Bmi1 overexpression in the cerebellar granule cell lineage of mice affects cell proliferation and survival without initiating medulloblastoma formation

DMM Disease Models and Mechanisms

Volumn 6, Issue 1, 2013, Pages 49-63

  Behesti, Hourinaz ^a,d   Bhagat, Heeta ^a   Dubuc, Adrian M ^b,c   Taylor, Michael D ^b,c   Marino, Silvia ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; GENE EXPRESSION; GRANULE CELL; HUMAN; HUMAN CELL; MEDULLOBLASTOMA; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL CYCLE; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLAR NEOPLASMS; CEREBELLUM; EPIGENESIS, GENETIC; FEMALE; GENES, P53; HUMANS; MALE; MEDULLOBLASTOMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NEURAL STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 1; PROTO-ONCOGENE PROTEINS; RECEPTORS, CELL SURFACE; TRANSCRIPTOME; UP-REGULATION;

MUS; MUS MUSCULUS;

EID: 84872056933     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.009506     Document Type: Article

References (55)

1. Ajioka, I., Martins, R. A., Bayazitov, I. T., Donovan, S., Johnson, D. A., Frase, S., Cicero, S. A., Boyd, K., Zakharenko, S. S. and Dyer, M. A. (2007). Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131, 378-390.
2. Ankarcrona, M., Dypbukt, J. M., Bonfoco, E., Zhivotovsky, B., Orrenius, S., Lipton, S. A. and Nicotera, P. (1995). Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
3. Bahn, S., Jones, A. and Wisden, W. (1997). Directing gene expression to cerebellar granule cells using gamma-aminobutyric acid type A receptor alpha6 subunit transgenes. Proc. Natl. Acad. Sci. USA 94, 9417-9421.
4. Behesti, H. and Marino, S. (2009). Cerebellar granule cells: insights into proliferation, differentiation, and role in medulloblastoma pathogenesis. Int. J. Biochem. Cell Biol. 41, 435-445.
5. Chatoo, W., Abdouh, M., David, J., Champagne, M. P., Ferreira, J., Rodier, F. and Bernier, G. (2009). The polycomb group gene Bmi1 regulates antioxidant defenses in neurons by repressing p53 pro-oxidant activity. J. Neurosci. 29, 529-542.
6. Chen, G., Ma, C., Bower, K. A., Shi, X., Ke, Z. and Luo, J. (2008). Ethanol promotes endoplasmic reticulum stress-induced neuronal death: involvement of oxidative stress. J. Neurosci. Res. 86, 937-946.
7. Chen, Y. and Swanson, R. A. (2003). Astrocytes and brain injury. J. Cereb. Blood Flow Metab. 23, 137-149.
8. Dai, Y. and Grant, S. (2003). New insights into checkpoint kinase 1 in the DNA damage response signaling network. Clin. Cancer Res. 16, 376-383.
9. Davies, N. P., Wilson, M., Harris, L. M., Natarajan, K., Lateef, S., Macpherson, L., Sgouros, S., Grundy, R. G., Arvanitis, T. N. and Peet, A. C. (2008). Identification and characterisation of childhood cerebellar tumours by in vivo proton MRS. NMR Biomed. 21, 908-918.
10. Dobles, M., Liberal, V., Scott, M. L., Benezra, R. and Sorger, P. K. (2000). Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101, 635-645.
11. Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A., Jr, Butel, J. S. and Bradley, A. (1992). Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356, 215-221.
12. Ellison, D. (2002). Classifying the medulloblastoma: insights from morphology and molecular genetics. Neuropathol. Appl. Neurobiol. 28, 257-282.
13. Facchino, S., Abdouh, M., Chatoo, W. and Bernier, G. (2010). BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J. Neurosci. 30, 10096-10111.
14. Fasano, C. A., Dimos, J. T., Ivanova, N. B., Lowry, N., Lemischka, I. R. and Temple, S. (2007). shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 1, 87-99.
15. Fasano, C. A., Phoenix, T. N., Kokovay, E., Lowry, N., Elkabetz, Y., Dimos, J. T., Lemischka, I. R., Studer, L. and Temple, S. (2009). Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. Genes Dev. 23, 561-574.
