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Changes in porcine nutrient transport physiology in response to Ascaris suum infection

BACKGROUND: The roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming. In this context, lower weight gain is hypothesized to be due to decreased nutrient absorption. This study aims at characterizing the effects of A. suum infection on intestinal nutrient tr...

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Autores principales: Koehler, Sarina, Springer, Andrea, Issel, Nicole, Klinger, Stefanie, Strube, Christina, Breves, Gerhard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8515719/
https://www.ncbi.nlm.nih.gov/pubmed/34649607
http://dx.doi.org/10.1186/s13071-021-05029-1
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author Koehler, Sarina
Springer, Andrea
Issel, Nicole
Klinger, Stefanie
Strube, Christina
Breves, Gerhard
author_facet Koehler, Sarina
Springer, Andrea
Issel, Nicole
Klinger, Stefanie
Strube, Christina
Breves, Gerhard
author_sort Koehler, Sarina
collection PubMed
description BACKGROUND: The roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming. In this context, lower weight gain is hypothesized to be due to decreased nutrient absorption. This study aims at characterizing the effects of A. suum infection on intestinal nutrient transport processes and potential molecular mechanisms. METHODS: Three groups of six piglets each were infected orally (10,000 embryonated A. suum eggs) in a single dose (“single infection”). Another three groups were infected orally (1000 embryonated eggs) for 10 consecutive days (“trickle infection”). Animals were necropsied 21, 35 and 49 days post-infection (dpi). Three groups served as respective controls. The Ussing chamber technique was applied for the functional characterization of small intestinal tissues [short-circuit currents (I(sc)) as induced by glucose, alanine and peptides; (3)H-glucose net flux rates; tissue conductance (G(t))]. Transcription and expression levels of relevant cytokines and nutrient transporters were evaluated (qPCR/western blot). RESULTS: Peptide- and alanine-induced changes in I(sc) were significantly decreased in the jejunum and ileum of the trickle-infected group at 49 dpi and in the ileum of the single-infected group at 49 dpi. No significant differences regarding glucose transport were observed between the Ascaris-infected groups and the control group in Ussing chamber experiments. Transcription levels of the glucose and peptide transporters as well as of selected transcription factors (transcription of signal transducer and activator of transcription 6 [STAT6] and hypoxia-inducible factor 1-alpha [Hif-1α]) were significantly increased in response to both infection types after some periods. The transcription of interleukins 4 and 13 varied between decrease and increase regarding the respective time points, as did the protein expression of glucose transporters. The expression of the peptide transporter PepT1 was significantly decreased in the ileal single-infected group at 35 dpi. Hif-1α was significantly increased in the ileal tissue from the single-infected group at 21 dpi and in the trickle-infected group at 35 dpi. The expression levels of Na(+)/K(+)-ATPase and ASCT1 remained unaffected. CONCLUSIONS: In contrast to the current hypothesis, these results indicate that the nutrient deprivation induced by A. suum cannot be explained by transcriptional or expression changes alone and requires further studies. GRAPHICAL ABSTRACT: [Image: see text]
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spelling pubmed-85157192021-10-20 Changes in porcine nutrient transport physiology in response to Ascaris suum infection Koehler, Sarina Springer, Andrea Issel, Nicole Klinger, Stefanie Strube, Christina Breves, Gerhard Parasit Vectors Research BACKGROUND: The roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming. In this context, lower weight gain is hypothesized to be due to decreased nutrient absorption. This study aims at characterizing the effects of A. suum infection on intestinal nutrient transport processes and potential molecular mechanisms. METHODS: Three groups of six piglets each were infected orally (10,000 embryonated A. suum eggs) in a single dose (“single infection”). Another three groups were infected orally (1000 embryonated eggs) for 10 consecutive days (“trickle infection”). Animals were necropsied 21, 35 and 49 days post-infection (dpi). Three groups served as respective controls. The Ussing chamber technique was applied for the functional characterization of small intestinal tissues [short-circuit currents (I(sc)) as induced by glucose, alanine and peptides; (3)H-glucose net flux rates; tissue conductance (G(t))]. Transcription and expression levels of relevant cytokines and nutrient transporters were evaluated (qPCR/western blot). RESULTS: Peptide- and alanine-induced changes in I(sc) were significantly decreased in the jejunum and ileum of the trickle-infected group at 49 dpi and in the ileum of the single-infected group at 49 dpi. No significant differences regarding glucose transport were observed between the Ascaris-infected groups and the control group in Ussing chamber experiments. Transcription levels of the glucose and peptide transporters as well as of selected transcription factors (transcription of signal transducer and activator of transcription 6 [STAT6] and hypoxia-inducible factor 1-alpha [Hif-1α]) were significantly increased in response to both infection types after some periods. The transcription of interleukins 4 and 13 varied between decrease and increase regarding the respective time points, as did the protein expression of glucose transporters. The expression of the peptide transporter PepT1 was significantly decreased in the ileal single-infected group at 35 dpi. Hif-1α was significantly increased in the ileal tissue from the single-infected group at 21 dpi and in the trickle-infected group at 35 dpi. The expression levels of Na(+)/K(+)-ATPase and ASCT1 remained unaffected. CONCLUSIONS: In contrast to the current hypothesis, these results indicate that the nutrient deprivation induced by A. suum cannot be explained by transcriptional or expression changes alone and requires further studies. GRAPHICAL ABSTRACT: [Image: see text] BioMed Central 2021-10-14 /pmc/articles/PMC8515719/ /pubmed/34649607 http://dx.doi.org/10.1186/s13071-021-05029-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Koehler, Sarina
Springer, Andrea
Issel, Nicole
Klinger, Stefanie
Strube, Christina
Breves, Gerhard
Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title_full Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title_fullStr Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title_full_unstemmed Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title_short Changes in porcine nutrient transport physiology in response to Ascaris suum infection
title_sort changes in porcine nutrient transport physiology in response to ascaris suum infection
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8515719/
https://www.ncbi.nlm.nih.gov/pubmed/34649607
http://dx.doi.org/10.1186/s13071-021-05029-1
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