LIN28 expression in malignant germ cell tumors downregulates let-7 and increases oncogene levels

Cancer Research

Volumn 73, Issue 15, 2013, Pages 4872-4884

  Murray, Matthew J ^a,b   Saini, Harpreet K ^d   Siegler, Charlotte A ^a   Hanning, Jennifer E ^a   Barker, Emily M ^a   Van Dongen, Stijn ^d   Ward, Dawn M ^a   Raby, Katie L ^a   Groves, Ian J ^a   Scarpini, Cinzia G ^a   Pett, Mark R ^a   Thornton, Claire M ^e   Enright, Anton J ^d   Nicholson, James C ^b   Coleman, Nicholas ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Department of Paediatric Oncology ^*  (United Kingdom)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^e ROYAL GROUP OF HOSPITALS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA LETHAL 7; PROTEIN LIN28; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADULT; AGE; ARTICLE; AURKB GENE; C12ORF5 GENE; CANCER CELL CULTURE; CCNF GENE; CELL PROLIFERATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONAL CARCINOMA; FEMALE; GENE EXPRESSION; GENE REPRESSION; GERM CELL; GERM CELL TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MKI67 GENE; MYCN GENE; NEGATIVE FEEDBACK; ONCOGENE; OVARY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RRM2 GENE; SOMATIC CELL; TESTIS; TUMOR CLASSIFICATION; TUMOR LOCALIZATION; TUMOR SUPPRESSOR GENE; UPREGULATION; YOLK SAC TUMOR;

ADULT; BLOTTING, WESTERN; CHILD; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICRORNAS; NEOPLASMS, GERM CELL AND EMBRYONAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; TRANSFECTION;

EID: 84881395046     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2085     Document Type: Article

References (50)

