<i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes

The influence of triterpenoid saponins on subcellular morphological changes in the cells of parasitic nematodes remains poorly understood. Our study examines the effect of oleanolic acid glucuronides from marigold (<i>Calendula officinalis</i>) on the possible modification of immunogenic...

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Main Authors: Maria Doligalska, Kinga Jóźwicka, Ludmiła Szewczak, Julita Nowakowska, Klaudia Brodaczewska, Katarzyna Goździk, Cezary Pączkowski, Anna Szakiel
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/10/3/296
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author Maria Doligalska
Kinga Jóźwicka
Ludmiła Szewczak
Julita Nowakowska
Klaudia Brodaczewska
Katarzyna Goździk
Cezary Pączkowski
Anna Szakiel
author_facet Maria Doligalska
Kinga Jóźwicka
Ludmiła Szewczak
Julita Nowakowska
Klaudia Brodaczewska
Katarzyna Goździk
Cezary Pączkowski
Anna Szakiel
author_sort Maria Doligalska
collection DOAJ
description The influence of triterpenoid saponins on subcellular morphological changes in the cells of parasitic nematodes remains poorly understood. Our study examines the effect of oleanolic acid glucuronides from marigold (<i>Calendula officinalis</i>) on the possible modification of immunogenic proteins from infective <i>Heligmosomoides polygyrus bakeri</i> larvae (L3). Our findings indicate that the triterpenoid saponins alter the subcellular morphology of the larvae and prevent recognition of nematode-specific proteins by rabbit immune-IgG. TEM ultrastructure and HPLC analysis showed that microtubule and cytoskeleton fibres were fragmented by saponin treatment. MASCOT bioinformatic analysis revealed that in larvae exposed to saponins, the immune epitopes of their proteins altered. Several mitochondrial and cytoskeleton proteins involved in signalling and cellular processes were downregulated or degraded. As possible candidates, the following set of recognised proteins may play a key role in the immunogenicity of larvae: beta-tubulin isotype, alpha-tubulin, myosin, paramyosin isoform-1, actin, disorganized muscle protein-1, ATP-synthase, beta subunit, carboxyl transferase domain protein, glutamate dehydrogenase, enolase (phosphopyruvate hydratase), fructose-bisphosphate aldolase 2, tropomyosin, arginine kinase or putative chaperone protein DnaK, and galactoside-binding lectin. Data are available via ProteomeXchange with identifier PXD024205.
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spelling doaj.art-d28558d686964603acdcee519eb94bfe2023-12-03T12:30:48ZengMDPI AGPathogens2076-08172021-03-0110329610.3390/pathogens10030296<i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic NematodesMaria Doligalska0Kinga Jóźwicka1Ludmiła Szewczak2Julita Nowakowska3Klaudia Brodaczewska4Katarzyna Goździk5Cezary Pączkowski6Anna Szakiel7Department of Parasitology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Parasitology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Parasitology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandLaboratory of Electron and Confocal Microscopy, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Parasitology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Parasitology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Plant Biochemistry, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandDepartment of Plant Biochemistry, Faculty of Biology, University of Warsaw, 02-096 Warsaw, PolandThe influence of triterpenoid saponins on subcellular morphological changes in the cells of parasitic nematodes remains poorly understood. Our study examines the effect of oleanolic acid glucuronides from marigold (<i>Calendula officinalis</i>) on the possible modification of immunogenic proteins from infective <i>Heligmosomoides polygyrus bakeri</i> larvae (L3). Our findings indicate that the triterpenoid saponins alter the subcellular morphology of the larvae and prevent recognition of nematode-specific proteins by rabbit immune-IgG. TEM ultrastructure and HPLC analysis showed that microtubule and cytoskeleton fibres were fragmented by saponin treatment. MASCOT bioinformatic analysis revealed that in larvae exposed to saponins, the immune epitopes of their proteins altered. Several mitochondrial and cytoskeleton proteins involved in signalling and cellular processes were downregulated or degraded. As possible candidates, the following set of recognised proteins may play a key role in the immunogenicity of larvae: beta-tubulin isotype, alpha-tubulin, myosin, paramyosin isoform-1, actin, disorganized muscle protein-1, ATP-synthase, beta subunit, carboxyl transferase domain protein, glutamate dehydrogenase, enolase (phosphopyruvate hydratase), fructose-bisphosphate aldolase 2, tropomyosin, arginine kinase or putative chaperone protein DnaK, and galactoside-binding lectin. Data are available via ProteomeXchange with identifier PXD024205.https://www.mdpi.com/2076-0817/10/3/296triterpenoid saponinsTEM nematode ultrastructureprotein patterns
spellingShingle Maria Doligalska
Kinga Jóźwicka
Ludmiła Szewczak
Julita Nowakowska
Klaudia Brodaczewska
Katarzyna Goździk
Cezary Pączkowski
Anna Szakiel
<i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
Pathogens
triterpenoid saponins
TEM nematode ultrastructure
protein patterns
title <i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
title_full <i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
title_fullStr <i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
title_full_unstemmed <i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
title_short <i>Calendula officinalis</i> Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes
title_sort i calendula officinalis i triterpenoid saponins impact the immune recognition of proteins in parasitic nematodes
topic triterpenoid saponins
TEM nematode ultrastructure
protein patterns
url https://www.mdpi.com/2076-0817/10/3/296
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