Targeting of BMI-1 with PTC-209 inhibits glioblastoma development

References

• Qazi MA, Vora P, Venugopal C, et al. Intratumoral heterogeneity: pathways to treatment resistance and relapse in human glioblastoma. Ann Oncol. 2017;28:1448–1456.
   PubMed Web of Science ®Google Scholar
• Osuka S, Van Meir EG. Overcoming therapeutic resistance in glioblastoma: the way forward. J Clin Invest. 2017;127:415–426.
   PubMed Web of Science ®Google Scholar
• Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14:275–291.
   PubMed Web of Science ®Google Scholar
• Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013;501:328–337.
   PubMed Web of Science ®Google Scholar
• Alvarado AG, Thiagarajan PS, Mulkearns-Hubert EE, et al. Glioblastoma cancer stem cells evade innate immune suppression of self-renewal through reduced TLR4 expression. Cell Stem Cell. 2017;20:450–461 e454.
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760.
   PubMed Web of Science ®Google Scholar
• Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488:522–526.
   PubMed Web of Science ®Google Scholar
• Triscott J, Rose Pambid M, Dunn SE. Concise review: bullseye: targeting cancer stem cells to improve the treatment of gliomas by repurposing disulfiram. Stem Cells (Dayton, Ohio). 2015;33:1042–1046.
   PubMed Web of Science ®Google Scholar
• Zhu Z, Khan MA, Weiler M, et al. Targeting self-renewal in high-grade brain tumors leads to loss of brain tumor stem cells and prolonged survival. Cell Stem Cell. 2014;15:185–198.
   PubMed Web of Science ®Google Scholar
• Di Croce L, Helin K. Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol. 2013;20:1147–1155.
   PubMed Web of Science ®Google Scholar
• Alkema MJ, Jacobs H, van Lohuizen M, et al. Pertubation of B and T cell development and predisposition to lymphomagenesis in Emu Bmi1 transgenic mice require the Bmi1 RING finger. Oncogene. 1997;15:899–910.
   PubMed Web of Science ®Google Scholar
• Bruggeman SW, Hulsman D, Tanger E, et al. Bmi1 controls tumor development in an ink4a/arf-independent manner in a mouse model for glioma. Cancer Cell. 2007;12:328–341.
   PubMed Web of Science ®Google Scholar
• Abdouh M, Facchino S, Chatoo W, et al. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci. 2009;29:8884–8896.
   PubMed Web of Science ®Google Scholar
• Chiba T, Miyagi S, Saraya A, et al. The polycomb gene product BMI1 contributes to the maintenance of tumor-initiating side population cells in hepatocellular carcinoma. Cancer Res. 2008;68:7742–7749.
   PubMed Web of Science ®Google Scholar
• Dovey JS, Zacharek SJ, Kim CF, et al. Bmi1 is critical for lung tumorigenesis and bronchioalveolar stem cell expansion. Proc Natl Acad Sci U S A. 2008.
   PubMed Web of Science ®Google Scholar
• Chen D, Wu M, Li Y, et al. Targeting BMI1+ cancer stem cells overcomes chemoresistance and inhibits metastases in squamous cell carcinoma. Cell Stem Cell. 2017;20:621–634 e626.
   PubMed Web of Science ®Google Scholar
• Ferretti R, Bhutkar A, McNamara MC, et al. BMI1 induces an invasive signature in melanoma that promotes metastasis and chemoresistance. Genes Dev. 2016;30:18–33.
   PubMed Web of Science ®Google Scholar
• Kreso A, van Galen P, Pedley NM, et al. Self-renewal as a therapeutic target in human colorectal cancer. Nat Med. 2014;20:29–36.
   PubMed Web of Science ®Google Scholar
• Bolomsky A, Schlangen K, Schreiner W, et al. Targeting of BMI-1 with PTC-209 shows potent anti-myeloma activity and impairs the tumour microenvironment. J Hematol Oncol. 2016;9:17.
   PubMed Web of Science ®Google Scholar
• Mayr C, Wagner A, Loeffelberger M, et al. The BMI1 inhibitor PTC-209 is a potential compound to halt cellular growth in biliary tract cancer cells. Oncotarget. 2016;7:745–758.
   PubMed Web of Science ®Google Scholar
• Gargiulo G, Cesaroni M, Serresi M, et al. In Vivo RNAi Screen for BMI1 Targets Identifies TGF-beta/BMP-ER stress pathways as key regulators of neural- and malignant glioma-stem cell homeostasis. Cancer Cell. 2013;23:660–676.
   PubMed Web of Science ®Google Scholar
• Jin X, Kim LJY, Wu Q, et al. Targeting glioma stem cells through combined BMI1 and EZH2 inhibition. Nat Med. 2017.
