Inhibition of miR-9 de-represses HuR and DICER1 and impairs Hodgkin lymphoma tumour outgrowth in vivo

Oncogene

Volumn 31, Issue 49, 2012, Pages 5081-5089

  Leucci, E ^a   Zriwil, A ^a   Gregersen, L H ^a,e   Jensen, K T ^a   Obad, S ^b   Bellan, C ^c   Leoncini, L ^c   Kauppinen, S ^b,d   Lund, A H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Santaris Pharma AS   (Denmark)

^c UNIVERSITY OF SIENA   (Italy)

^d AALBORG UNIVERSITY   (Denmark)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

cytokines; DICER1; Hodgkin lymphoma; HuR; miR 9

Indexed keywords

ANTIMICRORNA 9; ANTINEOPLASTIC AGENT; DICER1 PROTEIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HUR PROTEIN; INTERLEUKIN 6; MESSENGER RNA; MICRORNA 9; RANTES; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; B LYMPHOCYTE ACTIVATION; BINDING SITE; CANCER GROWTH; CANCER INHIBITION; CANCER MODEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REPRESSION; GENE TARGETING; HODGKIN DISEASE; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPHOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN SYNTHESIS INHIBITION;

3' UNTRANSLATED REGIONS; ANIMALS; B-LYMPHOCYTES; BINDING SITES; CELL LINE, TUMOR; CYTOKINES; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HODGKIN DISEASE; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MICE; MICRORNAS; RIBONUCLEASE III; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84870823182     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.15     Document Type: Article

References (45)

