Biological function of Dictyocaulus viviparus asparaginyl peptidase legumain-1 and its suitability as a vaccine target

Parasitology. 2018 Mar;145(3):378-392. doi: 10.1017/S0031182017001573. Epub 2017 Sep 25.

Abstract

The present study characterized the biological function of the asparaginyl peptidase legumain-1 (LEG-1) of the bovine lungworm Dictyocaulus viviparus and its suitability as a recombinant vaccine against dictyocaulosis. Quantitative real-time PCR and immunoblot analysis revealed LEG-1 to be almost exclusively transcribed and expressed in parasitic lungworm stages. Immunohistochemistry localized the enzyme in the parasite's gut, which was confirmed by immunoblots detecting LEG-1 in the gut as well as male testes. LEG-1 was recombinantly (rLEG-1) expressed in the yeast Pichia pastoris and subsequently analysed in activity assays for its enzyme functions and substrate specificity. For sufficient functionality, rLEG-1 needed trans-activation through D. viviparus cathepsin L-2, indicating a novel mechanism of legumain activation. After trans-activation, rLEG-1 worked best at pH 5·5 and 35-39 °C and cleaved a legumain-specific artificial substrate as well as the natural substrates bovine collagen types I and II. In a clinical vaccination trial, rLEG-1 did not protect against challenge infection. Results of in vitro characterization, transcription pattern and localization enhance the presumption that LEG-1 participates in digestion processes of D. viviparus. Since rLEG-1 needs trans-activation through a cathepsin, it is probably involved in an enzyme cascade and therefore remains interesting as a candidate in a multi-component vaccine.

Keywords: Legumain; bovine lungworm; enzyme activity; hidden antigen; immunization; immunohistochemistry; nematode; vaccination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Helminth / immunology
  • Cathepsin L / metabolism
  • Cattle
  • Cattle Diseases / parasitology
  • Cysteine Endopeptidases / classification
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / immunology*
  • Cysteine Endopeptidases / metabolism*
  • Dictyocaulus / chemistry*
  • Dictyocaulus / enzymology
  • Dictyocaulus / metabolism
  • Dictyocaulus Infections / prevention & control*
  • Male
  • Vaccination
  • Vaccines, Synthetic / chemistry
  • Vaccines, Synthetic / genetics
  • Vaccines, Synthetic / immunology

Substances

  • Antibodies, Helminth
  • Vaccines, Synthetic
  • Cysteine Endopeptidases
  • Cathepsin L
  • asparaginylendopeptidase