Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.

Extracellular vesicles (EVs) such as exosomes are key regulators of intercellular communication that can be found in almost all bio fluids. Although studies in the last decade have made great headway in discerning the role of EVs in many physiological and pathophysiological processes, the bioavailab...

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Main Authors: Benedikt Kirchner, Dominik Buschmann, Vijay Paul, Michael W Pfaffl
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0229606
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spelling doaj-b91f3bdec0584e7dad40de52719f3f622021-03-03T21:40:50ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01152e022960610.1371/journal.pone.0229606Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.Benedikt KirchnerDominik BuschmannVijay PaulMichael W PfafflExtracellular vesicles (EVs) such as exosomes are key regulators of intercellular communication that can be found in almost all bio fluids. Although studies in the last decade have made great headway in discerning the role of EVs in many physiological and pathophysiological processes, the bioavailability and impact of dietary EVs and their cargo still remain to be elucidated. Due to its widespread consumption and high content of EV-associated microRNAs and proteins, a major focus in this field has been set on EVs in bovine milk and colostrum. Despite promising in vitro studies in recent years that show high resiliency of milk EVs to degradation and uptake of milk EV cargo in a variety of intestinal and blood cell types, in vivo experiments continue to be inconclusive and sometimes outright contradictive. To resolve this discrepancy, we assessed the potential postprandial transfer of colostral EVs to the circulation of newborn calves by analysing colostrum-specific protein and miRNAs, including specific isoforms (isomiRs) in cells, EV isolations and unfractionated samples from blood and colostrum. Our findings reveal distinct populations of EVs in colostrum and blood from cows that can be clearly separated by density, particle concentration and protein content (BTN1A1, MFGE8). Postprandial blood samples of calves show a time-dependent increase in EVs that share morphological and protein characteristics of colostral EVs. Analysis of miRNA expression profiles by Next-Generation Sequencing gave a different picture however. Although significant postprandial expression changes could only be detected for calf EV samples, expression profiles show very limited overlap with highly expressed miRNAs in colostral EVs or colostrum in general. Taken together our results indicate a selective uptake of membrane-associated protein cargo but not luminal miRNAs from colostral EVs into the circulation of neonatal calves.https://doi.org/10.1371/journal.pone.0229606
collection DOAJ
language English
format Article
sources DOAJ
author Benedikt Kirchner
Dominik Buschmann
Vijay Paul
Michael W Pfaffl
spellingShingle Benedikt Kirchner
Dominik Buschmann
Vijay Paul
Michael W Pfaffl
Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
PLoS ONE
author_facet Benedikt Kirchner
Dominik Buschmann
Vijay Paul
Michael W Pfaffl
author_sort Benedikt Kirchner
title Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
title_short Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
title_full Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
title_fullStr Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
title_full_unstemmed Postprandial transfer of colostral extracellular vesicles and their protein and miRNA cargo in neonatal calves.
title_sort postprandial transfer of colostral extracellular vesicles and their protein and mirna cargo in neonatal calves.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description Extracellular vesicles (EVs) such as exosomes are key regulators of intercellular communication that can be found in almost all bio fluids. Although studies in the last decade have made great headway in discerning the role of EVs in many physiological and pathophysiological processes, the bioavailability and impact of dietary EVs and their cargo still remain to be elucidated. Due to its widespread consumption and high content of EV-associated microRNAs and proteins, a major focus in this field has been set on EVs in bovine milk and colostrum. Despite promising in vitro studies in recent years that show high resiliency of milk EVs to degradation and uptake of milk EV cargo in a variety of intestinal and blood cell types, in vivo experiments continue to be inconclusive and sometimes outright contradictive. To resolve this discrepancy, we assessed the potential postprandial transfer of colostral EVs to the circulation of newborn calves by analysing colostrum-specific protein and miRNAs, including specific isoforms (isomiRs) in cells, EV isolations and unfractionated samples from blood and colostrum. Our findings reveal distinct populations of EVs in colostrum and blood from cows that can be clearly separated by density, particle concentration and protein content (BTN1A1, MFGE8). Postprandial blood samples of calves show a time-dependent increase in EVs that share morphological and protein characteristics of colostral EVs. Analysis of miRNA expression profiles by Next-Generation Sequencing gave a different picture however. Although significant postprandial expression changes could only be detected for calf EV samples, expression profiles show very limited overlap with highly expressed miRNAs in colostral EVs or colostrum in general. Taken together our results indicate a selective uptake of membrane-associated protein cargo but not luminal miRNAs from colostral EVs into the circulation of neonatal calves.
url https://doi.org/10.1371/journal.pone.0229606
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