Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance

Multidrug resistance significantly impedes the efficacy of cancer chemotherapy. Resistance often arises from the reduced cellular uptake of chemotherapeutic drugs, a process crucial for their cytotoxic effects. This reduction is frequently due to transmembrane efflux pumps powered by ATP from mitoch...

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Main Authors: Wei Huang, Xuan Nie, Xiao-Hong Zhou, Lei Qiao, Hong-Jie Gao, Jing Zang, Long-Kang Yu, Long-Hai Wang, Ye-Zi You
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-12-01
Series:Supramolecular Materials
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667240524000060
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author Wei Huang
Xuan Nie
Xiao-Hong Zhou
Lei Qiao
Hong-Jie Gao
Jing Zang
Long-Kang Yu
Long-Hai Wang
Ye-Zi You
author_facet Wei Huang
Xuan Nie
Xiao-Hong Zhou
Lei Qiao
Hong-Jie Gao
Jing Zang
Long-Kang Yu
Long-Hai Wang
Ye-Zi You
author_sort Wei Huang
collection DOAJ
description Multidrug resistance significantly impedes the efficacy of cancer chemotherapy. Resistance often arises from the reduced cellular uptake of chemotherapeutic drugs, a process crucial for their cytotoxic effects. This reduction is frequently due to transmembrane efflux pumps powered by ATP from mitochondria and the cytoplasmic matrix, leading to lower intracellular concentrations of these drugs. This study introduces an amphiphilic molecule, bis(zinc-dipicolylamine) farnesol (Bis-ZnDPA), which targets phosphatidylserine (PS) – a negatively charged phospholipid prominently displayed on the outer leaflet of cancer cell plasma membranes. Integrating the hydrophobic segment of Bis-ZnDPA into the plasma membrane disrupts its integrity, potentially leading to hole formation and facilitating the uptake of chemotherapeutic drugs. Furthermore, the binding of Bis-ZnDPA to phosphatidylserine inhibits ATP production caused by Ca2+ influx and deregulation of the phosphoinositide 3-kinase/protein kinase B (PI3K/AKT) signaling pathway, reducing the efflux of drugs from cells. The results indicate the potent synergistic effect of Bis-ZnDPA with chemotherapeutic agents, suggesting that targeting PS is a viable strategy for overcoming multidrug resistance in cancer chemotherapy.
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publishDate 2024-12-01
publisher KeAi Communications Co., Ltd.
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spelling doaj-art-68bc7c1ac7614b3f8f4a2ee9a0c87e4a2025-08-20T02:52:58ZengKeAi Communications Co., Ltd.Supramolecular Materials2667-24052024-12-01310006810.1016/j.supmat.2024.100068Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistanceWei Huang0Xuan Nie1Xiao-Hong Zhou2Lei Qiao3Hong-Jie Gao4Jing Zang5Long-Kang Yu6Long-Hai Wang7Ye-Zi You8Key Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, China; Department of Pharmacy, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, China; Anhui Provincial Key Laboratory of Precision Pharmaceutical Preparations and Clinical Pharmacy, Hefei, Anhui, ChinaDepartment of Pharmacy, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, China; Anhui Provincial Key Laboratory of Precision Pharmaceutical Preparations and Clinical Pharmacy, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, ChinaKey Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, China; Corresponding author.Key Laboratory of Precision and Intelligent Chemistry, University of Science and Technology of China, Hefei, Anhui, China; Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, Anhui, China; Department of Pharmacy, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, China; Anhui Provincial Key Laboratory of Precision Pharmaceutical Preparations and Clinical Pharmacy, Hefei, Anhui, ChinaMultidrug resistance significantly impedes the efficacy of cancer chemotherapy. Resistance often arises from the reduced cellular uptake of chemotherapeutic drugs, a process crucial for their cytotoxic effects. This reduction is frequently due to transmembrane efflux pumps powered by ATP from mitochondria and the cytoplasmic matrix, leading to lower intracellular concentrations of these drugs. This study introduces an amphiphilic molecule, bis(zinc-dipicolylamine) farnesol (Bis-ZnDPA), which targets phosphatidylserine (PS) – a negatively charged phospholipid prominently displayed on the outer leaflet of cancer cell plasma membranes. Integrating the hydrophobic segment of Bis-ZnDPA into the plasma membrane disrupts its integrity, potentially leading to hole formation and facilitating the uptake of chemotherapeutic drugs. Furthermore, the binding of Bis-ZnDPA to phosphatidylserine inhibits ATP production caused by Ca2+ influx and deregulation of the phosphoinositide 3-kinase/protein kinase B (PI3K/AKT) signaling pathway, reducing the efflux of drugs from cells. The results indicate the potent synergistic effect of Bis-ZnDPA with chemotherapeutic agents, suggesting that targeting PS is a viable strategy for overcoming multidrug resistance in cancer chemotherapy.http://www.sciencedirect.com/science/article/pii/S2667240524000060Multidrug resistancePhosphatidylserineZn-dipicolylamine
spellingShingle Wei Huang
Xuan Nie
Xiao-Hong Zhou
Lei Qiao
Hong-Jie Gao
Jing Zang
Long-Kang Yu
Long-Hai Wang
Ye-Zi You
Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
Supramolecular Materials
Multidrug resistance
Phosphatidylserine
Zn-dipicolylamine
title Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
title_full Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
title_fullStr Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
title_full_unstemmed Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
title_short Phosphatidylserine-targeting bis(zinc-dipicolylamine) farnesol inhibits ATP production in cancer cells to overcome multidrug resistance
title_sort phosphatidylserine targeting bis zinc dipicolylamine farnesol inhibits atp production in cancer cells to overcome multidrug resistance
topic Multidrug resistance
Phosphatidylserine
Zn-dipicolylamine
url http://www.sciencedirect.com/science/article/pii/S2667240524000060
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