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Short-term Western-style diet negatively impacts reproductive outcomes in primates

A maternal Western-style diet (WSD) is associated with poor reproductive outcomes, but whether this is from the diet itself or underlying metabolic dysfunction is unknown. Here, we performed a longitudinal study using regularly cycling female rhesus macaques (n = 10) that underwent 2 consecutive in...

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Autores principales: Ravisankar, Sweta, Ting, Alison Y., Murphy, Melinda J., Redmayne, Nash, Wang, Dorothy, McArthur, Carrie A., Takahashi, Diana L., Kievit, Paul, Chavez, Shawn L., Hennebold, Jon D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Clinical Investigation 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934943/
https://www.ncbi.nlm.nih.gov/pubmed/33616080
http://dx.doi.org/10.1172/jci.insight.138312
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author Ravisankar, Sweta
Ting, Alison Y.
Murphy, Melinda J.
Redmayne, Nash
Wang, Dorothy
McArthur, Carrie A.
Takahashi, Diana L.
Kievit, Paul
Chavez, Shawn L.
Hennebold, Jon D.
author_facet Ravisankar, Sweta
Ting, Alison Y.
Murphy, Melinda J.
Redmayne, Nash
Wang, Dorothy
McArthur, Carrie A.
Takahashi, Diana L.
Kievit, Paul
Chavez, Shawn L.
Hennebold, Jon D.
author_sort Ravisankar, Sweta
collection PubMed
description A maternal Western-style diet (WSD) is associated with poor reproductive outcomes, but whether this is from the diet itself or underlying metabolic dysfunction is unknown. Here, we performed a longitudinal study using regularly cycling female rhesus macaques (n = 10) that underwent 2 consecutive in vitro fertilization (IVF) cycles, one while consuming a low-fat diet and another 6–8 months after consuming a high-fat WSD. Metabolic data were collected from the females prior to each IVF cycle. Follicular fluid (FF) and oocytes were assessed for cytokine/steroid levels and IVF potential, respectively. Although transition to a WSD led to weight gain and increased body fat, no difference in insulin levels was observed. A significant decrease in IL-1RA concentration and the ratio of cortisol/cortisone was detected in FF after WSD intake. Despite an increased probability of isolating mature oocytes, a 44% reduction in blastocyst number was observed with WSD consumption, and time-lapse imaging revealed delayed mitotic timing and multipolar divisions. RNA sequencing of blastocysts demonstrated dysregulation of genes involved in RNA binding, protein channel activity, mitochondrial function and pluripotency versus cell differentiation after WSD consumption. Thus, short-term WSD consumption promotes a proinflammatory intrafollicular microenvironment that is associated with impaired preimplantation development in the absence of large-scale metabolic changes.
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spelling pubmed-79349432021-03-09 Short-term Western-style diet negatively impacts reproductive outcomes in primates Ravisankar, Sweta Ting, Alison Y. Murphy, Melinda J. Redmayne, Nash Wang, Dorothy McArthur, Carrie A. Takahashi, Diana L. Kievit, Paul Chavez, Shawn L. Hennebold, Jon D. JCI Insight Research Article A maternal Western-style diet (WSD) is associated with poor reproductive outcomes, but whether this is from the diet itself or underlying metabolic dysfunction is unknown. Here, we performed a longitudinal study using regularly cycling female rhesus macaques (n = 10) that underwent 2 consecutive in vitro fertilization (IVF) cycles, one while consuming a low-fat diet and another 6–8 months after consuming a high-fat WSD. Metabolic data were collected from the females prior to each IVF cycle. Follicular fluid (FF) and oocytes were assessed for cytokine/steroid levels and IVF potential, respectively. Although transition to a WSD led to weight gain and increased body fat, no difference in insulin levels was observed. A significant decrease in IL-1RA concentration and the ratio of cortisol/cortisone was detected in FF after WSD intake. Despite an increased probability of isolating mature oocytes, a 44% reduction in blastocyst number was observed with WSD consumption, and time-lapse imaging revealed delayed mitotic timing and multipolar divisions. RNA sequencing of blastocysts demonstrated dysregulation of genes involved in RNA binding, protein channel activity, mitochondrial function and pluripotency versus cell differentiation after WSD consumption. Thus, short-term WSD consumption promotes a proinflammatory intrafollicular microenvironment that is associated with impaired preimplantation development in the absence of large-scale metabolic changes. American Society for Clinical Investigation 2021-02-22 /pmc/articles/PMC7934943/ /pubmed/33616080 http://dx.doi.org/10.1172/jci.insight.138312 Text en © 2021 Ravisankar et al. http://creativecommons.org/licenses/by/4.0/ This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Ravisankar, Sweta
Ting, Alison Y.
Murphy, Melinda J.
Redmayne, Nash
Wang, Dorothy
McArthur, Carrie A.
Takahashi, Diana L.
Kievit, Paul
Chavez, Shawn L.
Hennebold, Jon D.
Short-term Western-style diet negatively impacts reproductive outcomes in primates
title Short-term Western-style diet negatively impacts reproductive outcomes in primates
title_full Short-term Western-style diet negatively impacts reproductive outcomes in primates
title_fullStr Short-term Western-style diet negatively impacts reproductive outcomes in primates
title_full_unstemmed Short-term Western-style diet negatively impacts reproductive outcomes in primates
title_short Short-term Western-style diet negatively impacts reproductive outcomes in primates
title_sort short-term western-style diet negatively impacts reproductive outcomes in primates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934943/
https://www.ncbi.nlm.nih.gov/pubmed/33616080
http://dx.doi.org/10.1172/jci.insight.138312
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