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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

Kinetics of in vitro maturation in prepubertal and adult oocytes.Values are expressed as (A) percentages of prepubertal (n = 1186) and adult (n = 1139) oocytes that reached MI at 6 to 9 hrs of maturation culture and (B) percentages of prepubertal (n = 1026) and adult (n = 981) oocytes that reached MII stages between 19 and 22 hrs of maturation culture. *indicates statistical difference at each time point between the two experimental groups; (Chi square test: P<0.001).
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pone.0124911.g001: Kinetics of in vitro maturation in prepubertal and adult oocytes.Values are expressed as (A) percentages of prepubertal (n = 1186) and adult (n = 1139) oocytes that reached MI at 6 to 9 hrs of maturation culture and (B) percentages of prepubertal (n = 1026) and adult (n = 981) oocytes that reached MII stages between 19 and 22 hrs of maturation culture. *indicates statistical difference at each time point between the two experimental groups; (Chi square test: P<0.001).

Mentions: The kinetic of maturation differs between adult and prepubertal oocytes. As showed in Fig 1A, oocytes derived from adult (n = 1139) and prepubertal (n = 1186) ewes reached the MI stage with a different timing. At 7 hrs of culture, MI rates were higher in adult than in prepubertal oocytes (34.7% vs 14.1% in adult and prepubertal oocytes respectively; P<0.001). Prepubertal oocytes reached similar MI rates only between 8 and 9 hrs of culture, indicating a delay in the kinetic of maturation of at least 1 hour. The delay in meiotic progression in prepubertal oocytes was confirmed by data obtained during MI-MII transition, monitored from 19 to 22 hrs of IVM. As showed in Fig 1B, the MII stage was reached earlier in adult (n = 1026) than in prepubertal (n = 981) oocytes (P<0.001). In fact at 19 hrs of culture the MII nuclear plate was observed in the 70.4% of adult oocytes compared to the 36.4% of prepubertal ones. Prepubertal oocytes reached MII rates comparable with adult ones only at 22 hrs of in vitro culture.


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)

Kinetics of in vitro maturation in prepubertal and adult oocytes.Values are expressed as (A) percentages of prepubertal (n = 1186) and adult (n = 1139) oocytes that reached MI at 6 to 9 hrs of maturation culture and (B) percentages of prepubertal (n = 1026) and adult (n = 981) oocytes that reached MII stages between 19 and 22 hrs of maturation culture. *indicates statistical difference at each time point between the two experimental groups; (Chi square test: P<0.001).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0124911.g001: Kinetics of in vitro maturation in prepubertal and adult oocytes.Values are expressed as (A) percentages of prepubertal (n = 1186) and adult (n = 1139) oocytes that reached MI at 6 to 9 hrs of maturation culture and (B) percentages of prepubertal (n = 1026) and adult (n = 981) oocytes that reached MII stages between 19 and 22 hrs of maturation culture. *indicates statistical difference at each time point between the two experimental groups; (Chi square test: P<0.001).
Mentions: The kinetic of maturation differs between adult and prepubertal oocytes. As showed in Fig 1A, oocytes derived from adult (n = 1139) and prepubertal (n = 1186) ewes reached the MI stage with a different timing. At 7 hrs of culture, MI rates were higher in adult than in prepubertal oocytes (34.7% vs 14.1% in adult and prepubertal oocytes respectively; P<0.001). Prepubertal oocytes reached similar MI rates only between 8 and 9 hrs of culture, indicating a delay in the kinetic of maturation of at least 1 hour. The delay in meiotic progression in prepubertal oocytes was confirmed by data obtained during MI-MII transition, monitored from 19 to 22 hrs of IVM. As showed in Fig 1B, the MII stage was reached earlier in adult (n = 1026) than in prepubertal (n = 981) oocytes (P<0.001). In fact at 19 hrs of culture the MII nuclear plate was observed in the 70.4% of adult oocytes compared to the 36.4% of prepubertal ones. Prepubertal oocytes reached MII rates comparable with adult ones only at 22 hrs of in vitro culture.

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