Downregulation of TLX induces TET3 expression and inhibits glioblastoma stem cell self-renewal and tumorigenesis

Nature Communications

Volumn 7, Issue , 2016, Pages

  Cui, Qi ^a   Yang, Su ^a   Ye, Peng ^a   Tian, E ^a   Sun, Guoqiang ^a   Zhou, Jiehua ^a   Sun, Guihua ^a   Liu, Xiaoxuan ^b   Chen, Chao ^b   Murai, Kiyohito ^a   Zhao, Chunnian ^a   Azizian, Krist T ^a   Yang, Lu ^a   Warden, Charles ^a   Wu, Xiwei ^a   D'Apuzzo, Massimo ^a   Brown, Christine ^a   Badie, Behnam ^a   Peng, Ling ^b   Riggs, Arthur D ^a   Rossi, John J ^a   Shi, Yanhong ^a   more..

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; NUCLEAR RECEPTOR TLX; PROTEIN; SHORT HAIRPIN RNA; TEN ELEVEN TRANSLOCATION 3 PROTEIN; UNCLASSIFIED DRUG; VIRUS VECTOR; CELL RECEPTOR; DIOXYGENASE; NR2E1 PROTEIN, HUMAN; TET3 PROTEIN, HUMAN;

BRAIN; CANCER; CELLS AND CELL COMPONENTS; CHEMOTHERAPY; DISEASE VECTOR; ENZYME ACTIVITY; GENE EXPRESSION; PROTEIN; RODENT; TUMOR;

ANIMAL EXPERIMENT; ARTICLE; CANCER DIAGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CARCINOGENICITY; CONTROLLED STUDY; DOWN REGULATION; DRUG DELIVERY SYSTEM; GLIOBLASTOMA; HUMAN; IN VITRO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; STEM CELL SELF-RENEWAL; TUMOR GROWTH; ANIMAL; BRAIN TUMOR; CANCER STEM CELL; CANCER TRANSPLANTATION; CELL SELF-RENEWAL; CHROMATIN IMMUNOPRECIPITATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TUMOR STEM CELL ASSAY;

MUS;

ANIMALS; BRAIN NEOPLASMS; CARCINOGENESIS; CELL SELF RENEWAL; CHROMATIN IMMUNOPRECIPITATION; DIOXYGENASES; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; MICE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TUMOR STEM CELL ASSAY;

EID: 84957546014     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10637     Document Type: Article

References (58)

