Cyclin E1 is a common target of BMI1 and MYCN and a prognostic marker for neuroblastoma progression

Oncogene

Volumn 31, Issue 33, 2012, Pages 3785-3795

  Mao, L ^a,b   Ding, J ^a   Perdue, A ^a   Yang, L ^a   Zha, Y ^a,c   Ren, M ^a   Huang, S ^a   Cui, H ^d   Ding, H F ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c CHINA THREE GORGES UNIVERSITY   (China)

^d SOUTHWEST UNIVERSITY   (China)

Author keywords

BMI1; cyclin E1; FBXW7; MYCN; neuroblastoma

Indexed keywords

BMI1 PROTEIN; CYCLIN E; CYCLIN E1; MESSENGER RNA; MYC PROTEIN; TUMOR MARKER; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CANCER PROGNOSIS; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME SUBSTRATE; GENE LOCUS; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NEUROBLASTOMA; NEUROBLASTOMA CELL; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; TUMOR GROWTH;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CYCLIN E; DISEASE PROGRESSION; F-BOX PROTEINS; HUMANS; NEOPLASM PROTEINS; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PROGNOSIS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P14ARF; UBIQUITIN-PROTEIN LIGASES;

EID: 84865270072     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.536     Document Type: Article

References (51)

1. Asgharzadeh S, Pique-Regi R, Sposto R, Wang H, Yang Y, Shimada H et al. (2006). Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J Natl Cancer Inst 98: 1193-1203. (Pubitemid 44390990)
2. Brodeur GM. (2003). Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3: 203-216. (Pubitemid 37328872)
3. Bruggeman SW, Valk-Lingbeek ME, van der Stoop PP, Jacobs JJ, Kieboom K, Tanger E et al. (2005). Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev 19: 1438-1443. (Pubitemid 41003010)
4. Chang H-H, Lee H, Hu M-K, Tsao P-N, Juan H-F, Huang M-C et al. (2010). Notch1 expression predicts an unfavorable prognosis and serves as a therapeutic target of patients with neuroblastoma. Clin Cancer Res 16: 4411-4420.
5. Chen QR, Song YK, Wei JS, Bilke S, Asgharzadeh S, Seeger RC et al. (2008). An integrated cross-platform prognosis study on neuroblastoma patients. Genomics 92: 195-203.
6. Crusio KM, King B, Reavie LB, Aifantis I. (2010). The ubiquitous nature of cancer: the role of the SCF(Fbw7) complex in development and transformation. Oncogene 29: 4865-4873.
7. Cui H, Li T, Ding HF. (2005). Linking of N-Myc to death receptor machinery in neuroblastoma cells. J Biol Chem 280: 9474-9481. (Pubitemid 40409642)
8. Cui H, Hu B, Li T, Ma J, Alam G, Gunning WT et al. (2007). Bmi-1 is essential for the tumorigenicity of neuroblastoma cells. Am J Pathol 170: 1370-1378. (Pubitemid 47339343)
9. Cui H, Ma J, Ding J, Li T, Alam G, Ding HF. (2006). Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J Biol Chem 281: 34696-34704. (Pubitemid 46036675)
10. Ferrari-Toninelli G, Bonini SA, Uberti D, Buizza L, Bettinsoli P, Poliani PL et al. (2010). Targeting Notch pathway induces growth inhibition and differentiation of neuroblastoma cells. Neuro-Oncol 12: 1231-1243.
11. Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM. (1991). Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E mu-myc transgenic mice. Cell 65: 753-763. (Pubitemid 121001307)
12. Hwang HC, Clurman BE. (2005). Cyclin E in normal and neoplastic cell cycles. Oncogene 24: 2776-2786. (Pubitemid 40638089)
13. Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, Tsukui H et al. (2004). Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21: 843-851. (Pubitemid 39626674)
14. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. (1999a). The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168. (Pubitemid 29050921)
15. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. (1999b). Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ ARF. Genes Dev 13: 2678-2690. (Pubitemid 29508555)
16. Jansen-Durr P, Meichle A, Steiner P, Pagano M, Finke K, Botz J et al. (1993). Differential modulation of cyclin gene expression by MYC. Proc Natl Acad Sci USA 90: 3685-3689. (Pubitemid 23111432)
17. Kaghad M, Bonnet H, Yang A, Creancier L, Biscan JC, Valent A et al. (1997). Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90: 809-819. (Pubitemid 27357971)
18. Lessard J, Sauvageau G. (2003). Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260. (Pubitemid 40852690)
19. Lowe SW, Sherr CJ. (2003). Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev 13: 77-83. (Pubitemid 36143931)
20. Ma CX, Janetka JW, Piwnica-Worms H. (2011). Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol Med 17: 88-96.
21. Mao L, Ding J, Zha Y, Yang L, McCarthy BA, King W et al. (2011). HOXC9 links cell-cycle exit and neuronal differentiation and is a prognostic marker in neuroblastoma. Cancer Res 71: 4314-4324.
