Sonogenic malate depleting modulator for tumor metabolic reprogramming and antitumor immune activation.
Run Yang, Bowen Li, Yun Fu, Chenxu Shang, Guoqing Feng, Xuheng Chen, Huining He, Zhengmian Zhang, Yang Bai, Bin Zheng
Abstract
Open AccessThe malate/aspartate shuttle is essential for maintaining mitochondrial membrane potential (MMP) and supporting tumor metabolism and survival. However, developing effective, controllable strategies to manipulate malate metabolism in vivo remains a challenge. Here, we report a sonogenically activated malate depletion modulator (MDM), GO/BCT:Mn, which integrates graphene oxide (GO) with Ca/Mn co-doped barium titanate (BCT:Mn) nanoparticles, enabling simultaneous metabolic and immune modulation under ultrasonic stimulation. Mechanistic studies reveal ultrasound triggers spatial charge separation in GO/BCT:Mn, generating reductive electrons and oxidative holes. Electrons drive the reduction of H+ to H2, lowering MMP and providing a gas therapy effect, whereas oxidative holes convert NADH to NAD+, suppressing malate synthesis and disrupting the malate/aspartate shuttle, thereby impairing mitochondrial integrity. These synergistic actions induce mitochondrial depolarization, autophagy, and apoptosis. In a murine colon cancer model, treatment with GO/BCT:Mn markedly suppressed tumor cell proliferation (Ki67) and angiogenesis (VEGF, CD31), while promoting apoptosis (TUNEL, Caspase-3). Transcriptomic and flow cytometry analyses further revealed activation of immune-related pathways, accompanied by increased infiltration of CD4+/CD8+ T cells and mature dendritic cells, indicating that metabolic perturbation synergistically enhances anti-tumor immunity. Collectively, this work establishes a precise ultrasound-responsive nanoplatform that couples redox-mediated metabolic disruption with immune activation, offering a promising strategy for integrated metabolism-immune cancer therapy.