Ascaris suum Nutrient Uptake and Metabolic Release, and Modulation of Host Intestinal Nutrient Transport by Excretory-Secretory and Cuticle Antigens In Vitro.

Sarina Koehler,Nicole Issel,Andrea Springer,Stefanie Klinger,Christina Strube,Michael Wendt,Gerhard Breves

doi:10.3390/pathogens10111419

Sarina Koehler, Nicole Issel + Show 5 more

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https://doi.org/10.3390/pathogens10111419

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Abstract

Ascaris suum, the most important pig parasite, also infects humans as a zoonotic pathogen. Malabsorption upon infection probably results from impaired nutrient transport, presumably mediated by the parasite’s excretory-secretory (ES) or cuticle somatic (CSO) antigens. The present study investigated the electrogenic transport (ΔIsc) of glucose, alanine and the dipeptide glycyl-l-glutamine (glygln), as well as glucose net flux rates in pig jejunal tissue after in vitro exposure to adult A. suum total ES or CSO antigens in Ussing chambers. ΔIsc of glucose, alanine and glucose net flux rate were significantly decreased after one hour of exposure to total ES antigen. In contrast, CSO antigens increased the transport of glygln. Additionally, nutrient uptake and ES antigen pattern were compared in culture medium from untreated adult worms and those with sealed mouth and anal openings. Untreated worms completely absorbed glucose, while cuticular absorption in sealed worms led to 90% reduction. Amino acid absorption was 30% less effective in sealed worms, and ammonia excretion decreased by 20%. Overall, the results show that A. suum total ES antigen rapidly impairs nutrient transport in vitro. Future studies confirming the results in vivo, narrowing down the ES components responsible and investigating underlying molecular mechanisms are needed.

Highlights

The intestinal roundworm Ascaris suum is regarded, economically as the most important porcine parasite, but can infect humans as a zoonotic pathogen [1]
Total ES antigens obtained from untreated adult worms after cultivation in 0.9% NaCl or physiological intestinal buffer (Ussing buffer) and total ES antigen obtained by cultivation in RPMI medium and lyophilized to reduce its volume showed comparable banding patterns
A quite similar pattern was observed for the trans-cuticular ES antigen from RPMI-cultivated worms with sealed mouth and anal openings, representing the ES fractions secreted via the body surface

Summary

Introduction

The intestinal roundworm Ascaris suum is regarded, economically as the most important porcine parasite, but can infect humans as a zoonotic pathogen [1]. Economic losses in the pig industry are due to condemnation of livers showing traces of larval migration [2], as well as reduced feed efficiency and weight gain, e.g., [3,4]. Feed conversion and weight gain may be affected by direct parasite-host competition, e.g., for glucose, which is primarily absorbed via the worm’s cuticle [8]; parasite-induced modulation of the hosts’ intestinal nutrient absorption mechanisms may play a more important role. A negative impact of intestinal nematode infection on host glucose and protein transport has been shown. Regarding A. suum, infected pigs showed an impaired glucose transport at day 14, 17 and 21 post-infection [12,13]

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