Epigenetic regulation of survivin by Bmi1 is cell type specific during corticogenesis and in gliomas

Stem Cells

Volumn 31, Issue 1, 2013, Pages 190-202

  Acquati, Serena ^a   Greco, Azzura ^a   Licastro, Danilo ^b   Bhagat, Heeta ^a   Ceric, Dario ^a   Rossini, Zefferino ^a   Grieve, Joan ^c   Shaked Rabi, Maya ^d   Henriquez, Nick V ^d   Brandner, Sebastian ^d   Stupka, Elia ^a   Marino, Silvia ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b CBM Scrl   (Italy)

^c NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Bmi1; DNA damage; Glioma; Neural stem cells; Oxidative stress; Survivin

Indexed keywords

BMI1 PROTEIN; HISTONE H2AX; SURVIVIN; TRANSCRIPTOME;

APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; DNA DAMAGE; EPIGENETICS; GENE ACTIVATION; GLIOMA; HISTONE UBIQUITINATION; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN BINDING;

ANIMALS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBRAL CORTEX; CHROMATIN; DNA DAMAGE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GLIOMA; INHIBITOR OF APOPTOSIS PROTEINS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MICE; NEURAL STEM CELLS; NEUROGENESIS; OXIDATIVE STRESS; POLYCOMB REPRESSIVE COMPLEX 1; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; UBIQUITINATION;

MUS;

EID: 84871566623     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1274     Document Type: Article

References (51)

