A novel BCB-based classification system reveals distinct chromatin and nucleolar signatures associated with oocyte developmental competence

Oocyte maturity significantly influences developmental competence. Although individual aspects of oocyte quality have been relatively well characterized and supported by various methodological approaches, their interconnection and comprehensive evaluation are often lacking. On the one hand, cytoplasmic maturation plays an important role. On the other hand, chromatin configurational changes lead to the progressive silencing of transcriptional activity. Considerably less attention, however, has been devoted to the unique structure known as the nucleolus-like body (NLB), which plays a key role in chromatin organization and may significantly influence its remodelling during oocyte maturation. The present study introduces a novel three-category oocyte classification system based on modified native Brilliant Cresyl Blue staining and characterizes the individual categories according to their characteristic patterns of chromatin organization. The proposed classification distinguished BCB+, BCB+/- and BCB- oocytes and revealed category-specific patterns of chromatin organization associated with differences in developmental competence. We further investigated the relationship between this classification, oocyte developmental competence, and the functional relevance of the associated NLB. Micromanipulation transfer of NLBs from fully grown BCB+ oocytes markedly improved meiotic maturation of BCB+/- oocytes and partially restored their subsequent developmental performance. Together, these findings demonstrate that the proposed classification identifies oocyte populations differing in chromatin organization and developmental competence and provide further evidence of an association between NLB properties and the acquisition of developmental competence.