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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

Representative electrophoretic gels of 20 oocyte proteins at 0, 7, 19 and 24 hrs of maturation culture.Arrows represent one example of a spot detectable in both prepubertal and adult oocyte protein gels at 7 hrs of maturation and detectable only in prepubertals at 19 and 24 hrs of culture.
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pone.0124911.g003: Representative electrophoretic gels of 20 oocyte proteins at 0, 7, 19 and 24 hrs of maturation culture.Arrows represent one example of a spot detectable in both prepubertal and adult oocyte protein gels at 7 hrs of maturation and detectable only in prepubertals at 19 and 24 hrs of culture.

Mentions: Fig 2 resumes data on quantification of spots resolved in 2D electrophoretic gels of proteins extracted from prepubertal and adult oocytes at different time points of in vitro maturation. After 9 hrs of in vitro culture, the number of spots were statistically lower in prepubertal than in adult gels (295.6 ±12.8 vs 376±14.2 respectively; P<0.05), while at 24 hrs more spots were counted in prepubertal gels than in adults (573±11.9 vs 449.7±15.2; P<0.01). Qualitative differences in specific spots, (i.e. spots present in gels of only one experimental group at each time) after image analysis of prepubertal and adult gels are showed in Table 2. A representative panel of the electrophoretic gels of prepubertal and adult proteins at different hours of maturation is showed in Fig 3.


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)

Representative electrophoretic gels of 20 oocyte proteins at 0, 7, 19 and 24 hrs of maturation culture.Arrows represent one example of a spot detectable in both prepubertal and adult oocyte protein gels at 7 hrs of maturation and detectable only in prepubertals at 19 and 24 hrs of culture.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0124911.g003: Representative electrophoretic gels of 20 oocyte proteins at 0, 7, 19 and 24 hrs of maturation culture.Arrows represent one example of a spot detectable in both prepubertal and adult oocyte protein gels at 7 hrs of maturation and detectable only in prepubertals at 19 and 24 hrs of culture.
Mentions: Fig 2 resumes data on quantification of spots resolved in 2D electrophoretic gels of proteins extracted from prepubertal and adult oocytes at different time points of in vitro maturation. After 9 hrs of in vitro culture, the number of spots were statistically lower in prepubertal than in adult gels (295.6 ±12.8 vs 376±14.2 respectively; P<0.05), while at 24 hrs more spots were counted in prepubertal gels than in adults (573±11.9 vs 449.7±15.2; P<0.01). Qualitative differences in specific spots, (i.e. spots present in gels of only one experimental group at each time) after image analysis of prepubertal and adult gels are showed in Table 2. A representative panel of the electrophoretic gels of prepubertal and adult proteins at different hours of maturation is showed in Fig 3.

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