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Cardiovascular disease, mainly originated from atherosclerosis and its complication, has been the leading cause of death worldwide for the past 30 years. In a healthy vessel, T cells are located in the adventitia that are found repopulated predominately in the fibrous cap of the atherosclerotic lesions. CD8+ T cells outnumber CD4+ T cells in the advanced stage. Nevertheless, it has been generally acknowledged that CD8+ T cells contribute to atherogenesis but their action mechanism remains largely unknown. Here, we demonstrate that CD8+ T cells govern phenotypic switching of contractile vascular smooth muscle cells (VSMCs) during the formation of the atherosclerotic plaque. We also uncover the therapeutic potential of a non-lytic anti-CD8 monoclonal antibody in the induction of CD8+ Treg that regulate atherogenesis by targeting direct CD8-VSMC communication. Our studies could give clinically relevant insights into the development of CD8+ Treg-targeted therapy as an alternative treatment option against atherosclerotic cardiovascular diseases.