EIF1AX and RAS Mutations Cooperate to Drive Thyroid Tumorigenesis through ATF4 and c-MYC
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Abstract
Translation initiation is orchestrated by the cap binding and 43S preinitiation complexes (PIC). Eukaryotic initiation factor 1A (EIF1A) is essential for recruitment of the ternary complex and for assembling the 43S PIC. Recurrent EIF1AX mutations in papillary thyroid cancers are mutually exclusive with other drivers, including RAS. EIF1AX mutations are enriched in advanced thyroid cancers, where they display a striking co-occurrence with RAS, which cooperates to induce tumorigenesis in mice and isogenic cell lines. The C-terminal EIF1AX-A113splice mutation is the most prevalent in advanced thyroid cancer. EIF1AX-A113splice variants stabilize the PIC and induce ATF4, a sensor of cellular stress, which is co-opted to suppress EIF2α phosphorylation, enabling a general increase in protein synthesis. RAS stabilizes c-MYC, an effect augmented by EIF1AX-A113splice. ATF4 and c-MYC induce expression of amino acid transporters and enhance sensitivity of mTOR to amino acid supply. These mutually reinforcing events generate therapeutic vulnerabilities to MEK, BRD4, and mTOR kinase inhibitors. Significance: Mutations of EIF1AX, a component of the translation PIC, co-occur with RAS in advanced thyroid cancers and promote tumorigenesis. EIF1AX-A113splice drives an ATF4-induced dephosphorylation of EIF2α, resulting in increased protein synthesis. ATF4 also cooperates with c-MYC to sensitize mTOR to amino acid supply, thus generating vulnerability to mTOR kinase inhibitors. This article is highlighted in the In This Issue feature, p. 151
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Most oncogenic signaling pathways converge to enhance the translational capacity of tumor cells.
“Translational control plays a critical role in all steps of cancer progression, and most oncogenic signaling pathways converge to enhance the translational capacity of tumor cells (30–32).”
From Apolipoprotein E2 Stimulates Protein Synthesis and Promotes Melanoma Progression and Metastasis (2023) · cites this paper as [32]
The Introduction says deregulated translation initiation is common in cancer, and the Discussion reports increased global protein synthesis in thyroid cancer cells with EIF1AX and RAS mutations. Those passages support a link between oncogenic changes and translation, but do not establish that most oncogenic signaling pathways converge to enhance translational capacity. (LLM, conf=0.84)
Experimental — accuracy not yet measuredTranslational control plays a critical role in all steps of cancer progression.
“Translational control plays a critical role in all steps of cancer progression, and most oncogenic signaling pathways converge to enhance the translational capacity of tumor cells (30–32).”
From Apolipoprotein E2 Stimulates Protein Synthesis and Promotes Melanoma Progression and Metastasis (2023) · cites this paper as [32]
The Introduction (page unavailable) says deregulation of translation initiation is common in tumorigenesis, and the Discussion describes increased protein synthesis driven by EIF1AX and RAS mutations in thyroid cancer. The paper does not establish that translational control is critical at all steps of cancer progression or that most oncogenic signaling pathways converge to enhance tumor-cell translational capacity. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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- Authors
- Krishnamoorthy, G. P., Davidson, N. R., Leach, S. D., Zhao, Z., Lowe, S. W., Lee, G., Landa, I., Nagarajah, J., Saqcena, M., Singh, K., Wendel, H.-G., Dogan, S., Tamarapu, P. P., Blenis, J., Ghossein, R. A., Knauf, J. A., Rätsch, G., & Fagin, J. A.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Weill Cornell Medicine (US)
- 1Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York.
- 5Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York.
- Corresponding author
- Fagin, James A.
- ORCID
- Venue
- Cancer Discovery
- Published
- 2019-02-01
- Volume
- 9
- Issue
- 2
- Pages
- 264-281
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC6373451
- OpenAlex
- W2896801540
- Cited by
- 94
- References
- 67
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 13 · 2023: 12 · 2022: 14 · 2021: 20 · 2020: 6 · 2019: 6
- FWCI
- 6.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Discovery (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- NIH (P50-CA72012, R01-CA72597, and R01-CA50706, R01-CA204228, U54 OD020355-01)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Cancer Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
- Keywords
- EIF1AX, RAS mutations, papillary thyroid carcinoma, carcinogenesis, ATF4, c-Myc, 43S preinitiation complex, translation initiation, eIF2α dephosphorylation, amino acid transporters, amino acid supply, MEK inhibitors, BRD4 inhibitors, mTOR inhibitors
- MeSH terms
- Animals, Female, Humans, Mutation, Phosphorylation, Thyroid Neoplasms, Protein Biosynthesis, Tumor Cells, Cultured, Gene Expression Regulation, Neoplastic, Eukaryotic Initiation Factor-1, Mice, SCID, Mice, Inbred NOD, Apoptosis, Alternative Splicing, ras Proteins, Xenograft Model Antitumor Assays, Protein Kinase Inhibitors, Cell Proliferation, Mice, Activating Transcription Factor 4, TOR Serine-Threonine Kinases, Carcinogenesis
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