1. Schetter AJ, Nguyen GH, Bowman ED, Mathe EA, Yuen ST, Hawkes JE et al.Association of inflammation-related and microRNA gene expression with cancerspecificmortality of colon adenocarcinoma. Clin Cancer Res 2009; 15: 5878-5887.
2. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell MolLife Sci [Review] 2010; 140: 883-899.
3. Kuppers R. The biology of Hodgkin's lymphoma. Nat Rev Cancer 2009; 9: 15-27.
4. Brauninger A, Schmitz R, Bechtel D, Renne C, Hansmann ML, Kuppers R. Molecularbiology of Hodgkin's and Reed/Sternberg cells in Hodgkin's lymphoma. Int JCancer 2006; 118: 1853-1861.
5. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis,function and decay. Nat Rev Genet 2010; 11: 597-610.
6. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat RevCancer 2006; 6: 259-269.
7. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D et al. miR-9, a MYC/MYCNactivatedmicroRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol2010; 12: 247-256.
8. Bazzoni F, Rossato M, Fabbri M, Gaudiosi D, Mirolo M, Mori L et al. Induction andregulatory function of miR-9 in human monocytes and neutrophils exposed toproinflammatory signals. Proc Natl Acad Sci USA 2009; 106: 5282-5287.
9. Lawrie CH, Saunders NJ, Soneji S, Palazzo S, Dunlop HM, Cooper CD et al.MicroRNA expression in lymphocyte development and malignancy. Leukemia2008; 22: 1440-1446.
10. Van Vlierberghe P, De Weer A, Mestdagh P, Feys T, De Preter K, De Paepe P et al.Comparison of miRNA profiles of microdissected Hodgkin/Reed-Sternberg cellsand Hodgkin cell lines versus CD77+ B-cells reveals a distinct subset ofdifferentially expressed miRNAs. Br J Haematol 2009; 147: 686-690.
11. Navarro A, Gaya A, Martinez A, Urbano-Ispizua A, Pons A, Balague O et al.MicroRNA expression profiling in classic Hodgkin lymphoma. Blood 2008; 111:2825-2832.
12. Nie K, Gomez M, Landgraf P, Garcia JF, Liu Y, Tan LH et al. MicroRNA-mediateddown-regulation of PRDM1/Blimp-1 in Hodgkin/Reed-Sternberg cells: a potentialpathogenetic lesion in Hodgkin lymphomas. Am J Pathol 2008; 173: 242-252.
13. Lambertz I, Nittner D, Mestdagh P, Denecker G, Vandesompele J, Dyer MA et al.Monoallelic but not biallelic loss of Dicer1 promotes tumorigenesis in vivo Dicer1is a haploinsufficient tumor suppressor. Cell Death Differ 2010; 17: 8.
14. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J et al. Dicer1 functions as ahaploinsufficient tumor suppressor. Genes Dev 2009; 23: 4.
15. Khabar KS. Post-transcriptional control during chronic inflammation and cancer: afocus on AU-rich elements. Cell Mol Life Sci 2010; 67: 2937-2955.
16. Anderson P. Post-transcriptional control of cytokine production. Nat Immunol2008; 9: 353-359.
17. Obad S, dos Santos CO, Petri A, Heidenblad M, Broom O, Ruse C et al. Silencing ofmicroRNA families by seed-targeting tiny LNAs. Nat Genet 2011; 43: 371-378.
18. Lopez-Rodriguez C, Aramburu J, Jin L, Rakeman AS, Michino M, Rao A. Bridgingthe NFAT and NF-kappaB families: NFAT5 dimerization regulates cytokine genetranscription in response to osmotic stress. Immunity 2001; 15: 47-58.
19. Medzhitov R, Horng T. Transcriptional control of the inflammatory response. NatRev Immunol 2009; 9: 692-703.
20. Ørom UA NF, Lund AH. MicroRNA-10a binds the 50UTR of ribosomal proteinmRNAs and enhances their translation. Mol Cell 2008; 30: 11.
21. Christoffersen NR, Shalgi R, Frankel LB, Leucci E, Lees M, Klausen M et al. p53-independent upregulation of miR-34a during oncogene-induced senescencerepresses MYC. Cell Death Differ 2010; 17: 236-245.
22. Wynendaele J, Bohnke A, Leucci E, Nielsen SJ, Lambertz I, Hammer S et al. Anillegitimate microRNA target site within the 30 UTR of MDM4 affects ovariancancer progression and chemosensitivity. Cancer Res 2010; 70: 9641-9649.
23. Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M. Identification of a target RNAmotif for RNA-binding protein HuR. Proc Natl Acad Sci USA 2004; 101: 2987-2992.
24. Marstrand TT, Frellsen J, Moltke I, Thiim M, Valen E, Retelska D et al. Asap: aframework for over-representation statistics for transcription factor binding sites.PLoS One 2008; 3: e1623.
25. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M et al.Integrative regulatory mapping indicates that the RNA-binding protein HuRcouples pre-mRNA processing and mRNA stability. Mol Cell 2011; 43: 327-339.
26. Lebedeva S, Jens M, Theil K, Schwanhausser B, Selbach M, Landthaler M et al.Transcriptome-wide analysis of regulatory interactions of the RNA-bindingprotein HuR. Mol Cell 2011; 43: 340-352.
27. Dewan MZ WM, Ahmed S, Terashima K, Horiuchi S, Sata T, Honda M et al.Hodgkin's lymphoma cells are efficiently engrafted and tumor marker CD30 isexpressed with constitutive nuclear factor-kappaB activity in unconditioned NOD/SCID/gammac(null) mice. Cancer Sci 2005; 96: 7.
28. Ventura A, Jacks T. MicroRNAs and cancer: short RNAs go a long way. Cell 2009;136: 586-591.
29. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. MicroRNAexpression profiles classify human cancers. Nature 2005; 435: 834-838.
30. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processingenhances cellular transformation and tumorigenesis. Nat Genet 2007; 39: 673-677.
31. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S et al. AMicroRNA targeting dicer for metastasis control. Cell 2010; 141: 1195-1207.
32. Dean JL, Sully G, Clark AR, Saklatvala J. The involvement of AU-rich elementbindingproteins in p38 mitogen-activated protein kinase pathway-mediatedmRNA stabilisation. Cell Signal 2004; 16: 1113-1121.
33. Lu JY, Schneider RJ. Tissue distribution of AU-rich mRNA-binding proteinsinvolved in regulation of mRNA decay. J Biol Chem 2004; 279: 12974-12979.
34. Kawai T, Lal A, Yang X, Galban S, Mazan-Mamczarz K, Gorospe M. Translationalcontrol of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol Cell Biol2006; 26: 3295-3307.
35. Linker K, Pautz A, Fechir M, Hubrich T, Greeve J, Kleinert H. Involvement of KSRP inthe post-transcriptional regulation of human iNOS expression-complex interplayof KSRP with TTP and HuR. Nucleic Acids Res 2005; 33: 4813-4827.
36. Katsanou V PO, Milatos S, Blackshear PJ, Anderson P, Kollias G, Kontoyiannis DL.HuR as a negative posttranscriptional modulator in inflammation. Mol Cell 2005;19: 12.
37. Aldinucci D, Lorenzon D, Cattaruzza L, Pinto A, Gloghini A, Carbone A et al.Expression of CCR5 receptors on Reed-Sternberg cells and Hodgkin lymphomacell lines: involvement of CCL5/Rantes in tumor cell growth and microenvironmentalinteractions. Int J Cancer 2008; 122: 769-776.
38. Skinnider BF, Mak TW. The role of cytokines in classical Hodgkin lymphoma. Blood2002; 99: 4283-4297.
39. Khan G. Epstein-Barr virus, cytokines, and inflammation: a cocktail for thepathogenesis of Hodgkin's lymphoma? Exp Hematol 2006; 34: 399-406.
40. Kota SK, Balasubramanian S. Cancer therapy via modulation of micro RNA levels: apromising future. Drug Discov Today 2010; 15: 733-740.
41. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG et al. Therapeuticsilencing of miR-10b inhibits metastasis in a mouse mammary tumor model. NatBiotechnol 2010; 28: 341-347.
42. Stein CA, Hansen JB, Lai J, Wu S, Voskresenskiy A, Hog A et al. Efficient genesilencing by delivery of locked nucleic acid antisense oligonucleotides, unassistedby transfection reagents. Nucleic Acids Res 2010; 38: e3.
43. Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S. Bioinformatics andComputational Biology Solutions Using R and Bioconductor [Book] 2005; 473.
44. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M. Variancestabilization applied to microarray data calibration and to the quantification ofdifferential expression. Bioinformatics 2002; 18 (Suppl 1): S96-S104.
45. G S. Limma: linear models for microarray data. In: Gentleman RCV, Dudoit S,Irizarry R, Huber W (eds). Bioinformatics and Computational Biology, Solutions usingR and Bioconductor [Chapter] 2005; 23.