Inhibition of the miR-155 target NIAM phenocopies the growth promoting effect of miR-155 in B-cell lymphoma

Oncotarget

Volumn 7, Issue 3, 2016, Pages 2391-2400

  Slezak Prochazka, Izabella ^a,b   Kluiver, Joost ^a   Jong, Debora de ^a   Smigielska Czepiel, Katarzyna ^a   Kortman, Gertrud ^a   Winkle, Melanie ^a   Rutgers, Bea ^a   Koerts, Jasper ^a   Visser, Lydia ^a   Diepstra, Arjan ^a   Kroesen, Bart Jan ^a   van den Berg, Anke ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b SILESIAN UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Ago2 IP; B cell lymphoma; MiR 155; NIAM; TBRG1

Indexed keywords

ARGONAUTE 2 PROTEIN; MICRORNA 155; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; MICRORNA; MIRN155 MICRORNA, HUMAN; NUCLEAR PROTEIN; SIGNAL PEPTIDE; TBRG1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; B CELL LYMPHOMA; BINDING SITE; BURKITT LYMPHOMA CELL LINE; CARCINOGENESIS; CELL PROLIFERATION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DET1 GENE; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HODGKIN LYMPHOMA CELL LINE; HOMEZ GENE; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; JARID2 GENE; LYMPHOMA CELL LINE; NIAM GENE; PHENOTYPE; PROTEIN EXPRESSION; PSIP1 GENE; RNA ANALYSIS; RNA TRANSCRIPTION; TRIM32 GENE; TUMOR SUPPRESSOR GENE; ANTAGONISTS AND INHIBITORS; GENETICS; HODGKIN DISEASE; PATHOLOGY; TUMOR CELL LINE;

ARGONAUTE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HODGKIN DISEASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOMA, B-CELL; MICRORNAS; NUCLEAR PROTEINS;

EID: 84962324205     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6165     Document Type: Article

