LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression

Nature Genetics

Volumn 44, Issue 11, 2012, Pages 1199-1206

  Molenaar, Jan J ^a   Domingo Fernández, Raquel ^b,c   Ebus, Marli E ^a   Lindner, Sven ^d   Koster, Jan ^a   Drabek, Ksenija ^a   Mestdagh, Pieter ^e   Van Sluis, Peter ^a   Valentijn, Linda J ^a   Van Nes, Johan ^a   Broekmans, Marloes ^a   Haneveld, Franciska ^a   Volckmann, Richard ^a   Bray, Isabella ^b,c   Heukamp, Lukas ^f   Sprüssel, Annika ^d   Thor, Theresa ^d   Kieckbusch, Kristina ^d   Klein Hitpass, Ludger ^d   Fischer, Matthias ^g   Vandesompele, Jo ^e   Schramm, Alexander ^d   Van Noesel, Max M ^h   Varesio, Luigi ⁱ   Speleman, Frank ^e   Eggert, Angelika ^d   Stallings, Raymond L ^b,c   Caron, Huib N ^a   Versteeg, Rogier ^a   Schulte, Johannes H ^d   more..

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^c Children s Health Ireland   (Ireland)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

^e GHENT UNIVERSITY HOSPITAL   (Belgium)

^f UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^g UNIVERSITY OF COLOGNE   (Germany)

^h SOPHIA CHILDREN S HOSPITAL   (Netherlands)

ⁱ G GASLINI INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LET 7 PROTEIN; LIN28B PROTEIN; MESSENGER RNA; MICRORNA; MYCN PROTEIN; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ABDOMINAL TUMOR; ADRENAL TUMOR; ADVERSE OUTCOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELIAC GANGLION; CELL FRACTIONATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; INTERNAL RIBOSOME ENTRY SITE; MOUSE; NERVE CELL DIFFERENTIATION; NEUROBLAST; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERIOR CERVICAL GANGLION; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; MICE; MICE, TRANSGENIC; MICRORNAS; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84868210731     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2436     Document Type: Article

References (68)

