The initial segment (IS) in rodents is functionally and structurally distinct from other epididymal segments and plays an important role in sperm maturation. We previously showed that, in the mouse epididymis, basal cells (BCs) extend a narrow luminal-reaching projection only in the IS, while in all other regions, they mainly nestle at the base of the epithelium. We also found that BC projections are regulated by testicular luminal factors, and the present study was aimed at characterizing the signaling pathway involved in their formation and elongation. Previous studies reported that testicular luminal factors maintain the extracellular signal-regulated kinase (ERK) in a highly phosphorylated state in the IS. We report here that the BC projections, which we call axiopodia, periodically extend and retract over time. We found that axiopodia extensions and retractions follow an oscillatory pattern. This movement is controlled by MAPK/ERK signaling pathway. Our results suggest that ERK phosphorylation plays a key role in the formation and elongation of BC projections. Such unexpected cell motility may reflect a novel mechanism by which specialized epithelial cells sample the luminal environment.