Energy metabolism of the equine cumulus oocyte complex during in vitro maturation.
Abstract: Horses are one of the few species, beside humans, in which assisted reproductive technology has important clinical applications. Furthermore, the horse can serve as a valuable model for the study of comparative reproductive biology. Here we present the first comprehensive characterisation of energy metabolism and mitochondrial efficiency in equine cumulus-oocyte complexes (COCs) during in vitro maturation (IVM), as determined using a combination of non-invasive consumption and release assays and mitochondrial function analysis. These data reveal notable species-specific differences in the rate and kinetics of glucose consumption and glycolysis throughout IVM. Approximately 95% of glucose consumed was accounted for by lactate production; however, high concurrent oxygen consumption indicated a comparatively increased role for non-glycolytic oxidative phosphorylation. Up to 38% of equine COC oxygen consumption could be attributed to non-mitochondrial activities and there was a significant loss of spare respiratory capacity over the course of IVM. Notably, our data also revealed that current IVM protocols may be failing to satisfy the metabolic demands of the equine COC. Our findings constitute the first report on mitochondrial efficiency in the equine COC and provide new insight into comparative gamete biology as well as metabolism of the COC during in vitro maturation.
Publication Date: 2020-02-26 PubMed ID: 32103136PubMed Central: PMC7044441DOI: 10.1038/s41598-020-60624-zGoogle Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research presents the first detailed analysis of energy metabolism in horse cumulus-oocyte complexes (COCs) during in vitro maturation, revealing unique characteristics of glucose consumption, glycolysis, oxygen consumption and mitochondrial efficiency that suggests current maturation protocols may not meet the metabolic needs of the COC.
Study Overview
- This study is about understanding the intricate energy metabolism of a specific reproductive cell grouping in horses, called the cumulus-oocyte complexes (COCs) during in vitro (in the lab) maturation process.
- The purpose of this research is not only to understand this process in horses specifically, but also to use the horse as a model for studying reproduction in other species, including humans.
Methods and Findings
- The researchers used non-invasive consumption and release assays and mitochondrial function analysis to measure energy metabolism during COC’s in vitro maturation.
- One finding was that horse COCs displayed unique patterns of glucose consumption and glycolysis (breakdown of glucose for energy) throughout in vitro maturation, compared to other species.
- About 95% of glucose consumed was converted into lactate (a product of glycolysis). Simultaneously, high oxygen consumption indicated a significant role of non-glycolytic oxidative phosphorylation (a different energy-producing process).
- Up to 38% of the oxygen consumption of horse COCs, however, was attributed to non-mitochondrial activities—actions not related to the cell’s powerhouses.
- There was a significant loss of the COCs’ reserve energy over the course of in vitro maturation.
Implications
- These findings show that current in vitro maturation practices may be insufficient for the metabolic demands of horse COCs.
- This creates potential for improving these protocols to better accommodate the cell group’s unique metabolism during maturation.
- The researchers’ findings on the horse COCs’ mitochondrial efficiency were the first of their kind—bringing new insights into how gametes (reproductive cells) function and metabolize energy in horses and possibly in other species as well.
Cite This Article
APA
Lewis N, Hinrichs K, Leese HJ, McG Argo C, Brison DR, Sturmey R.
(2020).
Energy metabolism of the equine cumulus oocyte complex during in vitro maturation.
Sci Rep, 10(1), 3493.
https://doi.org/10.1038/s41598-020-60624-z Publication
Researcher Affiliations
- Institute of Ageing and Chronic Disease, University of Liverpool, Cheshire, UK. n.lewis@liv.ac.uk.
- Texas A&M University, College Station, Texas, USA.
- Cardiovascular and Metabolic Research, Hull York Medical School, University of Hull, Hull, Yorkshire, UK.
- Institute of Ageing and Chronic Disease, University of Liverpool, Cheshire, UK.
- Scotland's Rural College (SRUC), Northern Faculty, Craibstone Campus, Aberdeen, AB21 9YA, Scotland.
- Maternal and Fetal Health Research, Faculty of Biology, Medicine & Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK.
- Cardiovascular and Metabolic Research, Hull York Medical School, University of Hull, Hull, Yorkshire, UK.
MeSH Terms
- Animals
- Cells, Cultured
- Cumulus Cells / cytology
- Energy Metabolism
- Glucose / metabolism
- Glycolysis
- Horses
- In Vitro Oocyte Maturation Techniques
- Mitochondria / metabolism
- Oocytes / cytology
- Oocytes / metabolism
- Oxygen Consumption
Grant Funding
- Biotechnology and Biological Sciences Research Council
Conflict of Interest Statement
The authors declare no competing interests.
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Citations
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