NF-κB directly mediates epigenetic deregulation of common microRNAs in Epstein-Barr virus-mediated transformation of B-cells and in lymphomas

Nucleic Acids Research

Volumn 42, Issue 17, 2014, Pages 11025-11039

  Vento Tormo, Roser ^a   Rodríguez Ubreva, Javier ^a   Di Lisio, Lorena ^b   Islam, Abul B M M K ^c   Urquiza, Jose M ^a   Hernando, Henar ^a   López Bigas, Nuria ^d,e   Shannon Lowe, Claire ^f   Martínez, Nerea ^b   Montes Moreno, Santiago ^b   Piris, Miguel A ^b   Ballestar, Esteban ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^c UNIVERSITY OF DHAKA   (Bangladesh)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 4; MICRORNA; MICRORNA 101; MICRORNA 130B; MICRORNA 140 3P; MICRORNA 146A; MICRORNA 151 3P; MICRORNA 151 5P; MICRORNA 155; MICRORNA 18A; MICRORNA 18B; MICRORNA 193B; MICRORNA 195; MICRORNA 21 3P; MICRORNA 222; MICRORNA 29C; MICRORNA 335; MICRORNA 342 3P; MICRORNA 34A; MICRORNA 365; MICRORNA 486 5P; MICRORNA 497; MICRORNA 551B; MICRORNA 627; MICRORNA 708; MICRORNA LET 7G; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; EPSTEIN BARR VIRUS; HISTONE MODIFICATION; HUMAN; HUMAN CELL; LYMPHOCYTE TRANSFORMATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; UPREGULATION; VIRUS PARTICLE; CELL CULTURE; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRUS CELL TRANSFORMATION;

B-LYMPHOCYTES; CELL LINE, TUMOR; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; EPIGENESIS, GENETIC; HERPESVIRUS 4, HUMAN; HUMANS; LYMPHOMA, B-CELL; MICRORNAS; NF-KAPPA B; TRANSCRIPTION, GENETIC;

EID: 84939186158     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku826     Document Type: Article

References (55)