1. Morey L, Helin K. Polycomb group protein-mediated repression of transcription. Trends Biochem Sci 2010;35:323-332.
2. Jacobs JJ, Kieboom K, Marino S et al. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999;397:164-168. (Pubitemid 29050921)
3. Agger K, Cloos PA, Christensen J et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007;449:731-734. (Pubitemid 47552088)
4. Della Santa D, Schweighauser A, Forterre F et al. Imaging diagnosis-extrahepatic biliary tract obstruction secondary to a duodenal foreign body in a cat. Vet Radiol Ultrasound 2007;48:448-450. (Pubitemid 47319754)
5. Lee MG, Norman J, Shilatifard A et al. Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell 2007;128:877-887. (Pubitemid 46341414)
6. Pereira JD, Sansom SN, Smith J et al. Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci USA 2010;107: 15957-15962.
7. Hirabayashi Y, Suzki N, Tsuboi M et al. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 2009;63:600-613.
8. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-260. (Pubitemid 40852690)
9. Voncken JW, Schweizer D, Aagaard L et al. Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status. J Cell Sci 1999;112(Pt 24): 4627-4639. (Pubitemid 30034811)
10. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell 2004;118:409-418. (Pubitemid 39485661)
11. Qiang L, Yang Y, Ma YJ et al. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett 2009;279:13-21.
12. Hemmati HD, Nakano I, Lazareff JA et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003;100: 15178-15183. (Pubitemid 37518036)
13. Abdouh M, Facchino S, Chatoo W et al. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 2009;29: 8884-8896.
14. 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. (Pubitemid 47539307)
15. 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.
16. Zhen HN, Zhang X, Hu PZ et al. Survivin expression and its relation with proliferation, apoptosis, and angiogenesis in brain gliomas. Cancer 2005;104:2775-2783. (Pubitemid 41798288)
17. Reichert S, Rodel C, Mirsch J et al. Survivin inhibition and DNA double-strand break repair: A molecular mechanism to overcome radioresistance in glioblastoma. Radiother Oncol 2011;101:51-58.
18. Rietze RL, Reynolds BA. Neural stem cell isolation and characterization. Methods Enzymol 2006;419:3-23. (Pubitemid 44820360)
19. Conti L, Pollard SM, Gorba T et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005;3:e283.
20. Yang MH, Hsu DS, Wang HW et al. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol 2010;12:982-992.
21. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev 2006;6:846-856. (Pubitemid 44629896)
22. De Santa F, Narang V, Yap ZH et al. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J 2009;28: 3341-3352.
23. Won MH, Kang TC, Jeon GS et al. Immunohistochemical detection of oxidative DNA damage induced by ischemia-reperfusion insults in gerbil hippocampus in vivo. Brain Res 1999;836:70-78. (Pubitemid 29354472)
24. Gorgoulis VG, Vassiliou LV, Karakaidos P et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005;434:907-913. (Pubitemid 40559004)
25. Lee GM, Fong SS, Oh DJ et al. Characterization and efficacy of PKH26 as a probe to study the replication history of the human hematopoietic KG1a progenitor cell line. In Vitro Cell Dev Biol Anim 2002;38:90-96. (Pubitemid 34538201)
26. Pece S, Tosoni D, Confalonieri S et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140:62-73.
27. Seyed Jafari SS, Ali Aghaei A, Asadi-Shekaari M et al. Investigating the effects of adult neural stem cell transplantation by lumbar puncture in transient cerebral ischemia. Neurosci Lett 2011;495:1-5.
28. Altieri DC. Survivin and IAP proteins in cell-death mechanisms. Biochem J 2010;430:199-205.
29. Maxia C, Perra MT, Demurtas P et al. Expression of survivin protein in pterygium and relationship with oxidative DNA damage. J Cell Mol Med 2008;12:2372-2380.
30. Yamamoto H, Ngan CY, Monden M. Cancer cells survive with survivin. Cancer Sci 2008;99:1709-1714.
31. Stewart GS, Wang B, Bignell CR et al. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003;421:961-966. (Pubitemid 36288029)
32. Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009;458:461-467.
33. Ismail IH, Andrin C, McDonald D et al. BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 2010;191:45-60.
34. Pan MR, Peng G, Hung WC et al. Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 2011; 286:28599-28607.
35. Alcantara Llaguno S, Chen J, Kwon CH et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009;15:45-56.
36. Jacques TS, Swales A, Brzozowski MJ et al. Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J 2010;29:222-235.
37. Zheng H, Ying H, Yan H et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455:1129-1133.
38. Venere M, Fine HA, Dirks PB et al. Cancer stem cells in gliomas: Identifying and understanding the apex cell in cancer's hierarchy. Glia 2011;59:1148-1154.
39. Parsons DW, Jones S, Zhang X et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-1812.
40. Bracken AP, Dietrich N, Pasini D et al. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 2006;20:1123-1136.
41. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 2006;5:1087-1098. (Pubitemid 43881300)
42. Jiang Y, Su B, Meng X et al. Effect of siRNA-mediated silencing of Bmi-1 gene expression on HeLa cells. Cancer Sci 2010;101:379-386.
43. Sauvageau M, Sauvageau G. Polycomb group proteins: Multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 2010;7: 299-313.
44. Meng S, Luo M, Sun H et al. Identification and characterization of Bmi-1-responding element within the human p16 promoter. J Biol Chem 2010;285:33219-33229.
45. Barradas M, Anderton E, Acosta JC et al. Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 2009;23:1177-1182.
46. Bellot G, Garcia-Medina R, Gounon P et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 2009;29: 2570-2581.
47. Lee SJ, Park MH, Kim HJ et al. Metallothionein-3 regulates lysosomal function in cultured astrocytes under both normal and oxidative conditions. Glia 2010;58:1186-1196.
48. Massart C, Hoste C, Virion A et al. Cell biology of H2O2 generation in the thyroid: Investigation of the control of dual oxidases (DUOX) activity in intact ex vivo thyroid tissue and cell lines. Mol Cell Endocrinol 2011;343:32-44.
49. Chatoo W, Abdouh M, David J et al. The polycomb group gene Bmi1 regulates antioxidant defenses in neurons by repressing p53 pro-oxidant activity. J Neurosci 2009;29:529-542.
50. Baratchi S, Kanwar RK, Kanwar JR. Survivin mutant protects differentiated dopaminergic SK-N-SH cells against oxidative stress. PLoS One 2011;6:e15865.
51. Capalbo G, Dittmann K, Weiss C et al. Radiation-induced survivin nuclear accumulation is linked to DNA damage repair. Int J Radiat Oncol Biol Phys 2010;77:226-234.