The role of SRPK1-mediated phosphorylation of SR proteins in the chromatin configuration transition of mouse germinal vesicle oocytes.

Meiotic resumption in mammalian oocytes involves nuclear and organelle structural changes, notably the chromatin configuration transition from a non-surrounding nucleolus (NSN) to surrounding nucleolus (SN) in germinal vesicle oocytes. In the current study, we found that nuclear speckles (NSs), a subnuclear structure mainly composed of serine-arginine (SR) proteins, changed from a diffuse spotted distribution in mouse NSN oocytes to an aggregated pattern in SN oocytes. We also found that the SR protein-specific kinase 1 (SRPK1), an enzyme that phosphorylates SR proteins, co-localized with NSs at the SN stage, and that NSN oocytes failed to transition to SN oocytes after the inhibition of SRPK1 activity. Furthermore, the typical structure of the chromatin ring around the nucleolus in SN oocytes collapsed after treatment with an SRPK1 inhibitor. Mechanistically, phosphorylated SR proteins were found to be related to chromatin as shown by a salt extraction experiment, and in situ DNase I assay showed that the accessibility of chromatin was enhanced in SN oocytes when SRPK1 was inhibited, accompanied by a decreased repressive modification on histone and the abnormal recurrence of a transcriptional signal. In conclusion, our results indicated that SRPK1-regulated phosphorylation of SR proteins was involved in the NSN-SN transition and played an important role in maintaining the condensed nucleus of SN oocytes via interacting with chromatin.