The Central Nervous System-Restricted Transcription Factor Olig2 Opposes p53 Responses to Genotoxic Damage in Neural Progenitors and Malignant Glioma

Cancer Cell

Volumn 19, Issue 3, 2011, Pages 359-371

  Mehta, Shwetal ^a   Huillard, Emmanuelle ^b   Kesari, Santosh ^c,d   Maire, Cecile L ^c   Golebiowski, Diane ^a   Harrington, Emily P ^b   Alberta, John A ^a   Kane, Michael F ^a   Theisen, Matthew ^c   Ligon, Keith L ^c,e   Rowitch, David H ^b   Stiles, Charles D ^a  

^a Department of Cancer Biology ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN P21; PROTEIN P53;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DNA DAMAGE; GENE EXPRESSION; GENE TARGETING; GENOTOXICITY; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RADIOSENSITIVITY;

EID: 79952217981     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.01.035     Document Type: Article

References (72)

1. Bachoo R.M., Maher E.A., Ligon K.L., Sharpless N.E., Chan S.S., You M.J., Tang Y., DeFrances J., Stover E., Weissleder R., et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 2002, 1:269-277.
2. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
3. Barlev N.A., Liu L., Chehab N.H., Mansfield K., Harris K.G., Halazonetis T.D., Berger S.L. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol. Cell 2001, 8:1243-1254.
4. Boiko A.D., Razorenova O.V., van de Rijn M., Swetter S.M., Johnson D.L., Ly D.P., Butler P.D., Yang G.P., Joshua B., Kaplan M.J., et al. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 2010, 466:133-137.
5. Brugarolas J., Chandrasekaran C., Gordon J.I., Beach D., Jacks T., Hannon G.J. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995, 377:552-557.
6. Cairncross J.G., Macdonald D.R. Successful chemotherapy for recurrent malignant oligodendroglioma. Ann. Neurol. 1988, 23:360-364.
7. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068. Cancer Genome Atlas Research Network.
8. Donehower L.A., Harvey M., Slagle B.L., McArthur M.J., Montgomery C.A., Butel J.S., Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356:215-221.
9. Dornan D., Shimizu H., Perkins N.D., Hupp T.R. DNA-dependent acetylation of p53 by the transcription coactivator p300. J. Biol. Chem. 2003, 278:13431-13441.
10. Drost J., Mantovani F., Tocco F., Elkon R., Comel A., Holstege H., Kerkhoven R., Jonkers J., Voorhoeve P.M., Agami R., Del Sal G. BRD7 is a candidate tumour suppressor gene required for p53 function. Nat. Cell Biol. 2010, 12:380-389.
11. Eaves C.J. Cancer stem cells: here, there, everywhere?. Nature 2008, 456:581-582.
12. el-Deiry W.S., Tokino T., Velculescu V.E., Levy D.B., Parsons R., Trent J.M., Lin D., Mercer W.E., Kinzler K.W., Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993, 75:817-825.
13. Fei P., Bernhard E.J., El-Deiry W.S. Tissue-specific induction of p53 targets in vivo. Cancer Res. 2002, 62:7316-7327.
14. Fortin D., Cairncross G.J., Hammond R.R. Oligodendroglioma: an appraisal of recent data pertaining to diagnosis and treatment. Neurosurgery 1999, 45:1279-1291. discussion 1191.
15. Gartel A.L., Tyner A.L. Transcriptional regulation of the p21(WAF1/CIP1) gene. Exp. Cell Res. 1999, 246:280-289.
16. Hack M.A., Sugimori M., Lundberg C., Nakafuku M., Gotz M. Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol. Cell. Neurosci. 2004, 25:664-678.
17. Harvey M., McArthur M.J., Montgomery C.A., Butel J.S., Bradley A., Donehower L.A. Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat. Genet. 1993, 5:225-229.
18. Hollstein M., Hainaut P. Massively regulated genes: the example of TP53. J. Pathol. 2010, 220:164-173.
19. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
20. Horn H.F., Vousden K.H. Coping with stress: multiple ways to activate p53. Oncogene 2007, 26:1306-1316.
21. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
22. Kannan K., Amariglio N., Rechavi G., Jakob-Hirsch J., Kela I., Kaminski N., Getz G., Domany E., Givol D. DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene 2001, 20:2225-2234.
23. Kawamura T., Suzuki J., Wang Y.V., Menendez S., Morera L.B., Raya A., Wahl G.M., Belmonte J.C. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009, 460:1140-1144.
24. Kippin T.E., Martens D.J., van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 2005, 19:756-767.
25. Kleihues P., Cavenee W.K. Tumours of the Central Nervous System 2007, IARC Press, Lyon. Fourth Edition.
26. Kortmann R.D., Timmermann B., Taylor R.E., Scarzello G., Plasswilm L., Paulsen F., Jeremic B., Gnekow A.K., Dieckmann K., Kay S., Bamberg M. Current and future strategies in radiotherapy of childhood low-grade glioma of the brain. Part I: Treatment modalities of radiation therapy. Strahlenther. Onkol. 2003, 179:509-520.
27. Li H., Collado M., Villasante A., Strati K., Ortega S., Canamero M., Blasco M.A., Serrano M. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 460:1136-1139.
28. Ligon K.L., Alberta J.A., Kho A.T., Weiss J., Kwaan M.R., Nutt C.L., Louis D.N., Stiles C.D., Rowitch D.H. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J. Neuropathol. Exp. Neurol. 2004, 63:499-509.
29. Ligon K.L., Kesari S., Kitada M., Sun T., Arnett H.A., Alberta J.A., Anderson D.J., Stiles C.D., Rowitch D.H. Development of NG2 neural progenitor cells requires Olig gene function. Proc. Natl. Acad. Sci. USA 2006, 103:7853-7858.
30. Ligon K.L., Huillard E., Mehta S., Kesari S., Liu H., Alberta J.A., Bachoo R.M., Kane M., Louis D.N., Depinho R.A., et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007, 53:503-517.
31. Lu Q.R., Yuk D., Alberta J.A., Zhu Z., Pawlitzky I., Chan J., McMahon A.P., Stiles C.D., Rowitch D.H. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000, 25:317-329.
32. Lu Q.R., Cai L., Rowitch D., Cepko C.L., Stiles C.D. Ectopic expression of Olig1 promotes oligodendrocyte formation and reduces neuronal survival in developing mouse cortex. Nat. Neurosci. 2001, 4:973-974.
33. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109:75-86.
34. Macdonald D.R., Gaspar L.E., Cairncross J.G. Successful chemotherapy for newly diagnosed aggressive oligodendroglioma. Ann. Neurol. 1990, 27:573-574.
35. Magnus T., Coksaygan T., Korn T., Xue H., Arumugam T.V., Mughal M.R., Eckley D.M., Tang S.C., Detolla L., Rao M.S., et al. Evidence that nucleocytoplasmic Olig2 translocation mediates brain-injury-induceddifferentiation of glial precursors to astrocytes. J. Neurosci. Res. 2007, 85:2126-2137.
36. Marie Y., Sanson M., Mokhtari K., Leuraud P., Kujas M., Delattre J.Y., Poirier J., Zalc B., Hoang-Xuan K. OLIG2 as a specific marker of oligodendroglial tumour cells. Lancet 2001, 358:298-300.
37. Marion R.M., Strati K., Li H., Murga M., Blanco R., Ortega S., Fernandez-Capetillo O., Serrano M., Blasco M.A. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009, 460:1149-1153.
38. Meletis K., Wirta V., Hede S.M., Nister M., Lundeberg J., Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 133:363-369.
39. Menn B., Garcia-Verdugo J.M., Yaschine C., Gonzalez-Perez O., Rowitch D., Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 2006, 26:7907-7918.
40. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 2001, 31:757-771.
41. Moffat J., Grueneberg D.A., Yang X., Kim S.Y., Kloepfer A.M., Hinkle G., Piqani B., Eisenhaure T.M., Luo B., Grenier J.K., et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 2006, 124:1283-1298.
42. Molofsky A.V., He S., Bydon M., Morrison S.J., Pardal R. 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. 2005, 19:1432-1437.
