Foxg1 interacts with bmi1 to regulate self-renewal and tumorigenicity of Medulloblastoma stem cells

Stem Cells

Volumn 31, Issue 7, 2013, Pages 1266-1277

  Manoranjan, Branavan ^a   Wang, Xin ^b   Hallett, Robin M ^a   Venugopal, Chitra ^a   Mack, Stephen C ^b   McFarlane, Nicole ^a   Nolte, Sara M ^a   Scheinemann, Katrin ^a   Gunnarsson, Thorsteinn ^a   Hassell, John A ^a   Taylor, Michael D ^b,c   Lee, Cathy ^d   Triscott, Joanna ^d   Foster, Colleen M ^d   Dunham, Christopher ^e   Hawkins, Cynthia ^b,f   Dunn, Sandra E ^d   Singh, Sheila K ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b Division of Neurosurgery   (Canada)

^c Arthur and Sonia Labatt Brain Tumor Research Centre ^*  (Canada)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f BC CHILDREN S HOSPITAL   (Canada)

Author keywords

Bmi1; Brain tumor initiating cell; FoxG1; Medulloblastoma; Self renewal; Stem cells

Indexed keywords

BMI1 PROTEIN; CD15 ANTIGEN; FORKHEAD BOX G1 PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MEDULLOBLASTOMA; MEDULLOBLASTOMA STEM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PROTEIN INTERACTION; STEM CELL;

BMI1; BRAIN TUMOR-INITIATING CELL; FOXG1; MEDULLOBLASTOMA; SELF-RENEWAL; STEM CELLS;

ANIMALS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CEREBELLAR NEOPLASMS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MEDULLOBLASTOMA; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; POLYCOMB REPRESSIVE COMPLEX 1; PROGNOSIS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

MUS;

EID: 84879917277     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1401     Document Type: Article

References (73)

