Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway

The significantly rising incidence of oral cancer worldwide urgently requires the identification of novel, effective molecular targets to inhibit the progression of malignancy. DNA topoisomerase I (Topo I) is a well-established target for cancer treatment, and many studies have shown that different...

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Main Authors: Bin Zheng, Yi-Xiao Wang, Zi-Yan Wu, Xin-Wei Li, Li-Qing Qin, Nan-Ying Chen, Gui-Fa Su, Jun-Cheng Su, Cheng-Xue Pan
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Molecules
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Online Access:https://www.mdpi.com/1420-3049/30/4/894
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author Bin Zheng
Yi-Xiao Wang
Zi-Yan Wu
Xin-Wei Li
Li-Qing Qin
Nan-Ying Chen
Gui-Fa Su
Jun-Cheng Su
Cheng-Xue Pan
author_facet Bin Zheng
Yi-Xiao Wang
Zi-Yan Wu
Xin-Wei Li
Li-Qing Qin
Nan-Ying Chen
Gui-Fa Su
Jun-Cheng Su
Cheng-Xue Pan
author_sort Bin Zheng
collection DOAJ
description The significantly rising incidence of oral cancer worldwide urgently requires the identification of novel, effective molecular targets to inhibit the progression of malignancy. DNA topoisomerase I (Topo I) is a well-established target for cancer treatment, and many studies have shown that different cancer cell genes could be targeted more selectively with one type of Topo I inhibitor. In this report, a new scaffold pyridothieno[3,2-<i>c</i>]isoquinoline 11,11-dioxide was designed via the combination of the key fragment or bioisoster of Topo I inhibitor azaindenoisoquinolines and G-quadruplex binder quindoline. Thirty-two target derivatives were synthesized, among which compounds <b>7be,</b> with potent Topo I inhibition, exhibited effective antiproliferative activity against Cal27, one of the oral cancer cell lines highly expressing Topo I protein. Further studies indicated that <b>7be</b> could also inhibit the activation of PI3K/AKT/NF-κB pathway and downregulate the level of c-MYC, repress the colony formation and the migration of Cal27 cells and trigger apoptosis and autophagy. Molecular docking indicated that <b>7be</b> could interact with the complex of Topo I and DNA via a mode similar to the indenoisoquinolines. The results of the Cal27 xenograft model confirmed that <b>7be</b> exhibited promising anticancer efficacy in vivo, with tumor growth inhibition (TGI) of 64.7% at 20 mg/kg.
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spelling doaj-art-3665bf0b9b5a4468ab7fddd432d012e52025-08-20T03:12:12ZengMDPI AGMolecules1420-30492025-02-0130489410.3390/molecules30040894Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling PathwayBin Zheng0Yi-Xiao Wang1Zi-Yan Wu2Xin-Wei Li3Li-Qing Qin4Nan-Ying Chen5Gui-Fa Su6Jun-Cheng Su7Cheng-Xue Pan8State Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, 15 Yu Cai Road, Guilin 541004, ChinaThe significantly rising incidence of oral cancer worldwide urgently requires the identification of novel, effective molecular targets to inhibit the progression of malignancy. DNA topoisomerase I (Topo I) is a well-established target for cancer treatment, and many studies have shown that different cancer cell genes could be targeted more selectively with one type of Topo I inhibitor. In this report, a new scaffold pyridothieno[3,2-<i>c</i>]isoquinoline 11,11-dioxide was designed via the combination of the key fragment or bioisoster of Topo I inhibitor azaindenoisoquinolines and G-quadruplex binder quindoline. Thirty-two target derivatives were synthesized, among which compounds <b>7be,</b> with potent Topo I inhibition, exhibited effective antiproliferative activity against Cal27, one of the oral cancer cell lines highly expressing Topo I protein. Further studies indicated that <b>7be</b> could also inhibit the activation of PI3K/AKT/NF-κB pathway and downregulate the level of c-MYC, repress the colony formation and the migration of Cal27 cells and trigger apoptosis and autophagy. Molecular docking indicated that <b>7be</b> could interact with the complex of Topo I and DNA via a mode similar to the indenoisoquinolines. The results of the Cal27 xenograft model confirmed that <b>7be</b> exhibited promising anticancer efficacy in vivo, with tumor growth inhibition (TGI) of 64.7% at 20 mg/kg.https://www.mdpi.com/1420-3049/30/4/894Topo I inhibitor<i>c-MYC</i>PI3K/AKT/NF-κBoral cancerantitumor
spellingShingle Bin Zheng
Yi-Xiao Wang
Zi-Yan Wu
Xin-Wei Li
Li-Qing Qin
Nan-Ying Chen
Gui-Fa Su
Jun-Cheng Su
Cheng-Xue Pan
Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
Molecules
Topo I inhibitor
<i>c-MYC</i>
PI3K/AKT/NF-κB
oral cancer
antitumor
title Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
title_full Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
title_fullStr Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
title_full_unstemmed Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
title_short Design, Synthesis and Bioactive Evaluation of Topo I/<i>c-MYC</i> Dual Inhibitors to Inhibit Oral Cancer via Regulating the PI3K/AKT/NF-κB Signaling Pathway
title_sort design synthesis and bioactive evaluation of topo i i c myc i dual inhibitors to inhibit oral cancer via regulating the pi3k akt nf κb signaling pathway
topic Topo I inhibitor
<i>c-MYC</i>
PI3K/AKT/NF-κB
oral cancer
antitumor
url https://www.mdpi.com/1420-3049/30/4/894
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