Enhanced Delivery of Lipid Nanoparticle-Based Immunotherapy by Modulating the Tumor Tissue Stiffness Using Ultrasound-Activated Nanobubbles

Anubhuti, Bhalotia, Diarmuid W., Hutchinson, Theresa, Kosmides, Pinunta, Nittayacharn, Meghna, Mehta, Arya, Iyer, Andrew, Cheplyansky, Koki H., Takizawa, Abraham, Nidhiry, Anna M., Dever, Kyle A., Cousens, Inga M., Hwang, Gopalakrishnan, Ramamurthy, Agata A., Exner, Efstathios, Karathanasis

ACS nano |

Tumors often exhibit an extracellular matrix with elevated stiffness due to excessive accumulation and cross-linking of proteins, particularly collagen. This elevated stiffness acts as a physical barrier, impeding the infiltration of immune cells and the effective delivery of various immunotherapeutic agents, such as lipid nanoparticle-based RNA therapeutics. Here, we investigate the ability of ultrasound-activated nanobubbles (US-NBs) to increase the permeability and immunogenicity of tumors. Our results show that US-NBs physically remodel the tumor tissue by decreasing its stiffness by 60% 5 days after a single treatment. US-NB-treated tumors display randomly oriented collagen with a 5.47-fold lower deposition compared to untreated tumors. This leads to the effective delivery and widespread distribution of lipid nanoparticles (LNPs) in the tumor. Importantly, when assisted by US-NB, LNPs exhibit superior gene-transfection efficiency across pan-immune cells and achieve efficient genetic modification of T cells directly in vivo. This combined approach engages both innate and adaptive immunity, enhancing tumor immunogenicity and boosting cytotoxic cell infiltration by 4-fold compared to LNPs alone. These results indicate that gentle mechanical stimulation of the tumor using US-NB offers a promising strategy to augment the delivery and efficacy of existing immunotherapies.