Immune function modulation during artificial ovarian maturation in Japanese eel (Anguilla japonica): A transcriptome profiling approach

Abstract

The Japanese eel (Anguilla japonica) experiences dramatic internal and external environmental changes during its transoceanic reproductive migrations. Here, we assess immune function changes in the primary and secondary immune organs (head kidney and spleen) of A. japonica during artificial ovarian maturation at the previtellogenic (PV), midvitellogenic (MV), and ovulating (OV) stages by transcriptome analyses. Stress responses were also assessed by determining the serum concentrations of lysozyme, alkaline phosphatase, acid phosphatase, total antioxidant capacity, and superoxide dismutase. Our results showed that together with increased serum 17β-estrogen and testosterone, lysozyme activity and antioxidant capacity were suppressed during artificial ovarian maturation. Comparisons across these developmental stages identified 60 (head kidney) and 36 (spleen) differentially expressed genes associated with the immune system. Genes related to the key activation markers of innate immune function, such as CXCL10, CXCL11, CCL20, HSP90B, MMP9, and MMP13, were upregulated and significantly enriched in the interleukin-17 signaling pathway. Adaptive immune function-related genes (IGM and MHC1) were upregulated in the head kidney from PV to MV, and their levels increased thereafter in the spleen. Moreover, a correlation between Pax5 expression and IGM expression in the spleen of MV (IGM+/Pax5+) and OV (IGM++/Pax5−) stage suggests that adaptive immune function was enhanced during ovarian maturation. To our knowledge, the present study is the first to describe transcriptome profiling of immune organs during ovarian maturation in teleost. Our findings suggest that the interleukin-17 pathway and IgM may play important roles in spawning.