Effect of Obesity on the Preovulatory Follicle and Lipid Fingerprint of Equine Oocytes.
Abstract: Obesity is associated with disrupted reproductive cycles in mares, but the impact of obesity on follicles and oocytes has received minimal attention. We investigated the impact of obesity on 1) expression of selected genes in follicle cells for carbohydrate metabolism, inflammatory cytokines, lipid homeostasis, endoplasmic reticulum stress, and mitochondrial function; 2) follicular fluid content of metabolic hormones and metabolites; and 3) lipid fingerprint of oocytes. Mares (9-13 yr) were classified as control (n = 8, normal weight, body condition score [BCS] 5.1, 10.4% body fat) or obese (n = 9, BCS 7.9, 16.2% body fat). Gene expression from granulosa cells (GC) and cumulus cells (CC) was evaluated by RT-PCR. Serum and follicular fluid were evaluated for insulin, leptin, adiponectin, and metabolite profiling. Oocyte lipid fingerprints were acquired using matrix-assisted laser desorption/ionization mass spectrometry. Several genes for lipid homeostasis, endoplasmic reticulum stress, and mitochondrial function were different between groups in GC and CC. Obese had (P < 0.05) or tended to have (0.05 < P < 0.1) lower insulin sensitivity and higher insulin and leptin in serum and follicular fluid. Many metabolites differed between control and obese in serum and/or follicular fluid and correlated with BCS and/or insulin sensitivity. Oocytes from control had greater concentrations of lipids consistent with phosphatidylcholines, phosphatidylethanolamines, and sphingomyelins, while lipids consistent with triglycerides tended to be higher in obese. These findings suggest that maternal obesity causes alterations in the follicle and oocyte; the extent to which these alterations impact the conceptus and offspring is still to be determined.
© 2016 by the Society for the Study of Reproduction, Inc.
Publication Date: 2015-12-02 PubMed ID: 26632608DOI: 10.1095/biolreprod.115.130187Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This study explored the effects of obesity on the reproductive system of mares, particularly the genes within follicle cells and lipid content within the oocytes. The research revealed that obesity can lead to differences in the expression of genes in follicle cells related to various cellular functions and affect insulin sensitivity as well as lipid composition within oocytes.
Research Methodology
- The study involved mares aged between 9 and 13 years. These were divided into two groups: controls (n = 8, normal weight, body condition score [BCS] 5.1, 10.4% body fat) and obese subjects (n = 9, BCS 7.9, 16.2% body fat).
- The researchers evaluated gene expression from granulosa cells (GC) and cumulus cells (CC) using RT-PCR, focusing on genes related to carbohydrate metabolism, inflammatory cytokines, lipid homeostasis, endoplasmic reticulum stress, and mitochondrial function.
- Serum and follicular fluid from the mares were assessed for insulin, leptin, adiponectin, and metabolite profiling.
- Matrix-assisted laser desorption/ionization mass spectrometry (MALDI-MS) was used to acquire the lipid fingerprints of the oocytes from both groups.
Research Findings
- There were differences between the two groups concerning the expression of certain genes in GC and CC. In particular, genes for lipid homeostasis, endoplasmic reticulum stress, and mitochondrial function differed between the control and obese groups.
- Obese mares displayed lower insulin sensitivity and higher insulin and leptin levels in both serum and follicular fluid, with a noticeable difference to the control group.
- Several metabolites differed between control and obese subjects in serum and/or follicular fluid, showing correlations with the BCS and/or insulin sensitivity.
- Oocytes from control mares had greater concentrations of lipids consistent with phosphatidylcholines, phosphatidylethanolamines, and sphingomyelins, while lipids that matched triglycerides were higher in obese mares.
Conclusions
- The findings suggest that obesity causes alterations in the follicle and oocyte in mares.
- It is still uncertain how these alterations may affect the conceptus (the product of conception at any point between fertilization and birth) and offspring, indicating this as a direction for future research in understanding the reproductive impact of maternal obesity.
