A Three-In-One Heptamethine Cyanine Dye Induces Endoplasmic Reticulum Stress and Apoptosis in Colorectal Cancer

Adv Healthc Mater. 2024 Dec 25:e2404027. doi: 10.1002/adhm.202404027. Online ahead of print.

Abstract

One of the most significant challenges for image-guided cancer-targeted therapy is to develop multifunctional optical contrast agents enabling simultaneous targeting and therapy. Herein, a feasible strategy is based on the incorporation of therapeutic moieties into the non-delocalized structure of polymethine indocyanines, known as the "structure-inherent targeting" concept. By possessing a rigid chloro-cyclohexenyl ring in the heptamethine cyanine backbone, a new type of multifunctional near-infrared fluorescent dye, Ph790H, that targets tumor without the need for additional targeting ligands is synthesized. Armed with a phthalimide pharmacophore holding a prominent position in medicinal chemistry, Ph790H simultaneously induces endoplasmic reticulum (ER) stress to exert targeted therapeutic effects on HT-29 colorectal cancer xenografts. In terms of molecular mechanism, the lipophilic cationic Ph790H can be actively internalized into HT-29 cells through clathrin-mediated endocytosis. Consequently, mitochondrial reactive oxygen species (ROS) overproduction further induces activation of ER stress, demonstrated by increased ROS concentration and decreased mitochondrial membrane potential, which contributes to cell apoptosis and inhibition of tumor growth. Overall, Ph790H represents an effective "three-in-one" agent for the integration of cancer targeting, imaging, and therapy, which may provide a practical strategy to develop multifunctional small molecule theranostic agents for simultaneous cancer diagnosis and therapy.

Keywords: ER stress; heptamethine cyanine dyes; near‐infrared fluorescence imaging; reactive oxygen species; tumor targeting.