1. Crawford JR, MacDonald TJ, Packer RJ. Medulloblastoma in childhood: New biological advances. Lancet Neurol 2007;6:1073-1085.
2. Gilbertson RJ. Medulloblastoma: Signalling a change in treatment. Lancet Oncol 2004;5:209-218.
3. Huse JT, Holland EC. Targeting brain cancer: Advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 2010;10:1-13.
4. Ellison DW. Childhood medulloblastoma: Novel approaches to the classification of a heterogeneous disease. Acta Neuropathol 2010;120: 305-316.
5. Korshunov A, Remke M, Werft W et al. Adult and pediatric medulloblastomas are genetically distinct and require different algorithms for molecular risk stratification. J Clin Oncol 2010;28:3054-3060.
6. Cho YJ, Tsherniak A, Tamayo P et al. Integrative genomic analysis of medulloblastoma identifies a molecular subgroup that drives poor clinical outcome. J Clin Oncol 2011;29:1424-1130.
7. Kool M, Koster J, Bunt J et al. Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. Plos One 2008;3:e3088.
8. Northcott PA, Korshunov A, Witt H et al. Medulloblastoma comprises four distinct molecular variants. J Clin Oncol 2011;29:1408-1414.
9. Pomeroy SL, Tamayo P, Gaasenbeek M et al. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 2002;415:436-442.
10. Thompson MC, Fuller C, Hogg TL et al. Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J Clin Oncol 2006;24:1924-1931.
11. Ellison DW, Onilude OE, Lindsey JC et al. b-Catenin status predicts a favorable outcome in childhood medulloblastoma: The United Kingdom Children's Cancer Study Group Brain Tumour Committee. J Clin Oncol 2005;23:7951-7957.
12. Fattet S, Haberler C, Legoix P et al. b-Catenin status in paediatric medulloblastomas: Correlation of immunohistochemical expression with mutational status, genetic profiles, and clinical characteristics. J Pathol 2009;218:86-94.
13. Taylor MD, Northcott PA, Korshunov A et al. Molecular subgroups of medulloblastoma: The current consensus. Acta Neuropathol 2012; 123:465-472.
14. Pfister S, Remke M, Benner A et al. Outcome prediction in pediatric medulloblastoma based on DNA copy-number aberrations of chromosomes 6q and 17q and the MYC and MYCN loci. J Clin Oncol 2009; 27:1627-1636.
15. Romer JT, Kimura H, Magdaleno S et al. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1+/-p53-/- mice. Cancer Cell 2004;6:229-240.
16. Rudin CM, Hann CL, Laterra J et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449.N Engl J Med 2009;361: 1173-1178.
17. Kool M, Korshunov A, Remke M et al. Molecular subgroups of medulloblastoma: An international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, group 3, and group 4 medulloblastomas. Acta Neuropathol 2012;123:473-484.
18. Pei Y, Moore CE, Wang J et al. An animal model of MYC-driven medulloblastoma. Cancer Cell 2012;21:155-167.
19. Kawauchi D, Robinson G, Uziel T et al. A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer Cell 2012;21: 168-180.
20. Remke M, Hielscher T, Korshunov A et al. FSTL5 Is a marker of poor prognosis in non-WNT/non-SHH medulloblastoma. J Clin Oncol 2011;29:3852-3861.
21. Fan X, Khaki L, Zhu TS et al. Notch pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010;28:5-16.
22. Leung C, Lingbeek M, Shakhova O et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004;428:337-341.
23. Schreck KC, Taylor P, Marchionni L et al. The notch target Hes1 directly modulates Gli1 expression and hedgehog signaling: A potential mechanism of therapeutic resistance. Clin Cancer Res 2010;16: 6060-6070.
24. Panosyan EH, Laks DR, Masterman-Smith M et al. Clinical outcome in pediatric glial and embryonal brain tumors correlates with in vitro multi-passageable neurosphere formation. Pediatr Blood Cancer 2010; 55:644-651.
25. Clarke MF, Dick JE, Dirks PB et al. Cancer stem cells-Perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res 2006;66:9339-9944.
26. Reya T, Morrison S, Clarke M. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-111.
27. Singh S, Clarke I, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821-5828.
28. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401.
29. Gage F. Mammalian neural stem cells. Science 2000;287:1433-1438.
30. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 1996;175:1-13.
31. Laks DR, Masterman-Smith M, Visnyei K et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 2009;27:980-987.
32. Pallini R, Ricci-Vitiani L, Montano N et al. Expression of the stem cell marker CD133 in recurrent glioblastoma and its value for prognosis. Cancer 2010;117:162-174.
33. Irizarry RA, Hobbs B, Collin F et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4:249-264.
34. Gerlinger M, Rowan AJ, Horswell S et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012;366:883-892.
35. Lee C, Fotovati A, Triscott J et al. Polo-like kinase 1 (PLK1) inhibition kills glioblastoma multiforme brain tumour cells in part through loss of Sox2 and delays tumour progression in mice. Stem Cells 2012; 30:1064-1075.
36. Wang X, Venugopal C, Manoranjan B et al. Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells. Oncogene 2012;31:187-199.
37. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-260.
38. Read TA, Fogarty MP, Markant SL et al. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 2009;15:135-47.