1. Bornkamm, G.W. (2009) Epstein-Barr virus and its role in the pathogenesis of Burkitt's lymphoma: an unresolved issue. Semin. Cancer Biol., 19, 351-365.
2. Kaye, K.M., Izumi, K.M. and Kieff, E. (1993) Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. U.S.A., 90, 9150-9154.
3. Kilger, E., Kieser, A., Baumann, M. and Hammerschmidt, W. (1998) Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. EMBO J., 17, 1700-1709.
4. Feederle, R., Haar, J., Bernhardt, K., Linnstaedt, S.D., Bannert, H., Lips, H., Cullen, B.R. and Delecluse, H.J. (2011) The members of an Epstein-Barr virus microRNA cluster cooperate to transform B lymphocytes. J. Virol., 85, 9801-9810.
5. Hollyoake, M., Stuhler, A., Farrell, P., Gordon, J. and Sinclair, A. (1995) The normal cell cycle activation program is exploited during the infection of quiescent B lymphocytes by Epstein-Barr virus. Cancer Res., 55, 4784-4787.
6. Stewart, S., Dawson, C.W., Takada, K., Curnow, J., Moody, C.A., Sixbey, J.W. and Young, L.S. (2004) Epstein-Barr virus-encoded LMP2A regulates viral and cellular gene expression by modulation of the NF-kappaB transcription factor pathway. Proc. Natl. Acad. Sci. U.S.A., 101, 15730-15735.
7. Niller, H.H., Wolf, H. and Minarovits, J. (2009) Epigenetic dysregulation of the host cell genome in Epstein-Barr virus-associated neoplasia. Semin. Cancer Biol., 19, 158-164.
8. Hernando, H., Shannon-Lowe, C., Islam, A.B., Al-Shahrour, F., Rodriguez-Ubreva, J., Rodriguez-Cortez, V.C., Javierre, B.M., Mangas, C., Fernandez, A.F., Parra, M. et al. (2013) The B cell transcription program mediates hypomethylation and overexpression of key genes in Epstein-Barr virus-associated proliferative conversion. Genome Biol., 14, R3.
9. Hernando, H., Islam, A.B., Rodriguez-Ubreva, J., Forne, I., Ciudad, L., Imhof, A., Shannon-Lowe, C. and Ballestar, E. (2013) Epstein-Barr virus-mediated transformation of B cells induces global chromatin changes independent to the acquisition of proliferation. Nucleic Acids Res., 42, 249-263.
10. Forte, E., Salinas, R.E., Chang, C., Zhou, T., Linnstaedt, S.D., Gottwein, E., Jacobs, C., Jima, D., Li, Q.J., Dave, S.S. et al. (2012) The Epstein-Barr virus (EBV)-induced tumor suppressor microRNA MiR-34a is growth promoting in EBV-infected B cells. J. Vi rol., 86, 6889-6898.
11. Eis, P.S., Tam, W., Sun, L., Chadburn, A., Li, Z., Gomez, M.F., Lund, E. and Dahlberg, J.E. (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. U.S.A., 102, 3627-3632.
12. Arribas, A.J., Gomez-Abad, C., Sanchez-Beato, M., Martinez, N., Dilisio, L., Casado, F., Cruz, M.A., Algara, P., Piris, M.A. and Mollejo, M. (2013) Splenic marginal zone lymphoma: comprehensive analysis of gene expression and miRNA profling. Mod. Pathol., 26, 889-901.
13. Di Lisio, L., Martinez, N., Montes-Moreno, S., Piris-Villaespesa, M., Sanchez-Beato, M. and Piris, M.A. (2012) The role of miRNAs in the pathogenesis and diagnosis of B-cell lymphomas. Blood, 120, 1782-1790.
14. Campo, E., Swerdlow, S.H., Harris, N.L., Pileri, S., Stein, H. and Jaffe, E.S. (2011) The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood, 117, 5019-5032.
15. Rosenwald, A., Wright, G., Leroy, K., Yu, X., Gaulard, P., Gascoyne, R.D., Chan, W.C., Zhao, T., Haioun, C., Greiner, T.C. et al. (2003) Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J. Exp. Med., 198, 851-862.
16. Delecluse, H.J., Hilsendegen, T., Pich, D., Zeidler, R. and Hammerschmidt, W. (1998) Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. U.S.A., 95, 8245-8250.
17. Feederle, R., Bartlett, E.J. and Delecluse, H.J. (2010) Epstein-Barr virus genetics: talking about the BAC generation. Herpesviridae, 1, 6.
18. Ballestar, E., Paz, M.F., Valle, L., Wei, S., Fraga, M.F., Espada, J., Cigudosa, J.C., Huang, T.H. and Esteller, M. (2003) Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J., 22, 6335-6345.
19. Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
20. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
21. Hubbard, T.J., Aken, B.L., Beal, K., Ballester, B., Caccamo, M., Chen, Y., Clarke, L., Coates, G., Cunningham, F., Cutts, T. et al. (2007) Ensembl 2007. Nucleic Acids Res., 35, D610-D617.
22. Barrett, T., Wilhite, S.E., Ledoux, P., Evangelista, C., Kim, I.F., Tomashevsky, M., Marshall, K.A., Phillippy, K.H., Sherman, P.M., Holko, M. et al. (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res., 41, D991-D995.
23. Min, J.L., Barrett, A., Watts, T., Pettersson, F.H., Lockstone, H.E., Lindgren, C.M., Taylor, J.M., Allen, M., Zondervan, K.T. and McCarthy, M.I. (2010) Variability of gene expression profles in human blood and lymphoblastoid cell lines. BMC Genom., 11, 96.
24. Dessau, R.B. and Pipper, C.B. (2008) ["R"-project for statistical computing]. Ugeskr Laeger, 170, 328-330.
25. Chien, C.H., Sun, Y.M., Chang, W.C., Chiang-Hsieh, P.Y., Lee, T.Y., Tsai, W.C., Horng, J.T., Tsou, A.P. and Huang, H.D. (2011) Identifying transcriptional start sites of human microRNAs based on high-throughput sequencing data. Nucleic Acids Res., 39, 9345-9356.
26. Martin-Perez, D., Vargiu, P., Montes-Moreno, S., Leon, E.A., Rodriguez-Pinilla, S.M., Lisio, L.D., Martinez, N., Rodriguez, R., Mollejo, M., Castellvi, J. et al. (2012) Epstein-Barr virus microRNAs repress BCL6 expression in diffuse large B-cell lymphoma. Leukemia, 26, 180-183.
27. Lopez-Romero, P. (2011) Pre-processing and differential expression analysis of Agilent microRNA arrays using the AgiMicroRna Bioconductor library. BMC Genom., 12, 64.
