Abstract Microparticles (MPs) are secreted by all cells where they play a key role in intercellular communication, differentiation, inflammation, and cell energy transfer. P2×7 receptor (P2×7R) activation by extracellular ATP (eATP) causes a large MP release and affects their contents in a cell-specific fashion. We investigated MP release and functional impact in microglial cells from P2×7R-WT or P2×7R-KO mice, as well as mouse microglial cell lines characterized for high (N13-P2×7RHigh) or low (N13-P2×7RLow) P2×7R expression. P2×7R stimulation promoted release of a mixed MP population enriched with naked mitochondria. Released mitochondria were taken up and incorporated into the mitochondrial network of the recipient cells in a P2×7R-dependent fashion. NLRP3 and the P2×7R itself were also delivered to the recipient cells. MP transfer increased the energy level of the recipient cells and conferred a pro-inflammatory phenotype. These data show that the P2×7R is a master regulator of intercellular organelle and MP trafficking in immune cells.