Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.

Our objective was to understand how maternal age influences the mitochondrial population and ATP content of in vivo matured bovine oocytes. We hypothesized that in vivo matured oocytes from older cows would have altered mitochondrial number and distribution patterns and lower cytoplasmic ATP content...

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Main Authors: Dinesh Dadarwal, Luiz Pfeifer, Miriam Cervantes, Gregg P Adams, Jaswant Singh
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0302444&type=printable
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author Dinesh Dadarwal
Luiz Pfeifer
Miriam Cervantes
Gregg P Adams
Jaswant Singh
author_facet Dinesh Dadarwal
Luiz Pfeifer
Miriam Cervantes
Gregg P Adams
Jaswant Singh
author_sort Dinesh Dadarwal
collection DOAJ
description Our objective was to understand how maternal age influences the mitochondrial population and ATP content of in vivo matured bovine oocytes. We hypothesized that in vivo matured oocytes from older cows would have altered mitochondrial number and distribution patterns and lower cytoplasmic ATP content compared to the oocytes obtained from younger cows. Follicles ≥5mm were ablated in old cows (13 to 22 yrs, Old Group, n = 7) and their younger daughters (4 to 10 years old, Young Group; n = 7) to induce the emergence of a new follicular wave. Cows were treated twice daily with eight doses of FSH starting 24 hr after ablation (Day 0, day of wave emergence). Prostaglandin F2alpha (PGF) was given on Days 3 and 3.5, LH on Day 4.5, and cumulus-oocyte-complexes were collected 18-20 hours post-LH by ultrasound-guided follicular aspiration. Oocytes were either processed for staining with MitoTracker Deep Red FM or for ATP assay. Stained oocytes were imaged with a Zeiss LSM 710 confocal microscope, and mitochondria were segmented in the oocyte volume sets using Imaris Pro 7.4. In vivo matured oocytes obtained from old cows were similar in morphological grades to those from young cows. However, the oocytes of COC from older cows had 23% less intracellular ATP (27.4±1.9 vs 35.7±2.2 pmol per oocyte, P = 0.01) than those of young cows. Furthermore, the average volume of individual mitochondria, indicated by the number of image voxels, was greater (P<0.05) in oocytes from older cows than in those from younger cows. Oocytes from older cows also tended to have a greater number of mitochondrial clusters (P = 0.06) and an increased number of clusters in the central region of the oocytes (P = 0.04) compared to those from younger cows. In conclusion, our study demonstrated that maternal age was associated with a decrease in the cytoplasmic ATP content of in vivo mature oocytes and an altered distribution of mitochondrial structures. These findings suggest that maternal age may negatively influence the developmental competence of oocytes from older cows.
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spelling doaj.art-7cdf15c93ba440a88904ac5128aaf8462024-04-23T05:31:53ZengPublic Library of Science (PLoS)PLoS ONE1932-62032024-01-01194e030244410.1371/journal.pone.0302444Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.Dinesh DadarwalLuiz PfeiferMiriam CervantesGregg P AdamsJaswant SinghOur objective was to understand how maternal age influences the mitochondrial population and ATP content of in vivo matured bovine oocytes. We hypothesized that in vivo matured oocytes from older cows would have altered mitochondrial number and distribution patterns and lower cytoplasmic ATP content compared to the oocytes obtained from younger cows. Follicles ≥5mm were ablated in old cows (13 to 22 yrs, Old Group, n = 7) and their younger daughters (4 to 10 years old, Young Group; n = 7) to induce the emergence of a new follicular wave. Cows were treated twice daily with eight doses of FSH starting 24 hr after ablation (Day 0, day of wave emergence). Prostaglandin F2alpha (PGF) was given on Days 3 and 3.5, LH on Day 4.5, and cumulus-oocyte-complexes were collected 18-20 hours post-LH by ultrasound-guided follicular aspiration. Oocytes were either processed for staining with MitoTracker Deep Red FM or for ATP assay. Stained oocytes were imaged with a Zeiss LSM 710 confocal microscope, and mitochondria were segmented in the oocyte volume sets using Imaris Pro 7.4. In vivo matured oocytes obtained from old cows were similar in morphological grades to those from young cows. However, the oocytes of COC from older cows had 23% less intracellular ATP (27.4±1.9 vs 35.7±2.2 pmol per oocyte, P = 0.01) than those of young cows. Furthermore, the average volume of individual mitochondria, indicated by the number of image voxels, was greater (P<0.05) in oocytes from older cows than in those from younger cows. Oocytes from older cows also tended to have a greater number of mitochondrial clusters (P = 0.06) and an increased number of clusters in the central region of the oocytes (P = 0.04) compared to those from younger cows. In conclusion, our study demonstrated that maternal age was associated with a decrease in the cytoplasmic ATP content of in vivo mature oocytes and an altered distribution of mitochondrial structures. These findings suggest that maternal age may negatively influence the developmental competence of oocytes from older cows.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0302444&type=printable
spellingShingle Dinesh Dadarwal
Luiz Pfeifer
Miriam Cervantes
Gregg P Adams
Jaswant Singh
Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
PLoS ONE
title Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
title_full Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
title_fullStr Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
title_full_unstemmed Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
title_short Effect of maternal age on ATP content and distribution of mitochondria in bovine oocytes.
title_sort effect of maternal age on atp content and distribution of mitochondria in bovine oocytes
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0302444&type=printable
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