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Proteasome activator subunit 3 (PSME3) plays a key role in breast cancer by regulating the cell cycle. However, its role in other pathogenesis-related features of breast cancer is unclear. In this study, we found that overexpression of PSME3 induced the epithelial–mesenchymal transition and contributed to induce the expression of cancer stem cell markers of the MDA-MB-231 cell line, thus increasing the migration, and invasion of the cells. Moreover, overexpression of PSME3 reduced the chemotaxis of CD8+ T cells and induced the apoptosis of T cells in vitro. Furthermore, PSME3 knockdown increased the number of CD8+ T cells in vivo and reduced the subcutaneous tumor growth rate. These findings revealed that PSME3 induces epithelial–mesenchymal transition with inducing the expression of CSC markers and influencing the tumor immune microenvironment in breast cancer.PSME3 induces the epithelial–mesenchymal transition in the MDA-MB-231 cell line.PSME3 promotes the migration, invasion, and proliferation of MDA-MB-231 cells.PSME3 induces the expression of CSC markers of the MDA-MB-231 cell line.PSME3 expression induces T-cell apoptosis and increases subcutaneous tumor growth.