Precisely Controlling the Activation of an Iron-Locked Drug Generator in the Liver Sinusoid to Enhance Barrier Penetration and Reduction of Liver Fibrosis

J Am Chem Soc. 2024 Nov 25. doi: 10.1021/jacs.4c11988. Online ahead of print.

Abstract

Complex physical barriers and the nanomaterial's clearance mechanism in the liver greatly hinder the feasibility of using a conventional liver-targeting nanoplatform to deliver antifibrotic drugs to pathological sites for the treatment of liver fibrosis. Here, a novel drug delivery strategy was designed to overcome drug penetration barriers in a fibrotic liver and cooperated with oral nattokinase (NKase)-mediated antifibrosis therapy as a proof of concept, which relies on the coadministration of a nanosized iron-locked drug generator (named Pro-HAase) and orally absorbed iron chelator deferasirox (DFX). Such a strategy starts from the rapid accumulation of intravenously injected Pro-HAase in the microcapillaries of the fibrotic liver followed by disrupting the polyphenol-iron coordination inside Pro-HAase by DFX, liberating antifibrotic components, including procyanidine (PA) and hyaluronidase (HAase). Attractively, absorption of DFX requires the sequential processes of traversing the intestinal mucosa and targeting the liver, which enable DFX to preferentially disassemble Pro-HAase accumulated in the liver sinusoid rather than in systemic circulation or other organs, thus avoiding the off-target activation of Pro-HAase and depletion of the normal iron pool. The in situ disassembly process decreases the sequestration of Pro-HAase by cells of the mononuclear phagocyte system and promotes gradient-driven permeation of therapeutic components to surrounding liver tissues within 2 h, accompanied by biliary excretion of the inactive iron-DFX complex. As a result, the cooperation of Pro-HAase and DFX not only allows NKase-mediated therapy to completely reverse liver fibrosis but also suppresses the chronic hepatotoxicity of residual liver iron after multiple doses of Pro-HAase. The high spatiotemporal precision, unique barrier-penetration mechanism, and self-detoxification ability of this strategy will inspire the rational design of analogous iron-locked nanosystems to improve the therapeutic outcomes of liver fibrosis or other liver diseases.