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Molecular evolution of kalliklectin in teleost and identification of the novel type with eight apple domains in channel catfish, Ictalurus punctatus

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Abstract

Kalliklectin is a unique fish-specific lectin that demonstrates sequence similarity to mammalian plasma kallikrein and coagulation factor XI, which are not lectins but proteases. Reported fish kalliklectins and these mammalian proteases comprise four characteristic “apple domains” (APDs). Bioinformatics analysis revealed that Siluriformes species possess anomalous kalliklectins comprising 6 to 16 APDs. Complementary DNA cloning showed that the full-length nucleotide sequence of Ictalurus punctatus consists of 2240 bp that encode 720 amino acid residues to produce a mature protein with a putative 18 amino acid N-terminus peptide sequence. This protein has a predicted molecular mass of 83,417.23 Da. Reverse transcription-polymerase chain reaction (RT-PCR) showed that this lectin gene expresses in the liver but not in any other tissues, including the mucosal tissues. This differential expression pattern makes this lectin unique compared to other lectins described in previous studies. We successfully detected an 85-kDa protein in the serum using western blotting analysis, suggesting that this lectin protein is produced by the liver and secreted into the bloodstream. We characterized a novel cDNA sequence encoding a new type of kalliklectin with eight APDs isolated from channel catfish, I. punctatus. Based on phylogenetic analysis, we speculated that there was a duplication of the third and fourth APD set in a common Siluriformes ancestor at some point after its separation from the common teleost ancestor and that these duplications then underwent independent repeats in different lineages resulting in the generation of the [APD1]-[APD2]-{[APD3]-[APD-4]} × n structure in modern catfishes.

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Acknowledgements

We thank Namazuya Inc., a fish farm in Lake Kasumigaura, Ibaraki, Japan, for providing animals.

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Authors and Affiliations

  1. School of Marine Biosciences, Kitasato University, 1-15-1 Kitasato, Minami-ku, Sagamihara, Kanagawa, 252-0373, Japan

    Shigeyuki Tsutsui, Asuka Yoshimura, Yoshimi Kawakami & Osamu Nakamura

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  1. Shigeyuki Tsutsui
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  2. Asuka Yoshimura
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  3. Yoshimi Kawakami
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  4. Osamu Nakamura
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Contributions

ST designed the study. ST performed bioinfomatic analysis and cDNA cloning. AY took care of PCR and western blot analyses. YK discovered the new type for the first time. ST wrote the paper with input from all authors. ON discussed the results and commented on the manuscript.

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Correspondence to Shigeyuki Tsutsui.

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The authors have no conflicts of interest directly relevant to the content of this article.

Ethical approval

This study was approved by the Kitasato University Safety Committee for Recombinant DNA Experiments (Permission Number: 4536).

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Tsutsui, S., Yoshimura, A., Kawakami, Y. et al. Molecular evolution of kalliklectin in teleost and identification of the novel type with eight apple domains in channel catfish, Ictalurus punctatus. Mol Biol Rep 48, 4305–4318 (2021). https://doi.org/10.1007/s11033-021-06446-2

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