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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, Giovanni Giuseppe and Palmerini, Maria Grazia and Satta, Valentina and Succu, Sara and Pasciu, Valeria and Zinellu, Angelo and Carru, Ciriaco and Macchiarelli, Guido and Nottola, Stefania Annarita and Naitana, Salvatore and Berlinguer, Fiammetta (2015) 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. PLoS One, Vol. 10 (4), p. 25. ISSN 1932-6203. Article.

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DOI: 10.1371/journal.pone.0124911

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.

Item Type:Article
ID Code:10907
Status:Published
Refereed:Yes
Uncontrolled Keywords:Adult oocytes, mitochondria distribution, prepubertal oocytes, sheep model
Subjects:Area 07 - Scienze agrarie e veterinarie > VET/02 Fisiologia veterinaria
Area 05 - Scienze biologiche > BIO/10 Biochimica
Area 05 - Scienze biologiche > BIO/12 Biochimica clinica e biologia molecolare clinica
Divisions:001 Università di Sassari > 01-a Nuovi Dipartimenti dal 2012 > Scienze Biomediche
001 Università di Sassari > 01-a Nuovi Dipartimenti dal 2012 > Medicina Veterinaria
001 Università di Sassari > 02 Centri > Centro di competenza biodiversità animale
Publisher:Public Library of Science
ISSN:1932-6203
Copyright Holders:© 2015 Leoni et al.
Additional Information:This study was supported by the Fondazione Banco di Sardegna and the Sardinian Region Council
Deposited On:05 Jun 2015 18:02

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