Identification and characterization of WpDestabilase, a novel destabilase from the salivary glands of Whitmania pigra

Whitmania pigra is one of the primary sources of leeches used in traditional Chinese medicine, renowned for its anticoagulant and thrombolytic properties. In this study, a salivary gland transcriptome database of W. pigra was constructed, and 7 anticoagulation-related transcripts were identified, one of which was designated as "WpDestabilase". The unigenes producing these transcripts were functionally annotated to proteins with potential pharmacological activities, including fibrinolytic enzymes, neutrophil elastase inhibitors, elastase inhibitors, and factor Xa inhibitors. The cDNA sequence of the WpDestabilase gene (TRINITY_DN17453_c0_g1) showed significant homology to Destabilase I from Hirudo medicinalis, and its TPM value was significantly higher than that of the other identified transcripts. The WpDestabilase cDNA is 450 bp in length, encoding a protein of 149 amino acids. The amino acid sequence of the mature WpDestabilase protein contains seven disulfide bonds and a motif CTGGRTPTCQDYARIHxGGP, which are characteristic structural features of destabilases. The recombinant WpDestabilase protein exhibited isopeptidase activity together with blood-clot-destabilizing efficacy, suggesting that WpDestabilase may represent a major candidate molecule contributing to the thrombolytic activity of W. pigra. Removal of a 10-amino acid sequence (IPATETTTEI) at the C-terminal tail of the WpDestabilase protein significantly enhanced its isopeptidase activity while its lysozyme activity was not significantly reduced. This may reflect the evolutionary transition of anticoagulant genes to non-anticoagulant genes during the non-hematophagous adaptive evolution of W. pigra. These findings pave the way for further development and utilization of leeches and destabilases.

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Recombinant expression and biochemical characterization of WpDestabilase from Whitmania pigra. Demonstrates fibrinolytic and antibacterial activities via isopeptidolysis, mirroring H. medicinalis destabilase.

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