1. Louis, D. N. et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 114, 97-109 (2007).
2. Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004).
3. Bao, S. et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760 (2006).
4. Godlewski, J., Newton, H. B., Chiocca, E. A., Lawler, S. E. MicroRNAs and glioblastoma; the stem cell connection. Cell Death Differ. 17, 221-228 (2010).
5. Reya, T., Morrison, S. J., Clarke, M. F., Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001).
6. Tan, B. T., Park, C. Y., Ailles, L. E., Weissman, I. L. The cancer stem cell hypothesis: a work in progress. Lab. Invest. 86, 1203-1207 (2006).
7. Antoniou, A., Hebrant, A., Dom, G., Dumont, J. E., Maenhaut, C. Cancer stem cells, a fuzzy evolving concept: a cell population or a cell property? Cell Cycle 12, 3743-3748 (2013).
8. Sundar, S. J., Hsieh, J. K., Manjila, S., Lathia, J. D., Sloan, A. The role of cancer stem cells in glioblastoma. Neurosurg. Focus 37, E6 (2014).
9. Allegra, A. et al. The cancer stem cell hypothesis: a guide to potential molecular targets. Cancer Invest. 32, 470-495 (2014).
10. Yu, R. T., McKeown, M., Evans, R. M., Umesono, K. Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx. Nature 370, 375-379 (1994).
11. Shi, Y. et al. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427, 78-83 (2004).
12. Qu, Q. et al. Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat. Cell Biol. 12, 31-40 Suppl pp 31-39 (2010).
13. Park, H. J. et al. The neural stem cell fate determinant TLX promotes tumorigenesis and genesis of cells resembling glioma stem cells. Mol. Cells 30, 403-408 (2010).
14. Liu, H. K. et al. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev. 24, 683-695 (2010).
15. Yang, H. et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene 32, 663-669 (2013).
16. Haffner, M. C. et al. Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget 2, 627-637 (2011).
17. Lian, C. G. et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell 150, 1135-1146 (2012).
18. Orr, B. A., Haffner, M. C., Nelson, W. G., Yegnasubramanian, S., Eberhart, C. G. Decreased 5-hydroxymethylcytosine is associated with neural progenitor phenotype in normal brain and shorter survival in malignant glioma. PLoS ONE 7, e41036 (2012).
19. Jin, S. G. et al. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res. 71, 7360-7365 (2011).
20. Xu, W. et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17-30 (2011).
21. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
22. Kriaucionis, S., Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930 (2009).
23. Moran-Crusio, K. et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20, 11-24 (2011).
24. Quivoron, C. et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20, 25-38 (2011).
25. Song, S. J. et al. The oncogenic microRNA miR-22 targets the TET2 tumor suppressor to promote hematopoietic stem cell self-renewal and transformation. Cell Stem Cell 13, 87-101 (2013).
26. Song, S. J. et al. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell 154, 311-324 (2013).
27. Haussecker, D., Kay, M. A. RNA interference. Drugging RNAi. Science 347, 1069-1070 (2015).
28. Cambon, K., Deglon, N. Lentiviral-mediated gene transfer of siRNAs for the treatment of Huntington's disease. Methods Mol. Biol. 1010, 95-109 (2013).
29. Tseng, Y. C., Mozumdar, S., Huang, L. Lipid-based systemic delivery of siRNA. Adv. Drug Deliv. Rev. 61, 721-731 (2009).
30. Whitehead, K. A., Langer, R., Anderson, D. G. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 8, 129-138 (2009).
31. Dutta, T., Garg, M., Jain, N. K. Poly(propyleneimine) dendrimer and dendrosome mediated genetic immunization against hepatitis B. Vaccine 26, 3389-3394 (2008).
32. Wolinsky, J. B., Grinstaff, M. W. Therapeutic and diagnostic applications of dendrimers for cancer treatment. Adv. Drug Deliv. Rev. 60, 1037-1055 (2008).
33. Liu, X., Rocchi, P., Peng, L. Dendrimers as non-viral vectors for siRNA delivery. N. J. Chem. 36, 256-263 (2012).
34. Liu, X. et al. Structurally flexible triethanolamine-core poly(amidoamine) dendrimers as effective nanovectors to deliver RNAi-based therapeutics. Biotechnol. Adv. 32, 844-852 (2014).
35. Behr, J. P. The proton sponge: A trick to enter cells the viruses did not exploit. Chimia (Aarau). 51, 34-36 (1997).
36. Brown, C. E. et al. Recognition and killing of brain tumor stem-like initiating cells by CD8\+ cytolytic T cells. Cancer Res. 69, 8886-8893 (2009).
37. Verhaak, R. G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110 (2010).
38. Zhou, J. et al. PAMAM dendrimers for efficient siRNA delivery and potent gene silencing. Chem. Commun. (Camb) 2362-2364 (2006).
39. Zhou, J. et al. Systemic administration of combinatorial dsiRNAs via nanoparticles efficiently suppresses HIV-1 infection in humanized mice. Mol. Ther. 19, 2228-2238 (2011).
40. Liu, X. et al. Targeted delivery of Dicer-substrate siRNAs using a dual targeting peptide decorated dendrimer delivery system. Nanomedicine 10, 1627-1636 (2014).
41. Desgrosellier, J. S., Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9-22 (2010).
42. Teesalu, T., Sugahara, K. N., Kotamraju, V. R., Ruoslahti, E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl Acad. Sci. USA 106, 16157-16162 (2009).
43. Sugahara, K. N. et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 16, 510-520 (2009).
44. Zhou, J. et al. Biodegradable poly(amine-co-ester) terpolymers for targeted gene delivery. Nat. Mater. 11, 82-90 (2012).
45. Sun, G., Yu, R. T., Evans, R. M., Shi, Y. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc. Natl Acad. Sci. USA 104, 15282-15287 (2007).
46. Zou, Y. et al. The nuclear receptor TLX is required for gliomagenesis within the adult neurogenic niche. Mol. Cell Biol. 32, 4811-4820 (2012).
47. Zhu, Z. et al. Targeting self-renewal in high-grade brain tumors leads to loss of brain tumor stem cells and prolonged survival. Cell Stem Cell 15, 185-198 (2014).
48. Murai, K. et al. Nuclear receptor TLX stimulates hippocampal neurogenesis and enhances learning and memory in a transgenic mouse model. Proc. Natl Acad. Sci. USA 111, 9115-9120 (2014).
49. Liu, N. et al. Intrinsic and extrinsic connections of Tet3 dioxygenase with CXXC zinc finger modules. PLoS ONE 8, e62755 (2013).
50. Perera, A. et al. TET3 is recruited by REST for context-specific hydroxymethylation and induction of gene expression. Cell Rep. 11, 283-294 (2015).
51. Xu, Y. et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 151, 1200-1213 (2012).
52. Kim, Y. et al. Platelet-derived growth factor receptors differentially inform intertumoral and intratumoral heterogeneity. Genes Dev. 26, 1247-1262 (2012).
53. Yan, K. et al. Glioma cancer stem cells secrete Gremlin1 to promote their maintenance within the tumor hierarchy. Genes Dev. 28, 1085-1100 (2014).
54. Ito, S. et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133 (2010).
55. Jin, K. et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl Acad. Sci. USA 99, 11946-11950 (2002).
56. Zhao, C. et al. microRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc. Natl Acad. Sci. USA 107, 1876-1881 (2010).
57. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
58. Hu, Y., Smyth, G. K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70-78 (2009).