Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer

BackgroundDue to the lack of effective treatment methods and targeted drugs, triple-negative breast cancer (TNBC) is not only difficult to treat clinically, but also has a poor prognosis for patients. This study aims to develop novel anti-TNBC drug candidates by designing 90 derivatives of 3,4-seco-...

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Main Authors: Chunyu Gao, Hongbo Teng, Wenxin Zhang, Yaru Zhao, Chunguo Cui, Zerbo Patrice, Liyan Wang, Yan Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Chemistry
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Online Access:https://www.frontiersin.org/articles/10.3389/fchem.2025.1630939/full
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author Chunyu Gao
Chunyu Gao
Hongbo Teng
Hongbo Teng
Wenxin Zhang
Wenxin Zhang
Yaru Zhao
Yaru Zhao
Chunguo Cui
Zerbo Patrice
Liyan Wang
Liyan Wang
Yan Zhao
Yan Zhao
author_facet Chunyu Gao
Chunyu Gao
Hongbo Teng
Hongbo Teng
Wenxin Zhang
Wenxin Zhang
Yaru Zhao
Yaru Zhao
Chunguo Cui
Zerbo Patrice
Liyan Wang
Liyan Wang
Yan Zhao
Yan Zhao
author_sort Chunyu Gao
collection DOAJ
description BackgroundDue to the lack of effective treatment methods and targeted drugs, triple-negative breast cancer (TNBC) is not only difficult to treat clinically, but also has a poor prognosis for patients. This study aims to develop novel anti-TNBC drug candidates by designing 90 derivatives of 3,4-seco-lupane triterpene derivatives, a natural product of the genus Eleutherogenus.MethodsFirstly, 90 derivatives were synthesized and screened, and the compound I-27 showed excellent cytotoxicity (IC50=1.02 μM) for MDA-MB-231 cells for further activity verification. Then in vitro tests were carried out to detect the effects of the compound on the proliferation, migration, invasion and apoptosis of TNBC cells. With the help of transcriptomics, the mechanism of action was explored and verified. At the same time, its inhibitory effect on tumor volume and lung metastasis was verified through a mouse model of in vivo test, and its mechanism of action was further verified.ResultsIn vitro tests showed that compound I.-27 could effectively inhibit the proliferation, migration and invasion of TNBC cells, and induce apoptosis. Transcriptomic analysis revealed that it has a dual mechanism of action. On the one hand, it inhibits tumor angiogenesis through the ID1/TSP-1 pathway. On the other hand, it promotes apoptosis through the PI3K/AKT/FoxO1 signaling pathway. In vivo tests, the compound significantly reduced tumor volume and inhibited lung metastasis through mouse models. It further confirmed that ID1 is a key target for anti-tumor.ConclusionsIn this study, an anti-TNBC drug with multiple mechanisms was developed from the triterpenoids of 3,4-3,4-seco-lupane triterpene derivatives for the first time, and the mechanism of action was clarified by combining transcriptomics, molecular docking and gene knockout technologies. Compound I-27 provides a potential breakthrough for the treatment of triple-negative breast cancer as a potential therapeutic candidate with a novel action mechanism and high potency.
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spelling doaj-art-3c12a3e657a3495ca80c03d708ebf6f22025-08-20T02:46:29ZengFrontiers Media S.A.Frontiers in Chemistry2296-26462025-07-011310.3389/fchem.2025.16309391630939Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancerChunyu Gao0Chunyu Gao1Hongbo Teng2Hongbo Teng3Wenxin Zhang4Wenxin Zhang5Yaru Zhao6Yaru Zhao7Chunguo Cui8Zerbo Patrice9Liyan Wang10Liyan Wang11Yan Zhao12Yan Zhao13College of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaCollege of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaCollege of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaCollege of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaBreast Surgery Department of Bethune Third Hospital, Jilin University, Changchun, Jilin, ChinaDépartement: Biochimie / Microbiologie UFR Sciences de la Vie et de la Terre, Ouagadougou, Burkina FasoCollege of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaCollege of Chinese Medicinal Materials, Jilin Agricultural University, Changchun, Jilin, ChinaInternational Joint Laboratory for Development of Animal and Plant Resources for Food and Medicine, Changchun, Jilin, ChinaBackgroundDue to the lack of effective treatment methods and targeted drugs, triple-negative breast cancer (TNBC) is not only difficult to treat clinically, but also has a poor prognosis for patients. This study aims to develop novel anti-TNBC drug candidates by designing 90 derivatives of 3,4-seco-lupane triterpene derivatives, a natural product of the genus Eleutherogenus.MethodsFirstly, 90 derivatives were synthesized and screened, and the compound I-27 showed excellent cytotoxicity (IC50=1.02 μM) for MDA-MB-231 cells for further activity verification. Then in vitro tests were carried out to detect the effects of the compound on the proliferation, migration, invasion and apoptosis of TNBC cells. With the help of transcriptomics, the mechanism of action was explored and verified. At the same time, its inhibitory effect on tumor volume and lung metastasis was verified through a mouse model of in vivo test, and its mechanism of action was further verified.ResultsIn vitro tests showed that compound I.-27 could effectively inhibit the proliferation, migration and invasion of TNBC cells, and induce apoptosis. Transcriptomic analysis revealed that it has a dual mechanism of action. On the one hand, it inhibits tumor angiogenesis through the ID1/TSP-1 pathway. On the other hand, it promotes apoptosis through the PI3K/AKT/FoxO1 signaling pathway. In vivo tests, the compound significantly reduced tumor volume and inhibited lung metastasis through mouse models. It further confirmed that ID1 is a key target for anti-tumor.ConclusionsIn this study, an anti-TNBC drug with multiple mechanisms was developed from the triterpenoids of 3,4-3,4-seco-lupane triterpene derivatives for the first time, and the mechanism of action was clarified by combining transcriptomics, molecular docking and gene knockout technologies. Compound I-27 provides a potential breakthrough for the treatment of triple-negative breast cancer as a potential therapeutic candidate with a novel action mechanism and high potency.https://www.frontiersin.org/articles/10.3389/fchem.2025.1630939/fullseco-lupane triterpene derivativestriple-negative breast cancertranscriptomicsapoptosisangiogenesis
spellingShingle Chunyu Gao
Chunyu Gao
Hongbo Teng
Hongbo Teng
Wenxin Zhang
Wenxin Zhang
Yaru Zhao
Yaru Zhao
Chunguo Cui
Zerbo Patrice
Liyan Wang
Liyan Wang
Yan Zhao
Yan Zhao
Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
Frontiers in Chemistry
seco-lupane triterpene derivatives
triple-negative breast cancer
transcriptomics
apoptosis
angiogenesis
title Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
title_full Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
title_fullStr Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
title_full_unstemmed Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
title_short Design and synthesis of 3,4-seco-Lupane triterpene derivatives: targeting tumor angiogenesis and inducing apoptosis in triple-negative breast cancer
title_sort design and synthesis of 3 4 seco lupane triterpene derivatives targeting tumor angiogenesis and inducing apoptosis in triple negative breast cancer
topic seco-lupane triterpene derivatives
triple-negative breast cancer
transcriptomics
apoptosis
angiogenesis
url https://www.frontiersin.org/articles/10.3389/fchem.2025.1630939/full
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