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Reproduction (Cambridge, England)2021; 161(4); 399-409; doi: 10.1530/REP-20-0494

Equine maternal aging affects oocyte lipid content, metabolic function and developmental potential.

Abstract: Advanced maternal age is associated with a decline in fertility and oocyte quality. We used novel metabolic microsensors to assess effects of mare age on single oocyte and embryo metabolic function, which has not yet been similarly investigated in mammalian species. We hypothesized that equine maternal aging affects the metabolic function of oocytes and in vitro-produced early embryos, oocyte mitochondrial DNA (mtDNA) copy number, and relative abundance of metabolites involved in energy metabolism in oocytes and cumulus cells. Samples were collected from preovulatory follicles from young (≤14 years) and old (≥20 years) mares. Relative abundance of metabolites in metaphase II oocytes (MII) and their respective cumulus cells, detected by liquid and gas chromatography coupled to mass spectrometry, revealed that free fatty acids were less abundant in oocytes and more abundant in cumulus cells from old vs young mares. Quantification of aerobic and anaerobic metabolism, respectively measured as oxygen consumption rate (OCR) and extracellular acidification rate (ECAR) in a microchamber containing oxygen and pH microsensors, demonstrated reduced metabolic function and capacity in oocytes and day-2 embryos originating from oocytes of old when compared to young mares. In mature oocytes, mtDNA was quantified by real-time PCR and was not different between the age groups and not indicative of mitochondrial function. Significantly more sperm-injected oocytes from young than old mares resulted in blastocysts. Our results demonstrate a decline in oocyte and embryo metabolic activity that potentially contributes to the impaired developmental competence and fertility in aged females.
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Publication Date: 2021-02-05 PubMed ID: 33539317PubMed Central: PMC7969451DOI: 10.1530/REP-20-0494Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates how advanced maternal age in horses impacts the fertility and quality of eggs, specifically evaluating metabolic functions, differences in mitochondrial DNA, and relative abundance of energy metabolism elements in the oocytes and cumulus cells. The study found that aging negatively affects metabolic functionality and capacity, and fewer fertilized eggs from older mares result in blastocysts, indicating lowered fertility.

Effects of Maternal Age on Fertility and Oocyte Quality

  • The study started from the understanding that advanced maternal age associates with a decrease in fertility and quality of eggs.
  • Using metabolic microsensors, the research delved into the effect of a mare’s age on the metabolic functions of single oocytes and early embryos produced in vitro. This type of inquiry was yet unexplored in mammalian species.

Mitochondrial Function and Metabolites

  • The researchers hypothesized that equine maternal aging impacts the metabolic functions of oocytes and early-stage embryos that are produced through vitro.
  • They also theorized that this aging impacts the copy number of mitochondrial DNA in the oocytes, as well as the relative abundance of metabolites involved in energy metabolism in both the oocytes and the cumulus cells.
  • No difference was found in terms of mitochondrial DNA between the different age groups, suggesting that this is not a determinant of mitochondrial function.

Investigations and Results

  • Metaphase II oocytes and their respective cumulus cells were examined using liquid and gas chromatography, coupled with mass spectrometry.
  • It was found that in older mares, free fatty acids were less abundant in oocytes and more abundant in cumulus cells in comparison to younger mares.
  • Quantification of aerobic and anaerobic metabolism was carried out, measured as oxygen consumption rate and extracellular acidification rate using sensors in a microchamber. This examination revealed reduced metabolic function and capacity in oocytes and day-2 embryos from older mares.
  • In terms of developmental competence, significantly fewer fertilized eggs from older mares resulted in blastocysts.

Conclusion

  • The study concluded that there is a decline in metabolic activity in oocytes and embryos as a mare ages which potentially contributes to decreased fertility and developmental competence in aged females.

Cite This Article

APA
Catandi GD, Obeidat YM, Broeckling CD, Chen TW, Chicco AJ, Carnevale EM. (2021). Equine maternal aging affects oocyte lipid content, metabolic function and developmental potential. Reproduction, 161(4), 399-409. https://doi.org/10.1530/REP-20-0494

Publication

Reproduction (Cambridge, England)
ISSN: 1741-7899
NlmUniqueID: 100966036
Country: England
Language: English
Volume: 161
Issue: 4
Pages: 399-409
PII: REP-20-0494

Researcher Affiliations

Catandi, Giovana D
  • Equine Reproduction Laboratory, Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Obeidat, Yusra M
  • Electronic Engineering Department, Hijjawi Faculty for Engineering Technology, Yarmouk University, Irbid, Jordan.
Broeckling, Corey D
  • Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, Colorado, USA.
Chen, Thomas W
  • Department of Electrical and Computer Engineering, Colorado State University, Fort Collins, Colorado, USA.
Chicco, Adam J
  • Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Carnevale, Elaine M
  • Equine Reproduction Laboratory, Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.

MeSH Terms

  • Animals
  • Cumulus Cells / metabolism
  • Cumulus Cells / pathology
  • DNA, Mitochondrial / analysis
  • DNA, Mitochondrial / genetics
  • Female
  • Gene Expression Regulation, Developmental
  • Horses
  • In Vitro Oocyte Maturation Techniques / veterinary
  • Lipids / analysis
  • Maternal Age
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Oocytes / metabolism
  • Oocytes / pathology
  • Oogenesis
  • Oxygen Consumption

Grant Funding

  • R21 HD097601 / NICHD NIH HHS

Conflict of Interest Statement

Declaration of interest. The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

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