Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis

Abstract It is highly desired to achieve Type‐I photosensitizer (PS) to overcome the hypoxic limitation found in most clinically used PSs. Herein, a new heavy‐atom‐free Type‐I PS T‐BNCy5 is presented by incorporating a biotin‐modified naphthalimide (NI) unit into the meso‐position of a N‐benzyl‐func...

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Main Authors: Guangxiao Yao, Junfeng Miao, Yingying Huo, Wei Guo
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202417179
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author Guangxiao Yao
Junfeng Miao
Yingying Huo
Wei Guo
author_facet Guangxiao Yao
Junfeng Miao
Yingying Huo
Wei Guo
author_sort Guangxiao Yao
collection DOAJ
description Abstract It is highly desired to achieve Type‐I photosensitizer (PS) to overcome the hypoxic limitation found in most clinically used PSs. Herein, a new heavy‐atom‐free Type‐I PS T‐BNCy5 is presented by incorporating a biotin‐modified naphthalimide (NI) unit into the meso‐position of a N‐benzyl‐functionalized, strongly photon‐capturing pentamethine cyanine (Cy5) dye. Such molecular engineering induces a rigid orthogonal geometry between NI and Cy5 units by introducing an intramolecular sandwich‐like π–π stacking assembly, which effectively promotes intersystem crossing (ISC) and greatly extends the triplet‐state lifetime (τ = 389 µs), thereby markedly improving the superoxide (O2•−)‐generating ability. In vitro assays reveal that T‐BNCy5 specifically accumulates in mitochondria, where it not only generates O2•− under photoirradiation but also induces the burst of the most cytotoxic hydroxy radical (HO•) by a cascade of biochemical reactions, ultimately triggering cell ferroptosis with the IC50 value up to ≈0.45 µm whether under normoxia or hypoxia. In vivo assays manifest that, benefiting from its biotin unit, T‐BNCy5 displays a strong tumor‐targeting ability, and after a single PDT treatment, it can not only ablate the tumor almost completely but also be cleared from the body through biosafe urinary excretion, indicating its potential for future clinical translation.
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spelling doaj-art-2a3cdd456cfb43e4923424cf82a65b652025-08-20T03:48:47ZengWileyAdvanced Science2198-38442025-05-011217n/an/a10.1002/advs.202417179Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing FerroptosisGuangxiao Yao0Junfeng Miao1Yingying Huo2Wei Guo3School of Chemistry and Chemical Engineering Shanxi University Taiyuan 030006 ChinaSchool of Chemistry and Chemical Engineering Shanxi University Taiyuan 030006 ChinaSchool of Chemistry and Chemical Engineering Shanxi University Taiyuan 030006 ChinaSchool of Chemistry and Chemical Engineering Shanxi University Taiyuan 030006 ChinaAbstract It is highly desired to achieve Type‐I photosensitizer (PS) to overcome the hypoxic limitation found in most clinically used PSs. Herein, a new heavy‐atom‐free Type‐I PS T‐BNCy5 is presented by incorporating a biotin‐modified naphthalimide (NI) unit into the meso‐position of a N‐benzyl‐functionalized, strongly photon‐capturing pentamethine cyanine (Cy5) dye. Such molecular engineering induces a rigid orthogonal geometry between NI and Cy5 units by introducing an intramolecular sandwich‐like π–π stacking assembly, which effectively promotes intersystem crossing (ISC) and greatly extends the triplet‐state lifetime (τ = 389 µs), thereby markedly improving the superoxide (O2•−)‐generating ability. In vitro assays reveal that T‐BNCy5 specifically accumulates in mitochondria, where it not only generates O2•− under photoirradiation but also induces the burst of the most cytotoxic hydroxy radical (HO•) by a cascade of biochemical reactions, ultimately triggering cell ferroptosis with the IC50 value up to ≈0.45 µm whether under normoxia or hypoxia. In vivo assays manifest that, benefiting from its biotin unit, T‐BNCy5 displays a strong tumor‐targeting ability, and after a single PDT treatment, it can not only ablate the tumor almost completely but also be cleared from the body through biosafe urinary excretion, indicating its potential for future clinical translation.https://doi.org/10.1002/advs.202417179heptamethine cyaninenaphthalimidephotodynamic therapysuperoxidetumors
spellingShingle Guangxiao Yao
Junfeng Miao
Yingying Huo
Wei Guo
Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
Advanced Science
heptamethine cyanine
naphthalimide
photodynamic therapy
superoxide
tumors
title Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
title_full Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
title_fullStr Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
title_full_unstemmed Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
title_short Improved Orthogonality in Naphthalimide/Cyanine Dyad Boosts Superoxide Generation: a Tumor‐Targeted Type‐I Photosensitizer for Photodynamic Therapy of Tumor by Inducing Ferroptosis
title_sort improved orthogonality in naphthalimide cyanine dyad boosts superoxide generation a tumor targeted type i photosensitizer for photodynamic therapy of tumor by inducing ferroptosis
topic heptamethine cyanine
naphthalimide
photodynamic therapy
superoxide
tumors
url https://doi.org/10.1002/advs.202417179
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