39. Ward RJ, Lee L, Graham K et al. Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma. Cancer Res 2009; 69:4682-4890.
40. O'Brien CA, Pollett A, Gallinger S et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106-110.
41. Ricci-Vitiani L, Lombardi DG, Pilozzi E et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445: 111-115.
42. Fasano CA, Phoenix TN, Kokovay E et al. Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. Genes Dev 2009;23:561-574.
43. Regad T, Roth M, Bredenkamp N et al. The neural progenitor-specifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat Cell Biol 2007;9:532-540.
44. Barker N, Ridgway RA, van Es JH et al. Crypt stem cells as the cellsof- origin of intestinal cancer. Nature 2009;457:608-611.
45. Kanemura Y, Mori K, Sakakibara S et al. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 2001;68:141-152.
46. Po A, Ferretti E, Miele E et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J 2010;25:1-13.
47. Fareh M, Turchi L, Virolle V et al. The miR 302-367 cluster drastically affects self-renewal and infiltration properties of glioma-initiating cells through CXCR4 repression and consequent disruption of the SHH-GLI-NANOG network. Cell Death Differ 2012;19:232-244.
48. Jeter CR, Liu B, Liu X et al. NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene 2011;30:3833-3845.
49. Chiou SH, Wang ML, Chou YT et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res 2010;70:10433-10444.
50. Moon JH, Yoon BS, Kim B et al. Induction of neural stem cell-like cells (NSCLCs) from mouse astrocytes by Bmi1.Biochem Biophys Res Commun 2008;371:267-272.
51. Rodini CO, Suzuki DE, Saba-Silva N et al. Expression analysis of stem cell-related genes reveal OCT4 as a predictor of poor clinical outcome in medulloblastoma. J Neurooncol 2012;106:71-79.
52. Beltran AS, Rivenbark AG, Richardson BT et al. Generation of tumor- initiating cells by exogenous delivery of OCT4 transcription factor. Breast Cancer Res 2011;13:R94.
53. Hagerstrand D, He X, Bradic Lindh M et al. Identification of a SOX2- dependent subset of tumor- and sphere-forming glioblastoma cells with a distinct tyrosine kinase inhibitor sensitivity profile. Neuro Oncol 2011;13:1178-1191.
54. Sutter R, Shakhova O, Bhagat H et al. Cerebellar stem cells act as medulloblastoma-initiating cells in a mouse model and a neural stem cell signature characterizes a subset of human medulloblastomas. Oncogene 2010;29:1845-1856.
55. Leis O, Eguiara A, Lopez-Arribillaga E et al. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 2011;31:1354-1365.
56. Basu-Roy U, Seo E, Ramanathapuram L et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene 2012;31: 2270-2282.
57. Beck S, Jin X, Sohn YW et al. Telomerase activity-independent function of TERT allows glioma cells to attain cancer stem cell characteristics by inducing EGFR expression. Mol Cell 2011;31:9-15.
58. Didiano D, Shalaby T, Lang D et al. Telomere maintenance in childhood primitive neuroectodermal brain tumors. Neuro Oncol 2004;6:1-8.
59. Yang MH, Hsu DS, Wang HW et al. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol 2010;12:982-992.
60. Mikheeva SA, Mikheev AM, Petit A et al. TWIST1 promotes invasion through mesenchymal change in human glioblastoma. Mol Cancer 2010; 9:194.
61. Gibson P, Tong Y, Robinson G et al. Subtypes of medulloblastoma have distinct developmental origins. Nature 2010;468:1095-1099.
62. Kim J, Woo AJ, Chu J et al. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010;143:313-324.
63. Adesina AM, Nguyen Y, Mehta V et al. FOXG1 dysregulation is a frequent event in medulloblastoma. J Neurooncol 2007;85:111-122.
64. Northcott PA, Shih DJ, Peacock J et al. Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 2012;488:49-56.
65. Yadirgi G, Leinster V, Acquati S et al. Conditional activation of Bmi1 expression regulates self-renewal, apoptosis, and differentiation of neural stem/progenitor cells in vitro and in vivo. Stem Cells 2011;29:700-712.
66. Chan DW, Liu VW, To RM et al. Overexpression of FOXG1 contributes to TGF-beta resistance through inhibition of p21WAF1/CIP1 expression in ovarian cancer. Br J Cancer 2009;101:1433-1443.
67. Fasano CA, Dimos JT, Ivanova NB et al. shRNA knockdown of Bmi- 1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 2007;1:87-99.
68. Subkhankulova T, Zhang X, Leung C et al. Bmi1 directly represses p21Waf1/Cip1 in Shh-induced proliferation of cerebellar granule cell progenitors. Mol Cell Neurosci 2010;45:151-162.
69. Molofsky AV, Pardal R, Iwashita T et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003;425:962-967.
70. Venugopal C, Li N, Wang X et al. Bmi1 marks intermediate precursors during differentiation of human brain tumor initiating cells. Stem Cell Res 2012;8:141-153.
71. Gilbertson R, Wickramasinghe C, Hernan R et al. Clinical and molecular stratification of disease risk in medulloblastoma. Br J Cancer 2001;85:705-712.
72. Gilbertson RJ, Ellison DW. The origins of medulloblastoma subtypes. Annu Rev Pathol 2008;3:341-365.
73. Northcott PA, Shih DJ, Remke M et al. Rapid, reliable, and reproducible molecular sub-grouping of clinical medulloblastoma samples. Acta Neuropathol 2012;123:615-626.