Identification and characterization of three CXC chemokines in Asian swamp eel (Monopterus albus) uncovers a third CXCL11_like group in fish

Abstract

Chemokines direct cell migration in development and immune defense, and bridge between innate and adaptive immune responses. The chemokine gene family has been rapidly evolving and has undergone species/lineage-specific expansion. Mammals possess inflammatory CXC chemokines CXCL1-8/15 and CXCL9-11 sub-groups, and homeostatic CXCL12-14, 16–17. Orthologues of mammalian CXCL12-14, three chemokines related to CXCL1-8/15 (CXCL8_L1-3), two chemokines related to CXC9-11 (CXCL11_L1-2), and five fish-specific chemokines (CXCL_F1-5) have been described in teleosts. In this study, we reported three novel CXC chemokines in Asian swamp eel Monopterus albus, a commercially important freshwater fish species in China. Two of them belong to the fish-specific CXCL_F2 group, named CXCL_F2a/b, that share 89.5% amino acid identity. The other (CXCL11_L3) belongs to a third CXCL11_L related to the mammalian CXCL9-11 subfamily found only in percomorph fish species, and is the only CXCL9-11 related molecules in this lineage. Mammalian CXCL9-11 attract Th1 cells, and block the migration of Th2 cells in an immune response. This study suggests that all major lineages of teleosts have a CXCL9-11 related chemokine that will aid future functional investigation of CXCL11_L in fish. Cxcl_f2a is highly expressed constitutively in the skin of swamp eels that may attract immune cells to protect the skin in the absence of scales. Cxcl11_l3 and cxcl_f2b are highly expressed in immune tissues/organs and are up-regulated by the viral mimic poly I:C, but not bacterial infection in vivo, suggesting their role in anti-viral defense. The two cxcl_f2 paralogues are differentially expressed and modulated, indicating sub- and/or neo-functionalization.