22. Maris JM, Matthay KK. (1999). Molecular biology of neuroblastoma. J Clin Oncol 17: 2264-2279. (Pubitemid 29318861)
23. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM et al. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556.
24. Minella AC, Swanger J, Bryant E, Welcker M, Hwang H, Clurman BE. (2002). p53 and p21 form an inducible barrier that protects cells against cyclin E-cdk2 deregulation. Curr Biol 12: 1817-1827. (Pubitemid 35273901)
25. Molofsky AV, He S, Bydon M, Morrison SJ, 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. (Pubitemid 41003009)
26. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. (2003). Bmi-1 dependence distinguishes neural stem cell selfrenewal from progenitor proliferation. Nature 425: 962-967. (Pubitemid 37376927)
27. Nakayama KI, Nakayama K. (2006). Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 6: 369-381.
28. Nowak K, Kerl K, Fehr D, Kramps C, Gessner C, Killmer K et al. (2006). BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucleic Acids Res 34: 1745-1754.
29. Oberthuer A, Berthold F, Warnat P, Hero B, Kahlert Y, Spitz R et al. (2006). Customized oligonucleotide microarray gene expressionbased classification of neuroblastoma patients outperforms current clinical risk stratification. J Clin Oncol 24: 5070-5078. (Pubitemid 46631411)
30. Ochiai H, Takenobu H, Nakagawa A, Yamaguchi Y, Kimura M, Ohira M et al. (2010). Bmi1 is a MYCN target gene that regulates tumorigenesis through repression of KIF1Bbeta and TSLC1 in neuroblastoma. Oncogene 29: 2681-2690.
31. Onoyama I, Nakayama KI. (2008). Fbxw7 in cell cycle exit and stem cell maintenance: insight from gene-targeted mice. Cell Cycle (Georgetown, Tex) 7: 3307-3313.
32. Otto T, Horn S, Brockmann M, Eilers U, Schuttrumpf L, Popov N et al. (2009). Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell 15: 67-78.
33. Park IK, Morrison SJ, Clarke MF. (2004). Bmi1, stem cells, and senescence regulation. J Clin Invest 113: 175-179. (Pubitemid 38544200)
34. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL et al. (2003). Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305. (Pubitemid 40852701)
35. Perez-Roger I, Solomon DL, Sewing A, Land H. (1997). Myc activation of cyclin E/Cdk2 kinase involves induction of cyclin E gene transcription and inhibition of p27(Kip1) binding to newly formed complexes. Oncogene 14: 2373-2381. (Pubitemid 27268156)
36. Riccardi C, Nicoletti I. (2006). Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 1: 1458-1461.
37. Satyanarayana A, Kaldis P. (2009). Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28: 2925-2939.
38. Sauvageau M, Sauvageau G. (2010). Polycomb group proteins: multifaceted regulators of somatic stem cells and cancer. Cell Stem Cell 7: 299-313.
39. Schwab M. (2004). MYCN in neuronal tumours. Cancer Lett 204: 179-187. (Pubitemid 38167721)
40. Schwartz YB, Pirrotta V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22. (Pubitemid 46006046)
41. Silva JM, Marran K, Parker JS, Silva J, Golding M, Schlabach MR et al. (2008). Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319: 617-620. (Pubitemid 351197063)
42. Spruck CH, Won K-A, Reed SI. (1999). Deregulated cyclin E induces chromosome instability. Nature 401: 297-300.
43. Steiner P, Philipp A, Lukas J, Godden-Kent D, Pagano M, Mittnacht S et al. (1995). Identification of a Myc-dependent step during the formation of active G1 cyclin-cdk complexes. EMBO J 14: 4814-4826.
44. Thompson SL, Bakhoum SF, Compton DA. (2010). Mechanisms of chromosomal instability. Curr Biol 20: R285-R295.
45. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M. (2004). Stem cells and cancer; the polycomb connection. Cell 118: 409-418. (Pubitemid 39485661)
46. van der Lugt NM, Domen J, Linders K, van Roon M, Robanus-Maandag E, te Riele H 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.
47. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. (1991). Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65: 737-752. (Pubitemid 121001306)
48. Wei JS, Greer BT, Westermann F, Steinberg SM, Son CG, Chen QR et al. (2004). Prediction of clinical outcome using gene expression profiling and artificial neural networks for patients with neuroblastoma. Cancer Res 64: 6883-6891. (Pubitemid 39330995)
49. Wei W, Hemmer RM, Sedivy JM. (2001). Role of p14(ARF) in replicative and induced senescence of human fibroblasts. Mol Cell Biol 21: 6748-6757. (Pubitemid 32911237)
50. Welcker M, Clurman BE. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93. (Pubitemid 351161321)
51. Yamashita M, Kuwahara M, Suzuki A, Hirahara K, Shinnaksu R, Hosokawa H et al. (2008). Bmi1 regulates memory CD4T cell survival via repression of the Noxa gene. J ExpMed 205: 1109-1120. (Pubitemid 351679686)