   Web of Science ®Google Scholar
• Nawaz Z, Patil V, Arora A, et al. Cbx7 is epigenetically silenced in glioblastoma and inhibits cell migration by targeting YAP/TAZ-dependent transcription. Sci Rep. 2016;6:27753.
   PubMed Web of Science ®Google Scholar
• Pullen NA, Anand M, Cooper PS, et al. Matrix metalloproteinase-1 expression enhances tumorigenicity as well as tumor-related angiogenesis and is inversely associated with TIMP-4 expression in a model of glioblastoma. J Neurooncol. 2012;106:461–471.
   PubMed Web of Science ®Google Scholar
• Stricker SH, Feber A, Engstrom PG, et al. Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner. Genes Dev. 2013;27:654–669.
   PubMed Web of Science ®Google Scholar
• Ying M, Tilghman J, Wei Y, et al. Kruppel-like factor-9 (KLF9) inhibits glioblastoma stemness through global transcription repression and integrin alpha6 inhibition. J Biol Chem. 2014;289:32742–32756.
   PubMed Web of Science ®Google Scholar
• Huang K, Yang C, Wang QX, et al. The CRISPR/Cas9 system targeting EGFR exon 17 abrogates NF-kappaB activation via epigenetic modulation of UBXN1 in EGFRwt/vIII glioma cells. Cancer Lett. 2016;388:269–280.
   PubMed Web of Science ®Google Scholar
• Suva ML, Rheinbay E, Gillespie SM, et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell. 2014;157:580–594.
   PubMed Web of Science ®Google Scholar
• Mao DD, Gujar AD, Mahlokozera T, et al. A CDC20-APC/SOX2 signaling axis regulates human glioblastoma stem-like cells. Cell Rep. 2015;11:1809–1821.
   Google Scholar
• Cheng W, Ren X, Zhang C, et al. Bioinformatic profiling identifies an immune-related risk signature for glioblastoma. Neurology. 2016;86:2226–2234.
   PubMed Web of Science ®Google Scholar
• Sturm D, Bender S, Jones DT, et al. Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge. Nat Rev Cancer. 2014;14:92–107.
   PubMed Web of Science ®Google Scholar
• Natsume A, Ito M, Katsushima K, et al. Chromatin regulator PRC2 is a key regulator of epigenetic plasticity in glioblastoma. Cancer Res. 2013;73:4559–4570.
   PubMed Web of Science ®Google Scholar
• Li G, Warden C, Zou Z, et al. Altered expression of polycomb group genes in glioblastoma multiforme. PLoS ONE. 2013;8:e80970.
   PubMed Web of Science ®Google Scholar
• Melnick A. Epigenetic therapy leaps ahead with specific targeting of EZH2. Cancer Cell. 2012;22:569–570.
   PubMed Web of Science ®Google Scholar
• de Vries NA, Hulsman D, Akhtar W, et al. Prolonged Ezh2 depletion in glioblastoma causes a robust switch in cell fate resulting in tumor progression. Cell Rep. 2015;10:383–397.
   Web of Science ®Google Scholar
• Kim E, Kim M, Woo DH, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell. 2013;23:839–852.
   PubMed Web of Science ®Google Scholar
• Sashida G, Wang C, Tomioka T, et al. The loss of Ezh2 drives the pathogenesis of myelofibrosis and sensitizes tumor-initiating cells to bromodomain inhibition. J Exp Med. 2016;213:1459–1477.
   PubMed Web of Science ®Google Scholar
• Ntziachristos P, Tsirigos A, Van Vlierberghe P, et al. Genetic inactivation of the polycomb repressive complex 2 in T cell acute lymphoblastic leukemia. Nat Med. 2012;18:298–301.
   PubMed Web of Science ®Google Scholar
• Brennan CW, Verhaak RG, McKenna A, et al. The somatic genomic landscape of glioblastoma. Cell. 2013;155:462–477.
   PubMed Web of Science ®Google Scholar
• Riising EM, Comet I, Leblanc B, et al. Gene silencing triggers polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol Cell. 2014;55:347–360.
   PubMed Web of Science ®Google Scholar
• Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347:70–78.
   PubMed Web of Science ®Google Scholar
• Wu X, Bekker-Jensen IH, Christensen J, et al. Tumor suppressor ASXL1 is essential for the activation of INK4B expression in response to oncogene activity and anti-proliferative signals. Cell Res. 2015;25:1205–1218.
   PubMed Web of Science ®Google Scholar
• Voskoglou-Nomikos T, Pater JL, Seymour L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res. 2003;9:4227–4239.
   PubMed Web of Science ®Google Scholar