1. Moss, E.G., Lee, R.C. & Ambros, V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88, 637-646 (1997).
2. West, J.A. et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460, 909-913 (2009).
3. Polesskaya, A. et al. Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev. 21, 1125-1138 (2007).
4. Balzer, E., Heine, C., Jiang, Q., Lee, V.M. & Moss, E.G. LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 137, 891-900 (2010).
5. Zhu, H. et al. The Lin28/let-7 axis regulates glucose metabolism. Cell 147, 81-94 (2011).
6. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
7. Viswanathan, S.R. et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet. 41, 843-848 (2009).
8. Guo, Y. et al. Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene 384, 51-61 (2006).
9. Wang, Y.C. et al. Lin-28B expression promotes transformation and invasion in human hepatocellular carcinoma. Carcinogenesis 31, 1516-1522 (2010).
10. Permuth-Wey, J. et al. LIN28B polymorphisms influence susceptibility to epithelial ovarian cancer. Cancer Res. 71, 3896-3903 (2011).
11. King, C.E. et al. LIN28B promotes colon cancer progression and metastasis. Cancer Res. 71, 4260-4268 (2011).
12. Ong, K.K. et al. Genetic variation in LIN28B is associated with the timing of puberty. Nat. Genet. 41, 729-733 (2009).
13. Sulem, P. et al. Genome-wide association study identifies sequence variants on 6q21 associated with age at menarche. Nat. Genet. 41, 734-738 (2009).
14. Viswanathan, S.R., Daley, G.Q. & Gregory, R.I. Selective blockade of microRNA processing by Lin28. Science 320, 97-100 (2008).
15. Lee, Y., Jeon, K., Lee, J.T., Kim, S. & Kim, V.N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663-4670 (2002).
16. Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (2003).
17. Newman, M.A., Thomson, J.M. & Hammond, S.M. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14, 1539-1549 (2008).
18. Piskounova, E. et al. Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J. Biol. Chem. 283, 21310-21314 (2008).
19. Heo, I. et al. Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol. Cell 32, 276-284 (2008).
20. Piskounova, E. et al. Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms. Cell 147, 1066-1079 (2011).
21. Roush, S. & Slack, F.J. The let-7 family of microRNAs. Trends Cell Biol. 18, 505-516 (2008).
22. Lee, Y.S. & Dutta, A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21, 1025-1030 (2007).
23. Kumar, M.S., Lu, J., Mercer, K.L., Golub, T.R. & Jacks, T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673-677 (2007).
24. Johnson, C.D. et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 67, 7713-7722 (2007).
25. Boyerinas, B., Park, S.M., Hau, A., Murmann, A.E. & Peter, M.E. The role of let-7 in cell differentiation and cancer. Endocr. Relat. Cancer 17, F19-F36 (2010).
26. Takamizawa, J. et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 64, 3753-3756 (2004).
27. Shell, S. et al. Let-7 expression defines two differentiation stages of cancer. Proc. Natl. Acad. Sci. USA 104, 11400-11405 (2007).
28. Øra, I. & Eggert, A. Progress in treatment and risk stratification of neuroblastoma: impact on future clinical and basic research. Semin. Cancer Biol. 21, 217-228 (2011).
29. Maris, J.M., Hogarty, M.D., Bagatell, R. & Cohn, S.L. Neuroblastoma. Lancet 369, 2106-2120 (2007).
30. Westermann, F. et al. Distinct transcriptional MYCN/c-MYC activities are associated with spontaneous regression or malignant progression in neuroblastomas. Genome Biol. 9, R150 (2008).
31. Bray, I. et al. Widespread dysregulation of miRNAs by MYCN amplification and chromosomal imbalances in neuroblastoma: association of miRNA expression with survival. PLoS ONE 4, e7850 (2009).
32. De Preter, K. et al. miRNA expression profiling enables risk stratification in archived and fresh neuroblastoma tumor samples. Clin. Cancer Res. 17, 7684-7692 (2011).
33. Shohet, J.M. et al. A genome-wide search for promoters that respond to increased MYCN reveals both new oncogenic and tumor suppressor microRNAs associated with aggressive neuroblastoma. Cancer Res. 71, 3841-3851 (2011).
34. Schulte, J.H. et al. MYCN regulates oncogenic microRNAs in neuroblastoma. Int. J. Cancer 122, 699-704 (2008).
35. Ma, L. et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 12, 247-256 (2010).
36. Lovén, J. et al. MYCN-regulated microRNAs repress estrogen receptor-α (ESR1) expression and neuronal differentiation in human neuroblastoma. Proc. Natl. Acad. Sci. USA 107, 1553-1558 (2010).
37. Tivnan, A. et al. MicroRNA-34a is a potent tumor suppressor molecule in vivo in neuroblastoma. BMC Cancer 11, 33 (2011).
