Diverse patterns of cumulus cell expansion during in vitro maturation reveal heterogeneous cellular and molecular features of oocyte competence in dromedary camel

Abstract

During in vitro maturation (IVM), the degree and pattern of cumulus cells expansion vary between cumulus oocyte complexes (COCs). This study investigated the relationship between expansion morphology of cumulus cells with the oocyte maturation quality in dromedary camel. Following IVM for 30–32 h, COCs were classified into four distinct groups according to the morphological features of COCs (adherent vs. non-adherent to the bottom of culture dish) and cumulus cells (compact vs. expanded vs. dissociated). The predominant morphology was adherent/dissociated (45.6 ± 7.1%), followed by adherent/compact (31.2 ± 6.5%), and then non-adherent/expanded (13.1 ± 2.8%) and non-adherent/compact (10.2 ± 2.4%). The adherent/dissociated morphology was correlated with the best oocyte quality in terms of MII-maturation (90.6 ± 5.0%), degeneration (22.4 ± 5.3%), reactive oxygen species (2.5 ± 0.5 arbitrary units), mitochondrial potential (12.9 ± 2.4 orange/green fluorescence intensity ratio), zona dissolution time (46 s), peripheral distribution of cortical granules (92%), and also cleavage and blastocyst development (81.3 ± 5.2 and 48.7 ± 7.2%, respectively). In contrast, adherent/compact morphology was correlated with the lowest oocyte competence when examined for the aforementioned criteria (28.1 ± 5.3%, 62.7 ± 9.2%, 6.0 ± 0.8, 2.5 ± 1.3, 102 s, 36%, and 25.7 ± 4.5 and 11.6 ± 5.1%, respectively). Non-adherent COCs, either expanded or compact, were correlated with an intermediate oocyte competence compared to the two extreme groups. In short, diverse pattern of cumulus expansion reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity in camel. Cumulus expansion morphology can be used as a non-invasive predictive marker of oocyte competence to optimize assisted reproductive technologies in camels.