Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice

BACKGROUND: Mammals have two types of full-grown oocytes: those with germinal vesicles (GVs) in which the chromatin is condensed and surrounds the nucleolus (surrounded-nucleolus (SN)-type) and those in which the chromatin is less condensed and does not surround the nucleolus (non-surrounded-nucleolus (NSN)-type). Although SN oocytes possess higher meiotic and developmental competence than NSN oocytes, the factors underlying this difference are unknown. METHODS AND RESULTS: The GVs of murine SN and NSN oocytes were exchanged by nuclear transfer and the nucleus/cytoplasm of each reconstructed oocyte was classified as follows: SN/SN, NSN/SN, SN/NSN or NSN/NSN. After reconstruction, the meiotic maturation and preimplantation development of the oocytes were analysed. Few mature SN/NSN and NSN/NSN oocytes were observed (20-26%). In contrast, 88% of the NSN/SN oocytes matured; however, they rarely developed to the blastocyst stage after fertilization (4%), whereas most of the SN/SN oocytes matured (84%) and reached the blastocyst stage (83%). When the metaphase II (MII) plates of in vitro-matured NSN/SN oocytes were transferred into enucleated MII oocytes in which the contents of the SN-type GVs were spread into the cytoplasm, they completed full-term development. CONCLUSIONS:The differences in meiotic and developmental competence between SN and NSN oocytes are determined by factors in the cytoplasm and nucleus, respectively. In addition, material(s) within SN-type GVs, and not the chromatin configuration itself, is essential for full-term development.