38. Le, M.T. et al. MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol. Cell. Biol. 29, 5290-5305 (2009).
39. Cole, K.A. et al. A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol. Cancer Res. 6, 735-742 (2008).
40. Welch, C., Chen, Y. & Stallings, R.L. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26, 5017-5022 (2007).
41. Buechner, J. et al. Tumour-suppressor microRNAs let-7 and mir-101 target the proto-oncogene MYCN and inhibit cell proliferation in MYCN-amplified neuroblastoma. Br. J. Cancer 105, 296-303 (2011).
42. Molenaar, J.J. et al. Copy number defects of G1-cell cycle genes in neuroblastoma are frequent and correlate with high expression of E2F target genes and a poor prognosis. Genes Chromosom. Cancer 51, 10-19 (2012).
43. Huntzinger, E. & Izaurralde, E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110 (2011).
44. Schulte, J.H. et al. MYCN and ALKF1174L are sufficient to drive neuroblastoma development from neural crest progenitor cells. Oncogene published online, doi:10.1038/onc.2012.106 (9 April 2012).
45. Stanke, M. et al. Target-dependent specification of the neurotransmitter phenotype: cholinergic differentiation of sympathetic neurons is mediated in vivo by gp 130 signaling. Development 133, 141-150 (2006).
46. Weiss, W.A., Aldape, K., Mohapatra, G., Feuerstein, B.G. & Bishop, J.M. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J. 16, 2985-2995 (1997).
47. Mertz, J.A. et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc. Natl. Acad. Sci. USA 108, 16669-16674 (2011).
48. Liang, L. et al. MicroRNA-125b suppressesed human liver cancer cell proliferation and metastasis by directly targeting oncogene LIN28B2. Hepatology 52, 1731-1740 (2010).
49. Wang, J. et al. MicroRNA-125b/Lin28 pathway contributes to the mesendodermal fate decision of embryonic stem cells. Stem Cells Dev. 21, 1524-1537 (2012).
50. Rybak, A. et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 10, 987-993 (2008).
51. Helland, Å. et al. Deregulation of MYCN, LIN28B and LET7 in a molecular subtype of aggressive high-grade serous ovarian cancers. PLoS ONE 6, e18064 (2011).
52. Cotterman, R. & Knoepfler, P.S. N-Myc regulates expression of pluripotency genes in neuroblastoma including lif, klf2, klf4, and lin28b. PLoS ONE 4, e5799 (2009).
53. Molenaar, J.J. et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 483, 589-593 (2012).
54. Valentijn, L.J. et al. Inhibition of a new differentiation pathway in neuroblastoma by copy number defects of N-myc, Cdc42, and nm23 genes. Cancer Res. 65, 3136-3145 (2005).
55. Eda, A., Tamura, Y., Yoshida, M. & Hohjoh, H. Systematic gene regulation involving miRNAs during neuronal differentiation of mouse P19 embryonic carcinoma cell. Biochem. Biophys. Res. Commun. 388, 648-653 (2009).
56. Olsson-Carter, K. & Slack, F.J. A developmental timing switch promotes axon outgrowth independent of known guidance receptors. PLoS Genet. 6 pii: e1001054 (2010).
57. Caron, H. et al. Allelic loss of chromosome 1p36 in neuroblastoma is of preferential maternal origin and correlates with N-myc amplification. Nat. Genet. 4, 187-190 (1993).
58. Molenaar, J.J., van Sluis, P., Boon, K., Versteeg, R. & Caron, H.N. Rearrangements and increased expression of cyclin D1 (CCND1) in neuroblastoma. Genes Chromosom. Cancer 36, 242-249 (2003).
59. Fieuw, A. et al. Identification of a novel recurrent 1q42.2-1qter deletion in high risk MYCN single copy 11q deleted neuroblastomas. Int. J. Cancer 130, 2599-2606 (2012).
60. Molenaar, J.J. et al. Cyclin D1 and CDK4 activity contribute to the undifferentiated phenotype in neuroblastoma. Cancer Res. 68, 2599-2609 (2008).
61. Cheng, A.J. et al. Cell lines from MYCN transgenic murine tumours reflect the molecular and biological characteristics of human neuroblastoma. Eur. J. Cancer 43, 1467-1475 (2007).
62. Molenaar, J.J. et al. Cyclin D1 is a direct transcriptional target of GATA3 in neuroblastoma tumor cells. Oncogene 29, 2739-2745 (2010).
63. Molenaar, J.J. et al. Inactivation of CDK2 is synthetically lethal to MYCN over-expressing cancer cells. Proc. Natl. Acad. Sci. USA 106, 12968-12973 (2009).
64. Schulte, J.H. et al. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res. 69, 2065-2071 (2009).
65. Mestdagh, P. et al. High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA. Nucleic Acids Res. 36, e143 (2008).
66. Mestdagh, P. et al. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 10, R64 (2009).
67. Heukamp, L.C. et al. Targeted expression of mutated ALK induces neuroblastoma in transgenic mice. Sci. Transl. Med. 4, 141ra91 (2012).
68. Bill, A. et al. Cytohesins are cytoplasmic ErbB receptor activators. Cell 143, 201-211 (2010).