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FAK-LINC01089 negative regulatory loop controls chemoresistance and progression of small cell lung cancer

Oncogene volume 43, pages 1669–1687 (2024)Cite this article

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Abstract

The focal adhesion kinase (FAK) tyrosine kinase is activated and upregulated in multiple cancer types including small cell lung cancer (SCLC). However, FAK inhibitors have shown limited efficacy in clinical trials for cancer treatment. With the aim of identifying potential therapeutic strategies to inhibit FAK for cancer treatment, we investigated long non-coding RNAs (lncRNAs) that potentially regulate FAK in SCLC. In this study, we identified a long non-coding RNA LINC01089 that binds and inhibits FAK phosphorylation (activation). Expression analysis revealed that LINC01089 was downregulated in SCLC tissues and negatively correlated with chemoresistance and survival in SCLC patients. Functionally, LINC01089 inhibited chemoresistance and progression of SCLC in vitro and in vivo. Mechanistically, LINC01089 inhibits FAK activation by blocking binding with Src and talin kinases, while FAK negatively regulates LINC01089 transcription by activating the ERK signaling pathway to recruit the REST transcription factor. Furthermore, LINC01089-FAK axis mediates the expression of drug resist-related genes by modulating YBX1 phosphorylation, leading to drug resistance in SCLC. Intriguingly, the FAK-LINC01089 interaction depends on the co-occurrence of the novel FAK variant and the non-conserved region of LINC01089 in primates. In Conclusion, our results indicated that LINC01089 may serve as a novel high-efficiency FAK inhibitor and the FAK-LINC01089 axis represents a valuable prognostic biomarker and potential therapeutic target in SCLC.

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Fig. 1: Identification of lncRNAs regulating FAK phosphorylation.
Fig. 2: LINC01089 controls chemoresistance and progression of SCLC.
Fig. 3: Characterization of the FAK-LINC01089 interaction.
Fig. 4: LINC01089 regulated the major molecular functions of FAK.
Fig. 5: LINC01089 regulates the biological functions of FAK.
Fig. 6: Physiological relevance of LINC01089 and FAK in SCLC.
Fig. 7: FAK regulates the transcriptional expression of LINC01089 through recruiting REST.
Fig. 8: Human LINC01089, but not mouse Linc01089, restricted FAK activity.

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Data availability

The RIP-RNA sequencing data was available in the Sequence Read Archive (SRA) with the accession number PRJNA1002414.

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Acknowledgements

This work was supported by the National Key R&D Program of China (2019YFA0906000), the National Natural Science Foundation of China (82203459), China Postdoctoral Science Foundation (2023T160436), Guangdong Special Support Program (2021JC06Y578), the CSCO-Genecast Cancer Precision Therapy Research Fund (2019-056-ZZ), the Shenzhen Municipal Government of China (JCYJ20200109120016553, CJGJZD20200617102403009), the Sanming Project of Shenzhen Health and Family Planning Commission (SZSM202011017), Shenzhen High-level Hospital Construction Fund and the Shenzhen Institute of Synthetic Biology Scientific Research Program (ZTXM20214005), Shenzhen Portion of Shenzhen-Hong Kong Science and Technology Innovation Cooperation Zone (HTHZQSWS- KCCYB-2023060).

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Author notes

  1. These authors contributed equally: Xianteng Wang, Xingkai Li, Liman Niu, Fang Lv.

Authors and Affiliations

  1. Department of Urology, Shenzhen Institute of Translational Medicine, Shenzhen Second People’s Hospital, The First Affiliated Hospital of Shenzhen University, Guangdong Key Laboratory for Biomedical Measurements and Ultrasound Imaging, National-Regional Key Technology Engineering Laboratory for Medical Ultrasound, School of Biomedical Engineering, Shenzhen University Medical school, Shenzhen, 518060, China

    Xianteng Wang & Weiren Huang

  2. Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China

    Xianteng Wang & Weiren Huang

  3. Guangdong Key Laboratory of Systems Biology and Synthetic Biology for Urogenital Tumors, Shenzhen Second People’s Hospital, The First Affiliated Hospital of Shenzhen University, Shenzhen, China

    Xianteng Wang & Weiren Huang

  4. School of Medicine, Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University, Shenzhen, 518107, China

    Xianteng Wang

  5. Department of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

    Xingkai Li, Fang Lv, Yushun Gao & Bing Wang

  6. State Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China

    Xingkai Li & Yuliang Ran

  7. Chongqing Key Laboratory of Sichuan-Chongging Co-construction for Diagnosis and Treatment of Infectious Diseases Integrated Traditional Chinese and Western Medicine College of Medical Technology, Chengdu University of Traditional Chinese Medicine, Chengdu, China

    Liman Niu

  8. Graduate School, Guangxi University of Chinese Medicine, Nanning, China

    Ting Guo

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Contributions

XTW, XKL, LMN, and FL contributed equally to this work. XTW, XKL, FL, and LMN conducted experiments and wrote the manuscript. TG prepared and processed the clinical samples. BW, YSG, WRH, YLR, and XTW conceived the project. WRH, YLR, and BW supervised the study and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yuliang Ran, Weiren Huang or Bing Wang.

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Wang, X., Li, X., Niu, L. et al. FAK-LINC01089 negative regulatory loop controls chemoresistance and progression of small cell lung cancer. Oncogene 43, 1669–1687 (2024). https://doi.org/10.1038/s41388-024-03027-y

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