Trophoblast stem cells (TSC) give rise to all mature trophoblast lineages of the human placenta (cytotrophoblast, syncytiotrophoblast (STB) extravillous trophoblast (EVT)). The side-population technique allowed the isolation of TSCs directly from first-trimester placentae1. A similar trophoblast side-population can be isolated from term placentae, and are reduced 10-fold in fetal growth restriction. Our prior work established that term side-population trophoblasts require different culture conditions to first-trimester TSCs, in line with morphological/transcriptomic placental differences across gestation. Here, we aimed to use these refined conditions to determine whether term side-population trophoblasts exhibit similar functional capacity as their first-trimester counterparts.
Term side-population trophoblasts1 were seeded at 6000 cells/well in a 96-well plate coated with Laminin-521. Differentiation to STB/EVT was undertaken by modifying prior TSC differentiation protocols2. Undifferentiated controls were maintained in TSC-Medium containing 25ng/mL decorin and 50ng/mL IL-8. Organoid formation was undertaken in Matrigel domes3, with halved dome volume for term side-population trophoblasts, and decorin and IL-8 medium supplementation. All experiments were run in triplicate. Data are mean±SEM.
Term side-population trophoblasts could be differentiated into; a) STB as shown by up-regulation of Syncytin-1 (66.09%±9.428 in STB-Medium; 23.37%±2.307 in undifferentiated controls, p<0.05) and hCG, (25.28%±11.09 in STB-Medium, no expression in undifferentiated controls, ), or b) EVT as shown by up-regulation of HLA-G (29.05%±11.42 of cells in EVT-Medium; no expression in undifferentiated controls, p=0.0637). First-trimester side-population trophoblasts formed organoids (90.53±29.93μm diameter at 28 days), demonstrating self-renewing capacity. Term side-population trophoblasts formed smaller organoids (38.57±5.568μm diameter at day 28). Organoids could not form from pure FACS-sorted first-trimester cytotrophoblasts that had side-population trophoblasts excluded, demonstrating that side-population trophoblasts are required for organoid formation.
These data indicate term side-population trophoblasts exhibit the differentiation potential expected of a TSC population. Formation of the first term trophoblast organoids opens up their potential use as disease models.