Cargando…

The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens

P-glycoproteins (Pgp) have been proposed as contributors to the widespread macrocyclic lactone (ML) resistance in several nematode species including a major pathogen of foals, Parascaris univalens. Using new and available RNA-seq data, ten different genomic loci encoding Pgps were identified and cha...

Descripción completa

Detalles Bibliográficos
Autores principales: Gerhard, Alexander P., Krücken, Jürgen, Heitlinger, Emanuel, Janssen, I. Jana I., Basiaga, Marta, Kornaś, Sławomir, Beier, Céline, Nielsen, Martin K., Davis, Richard E., Wang, Jianbin, von Samson-Himmelstjerna, Georg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423980/
https://www.ncbi.nlm.nih.gov/pubmed/32788636
http://dx.doi.org/10.1038/s41598-020-70529-6
_version_ 1783570239455232000
author Gerhard, Alexander P.
Krücken, Jürgen
Heitlinger, Emanuel
Janssen, I. Jana I.
Basiaga, Marta
Kornaś, Sławomir
Beier, Céline
Nielsen, Martin K.
Davis, Richard E.
Wang, Jianbin
von Samson-Himmelstjerna, Georg
author_facet Gerhard, Alexander P.
Krücken, Jürgen
Heitlinger, Emanuel
Janssen, I. Jana I.
Basiaga, Marta
Kornaś, Sławomir
Beier, Céline
Nielsen, Martin K.
Davis, Richard E.
Wang, Jianbin
von Samson-Himmelstjerna, Georg
author_sort Gerhard, Alexander P.
collection PubMed
description P-glycoproteins (Pgp) have been proposed as contributors to the widespread macrocyclic lactone (ML) resistance in several nematode species including a major pathogen of foals, Parascaris univalens. Using new and available RNA-seq data, ten different genomic loci encoding Pgps were identified and characterized by transcriptome-guided RT-PCRs and Sanger sequencing. Phylogenetic analysis revealed an ascarid-specific Pgp lineage, Pgp-18, as well as two paralogues of Pgp-11 and Pgp-16. Comparative gene expression analyses in P. univalens and Caenorhabditis elegans show that the intestine is the major site of expression but individual gene expression patterns were not conserved between the two nematodes. In P. univalens, PunPgp-9, PunPgp-11.1 and PunPgp-16.2 consistently exhibited the highest expression level in two independent transcriptome data sets. Using RNA-Seq, no significant upregulation of any Pgp was detected following in vitro incubation of adult P. univalens with ivermectin suggesting that drug-induced upregulation is not the mechanism of Pgp-mediated ML resistance. Expression and functional analyses of PunPgp-2 and PunPgp-9 in Saccharomyces cerevisiae provide evidence for an interaction with ketoconazole and ivermectin, but not thiabendazole. Overall, this study established reliable reference gene models with significantly improved annotation for the P. univalens Pgp repertoire and provides a foundation for a better understanding of Pgp-mediated anthelmintic resistance.
format Online
Article
Text
id pubmed-7423980
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-74239802020-08-14 The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens Gerhard, Alexander P. Krücken, Jürgen Heitlinger, Emanuel Janssen, I. Jana I. Basiaga, Marta Kornaś, Sławomir Beier, Céline Nielsen, Martin K. Davis, Richard E. Wang, Jianbin von Samson-Himmelstjerna, Georg Sci Rep Article P-glycoproteins (Pgp) have been proposed as contributors to the widespread macrocyclic lactone (ML) resistance in several nematode species including a major pathogen of foals, Parascaris univalens. Using new and available RNA-seq data, ten different genomic loci encoding Pgps were identified and characterized by transcriptome-guided RT-PCRs and Sanger sequencing. Phylogenetic analysis revealed an ascarid-specific Pgp lineage, Pgp-18, as well as two paralogues of Pgp-11 and Pgp-16. Comparative gene expression analyses in P. univalens and Caenorhabditis elegans show that the intestine is the major site of expression but individual gene expression patterns were not conserved between the two nematodes. In P. univalens, PunPgp-9, PunPgp-11.1 and PunPgp-16.2 consistently exhibited the highest expression level in two independent transcriptome data sets. Using RNA-Seq, no significant upregulation of any Pgp was detected following in vitro incubation of adult P. univalens with ivermectin suggesting that drug-induced upregulation is not the mechanism of Pgp-mediated ML resistance. Expression and functional analyses of PunPgp-2 and PunPgp-9 in Saccharomyces cerevisiae provide evidence for an interaction with ketoconazole and ivermectin, but not thiabendazole. Overall, this study established reliable reference gene models with significantly improved annotation for the P. univalens Pgp repertoire and provides a foundation for a better understanding of Pgp-mediated anthelmintic resistance. Nature Publishing Group UK 2020-08-12 /pmc/articles/PMC7423980/ /pubmed/32788636 http://dx.doi.org/10.1038/s41598-020-70529-6 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Gerhard, Alexander P.
Krücken, Jürgen
Heitlinger, Emanuel
Janssen, I. Jana I.
Basiaga, Marta
Kornaś, Sławomir
Beier, Céline
Nielsen, Martin K.
Davis, Richard E.
Wang, Jianbin
von Samson-Himmelstjerna, Georg
The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title_full The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title_fullStr The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title_full_unstemmed The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title_short The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens
title_sort p-glycoprotein repertoire of the equine parasitic nematode parascaris univalens
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423980/
https://www.ncbi.nlm.nih.gov/pubmed/32788636
http://dx.doi.org/10.1038/s41598-020-70529-6
work_keys_str_mv AT gerhardalexanderp thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT kruckenjurgen thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT heitlingeremanuel thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT janssenijanai thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT basiagamarta thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT kornassławomir thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT beierceline thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT nielsenmartink thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT davisricharde thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT wangjianbin thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT vonsamsonhimmelstjernageorg thepglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT gerhardalexanderp pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT kruckenjurgen pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT heitlingeremanuel pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT janssenijanai pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT basiagamarta pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT kornassławomir pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT beierceline pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT nielsenmartink pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT davisricharde pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT wangjianbin pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens
AT vonsamsonhimmelstjernageorg pglycoproteinrepertoireoftheequineparasiticnematodeparascarisunivalens