Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues

Abstract Background Ascaris roundworms are the parasitic nematodes responsible for causing human and porcine ascariasis. Whereas A. lumbricoides is the most common soil-transmitted helminth infecting humans in the world, A. suum causes important economic losses in the porcine industry. The latter ha...

Full description

Bibliographic Details
Main Authors: Alicia Diosdado, Fernando Simón, Rodrigo Morchón, Javier González-Miguel
Format: Article
Language:English
Published: BMC 2020-04-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04067-5
_version_ 1818516621169262592
author Alicia Diosdado
Fernando Simón
Rodrigo Morchón
Javier González-Miguel
author_facet Alicia Diosdado
Fernando Simón
Rodrigo Morchón
Javier González-Miguel
author_sort Alicia Diosdado
collection DOAJ
description Abstract Background Ascaris roundworms are the parasitic nematodes responsible for causing human and porcine ascariasis. Whereas A. lumbricoides is the most common soil-transmitted helminth infecting humans in the world, A. suum causes important economic losses in the porcine industry. The latter has been proposed as a model for the study of A. lumbricoides since both species are closely related. The third larval stage of these parasites carries out an intriguing and complex hepatopulmonary route through the bloodstream of its hosts. This allows the interaction between larvae and the physiological mechanisms of the hosts circulatory system, such as the fibrinolytic system. Parasite migration has been widely linked to the activation of this system by pathogens that are able to bind plasminogen and enhance plasmin generation. Therefore, the aim of this study was to examine the interaction between the infective third larval stage of A. suum and the host fibrinolytic system as a model of the host-Ascaris spp. relationships. Methods Infective larvae were obtained after incubating and hatching fertile eggs of A. suum in order to extract their cuticle and excretory/secretory antigens. The ability of both extracts to bind and activate plasminogen, as well as promote plasmin generation were assayed by ELISA and western blot. The location of plasminogen binding on the larval surface was revealed by immunofluorescence. The plasminogen-binding proteins from both antigenic extracts were revealed by two-dimensional electrophoresis and plasminogen-ligand blotting, and identified by mass spectrometry. Results Cuticle and excretory/secretory antigens from infective larvae of A. suum were able to bind plasminogen and promote plasmin generation in the presence of plasminogen activators. Plasminogen binding was located on the larval surface. Twelve plasminogen-binding proteins were identified in both antigenic extracts. Conclusions To the best of our knowledge, the present results showed for the first time, the pro-fibrinolytic potential of infective larvae of Ascaris spp., which suggests a novel parasite survival mechanism by facilitating the migration through host tissues.
first_indexed 2024-12-11T00:44:45Z
format Article
id doaj.art-211e05983e7f4d35b02ce75bb44ba9ef
institution Directory Open Access Journal
issn 1756-3305
language English
last_indexed 2024-12-11T00:44:45Z
publishDate 2020-04-01
publisher BMC
record_format Article
series Parasites & Vectors
spelling doaj.art-211e05983e7f4d35b02ce75bb44ba9ef2022-12-22T01:26:48ZengBMCParasites & Vectors1756-33052020-04-0113111310.1186/s13071-020-04067-5Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissuesAlicia Diosdado0Fernando Simón1Rodrigo Morchón2Javier González-Miguel3Laboratory of Parasitology, Faculty of Pharmacy, University of SalamancaLaboratory of Parasitology, Faculty of Pharmacy, University of SalamancaLaboratory of Parasitology, Faculty of Pharmacy, University of SalamancaLaboratory of Parasitology, Institute of Natural Resources and Agrobiology of Salamanca (IRNASA-CSIC)Abstract Background Ascaris roundworms are the parasitic nematodes responsible for causing human and porcine ascariasis. Whereas A. lumbricoides is the most common soil-transmitted helminth infecting humans in the world, A. suum causes important economic losses in the porcine industry. The latter has been proposed as a model for the study of A. lumbricoides since both species are closely related. The third larval stage of these parasites carries out an intriguing and complex hepatopulmonary route through the bloodstream of its hosts. This allows the interaction between larvae and the physiological mechanisms of the hosts circulatory system, such as the fibrinolytic system. Parasite migration has been widely linked to the activation of this system by pathogens that are able to bind plasminogen and enhance plasmin generation. Therefore, the aim of this study was to examine the interaction between the infective third larval stage of A. suum and the host fibrinolytic system as a model of the host-Ascaris spp. relationships. Methods Infective larvae were obtained after incubating and hatching fertile eggs of A. suum in order to extract their cuticle and excretory/secretory antigens. The ability of both extracts to bind and activate plasminogen, as well as promote plasmin generation were assayed by ELISA and western blot. The location of plasminogen binding on the larval surface was revealed by immunofluorescence. The plasminogen-binding proteins from both antigenic extracts were revealed by two-dimensional electrophoresis and plasminogen-ligand blotting, and identified by mass spectrometry. Results Cuticle and excretory/secretory antigens from infective larvae of A. suum were able to bind plasminogen and promote plasmin generation in the presence of plasminogen activators. Plasminogen binding was located on the larval surface. Twelve plasminogen-binding proteins were identified in both antigenic extracts. Conclusions To the best of our knowledge, the present results showed for the first time, the pro-fibrinolytic potential of infective larvae of Ascaris spp., which suggests a novel parasite survival mechanism by facilitating the migration through host tissues.http://link.springer.com/article/10.1186/s13071-020-04067-5Ascaris suumThird-stage larvaeFibrinolytic systemPlasminogenPlasminLarval migration
spellingShingle Alicia Diosdado
Fernando Simón
Rodrigo Morchón
Javier González-Miguel
Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
Parasites & Vectors
Ascaris suum
Third-stage larvae
Fibrinolytic system
Plasminogen
Plasmin
Larval migration
title Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
title_full Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
title_fullStr Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
title_full_unstemmed Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
title_short Pro-fibrinolytic potential of the third larval stage of Ascaris suum as a possible mechanism facilitating its migration through the host tissues
title_sort pro fibrinolytic potential of the third larval stage of ascaris suum as a possible mechanism facilitating its migration through the host tissues
topic Ascaris suum
Third-stage larvae
Fibrinolytic system
Plasminogen
Plasmin
Larval migration
url http://link.springer.com/article/10.1186/s13071-020-04067-5
work_keys_str_mv AT aliciadiosdado profibrinolyticpotentialofthethirdlarvalstageofascarissuumasapossiblemechanismfacilitatingitsmigrationthroughthehosttissues
AT fernandosimon profibrinolyticpotentialofthethirdlarvalstageofascarissuumasapossiblemechanismfacilitatingitsmigrationthroughthehosttissues
AT rodrigomorchon profibrinolyticpotentialofthethirdlarvalstageofascarissuumasapossiblemechanismfacilitatingitsmigrationthroughthehosttissues
AT javiergonzalezmiguel profibrinolyticpotentialofthethirdlarvalstageofascarissuumasapossiblemechanismfacilitatingitsmigrationthroughthehosttissues