28. Lymma, G.K. (2005) Limma: linear models for microarray data. In: Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W. (eds.). Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer, New York. pp. 397-420.
29. Yin, Q., McBride, J., Fewell, C., Lacey, M., Wang, X., Lin, Z., Cameron, J. and Flemington, E.K. (2008) MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J. Virol., 82, 5295-5306.
30. Jiang, J., Lee, E.J. and Schmittgen, T.D. (2006) Increased expression of microRNA-155 in Epstein-Barr virus transformed lymphoblastoid cell lines. Genes Chromosomes Cancer, 45, 103-106.
31. Linnstaedt, S.D., Gottwein, E., Skalsky, R.L., Luftig, M.A. and Cullen, B.R. (2010) Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus. J. Virol., 84, 11670-11678.
32. Chen, S., Wang, Z., Dai, X., Pan, J., Ge, J., Han, X., Wu, Z., Zhou, X. and Zhao, T. (2013) Re-expression of microRNA-150 induces EBV-positive Burkitt lymphoma differentiation by modulating c-Myb in vitro. Cancer Sci., 104, 826-834.
33. Thorley-Lawson, D.A. (2001) Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol., 1, 75-82.
34. Gatto, G., Rossi, A., Rossi, D., Kroening, S., Bonatti, S. and Mallardo, M. (2008) Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res., 36, 6608-6619.
35. Strickson, S., Campbell, D.G., Emmerich, C.H., Knebel, A., Plater, L., Ritorto, M.S., Shpiro, N. and Cohen, P. (2013) The anti-inflammatory drug BAY 11-7082 suppresses the MyD88-dependent signalling network by targeting the ubiquitin system. Biochem. J., 451, 427-437.
36. Krishnan, N., Bencze, G., Cohen, P. and Tonks, N.K. (2013) The anti-inflammatory compound BAY-11-7082 is a potent inhibitor of protein tyrosine phosphatases. FEBS J., 280, 2830-2841.
37. Jeon, K.I., Jeong, J.Y. and Jue, D.M. (2000) Thiol-reactive metal compounds inhibit NF-kappa B activation by blocking I kappa B kinase. J. Immunol., 164, 5981-5989.
38. Rauert-Wunderlich, H., Siegmund, D., Maier, E., Giner, T., Bargou, R.C., Wajant, H. and Stuhmer, T. (2013) The IKK inhibitor Bay 11-7082 induces cell death independent from inhibition of activation of NFkappaB transcription factors. PLoS ONE, 8, e59292.
39. Mott, J.L., Kurita, S., Cazanave, S.C., Bronk, S.F., Werneburg, N.W. and Fernandez-Zapico, M.E. (2010) Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB. J. Cell. Biochem., 110, 1155-1164.
40. Davis, R.E., Brown, K.D., Siebenlist, U. and Staudt, L.M. (2001) Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med., 194, 1861-1874.
41. Dweep, H., Sticht, C., Pandey, P. and Gretz, N. (2011) miRWalk-database: prediction of possible miRNA binding sites by 'walking' the genes of three genomes. J. Biomed. Inform., 44, 839-847.
42. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
43. Wang, X. (2008) miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA, 14, 1012-1017.
44. Di Lisio, L., Gomez-Lopez, G., Sanchez-Beato, M., Gomez-Abad, C., Rodriguez, M.E., Villuendas, R., Ferreira, B.I., Carro, A., Rico, D., Mollejo, M. et al. Mantle cell lymphoma: transcriptional regulation by microRNAs. Leukemia, 24, 1335-1342.
45. Gerdes, J. (1990) Ki-67 and other proliferation markers useful for immunohistological diagnostic and prognostic evaluations in human malignancies. Semin. Cancer Biol., 1, 199-206.
46. Mosialos, G., Birkenbach, M., Yalamanchili, R., VanArsdale, T., Ware, C. and Kieff, E. (1995) The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell, 80, 389-399.
47. Zhang, B., Wang, Z., Li, T., Tsitsikov, E.N. and Ding, H.F. (2007) NF-kappaB2 mutation targets TRAF1 to induce lymphomagenesis. Blood, 110, 743-751.
48. Ayllon, V. and O'Connor, R. (2007) PBK/TOPK promotes tumour cell proliferation through p38 MAPK activity and regulation of the DNA damage response. Oncogene, 26, 3451-3461.
49. Homig-Holzel, C., Hojer, C., Rastelli, J., Casola, S., Strobl, L.J., Muller, W., Quintanilla-Martinez, L., Gewies, A., Ruland, J., Rajewsky, K. et al. (2008) Constitutive CD40 signaling in B cells selectively activates the noncanonical NF-kappaB pathway and promotes lymphomagenesis. J. Exp. Med., 205, 1317-1329.
50. Luftig, M., Yasui, T., Soni, V., Kang, M.S., Jacobson, N., Cahir-McFarland, E., Seed, B. and Kieff, E. (2004) Epstein-Barr virus latent infection membrane protein 1 TRAF-binding site induces NIK/IKK alpha-dependent noncanonical NF-kappaB activation. Proc. Natl. Acad. Sci. U.S.A., 101, 141-146.
51. Zhao, J., Liang, Q., Cheung, K.F., Kang, W., Lung, R.W., Tong, J.H., To, K.F., Sung, J.J. and Yu, J. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profles of human genes in gastric cancer cells. Cancer, 119, 304-312.
52. Compagno, M., Lim, W.K., Grunn, A., Nandula, S.V., Brahmachary, M., Shen, Q., Bertoni, F., Ponzoni, M., Scandurra, M., Califano, A. et al. (2009) Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature, 459, 717-721.
53. Xiao, C., Calado, D.P., Galler, G., Thai, T.H., Patterson, H.C., Wang, J., Rajewsky, N., Bender, T.P. and Rajewsky, K. (2007) MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell, 131, 146-159.
54. Rao, D.S., O'Connell, R.M., Chaudhuri, A.A., Garcia-Flores, Y., Geiger, T.L. and Baltimore, D. MicroRNA-34a perturbs B lymphocyte development by repressing the forkhead box transcription factor Foxp1. Immunity, 33, 48-59.
55. Vigorito, E., Perks, K.L., Abreu-Goodger, C., Bunting, S., Xiang, Z., Kohlhaas, S., Das, P.P., Miska, E.A., Rodriguez, A., Bradley, A. et al. (2007) microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity, 27, 847-859.