Cite This Article
APA
Sessions-Bresnahan DR, Schauer KL, Heuberger AL, Carnevale EM.
(2015).
Effect of Obesity on the Preovulatory Follicle and Lipid Fingerprint of Equine Oocytes.
Biol Reprod, 94(1), 15.
https://doi.org/10.1095/biolreprod.115.130187 Publication
Researcher Affiliations
- Department of Animal Science, Berry College, Mount Berry, Georgia Biomedical Sciences, Colorado State University, Fort Collins, Colorado.
- Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, Colorado.
- Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, Colorado Horticulture and Landscape Architecture, Colorado State University, Fort Collins, Colorado.
- Biomedical Sciences, Colorado State University, Fort Collins, Colorado elaine.carnevale@colostate.edu.
MeSH Terms
- Animals
- Body Composition
- Body Weight
- Cumulus Cells / metabolism
- Endoplasmic Reticulum Stress
- Female
- Follicular Phase
- Granulosa Cells / metabolism
- Horses
- Insulin / blood
- Insulin Resistance
- Leptin / blood
- Lipid Metabolism
- Metabolomics
- Obesity / metabolism
- Obesity / pathology
- Oocytes / metabolism
- Oocytes / pathology
- Ovarian Follicle / metabolism
- Ovarian Follicle / pathology
Citations
This article has been cited 9 times.- Catandi GD, LiPuma L, Obeidat YM, Maclellan LJ, Broeckling CD, Chen T, Chicco AJ, Carnevale EM. Oocyte metabolic function, lipid composition, and developmental potential are altered by diet in older mares.. Reproduction 2022 Apr 1;163(4):183-198.
- Hallman I, Karikoski N, Kareskoski M. The effects of obesity and insulin dysregulation on mare reproduction, pregnancy, and foal health: a review.. Front Vet Sci 2023;10:1180622.
- D' Fonseca NMM, Gibson CME, van Doorn DA, Roelfsema E, de Ruijter-Villani M, Stout TAE. Effect of Overfeeding Shetland Pony Mares on Embryonic Glucose and Lipid Accumulation, and Expression of Imprinted Genes.. Animals (Basel) 2021 Aug 26;11(9).
- Benammar A, Derisoud E, Vialard F, Palmer E, Ayoubi JM, Poulain M, Chavatte-Palmer P. The Mare: A Pertinent Model for Human Assisted Reproductive Technologies?. Animals (Basel) 2021 Aug 4;11(8).
- D'Fonseca NMM, Gibson CME, Hummel I, van Doorn DA, Roelfsema E, Stout TAE, van den Broek J, de Ruijter-Villani M. Overfeeding Extends the Period of Annual Cyclicity but Increases the Risk of Early Embryonic Death in Shetland Pony Mares.. Animals (Basel) 2021 Feb 1;11(2).
- Song J, Xiang S, Pang C, Guo J, Sun Z. Metabolomic alternations of follicular fluid of obese women undergoing in-vitro fertilization treatment.. Sci Rep 2020 Apr 6;10(1):5968.
- Walter J, Huwiler F, Fortes C, Grossmann J, Roschitzki B, Hu J, Naegeli H, Laczko E, Bleul U. Analysis of the equine "cumulome" reveals major metabolic aberrations after maturation in vitro.. BMC Genomics 2019 Jul 17;20(1):588.
- Ruebel ML, Piccolo BD, Mercer KE, Pack L, Moutos D, Shankar K, Andres A. Obesity leads to distinct metabolomic signatures in follicular fluid of women undergoing in vitro fertilization.. Am J Physiol Endocrinol Metab 2019 Mar 1;316(3):E383-E396.
- Huang N, Yu Y, Qiao J. Dual role for the unfolded protein response in the ovary: adaption and apoptosis.. Protein Cell 2017 Jan;8(1):14-24.
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