Haemonchus contortus Transthyretin-Like Protein TTR-31 Plays Roles in Post-Embryonic Larval Development and Potentially Apoptosis of Germ Cells.

Hengzhi Shi,Aifang Du,Xiaocui Huang,Guangxu Ma,Chaoqun Yao,Xueqiu Chen,Fei Wu,Yi Yang

doi:10.3389/fcell.2021.753667

Abstract

Transthyretin (TTR)-like proteins play multi-function roles in nematode and are important component of excretory/secretory product in Haemonchus contortus. In this study, we functionally characterised a secretory transthyretin-like protein in the barber’s pole worm H. contortus. A full-length of transthyretin-like protein-coding gene (Hc-ttr-31) was identified in this parasitic nematode, representing a counterpart of Ce-ttr-31 in Caenorhabditis elegans. High transcriptional levels of Hc-ttr-31 were detected in the egg and early larval stages of H. contortus, with the lowest level measured in the adult stage, indicating a decreased transcriptional pattern of this gene during nematode development. Localisation analysis indicated a secretion of TTR-31 from the intestine to the gonad, suggesting additional roles of Hc-ttr-31 in nematode reproduction. Expression of Hc-ttr-31 and Ce-ttr-31 in C. elegans did not show marked influence on the nematode development and reproduction, whereas Hc-ttr-31 RNA interference-mediated gene knockdown of Ce-ttr-31 shortened the lifespan, decreased the brood size, slowed the pumping rate and inhibited the growth of treated worms. Particularly, gene knockdown of Hc-ttr-31 in C. elegans was linked to activated apoptosis signalling pathway, increased general reactive oxygen species (ROS) level, apoptotic germ cells and facultative vivipary phenotype, as well as suppressed germ cell removal signalling pathways. Taken together, Hc-ttr-31 appears to play roles in regulating post-embryonic larval development, and potentially in protecting gonad from oxidative stress and mediating engulfment of apoptotic germ cells. A better knowledge of these aspects should contribute to a better understanding of the developmental biology of H. contortus and a discovery of potential targets against this and related parasitic worms.

Highlights

The strongylid nematode Haemonchus contortus is one of the most important parasitic nematodes of sheep, goats and other ruminants (Chilton et al, 2006)
In this study, we reported the functional roles of Hcttr-31 in a strongylid nematode H. contortus
We found that this gene was transcribed in all developmental stages of H. contortus, with a decreasing transcriptional pattern during the development from the egg to the adult stage

Summary

Introduction

The strongylid nematode Haemonchus contortus ( known as barber’s pole worm) is one of the most important parasitic nematodes of sheep, goats and other ruminants (Chilton et al, 2006) It feeds on blood in the abomasa of small ruminants and causes the parasitic disease haemonchosis characterised by anemia, hemorrhagic gastritis, oedema and associated complications (Zajac and Garza., 2020). Current control strategies against H. contortus infection in ruminants rely heavily on anthelmintic chemotherapy, especially in the absence of efficient alternative methods in many countries (Blanchard et al, 2018). Frequent and indiscriminate administration of anthelmintics has led to the development of drug resistance worldwide (Arsenopoulos et al, 2021), including drugs recently introduced into the market (Mederos et al, 2014; Niciura et al, 2019).

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