Twist1-induced suppression of oncogene-induced senescence in non-small cell lung cancer requires the transactivation domain of Twist1

Non-small cell lung carcinoma (NSCLC) is a major cause of cancer mortality. High expression of the epithelial-to-mesenchymal transition transcription factor (EMT-TF) Twist1 is strongly associated with metastatic cancers and with treatment resistance. Twist1 can also upregulate O-GlcNAcylation to sup...

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Main Authors: Audrey Lafargue, Hailun Wang, Sivarajan T. Chettiar, Rajendra P. Gajula, Amol C. Shetty, Yang Song, Brian W. Simons, Muhammad Ajmal Khan, Triet Nguyen, Hwai-Wei Tseng, Jinhee Chang, Danielle N. Waters, Aaron Chan, Christine Lam, Francesca A. Carrieri, Caleb Smack, Nick Connis, Dipanwita Dutta Chowdhury, Katriana Nugent, Ismaeel Siddiqui, Kekoa Taparra, Mohammad Rezaee, Natasha Zachara, Zachary S. Morris, Christopher McFarland, Sarki Abba Abdulkadir, Christine L. Hann, Phuoc T. Tran
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Neoplasia: An International Journal for Oncology Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S1476558625000582
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Summary:Non-small cell lung carcinoma (NSCLC) is a major cause of cancer mortality. High expression of the epithelial-to-mesenchymal transition transcription factor (EMT-TF) Twist1 is strongly associated with metastatic cancers and with treatment resistance. Twist1 can also upregulate O-GlcNAcylation to suppress fail-safe programs such as KrasG12D oncogene-induced senescence (OIS) that accelerates NSCLC tumorigenesis. We wanted to decipher the critical domains and transcriptional targets required for Twist1 acceleration of lung tumorigenicity. We created a novel genetically-engineered mouse model for autochthonous lung cancer through lung epithelial expression of KrasG12D oncogene (CR) concomitantly with Twist1wt (CRT) or a Twist1F191G transactivation-deficient mutant (CRF191G). Compared to CR and CRF191G, CRT mice had shorter tumor-free survival and more aggressive tumors histologically. CRT lung tumors also showed higher proliferation and lower cell-cycle arrest suggesting that the Twist1 transactivation-domain is important for OIS suppression. Supporting these data, we observed in non-cancer human bronchial epithelial cells (HBECs) that the co-expression of human TWIST1wt enhanced tumorigenic/invasive programs and could suppress HRasG12V-induced senescence while co-expressing TWIST1F187G transactivation-deficient mutant could not. TWIST1wt co-expression with HRasG12V in HBECs differentially modulated MYC downstream transcriptional programs. Finally, OIS induction in HBECHRasG12V-TWIST1wt was rescued by O-GlcNAcylation inhibition or by treatment with a novel MYC inhibitor MYCi975 or by MYC knockdown. Altogether, these results indicate that the Twist1 transactivation domain is required for Twist1-dependent acceleration of lung tumorigenesis via MYC and nominate MYCi975 as a means to activate latent OIS programs. MYC targeting strategies could limit pro-tumorigenic programs and serve as a therapeutic for TWIST1-overexpressing NSCLCs.
ISSN:1476-5586