16. Frandsen, A. and Schousboe, A. (1990). Development of excitatory amino acid induced cytotoxicity in cultured neurons. Int. J. Dev. Neurosci. 8, 209-216.
17. Fujita, S. (1967). Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. J. Cell Biol. 32, 277-287.
18. Fujita, S., Shimada, M. and Nakamura, T. (1966). H3-thymidine autoradiographic studies on the cell proliferation and differentiation in the external and the internal granular layers of the mouse cerebellum. J. Comp. Neurol. 128, 191-208.
19. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
20. Halfter, H., Friedrich, M., Resch, A., Kullmann, M., Stogbauer, F., Ringelstein, E. B. and Hengst, L. (2006). Oncostatin M induces growth arrest by inhibition of Skp2, Cks1, and cyclin A expression and induced p21 expression. Cancer Res. 66, 6530-6539.
21. Harvey, M., McArthur, M. J., Montgomery, C. A., Jr, Butel, J. S., Bradley, A. and Donehower, L. A. (1993). Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat. Genet. 5, 225-229.
22. Haupt, Y., Bath, M. L., Harris, A. W. and Adams, J. M. (1993). bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene 8, 3161-3164.
23. He, S., Iwashita, T., Buchstaller, J., Molofsky, A. V., Thomas, D. and Morrison, S. J. (2009). Bmi-1 over-expression in neural stem/progenitor cells increases proliferation and neurogenesis in culture but has little effect on these functions in vivo. Dev. Biol. 328, 257-272.
24. Jackson, S. P. and Bartek, J. (2009). The DNA-damage response in human biology and disease. Nature 461, 1071-1078.
25. Kato, K. (1990). Novel GABAA receptor alpha subunit is expressed only in cerebellar granule cells. J. Mol. Biol. 214, 619-624.
26. Kessler, J. D., Hasegawa, H., Brun, S. N., Emmenegger, B. A., Yang, Z. J., Dutton, J. W., Wang, F. and Wechsler-Reya, R. J. (2009). N-myc alters the fate of preneoplastic cells in a mouse model of medulloblastoma. Genes Dev. 23, 157-170.
27. Kool, M., Koster, J., Bunt, J., Hasselt, N. E., Lakeman, A., van Sluis, P., Troost, D., Meeteren, N. S., Caron, H. N., Cloos, J. et al. (2008). Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS ONE 3, e3088.
28. Leung, C., Lingbeek, M., Shakhova, O., Liu, J., Tanger, E., Saremaslani, P., Van Lohuizen, M. and Marino, S. (2004). Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 428, 337-341.
29. Liu, J., Cao, L., Chen, J., Song, S., Lee, I. H., Quijano, C., Liu, H., Keyvanfar, K., Chen, H., Cao, L. Y. et al. (2009). Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459, 387-392.
30. Lumpkin, E. A., Collisson, T., Parab, P., Omer-Abdalla, A., Haeberle, H., Chen, P., Doetzlhofer, A., White, P., Groves, A., Segil, N. et al. (2003). Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene. Expr. Patterns 3, 389-395.
31. Machold, R. and Fishell, G. (2005). Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48, 17-24.
32. Marino, S., Vooijs, M., van der Gulden, H., Jonkers, J. and Berns, A. (2000). Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14, 994-1004.
33. Molofsky, A. V., Pardal, R., Iwashita, T., Park, I. K., Clarke, M. F. and Morrison, S. J. (2003). Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425, 962-967.
34. Molofsky, A. V., He, S., Bydon, M., Morrison, S. J. and Pardal, R. (2005). Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 19, 1432-1437.
35. Mullen, R. J., Buck, C. R. and Smith, A. M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211.
36. Northcott, P. A., Korshunov, A., Witt, H., Hielscher, T., Eberhart, C. G., Mack, S., Bouffet, E., Clifford, S. C., Hawkins, C. E., French, P. et al. (2011). Medulloblastoma comprises four distinct molecular variants. J. Clin. Oncol. 29, 1408-1414.