1. Murray MJ, Nicholson JC. Germ cell tumours in children and adolescents. paediatrics and child health 2010;20:109-16.
2. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol 2003;170:5-11.
3. Palmer RD, Murray MJ, Saini HK, van Dongen S, Abreu-Goodger C, Muralidhar B, et al. Malignant germ cell tumors display common microRNA profiles resulting in global changes in expression of messenger RNA targets. Cancer Res 2010;70:2911-23.
4. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003;115:787-98.
5. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are micro- RNA targets. Cell 2005;120:15-20.
6. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004;64:3753-6.
7. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 2007;67:7713-22.
8. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of micro- RNA processing by Lin28. Science 2008;320:97-100.
9. Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet 2009;41:843-8.
10. Hagan JP, Piskounova E, Gregory RI. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 2009;16:1021-5.
11. Viswanathan SR, Daley GQ. Lin28: A microRNA regulator with a macro role. Cell 2010;140:445-9.
12. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009;138:696-708.
13. Loughlin FE, Gebert LF, Towbin H, Brunschweiger A, Hall J, Allain FH. Structural basis of pre-let-7 miRNA recognition by the zinc knuckles of pluripotency factor Lin28. Nat Struct Mol Biol 2012;19:84-9.
14. Heo I, Joo C, Cho J, Ha M, Han J, Kim VN. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol Cell 2008;32:276-84.
15. Peng S, Maihle NJ, Huang Y. Pluripotency factors Lin28 and Oct4 identify a sub-population of stem cell-like cells in ovarian cancer. Oncogene 2010;29:2153-9.
16. West JA, Viswanathan SR, Yabuuchi A, Cunniff K, Takeuchi A, Park IH, et al. A role for Lin28 in primordial germ-cell development and germcell malignancy. Nature 2009;460:909-13.
17. Cao D, Allan RW, Cheng L, Peng Y, Guo CC, Dahiya N, et al. RNAbinding protein LIN28 is a marker for testicular germ cell tumors. Hum Pathol 2011;42:710-8.
18. Cao D, Liu A, Wang F, Allan RW, Mei K, Peng Y, et al. RNA-binding protein LIN28 is a marker for primary extragonadal germ cell tumors: an immunohistochemical study of 131 cases. Mod Pathol 2011;24: 288-96.
19. Xue D, Peng Y, WangF, Allan RW, Cao D. RNA-binding protein LIN28 is a sensitive marker of ovarian primitive germ cell tumours. Histopathology 2011;59:452-9.
20. Gillis AJ, Stoop H, Biermann K, van Gurp RJ, Swartzman E, Cribbes S, et al. Expression and interdependencies of pluripotency factors LIN28, OCT3/4, NANOG and SOX2 in human testicular germ cells and tumours of the testis. Int J Androl 2011;34:e160-74.
21. Mills SE. Sternbergs histology for pathologists. 3rd ed. New York: Lippincott, Williams and Wilkins; 2006.
22. Korkola JE, Houldsworth J, Chadalavada RS, Olshen AB, Dobrzynski D, Reuter VE, et al. Down-regulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res 2006;66:820-7.
23. Benjamini Y HY. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995;57: 289-300.
24. van Dongen S, Abreu-Goodger C, Enright AJ. Detecting microRNA binding and siRNA off-target effects from expression data. Nat Methods 2008;5:1023-5.
25. Primer 3.[cited 26th August 2012]; Available from: http://frodo.wi.mit. edu/primer3/
26. Herdman MT, Pett MR, Roberts I, Alazawi WO, Teschendorff AE, Zhang XY, et al. Interferon-beta treatment of cervical keratinocytes naturally infected with human papillomavirus 16 episomes promotes rapid reduction in episome numbers and emergence of latent integrants. Carcinogenesis 2006;27:2341-53.
27. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. GenomeBiol 2002;3:RESEARCH0034.
28. Murray MJ, Saini HK, van Dongen S, Palmer RD, Muralidhar B, Pett MR, et al. The two most common histological subtypes of malignant germ cell tumour are distinguished by global microRNA profiles, associated with differential transcription factor expression. Mol Cancer 2010;9:290.
29. Damjanov I, Andrews PW. Ultrastructural differentiation of a clonal human embryonal carcinoma cell line in vitro. Cancer Res 1983;43: 2190-8.
30. de Jong J, Stoop H, Gillis AJ, HersmusR, van Gurp RJ, van de Geijn GJ, et al. Further characterization of the first seminoma cell line TCam-2. Genes Chromosomes Cancer 2008;47:185-96.
31. Birmingham A, Anderson EM, Reynolds A, Ilsley-Tyree D, Leake D, Fedorov Y, et al. 30 UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006;3:199-204.
32. Muralidhar B, Winder D, Murray M, Palmer R, Barbosa-Morais N, Saini H, et al. Functional evidence that Drosha overexpression in cervical squamous cell carcinoma affects cell phenotype and microRNA profiles. J Pathol 2011;224:496-507.
33. Li Z, Wu F, Brant SR, Kwon JH. IL-23 receptor regulation by Let-7f in human CD4 +memory T cells. J Immunol 2011;186:6182-90.
34. Pett MR, Alazawi WO, Roberts I, Dowen S, Smith DI, Stanley MA, et al. Acquisition of high-level chromosomal instability is associated with integration of human papillomavirus type 16 in cervical keratinocytes. Cancer Res 2004;64:1359-68.
35. Boyerinas B, Park SM, Shomron N, Hedegaard MM, Vinther J, Andersen JS, et al. Identification of let-7-regulated oncofetal genes. Cancer Res 2008;68:2587-91.
36. Buechner J, Tomte E, Haug BH, Henriksen JR, Lokke C, Flaegstad T, 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 2011;105:296-303.
37. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008;455:58-63.
38. Chang TC, Zeitels LR,Hwang HW, Chivukula RR, Wentzel EA, Dews M, et al. Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation. Proc Natl Acad Sci U S A 2009;106: 3384-9.
39. Cotterman R, Knoepfler PS. N-Myc regulates expression of pluripotency genes in neuroblastoma including lif, klf2, klf4, and lin28b. PLoS ONE 2009;4:e5799.
40. Helland A, Anglesio MS, George J, Cowin PA, Johnstone CN, House CM, et al. Deregulation of MYCN, LIN28B and LET7 in a molecular subtype of aggressive high-grade serous ovarian cancers. PLoS ONE 2011;6:e18064.
41. Molenaar JJ, Domingo-Fernandez R, Ebus ME, Lindner S, Koster J, Drabek K, et al. LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat Genet 2012;44:1199- 206.
42. Alagaratnam S, Lind GE, Kraggerud SM, Lothe RA, Skotheim RI. The testicular germ cell tumour transcriptome. Int J Androl 2011;34:e133- 50; discussion e50-1.
43. Kraggerud SM, Skotheim RI, Szymanska J, Eknaes M, Fossa SD, Stenwig AE, et al. Genome profiles of familial/bilateral and sporadic testicular germ cell tumors. Genes Chromosomes Cancer 2002;34: 168-74.
44. Palmer RD, Foster NA, Vowler SL, Roberts I, Thornton CM, Hale JP, et al. Malignant germ cell tumours of childhood: new associations of genomic imbalance. Br J Cancer 2007;96:667-76.
45. Chen AX, Yu KD, Fan L, Li JY, Yang C, Huang AJ, et al. Germline genetic variants disturbing the Let-7/LIN28 double-negative feedback loop alter breast cancer susceptibility. PLoS Genet 2011;7: e1002259.
46. Yang X, Lin X, Zhong X, Kaur S, Li N, Liang S, et al. Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells. Cancer Res 2010;70:9463-72.
47. Zhong X, Li N, Liang S, Huang Q, Coukos G, Zhang L. Identification of microRNAs regulating reprogramming factor LIN28 in embryonic stem cells and cancer cells. J Biol Chem 2010;285:41961-71.
48. WuL, Belasco JG. Micro-RNAregulation of themammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol 2005;25:9198-208.
49. Li X, Zhang J, Gao L, McClellan S, Finan MA, Butler TW, et al. MiR-181 mediates cell differentiation by interrupting the Lin28 and let-7 feedback circuit. Cell Death Differ 2012;19:378-86.
50. Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A, et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009;459:1010-4.