PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors

Abstract The hyperactivation of the PI3K pathway in head and neck squamous cell carcinoma (HNSCC) suggests that targeting PI3K is a potential therapeutic strategy. CYH33 is a novel PI3Kα-selective inhibitor discovered by our group, which is currently undergoing a phase I clinical trial (NCT03544905)...

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Main Authors: Xu Zhang, Jiao Xu, Xuan Wang, Lan Xu, Xi Zhang, Yi Wang, Shujuan Jiang, Yixiang Zhang, Jian Ding, Chen Qing, Linghua Meng
Format: Article
Language:English
Published: Nature Publishing Group 2025-06-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07767-x
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author Xu Zhang
Jiao Xu
Xuan Wang
Lan Xu
Xi Zhang
Yi Wang
Shujuan Jiang
Yixiang Zhang
Jian Ding
Chen Qing
Linghua Meng
author_facet Xu Zhang
Jiao Xu
Xuan Wang
Lan Xu
Xi Zhang
Yi Wang
Shujuan Jiang
Yixiang Zhang
Jian Ding
Chen Qing
Linghua Meng
author_sort Xu Zhang
collection DOAJ
description Abstract The hyperactivation of the PI3K pathway in head and neck squamous cell carcinoma (HNSCC) suggests that targeting PI3K is a potential therapeutic strategy. CYH33 is a novel PI3Kα-selective inhibitor discovered by our group, which is currently undergoing a phase I clinical trial (NCT03544905) for the treatment of advanced solid tumors including HNSCC. However, there is an urgent need to elucidate its mechanism of action and improve its efficacy against HNSCC. In this study, we found that CYH33 displayed promising but variable therapeutic activity against HNSCC. Inhibition of PI3K/Akt pathway by CYH33 was not sufficient for its activity against HNSCC. Tandem-Mass-Tag (TMT) phosphoproteomics were performed to reveal comprehensive regulation of kinome by CYH33. Particularly, attenuation of Erk phosphorylation was associated with the sensitivity of HNSCC cells to CYH33. Mechanistically, inhibition of PI3K by CYH33 blocked the PIP3 production and attenuated the membrane localization and phosphorylation of GAB1, resulting in reduced Erk phosphorylation and ultimately inhibition of cell proliferation in sensitive HNSCC cells. Meanwhile, activation of EGFR induced GAB1 phosphorylation independent of PI3K in HNSCC cells. Concurrent inhibition of EGFR synergistically potentiated the activity of CYH33 against HNSCC. These findings revealed the insight mechanism of CYH33 against HNSCC and provided rational combination regimen for HNSCC treatment.
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spelling doaj-art-3b7cb456692f4022bd587fb2726f81e42025-08-20T03:47:17ZengNature Publishing GroupCell Death and Disease2041-48892025-06-0116111310.1038/s41419-025-07767-xPI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitorsXu Zhang0Jiao Xu1Xuan Wang2Lan Xu3Xi Zhang4Yi Wang5Shujuan Jiang6Yixiang Zhang7Jian Ding8Chen Qing9Linghua Meng10Division of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesHaihe Biopharma Co. LtdHaihe Biopharma Co. LtdSchool of Life Science and Technology, ShanghaiTech UniversitySchool of Pharmaceutical Sciences & Yunnan Key Laboratory of Pharmacology for Natural Products, Kunming Medical UniversityDivision of Anti-tumor Pharmacology, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of SciencesAbstract The hyperactivation of the PI3K pathway in head and neck squamous cell carcinoma (HNSCC) suggests that targeting PI3K is a potential therapeutic strategy. CYH33 is a novel PI3Kα-selective inhibitor discovered by our group, which is currently undergoing a phase I clinical trial (NCT03544905) for the treatment of advanced solid tumors including HNSCC. However, there is an urgent need to elucidate its mechanism of action and improve its efficacy against HNSCC. In this study, we found that CYH33 displayed promising but variable therapeutic activity against HNSCC. Inhibition of PI3K/Akt pathway by CYH33 was not sufficient for its activity against HNSCC. Tandem-Mass-Tag (TMT) phosphoproteomics were performed to reveal comprehensive regulation of kinome by CYH33. Particularly, attenuation of Erk phosphorylation was associated with the sensitivity of HNSCC cells to CYH33. Mechanistically, inhibition of PI3K by CYH33 blocked the PIP3 production and attenuated the membrane localization and phosphorylation of GAB1, resulting in reduced Erk phosphorylation and ultimately inhibition of cell proliferation in sensitive HNSCC cells. Meanwhile, activation of EGFR induced GAB1 phosphorylation independent of PI3K in HNSCC cells. Concurrent inhibition of EGFR synergistically potentiated the activity of CYH33 against HNSCC. These findings revealed the insight mechanism of CYH33 against HNSCC and provided rational combination regimen for HNSCC treatment.https://doi.org/10.1038/s41419-025-07767-x
spellingShingle Xu Zhang
Jiao Xu
Xuan Wang
Lan Xu
Xi Zhang
Yi Wang
Shujuan Jiang
Yixiang Zhang
Jian Ding
Chen Qing
Linghua Meng
PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
Cell Death and Disease
title PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
title_full PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
title_fullStr PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
title_full_unstemmed PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
title_short PI3K-dependent GAB1/Erk phosphorylation renders head and neck squamous cell carcinoma sensitive to PI3Kα inhibitors
title_sort pi3k dependent gab1 erk phosphorylation renders head and neck squamous cell carcinoma sensitive to pi3kα inhibitors
url https://doi.org/10.1038/s41419-025-07767-x
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