43. Nakamura M., Watanabe T., Klangby U., Asker C., Wiman K., Yonekawa Y., Kleihues P., Ohgaki H. p14ARF deletion and methylation in genetic pathways to glioblastomas. Brain Pathol. 2001, 11:159-168.
44. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 2001, 31:773-789.
45. Olson M.F., Paterson H.F., Marshall C.J. Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature 1998, 394:295-299.
46. Packer R.J., Ater J., Allen J., Phillips P., Geyer R., Nicholson H.S., Jakacki R., Kurczynski E., Needle M., Finlay J., et al. Carboplatin and vincristine chemotherapy for children with newly diagnosed progressive low-grade gliomas. J. Neurosurg. 1997, 86:747-754.
47. Pandita A., Aldape K.D., Zadeh G., Guha A., James C.D. Contrasting in vivo and in vitro fates of glioblastoma cell subpopulations with amplified EGFR. Genes Chromosomes Cancer 2004, 39:29-36.
48. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
49. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
50. Prados M.D., Edwards M.S., Rabbitt J., Lamborn K., Davis R.L., Levin V.A. Treatment of pediatric low-grade gliomas with a nitrosourea-based multiagent chemotherapy regimen. J. Neurooncol. 1997, 32:235-241.
51. Prives C., Hall P.A. The p53 pathway. J. Pathol. 1999, 187:112-126.
52. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456:593-598.
53. Reifenberger G., Liu L., Ichimura K., Schmidt E.E., Collins V.P. Amplification and overexpression of the MDM2 gene in a subset of human malignant gliomas without p53 mutations. Cancer Res. 1993, 53:2736-2739.
54. Reynolds B.A., 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.
55. Riley T., Sontag E., Chen P., Levine A. Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 2008, 9:402-412.
56. 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. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008, 14:123-134.
57. Shackleton M., Quintana E., Fearon E.R., Morrison S.J. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009, 138:822-829.
58. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13:1501-1512.
59. Stiles C.D., Rowitch D.H. Glioma stem cells: a midterm exam. Neuron 2008, 58:832-846.
60. Sun Y., Meijer D.H., Alberta J.A., Mehta S., Kane M.F., Tien A.-C., Fu H., Petryniak M., Potter G., Liu Z., et al. Phosphorylation state of Olig2 regulates proliferation of neural progenitors. Neuron 2011, in press.
61. Takebayashi H., Nabeshima Y., Yoshida S., Chisaka O., Ikenaka K. The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr. Biol. 2002, 12:1157-1163.
62. Tan B.T., Park C.Y., Ailles L.E., Weissman I.L. The cancer stem cell hypothesis: a work in progress. Lab. Invest. 2006, 86:1203-1207.
63. Utikal J., Polo J.M., Stadtfeld M., Maherali N., Kulalert W., Walsh R.M., Khalil A., Rheinwald J.G., Hochedlinger K. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009, 460:1145-1148.
64. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., Kong N., Kammlott U., Lukacs C., Klein C., et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004, 303:844-848.
65. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
66. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
67. Vousden K.H., Prives C. Blinded by the Light: The Growing Complexity of p53. Cell 2009, 137:413-431.
68. Wang Y., Yang J., Zheng H., Tomasek G.J., Zhang P., McKeever P.E., Lee E.Y., Zhu Y. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell 2009, 15:514-526.
69. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
70. Wynford-Thomas D. Cellular senescence and cancer. J. Pathol. 1999, 187:100-111.
71. Zhou Q., Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002, 109:61-73.
72. Zilfou J.T., Lowe S.W. Tumor suppressive functions of p53. Cold Spring Harb. Perspect. Biol 2009, 1:a001883.