The small molecule, LLL12, inhibits STAT3 phosphorylation and induces apoptosis in medulloblastoma and glioblastoma cells - PubMed (original) (raw)
The small molecule, LLL12, inhibits STAT3 phosphorylation and induces apoptosis in medulloblastoma and glioblastoma cells
Sarah Ball et al. PLoS One. 2011.
Abstract
Tumors of the central nervous system represent a major source of cancer-related deaths, with medulloblastoma and glioblastoma being the most common malignant brain tumors in children and adults respectively. While significant advances in treatment have been made, with the 5-year survival rate for medulloblastoma at 70-80%, treating patients under 3 years of age still poses a problem due to the deleterious effects of radiation on the developing brain, and the median survival for patients with glioblastoma is only 15 months. The transcription factor, STAT3, has been found constitutively activated in a wide variety of cancers and in recent years it has become an attractive therapeutic target. We designed a non-peptide small molecule STAT3 inhibitor, LLL12, using structure-based design. LLL12 was able to inhibit STAT3 phosphorylation, decrease cell viability and induce apoptosis in medulloblastoma and glioblastoma cell lines with elevated levels of p-STAT3 (Y705). IC(50) values for LLL12 were found to be between 1.07 µM and 5.98 µM in the five cell lines expressing phosphorylated STAT3. STAT3 target genes were found to be downregulated and a decrease in STAT3 DNA binding was observed following LLL12 treatment, indicating that LLL12 is an effective STAT3 inhibitor. LLL12 was also able to inhibit colony formation, wound healing and decreased IL-6 and LIF secretion. Our results suggest that LLL12 is a potent STAT3 inhibitor and that it may be a potential therapeutic treatment for medulloblastoma and glioblastoma.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
Figure 1. Western blot analysis of cells treated with LLL12.
(A) Medulloblastoma cell lines and (B) glioblastoma cell lines which express constitutively active STAT3 exhibit a decrease in p-STAT3 (Y705) following treatment with LLL12 for 6 and 24 hours respectively. No effect is seen on other kinases such as p-AKTand pERK. Apoptosis is indicated by the cleavage of caspase 3. (C) Normal human lung fibroblasts (WI-38) and human hepatocytes (HH) that do not express p-STAT3, did not show an induction of cleaved caspase-3.
Figure 2. Cell Death ELISA analysis following LLL12 treatment.
(A) UW288-1, (B) U87, and (C) U87Δ exhibit a dose dependent increase in apoptosis following treatment with LLL12 for either 18 hours (UW288-1) or 24 hours (U87 and U87Δ).
Figure 3. RT-PCR Analysis of STAT3 target genes.
LLL12 treatment was able to downregulate the expression of STAT3 target genes: Cyclin D1, Survivin, Bcl-2 and Bcl-xL following 24 hours of treatment.
Figure 4. STAT3 DNA Binding Assay.
Cells showed a dose-dependent decrease in STAT3 activation following treatment with LLL12 for either 18 hours (UW288-1) or 24 hours (u87 and U87Δ), indicating that LLL12 is able to effectively inhibit STAT3's ability to bind DNA.
Figure 5. Wound Healing Assay.
Cells showed a dose-dependent decrease in their ability to migrate and heal the created wound following treatment with LLL12.
Figure 6. Colony Formation Assay.
Medulloblastoma and glioblastoma cell lines showed a decreased ability to form colonies following treatment with LLL12 for either 6 hours (UW288-1) or 24 hours (U87 and U87Δ).
Figure 7. IL-6 secretion in medulloblastoma and glioblastoma cell lines.
IL-6 secretion was measured by ELISA after 48 hours. The cell lines UW288-1, UW426 and U87Δ secreted elevated levels of IL-6.
Figure 8. LLL12 inhibition of IL-6 secretion.
(A–C) Cells were treated with LLL12 for 8, 16 and 24 hours and IL-6 levels were measured using an ELISA. IL-6 secretion was reduced at all three time points. (D) LLL12 inhibits the expression of IL-6 mRNA.
Figure 9. LLL12 inhibits IL-6 and LIF induced STAT3 phosphorylation.
(A) D283 and (B) U373 cells were pretreated with LLL12 for 2 hours and then treated with IL-6 for 30 minutes to induce p-STAT3. LLL12 was able to block STAT3 activation by IL-6 and did not have an effect of p-AKT or p-ERK. (C) D283 cells were pretreated with LLL12 for 2 hours and then treated with LIF for 24 hours to activate STAT3. LLL12 was able to inhibit the phosphorylation of STAT3 induced by LIF and did not inhibit p-AKT or p-ERK expression.
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References
- CBTRUS, Central Brain Tumor Registry of the United States. Primary brain tumors of the United States, Statistical Report (2000–2004), Years of Data Collected 2007–2008.
- Huse JT, Holland EC. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer. 2010;10:319–331. - PubMed
- Collins VP. Gliomas. Cancer Surv. 1998;32:37–51. - PubMed
- Dohrmann GJ, Farwell JR, Flannery JT. Glioblastoma multiforme in children. J Neurosurg. 1976;44:442–448. - PubMed
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