Interaction between STAT3 and GLI1/tGLI1 oncogenic transcription factors promotes the aggressiveness of triple-negative breast cancers and HER2-enriched breast cancer
Open accessAbstract
Signal transducer and activator of transcription 3 (STAT3), glioma oncogene homolog 1 (GLI1), and truncated GLI1 (tGLI1) are oncogenic transcription factors playing important roles in breast cancer. tGLI1 is a gain-of-function GLI1 isoform. Whether STAT3 physically and/or functionally interacts with GLI1/tGLI1 has not been explored. To address this knowledge gap, we analyzed 47 node-positive breast cancer specimens using immunohistochemical staining and found that phosphorylated-STAT3 (Y705), GLI1, and tGLI1 are co-overexpressed in the majority of triple-negative breast carcinomas (64%) and HER2-enriched (68%) breast carcinomas, and in lymph node metastases (65%). Using gene set enrichment analysis, we analyzed 710 breast tumors and found that STAT3 activation and GLI1/tGLI1 activation signatures are co-enriched in triple-negative subtypes of breast cancers and HER2-enriched subtypes of breast cancers, but not in luminal subtypes of breast cancers. Patients with high levels of STAT3 and GLI1/tGLI1 co-activation in their breast tumors had worse metastasis-free survival compared to those with low levels. Since these proteins co-overexpress in breast tumors, we examined whether they form complexes and observed that STAT3 interacted with both GLI1 and tGLI1. We further found that the STAT3-GLI1 and STAT3-tGLI1 complexes bind to both consensus GLI1-binding and STAT3-binding sites using chromatin immunoprecipitation (ChIP) assay, and that the co-overexpression markedly activated a promoter controlled by GLI1-binding sites. To identify genes that can be directly co-activated by STAT3 and GLI1/tGLI1, we analyzed three ChIP-seq datasets and identified 34 potential target genes. Following validations using reverse transcription polymerase chain reaction and survival analysis, we identified three genes as novel transcriptional targets of STAT3 and GLI1/tGLI1, R-Ras2, Cep70, and UPF3A. Finally, we observed that co-overexpression of STAT3 with GLI1/tGLI1 promoted the ability of breast cancer cells to form mammospheres and that STAT3 only cooperates with tGLI1 in immortalized mammary epithelial cells. In summary, our study identified novel physical and functional cooperation between two families of oncogenic transcription factors, and the interaction contributes to aggressiveness of breast cancer cells and poor prognosis of triple-negative breast cancers and HER2-enriched breast cancers.
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Activated STAT3 can physically interact with Gli1 and lead to Gli1 enrichment in promoters of target genes controlled by Gli1-binding sites.
“Aside from the direct regulation of Gli1 expression, recent evidence indicates that activated STAT3 can physically interact with Gli1 and lead to Gli1 enrichment in the promoters of target genes controlled by Gli1‐binding sites [32, 35].”
From Saikosaponin b1 Attenuates Liver Fibrosis by Blocking STAT3/Gli1 Interaction and Inducing Gli1 Degradation (2025) · cites this paper as [32]
In Results, ‘STAT3 forms complexes with GLI1 and tGLI1’ (page not available), immunoprecipitation shows a physical interaction, and ChIP shows GLI1 binding at GLI1-binding sites in the PTCH1 and GLI1 promoters. Co-expression with constitutively active STAT3 also enhances a GLI1-binding-site reporter. The passage does not show that activated STAT3 causes increased GLI1 enrichment at those promoters; it establishes promoter binding and enhanced reporter activity, not that causal change in occupancy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSTAT3 binds to the promoter of the Gli1 gene and controls Gli1 expression.
“Recent reports showed that STAT3 binds to the promoter of the Gli1 gene and controls Gli1 expression [32, 33, 34].”
From Saikosaponin b1 Attenuates Liver Fibrosis by Blocking STAT3/Gli1 Interaction and Inducing Gli1 Degradation (2025) · cites this paper as [32]
The Results section (‘STAT3 forms complexes with GLI1 and tGLI1,’ page not provided) reports ChIP evidence that STAT3 binds the GLI1 gene promoter. The expression results concern other genes, including Cep70 and UPF3A; the passages do not establish that STAT3 controls GLI1 expression. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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- Authors
- Sirkisoon, S. R., Carpenter, R. L., Rimkus, T., Anderson, A., Harrison, A., Lange, A. M., Jin, G., Watabe, K., & Lo, H.-W.
- Affiliations
- Wake Forest University (US)
- Atrium Health Wake Forest Baptist (US)
- Corresponding author
- Lo, Hui-Wen
- Venue
- Oncogene
- Published
- 2018-02-16
- Volume
- 37
- Issue
- 19
- Pages
- 2502-2514
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- PMC
- PMC5948110
- OpenAlex
- W2792908157
- Cited by
- 96
- References
- 71
- Citations by year
- 2026: 1 · 2025: 11 · 2024: 13 · 2023: 6 · 2022: 24 · 2021: 8 · 2020: 19 · 2019: 13 · 2018: 1
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Update notices
- correction (2024-06-12)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5t32ca079448-15)
- National Cancer Institute (T32-CA079448, P30CA012197)
- National Institute of Neurological Disorders and Stroke (R01NS087169)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
- Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Keywords
- STAT3, Gli1, triple-negative breast cancer, HER2-enriched breast cancer, oncogenic transcription factor, protein-protein interaction, transcriptional coactivation, UPF3A, mammosphere formation, lymph node metastasis, metastasis-free survival, transcription factor target genes, Hedgehog signaling
- MeSH terms
- Zinc Finger Protein GLI1, Animals, Brain Neoplasms, Female, Humans, Membrane Proteins, Microtubule-Associated Proteins, Neoplasm Transplantation, Phosphorylation, Prognosis, Up-Regulation, Gene Expression Regulation, Neoplastic, Survival Analysis, RNA-Binding Proteins, Receptor, ErbB-2, Erb-b2 Receptor Tyrosine Kinases, Cell Cycle Proteins, Spheroids, Cellular, Monomeric GTP-Binding Proteins, Gene Expression Profiling, Cell Line, Tumor, STAT3 Transcription Factor, Mice, Triple Negative Breast Neoplasms
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