37. Pomeroy, S. L., Tamayo, P., Gaasenbeek, M., Sturla, L. M., Angelo, M., McLaughlin, M. E., Kim, J. Y., Goumnerova, L. C., Black, P. M., Lau, C. et al. (2002). Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415, 436-442.
38. Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K. and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85.
39. Sasaki, T., Ito, Y., Xu, X., Han, J., Bringas, P., Jr, Maeda, T., Slavkin, H. C., Grosschedl, R. and Chai, Y. (2005). LEF1 is a critical epithelial survival factor during tooth morphogenesis. Dev. Biol. 278, 130-143.
40. Schafer, Z. T., Grassian, A. R., Song, L., Jiang, Z., Gerhart-Hines, Z., Irie, H. Y., Gao, S., Puigserver, P. and Brugge, J. S. (2009). Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 461, 109-113.
41. Schuller, U., Heine, V. M., Mao, J., Kho, A. T., Dillon, A. K., Han, Y. G., Huillard, E., Sun, T., Ligon, A. H., Qian, Y. et al. (2008). Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14, 123-134.
42. Skokowa, J., Cario, G., Uenalan, M., Schambach, A., Germeshausen, M., Battmer, K., Zeidler, C., Lehmann, U., Eder, M., Baum, C. et al. (2006). LEF-1 is crucial for neutrophil granulocytopoiesis and its expression is severely reduced in congenital neutropenia. Nat. Med. 12, 1191-1197.
43. Spaulding, C., Reschly, E. J., Zagort, D. E., Yashiro-Ohtani, Y., Beverly, L. J., Capobianco, A., Pear, W. S. and Kee, B. L. (2007). Notch1 co-opts lymphoid enhancer factor 1 for survival of murine T-cell lymphomas. Blood 110, 2650-2658.
44. Subkhankulova, T., Zhang, X., Leung, C. and Marino, S. (2010). Bmi1 directly represses p21Waf1/Cip1 in Shh-induced proliferation of cerebellar granule cell progenitors. Mol. Cell Neurosci. 45, 151-162.
45. Taylor, M. D., Northcott, P. A., Korshunov, A., Remke, M., Cho, Y. J., Clifford, S. C., Eberhart, C. G., Parsons, D. W., Rutkowski, S., Gajjar, A. et al. (2012). Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 123, 465-472.
46. Thompson, M. C., Fuller, C., Hogg, T. L., Dalton, J., Finkelstein, D., Lau, C. C., Chintagumpala, M., Adesina, A., Ashley, D. M., Kellie, S. J. et al. (2006). Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J. Clin. Oncol. 24, 1924-1931.
47. Valk-Lingbeek, M. E., Bruggeman, S. W. and van Lohuizen, M. (2004). Stem cells and cancer; the polycomb connection. Cell 118, 409-418.
48. van der Lugt, N. M., Domen, J., Linders, K., van Roon, M., Robanus-Maandag, E., te Riele, H., van der Valk, M., Deschamps, J., Sofroniew, M., van Lohuizen, M. et al. (1994). Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 8, 757-769.
49. Wingate, R. J. and Hatten, M. E. (1999). The role of the rhombic lip in avian cerebellum development. Development 126, 4395-4404.
50. Wu, V. W. and Schwartz, J. P. (1998). Cell culture models for reactive gliosis: new perspectives. J. Neurosci. Res. 51, 675-681.
51. Yadirgi, G., Leinster, V. H., Acquati, S., Bhagat, H., Shakhova, O. and Marino, S. (2011). Conditional activation of Bmi1 expression regulates self renewal, apoptosis and differentiation of neural stem/progenitor cells in vitro and in vivo. Stem Cells 29, 700-712.
52. Yang, Z. J., Ellis, T., Markant, S. L., Read, T. A., Kessler, J. D., Bourboulas, M., Schuller, U., Machold, R., Fishell, G., Rowitch, D. H. et al. (2008). Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 14, 135-145.
53. Yoshioka, A., Ikegaki, N., Williams, M. and Pleasure, D. (1996). Expression of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor genes in neuroblastoma, medulloblastoma, and other cells lines. J. Neurosci. Res. 46, 164-178.
54. Yoshioka, H., Mino, M., Morikawa, Y., Kasubuchi, Y. and Kusunoki, T. (1985). Changes in cell proliferation kinetics in the mouse cerebellum after total asphyxia. Pediatrics 76, 965-969.
55. Zinkel, S., Gross, A. and Yang, E. (2006). BCL2 family in DNA damage and cell cycle control. Cell Death Differ. 13, 1351-1359.