Mechanisms by which a lack of germinal vesicle (GV) material causes oocyte meiotic defects: a study using oocytes manipulated to replace GV with primary spermatocyte nuclei.
Oocytes with germinal vesicles (GVs) replaced with somatic nuclei exhibit meiotic abnormalities. Although this suggests an exclusive role for GV material in meiosis, mechanisms by which a lack of GV material causes meiotic defects are unknown. Knowledge of these mechanisms will help us to understand meiotic control, nuclear-cytoplasmic interactions, and cellular reprogramming. This study showed that although oocytes with prometaphase I chromosomes replaced with primary spermatocyte nuclei (PSN) did not, oocytes with GV replaced with PSN (PSG oocytes) did display meiotic defects. Among the defects, insufficient chromosome condensation with chromosome bridges was associated with spindle abnormalities. Abnormal spindle migration, cortical nonpolarization, and the aberrant spindle caused randomly positioning of cleavage furrows, leading to large first polar bodies (PB1) and unequal allocation of chromosomes and mitogen-activated protein kinases (MAPK) between oocyte and PB1. Spindle assembly checkpoint was activated but did not stop the incorrect division. The unequal MAPK allocation resulted in differences in pronuclear formation and PB1 degeneration; oocytes receiving more MAPK were more capable of forming pronuclear rudiments, whereas PB1 receiving more MAPK degenerated sooner than those that received less. Because none of the PSG oocytes or the enucleated GV oocytes injected with sperm heads showed cortical polarization in spite of chromosome localization close to the oolemma and because the PSG oocytes receiving more MAPK could form only pronuclear rudiments and not normal pronuclei, we suggest that the GV material plays essential roles in polarization and pronuclear formation on top of those played by chromosomes or MAPK. In conclusion, using PSG oocytes as models, this study has revealed the primary pathways by which a lack of GV material cause meiotic defects, laying a foundation for future research on the role of GV material in oocyte meiotic control.
College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City, People's Republic of China.
Jie
J
Zhang
Wei
W
Cui
Qing
Q
Li
Tian-Yang
TY
Wang
Hong-Shu
HS
Sui
Jun-Zuo
JZ
Wang
Ming-Jiu
MJ
Luo
Jing-He
JH
Tan
D000818:Animals; D002455:Cell Division / Q000187:drug effects; D002467:Cell Nucleus / Q000187:drug effects / Q000378:metabolism; D002478:Cells, Cultured; D022162:Cytoplasmic Vesicles / Q000187:drug effects / Q000378:metabolism*; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005260:Female; D059471:In Vitro Oocyte Maturation Techniques; D020935:MAP Kinase Signaling System / Q000187:drug effects; D008297:Male; D008540:Meiosis; D051379:Mice; D008815:Mice, Inbred Strains; D008954:Models, Biological; D053652:Nuclear Transfer Techniques; D009865:Oocytes / Q000166:cytology* / Q000187:drug effects / Q000378:metabolism; D009866:Oogenesis / Q000187:drug effects; D059705:Polar Bodies / Q000187:drug effects; D013084:Sperm-Ovum Interactions / Q000187:drug effects; D013090:Spermatocytes / Q000166:cytology* / Q000187:drug effects / Q000378:metabolism; D008941:Spindle Apparatus / Q000187:drug effects / Q000378:metabolism
D004791:Enzyme Inhibitors
GV material; chromosome condensation; cortical polarization; oocyte meiosis; somatic cell haploidization