan,
R.Z. Zhong,
S.X. Tang,
J.J. Loor,
Z.L. Tan
Affiliations
W.X. Chen
CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, the Chinese Academy of Sciences, Changsha, Hunan 410125, PR China; Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University, Wuhan 430023, PR China
Q.X. Yan
CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, the Chinese Academy of Sciences, Changsha, Hunan 410125, PR China; Corresponding author.
R.Z. Zhong
Jilin Provincial Key Laboratory of Grassland Farming, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, Jilin, PR China
S.X. Tang
CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, the Chinese Academy of Sciences, Changsha, Hunan 410125, PR China
J.J. Loor
Department of Animal Sciences, Division of Nutritional Sciences, University of Illinois, Urbana, IL 61801, USA
Z.L. Tan
CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, the Chinese Academy of Sciences, Changsha, Hunan 410125, PR China
The gastrointestinal nematode infection poses a covert threat to both humans and domestic animals worldwide, eliciting a type 2 immune response within the small intestine. Intestinal tuft cells detect the nematode and activated group 2 innate lymphoid cells. Tuft cell−derived leukotrienes (one of the metabolites of arachidonic acid) were found to drive rapid anti-helminth immunity, but it is still poorly understood whether the tuft cell−mediated type 2 immune circuit and arachidonic acid metabolism modulate anti-parasitic immunity in the gastric epithelium. This study was designed to evaluate the immunological responses of goats inoculated with or without H. contortus. Results showed that H. contortus infection induced a systemic type 2 immune response, characterised by lymphocyte proliferation and greater eosinophils both in peripheral blood and abomasal mucosa, as well as increased type 2 cytokines IL-4, IL-5, and IL-13. Infection of H. contortus altered the transcriptome of the abomasum epithelium, especially tuft cell−mediated circuit-key genes. The infection also influenced the abomasal microbiota, arachidonic acid metabolism and related lipid metabolites, accompanying with great increases in the secretion of leukotrienes and prostaglandins. These findings demonstrate the role of tuft cells mediated circuit in sensing H. contortus infection and immune activation, reveal the candidate function of arachidonic acid involved in anti-helminth immunity, and suggest novel strategies for the control of parasitic diseases in livestock and humans.