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Structure and the evolutionary implication of the triplicated complement factor B genes of a urochordate ascidian, Ciona intestinalis

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Abstract

To elucidate the evolution of the complement system and MHC class III region, we analyzed the complement factor B (Bf) genes of a urochordate ascidian, Ciona intestinalis. Three different cDNA species, termed CiBf-1, CiBf-2 and CiBf-3, were identified. The deduced amino-acid sequences all contained the usual domains of vertebrate Bf and, in addition, three extra domains at the N-terminus. Furthermore, the serine protease domain of these CiBfs shared unique features with vertebrate complement components C1r/s and mannose-binding lectin-associated serine protease (MASP)-2/3, the absence of the disulfide bond designated histidine loop, and the usage of the AGY codon for the catalytic serine residue. These results indicate that complement genes have evolved through extensive exon shuffling events in the early stage of chordate evolution. Overall deduced amino-acid identity between CiBf-1 and -2 was 88%, whereas CiBf-3 showed 49% identity to both CiBf-1 and CiBf-2. These three CiBf genes were located within an approximately 50-kb genomic region, and exons 3 and 5 of all the three Bf genes showed an extremely high degree of nucleotide identity, indicating that the CiBf genes experienced extensive reorganization, such as duplication and gene conversion, since its divergence from the vertebrate Bf/C2 gene. Fluorescent in situ hybridization (FISH) to the chromosomes showed that genetic loci for the CiBfs, CiC3-1 and CiC3-2 genes are present on three different chromosomes, suggesting the possibility that the linkage among the MHC class III complement genes was established in the vertebrate lineage after its divergence from urochordates.

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Acknowledgements

We thank Dr. Kaoru Azumi for supplying Ciona hemocyte RNA, Dr. Mari Kobayashi for supplying Ciona BAC clones, Dr. Yuji Kohara for supplying the ciad66f24 clone, Dr. Mariko Kondo for critical reading of the manuscript, Dr. Masanori Taira for allowing us to use the microscope, Mr. Tetsuro Ikuta and Dr. Hidetoshi Saiga for giving instruction in FISH technique, and the staff of the Misaki Marine Biological Station for supplying and keeping ascidians. This work was supported by grant no. 15207019 to M.N. from the Ministry of Education, Culture, Sports, Science and Technology of Japan

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Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, 113-0033, Japan

    Fumiko Y. Yoshizaki & Masaru Nonaka

  2. Institute of Development, Aging and Cancer, Tohoku University, Sendai, 980-8575, Japan

    Shuntaro Ikawa & Masanobu Satake

  3. Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan

    Nori Satoh

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  1. Fumiko Y. Yoshizaki
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  2. Shuntaro Ikawa
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  3. Masanobu Satake
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  4. Nori Satoh
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  5. Masaru Nonaka
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Correspondence to Masaru Nonaka.

Additional information

The sequences reported in this paper have been deposited in the DDBJ database (accession nos. AB180044–AB180051).

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Yoshizaki, F.Y., Ikawa, S., Satake, M. et al. Structure and the evolutionary implication of the triplicated complement factor B genes of a urochordate ascidian, Ciona intestinalis. Immunogenetics 56, 930–942 (2005). https://doi.org/10.1007/s00251-004-0752-4

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