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Differences in the Kinetic of the First Meiotic Division and in Active Mitochondrial Distribution between Prepubertal and Adult Oocytes Mirror Differences in their Developmental Competence in a Sheep Model.

Leoni GG, Palmerini MG, Satta V, Succu S, Pasciu V, Zinellu A, Carru C, Macchiarelli G, Nottola SA, Naitana S, Berlinguer F - PLoS ONE (2015)

Bottom Line: Maturation and fertilization rates did not differ between prepubertal and adult oocytes (95.1% vs 96.7% and 66.73% vs 70.62% respectively for prepubertal and adult oocytes).In prepubertal oocytes ATP rise is delayed and did not reach levels comparable to adult ones.Taken together our data suggest that oocytes with low developmental competence have a slowed down energetic metabolism which delays later development.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Medicine, Sassari University, Sassari, Italy; Sardinian Animal Biodiversity Center (Centro di Competenza per la Biodiversità Animale-CCBA), Sassari, Italy.

ABSTRACT
Our aim is to verify if oocyte developmental potential is related to the timing of meiotic progression and to mitochondrial distribution and activity using prepubertal and adult oocytes as models of low and high developmental capacity respectively. Prepubertal and adult oocytes were incorporated in an in vitro maturation system to determine meiotic and developmental competence and to assess at different time points kinetic of meiotic maturation, 2D protein electrophoresis patterns, ATP content and mitochondria distribution. Maturation and fertilization rates did not differ between prepubertal and adult oocytes (95.1% vs 96.7% and 66.73% vs 70.62% respectively for prepubertal and adult oocytes). Compared to adults, prepubertal oocytes showed higher parthenogenesis (17.38% vs 2.08% respectively in prepubertals and adults; P<0.01) and polispermy (14.30% vs 2.21% respectively in prepubertals and adults; P<0.01), lower cleavage rates (60.00% vs 67.08% respectively in prepubertals and adults; P<0.05) and blastocyst output (11.94% vs 34.% respectively in prepubertals and adults; P<0.01). Prepubertal oocytes reached MI stage 1 hr later than adults and this delay grows as the first meiotic division proceeds. Simultaneously, the protein pattern was altered since in prepubertal oocytes it fluctuates, dropping and rising to levels similar to adults only at 24 hrs. In prepubertal oocytes ATP rise is delayed and did not reach levels comparable to adult ones. CLSM observations revealed that at MII, in the majority of prepubertal oocytes, the active mitochondria are homogenously distributed, while in adults they are aggregated in big clusters. Our work demonstrates that mitochondria and their functional aggregation during maturation play an active role to provide energy in terms of ATP. The oocyte ATP content determines the timing of the meiotic cycle and the acquisition of developmental competence. Taken together our data suggest that oocytes with low developmental competence have a slowed down energetic metabolism which delays later development.

No MeSH data available.


Related in: MedlinePlus

Morphology of prepubertal (a) and adult (b) ovine oocytes at 7 hrs of IVM.Representative low magnification TEM micrograph, showing the oocytes surrounded by a continuous zona pellucida (ZP), with clusters of mitochondria (m) located in the cortex. Bar: 5 μm. Inset: high magnification of a rosette-like arrangement of mitochondria (m). GCs: granulosa cells. ZP: zona pellucida. LD: lipid droplets. V: vacuoles. Bar: 1 μm.
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pone.0124911.g007: Morphology of prepubertal (a) and adult (b) ovine oocytes at 7 hrs of IVM.Representative low magnification TEM micrograph, showing the oocytes surrounded by a continuous zona pellucida (ZP), with clusters of mitochondria (m) located in the cortex. Bar: 5 μm. Inset: high magnification of a rosette-like arrangement of mitochondria (m). GCs: granulosa cells. ZP: zona pellucida. LD: lipid droplets. V: vacuoles. Bar: 1 μm.

Mentions: The ooplasm of prepubertal and adult oocytes was rich of clusters of mitochondria dispersed among clear vacuoles of different shape and dimension, tubules of SER or elements of the Golgi apparatus (Fig 7). Mitochondrial clusters appeared sometime more prominent in prepubertal than in adult oocytes, and mostly located in the cortical ooplasm (Fig 7).