References (38)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-297.
2. Musilova K, Mraz M. MicroRNAs in B-cell lymphomas: how a complex biology gets more complex. Leukemia. 2015; 29: 1004-1017.
3. Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, Schmidt-Supprian M, Rajewsky N, Yancopoulos G, et al. Regulation of the germinal center response by microRNA-155. Science (New York, N.Y.). 2007; 316: 604-608.
4. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, Heerema N, Croce CM. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103: 7024-7029.
5. Babar IA, Cheng CJ, Booth CJ, Liang X, Weidhaas JB, Saltzman WM, Slack FJ. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109: E1695-704.
6. Ferrajoli A, Shanafelt TD, Ivan C, Shimizu M, Rabe KG, Nouraee N, Ikuo M, Ghosh AK, Lerner S, Rassenti LZ, Xiao L, Hu J, Reuben JM, et al. Prognostic value of miR-155 in individuals with monoclonal B-cell lymphocytosis and patients with B chronic lymphocytic leukemia. Blood. 2013; 122: 1891-1899.
7. Kluiver J, Poppema S, de Jong D, Blokzijl T, Harms G, Jacobs S, Kroesen BJ, van den Berg A. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. The Journal of pathology. 2005; 207: 243-249.
8. van den Berg A, Kroesen BJ, Kooistra K, de Jong D, Briggs J, Blokzijl T, Jacobs S, Kluiver J, Diepstra A, Maggio E, Poppema S. High expression of B-cell receptor inducible gene BIC in all subtypes of Hodgkin lymphoma. Genes, chromosomes & cancer. 2003; 37: 20-28.
9. Kluiver J, Haralambieva E, de Jong D, Blokzijl T, Jacobs S, Kroesen BJ, Poppema S, van den Berg A. Lack of BIC and microRNA miR-155 expression in primary cases of Burkitt lymphoma. Genes, chromosomes & cancer. 2006; 45: 147-153.
10. Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T, Casellas R, Papavasiliou FN. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity. 2008; 28: 621-629.
11. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106: 7113-7118.
12. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z, Kohlhaas S, Das PP, Miska EA, Rodriguez A, Bradley A, Smith KG, Rada C, Enright AJ, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007; 27: 847-859.
13. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005; 120: 15-20.
14. Deng N, Puetter A, Zhang K, Johnson K, Zhao Z, Taylor C, Flemington EK, Zhu D. Isoform-level microRNA-155 target prediction using RNA-seq. Nucleic acids research. 2011; 39: e61.
15. Meier J, Hovestadt V, Zapatka M, Pscherer A, Lichter P, Seiffert M. Genome-wide identification of translationally inhibited and degraded miR-155 targets using RNA-interacting protein-IP. RNA biology. 2013; 10: 1018-1029.
16. Kluiver J, Gibcus JH, Hettinga C, Adema A, Richter MK, Halsema N, Slezak-Prochazka I, Ding Y, Kroesen BJ, van den Berg A. Rapid generation of microRNA sponges for microRNA inhibition. PloS one. 2012; 7: e29275.
17. Brown BD, Naldini L. Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nature reviews. Genetics. 2009; 10: 578-585.
18. Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA (New York, N.Y.). 2010; 16: 2043-2050.
19. Dorsett Y, McBride KM, Jankovic M, Gazumyan A, Thai TH, Robbiani DF, Di Virgilio M, Reina San-Martin B, Heidkamp G, Schwickert TA, Eisenreich T, Rajewsky K, Nussenzweig MC. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity. 2008; 28: 630-638.
20. Bouamar H, Jiang D, Wang L, Lin AP, Ortega M, Aguiar RC. MicroRNA 155 control of p53 activity is context dependent and mediated by Aicda and Socs1. Molecular and cellular biology. 2015; 35: 1329-1340.
21. Hagen J, Tompkins V, Dudakovic A, Weydert JA, Quelle DE. Generation and characterization of monoclonal antibodies to NIAM: a nuclear interactor of ARF and Mdm2. Hybridoma (2005). 2008; 27: 159-166.
22. Tompkins VS, Hagen J, Frazier AA, Lushnikova T, Fitzgerald MP, di Tommaso A, Ladeveze V, Domann FE, Eischen CM, Quelle DE. A novel nuclear interactor of ARF and MDM2 (NIAM) that maintains chromosomal stability. The Journal of biological chemistry. 2007; 282: 1322-1333.
23. Reed SM, Hagen J, Tompkins VS, Thies K, Quelle FW, Quelle DE. Nuclear interactor of ARF and Mdm2 regulates multiple pathways to activate p53. Cell cycle (Georgetown, Tex.). 2014; 13: 1288-1298.
24. Reed SM, Hagen J, Muniz VP, Rosean TR, Borcherding N, Sciegienka S, Goeken JA, Naumann PW, Zhang W, Tompkins VS, Janz S, Meyerholz DK, Quelle DE. NIAM-Deficient Mice Are Predisposed to the Development of Proliferative Lesions including B-Cell Lymphomas. PloS one. 2014; 9: e112126.
25. Tompkins VS, Hagen J, Frazier AA, Lushnikova T, Fitzgerald MP, di Tommaso A, Ladeveze V, Domann FE, Eischen CM, Quelle DE. A novel nuclear interactor of ARF and MDM2 (NIAM) that maintains chromosomal stability. The Journal of biological chemistry. 2007; 282: 1322-1333.
26. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. 2008.
27. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004; 103: 275-282.
28. Slezak-Prochazka I, Kluiver J, de Jong D, Kortman G, Halsema N, Poppema S, Kroesen BJ, van den Berg A. Cellular localization and processing of primary transcripts of exonic microRNAs. PloS one. 2013; 8: e76647.
29. Pajic A, Spitkovsky D, Christoph B, Kempkes B, Schuhmacher M, Staege MS, Brielmeier M, Ellwart J, Kohlhuber F, Bornkamm GW, Polack A, Eick D. Cell cycle activation by c-myc in a burkitt lymphoma model cell line. International journal of cancer. Journal international du cancer. 2000; 87: 787-793.
30. Mao TK, Chen CZ. Dissecting microRNA-mediated gene regulation and function in T-cell development. Methods in enzymology. 2007; 427: 171-189.
31. Kluiver J, Slezak-Prochazka I, van den Berg A. Studying microRNAs in lymphoma. Methods in molecular biology (Clifton, N.J.). 2013; 971: 265-276.
32. Robertus JL, Harms G, Blokzijl T, Booman M, de Jong D, van ImhoffG, Rosati S, Schuuring E, Kluin P, van den Berg A. Specific expression of miR-17-5p and miR-127 in testicular and central nervous system diffuse large B-cell lymphoma. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2009; 22: 547-555.
33. Specht K, Richter T, Muller U, Walch A, Werner M, Hofler H. Quantitative gene expression analysis in microdissected archival formalin-fixed and paraffin-embedded tumor tissue. The American journal of pathology. 2001; 158: 419-429.
34. Tan LP, Seinen E, Duns G, de Jong D, Sibon OC, Poppema S, Kroesen BJ, Kok K, van den Berg A. A high throughput experimental approach to identify miRNA targets in human cells. Nucleic acids research. 2009; 37: e137.
35. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic acids research. 2002; 30: 207-210.
36. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102: 15545-15550.
37. Gibcus JH, Tan LP, Harms G, Schakel RN, de Jong D, Blokzijl T, Moller P, Poppema S, Kroesen BJ, van den Berg A. Hodgkin lymphoma cell lines are characterized by a specific miRNA expression profile. Neoplasia (New York, N.Y.). 2009; 11: 167-176.
38. Winkle M, van den Berg A, Tayari M, Sietzema J, Terpstra M, Kortman G, de Jong D, Visser L, Diepstra A, Kok K, Kluiver J. Long noncoding RNAs as a novel component of the Myc transcriptional network. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2015; 29: 2338-2346.