A novel third complement component C3 gene of Ciona intestinalis expressed in the endoderm at the early developmental stages

Abstract

The third complement component (C3) in ascidian was reported to function as an opsonin to
enhance phagocytosis and as a chemotactic factor for phagocytes, indicating that ascidian C3 works in mesodermal cavity as a humoral factor like vertebrate C3s. In the basal Eumetazoa, Cnidaria lacking mesodermal tissues, C3 was reported to work in an endodermal cavity. Evolution of structure and function of C3 is still to be clarified. Here we report the identification of the third C3 gene, CiC3-3, in the genome of an ascidian, Ciona intestinalis. Phylogenetic analysis using the entire amino acid sequences of Eumetazoan C3s indicated that CiC3-3 possess a closer relationship to vertebrate C3, C4 and C5 than other ascidian C3s. Although CiC3-3 retained the α-β processing site and 6 cysteine residues in the C3a region, it lacked the intra-molecular thioester bond and the catalytic histidine residue. Instead, CiC3-3 had a unique insertion of about 70 residues long Lys/Arg-rich sequence. CiC3-3 was expressed highly in the embryonic stages, but little in the adult in contradistinction to CiC3-1 and CiC3-2. The expression of CiC3-3 in early embryonic stages was restricted to endoderm similar to cnidarian C3s. Thus, the ascidian complement system could represent a unique evolutionary stage sharing a primitive endodermal function with Cnidaria, and newly developed humoral function with vertebrates.