Differences in the Kinetic of the First Meiotic Division and in Active Mitochondrial Distribution between Prepubertal and Adult Oocytes Mirror Differences in their Developmental Competence in a Sheep Model.

Leoni GG, Palmerini MG, Satta V, Succu S, Pasciu V, Zinellu A, Carru C, Macchiarelli G, Nottola SA, Naitana S, Berlinguer F - PLoS ONE (2015)

Morphology of prepubertal (a) and adult (b) ovine oocytes at 7 hrs of IVM.Representative low magnification TEM micrograph, showing the oocytes surrounded by a continuous zona pellucida (ZP), with clusters of mitochondria (m) located in the cortex. Bar: 5 μm. Inset: high magnification of a rosette-like arrangement of mitochondria (m). GCs: granulosa cells. ZP: zona pellucida. LD: lipid droplets. V: vacuoles. Bar: 1 μm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4403920&req=5

pone.0124911.g007: Morphology of prepubertal (a) and adult (b) ovine oocytes at 7 hrs of IVM.Representative low magnification TEM micrograph, showing the oocytes surrounded by a continuous zona pellucida (ZP), with clusters of mitochondria (m) located in the cortex. Bar: 5 μm. Inset: high magnification of a rosette-like arrangement of mitochondria (m). GCs: granulosa cells. ZP: zona pellucida. LD: lipid droplets. V: vacuoles. Bar: 1 μm.
Mentions: The ooplasm of prepubertal and adult oocytes was rich of clusters of mitochondria dispersed among clear vacuoles of different shape and dimension, tubules of SER or elements of the Golgi apparatus (Fig 7). Mitochondrial clusters appeared sometime more prominent in prepubertal than in adult oocytes, and mostly located in the cortical ooplasm (Fig 7).

Bottom Line: Maturation and fertilization rates did not differ between prepubertal and adult oocytes (95.1% vs 96.7% and 66.73% vs 70.62% respectively for prepubertal and adult oocytes).In prepubertal oocytes ATP rise is delayed and did not reach levels comparable to adult ones.Taken together our data suggest that oocytes with low developmental competence have a slowed down energetic metabolism which delays later development.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Medicine, Sassari University, Sassari, Italy; Sardinian Animal Biodiversity Center (Centro di Competenza per la Biodiversità Animale-CCBA), Sassari, Italy.

ABSTRACT
Our aim is to verify if oocyte developmental potential is related to the timing of meiotic progression and to mitochondrial distribution and activity using prepubertal and adult oocytes as models of low and high developmental capacity respectively. Prepubertal and adult oocytes were incorporated in an in vitro maturation system to determine meiotic and developmental competence and to assess at different time points kinetic of meiotic maturation, 2D protein electrophoresis patterns, ATP content and mitochondria distribution. Maturation and fertilization rates did not differ between prepubertal and adult oocytes (95.1% vs 96.7% and 66.73% vs 70.62% respectively for prepubertal and adult oocytes). Compared to adults, prepubertal oocytes showed higher parthenogenesis (17.38% vs 2.08% respectively in prepubertals and adults; P<0.01) and polispermy (14.30% vs 2.21% respectively in prepubertals and adults; P<0.01), lower cleavage rates (60.00% vs 67.08% respectively in prepubertals and adults; P<0.05) and blastocyst output (11.94% vs 34.% respectively in prepubertals and adults; P<0.01). Prepubertal oocytes reached MI stage 1 hr later than adults and this delay grows as the first meiotic division proceeds. Simultaneously, the protein pattern was altered since in prepubertal oocytes it fluctuates, dropping and rising to levels similar to adults only at 24 hrs. In prepubertal oocytes ATP rise is delayed and did not reach levels comparable to adult ones. CLSM observations revealed that at MII, in the majority of prepubertal oocytes, the active mitochondria are homogenously distributed, while in adults they are aggregated in big clusters. Our work demonstrates that mitochondria and their functional aggregation during maturation play an active role to provide energy in terms of ATP. The oocyte ATP content determines the timing of the meiotic cycle and the acquisition of developmental competence. Taken together our data suggest that oocytes with low developmental competence have a slowed down energetic metabolism which delays later development.

No MeSH data available.


Related in: MedlinePlus