The 5' regulatory sequences of active miR-146a promoters are hypomethylated and associated with euchromatic histone modification marks in B lymphoid cells

Biochemical and Biophysical Research Communications

Volumn 433, Issue 4, 2013, Pages 489-495

  Szenthe, Kalman ^a,b   Koroknai, Anita ^a   Banati, Ferenc ^a,b   Bathori, Zoltan ^a   Lozsa, Rita ^c   Burgyan, Jozsef ^c   Wolf, Hans ^d   Salamon, Daniel ^e   Nagy, Katalin ^f   Niller, Hans Helmut ^d   Minarovits, Janos ^a,f  

^a NATIONAL CENTER FOR EPIDEMIOLOGY   (Hungary)

^b RT Europe Nonprofit Ltd   (Hungary)

^c SZENT ISTVÁN UNIVERSITY   (Hungary)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF SZEGED   (Hungary)

Author keywords

B cell lines; Cell type specific expression; CpG island; DNA methylation; Euchromatic histone modification; MiR 146a

Indexed keywords

DINUCLEOTIDE; HISTONE; MICRORNA 146A;

5' REGULATORY SEQUENCE; ARTICLE; B LYMPHOCYTE; BREAST CARCINOMA; BURKITT LYMPHOMA; CANCER CELL CULTURE; CONTROLLED STUDY; CPG ISLAND; DNA FLANKING REGION; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; EPSTEIN BARR VIRUS; GENE EXPRESSION; HISTONE MODIFICATION; HYPOMETHYLATION; INTRON; METHYLATION; MOLECULAR MECHANICS; NASOPHARYNX CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; REGULATORY SEQUENCE; TRANSCRIPTION INITIATION;

5' FLANKING REGION; ACETYLATION; B-LYMPHOCYTES; BIOLOGICAL MARKERS; BLOTTING, NORTHERN; BURKITT LYMPHOMA; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; EUCHROMATIN; GENOME, VIRAL; HERPESVIRUS 4, HUMAN; HISTONES; HUMANS; INTRONS; LYSINE; MICRORNAS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION INITIATION SITE; VIRUS LATENCY;

HUMAN HERPESVIRUS 4;

EID: 84876477073     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.03.022     Document Type: Article

References (53)

1. Okamura K., Chung W.J., Lai E.C. The long and short inverted repeat genes in animals: microRNAs, mirtrons and hairpin RNAs. Cell Cycle 2008, 7:2840-2845.
2. Perron M.P., Provost P. Protein components of the microRNA pathway and human diseases. Methods Mol. Biol. 2009, 487:369-385.
3. Lodish H.F., Zhou B., Liu G., Chen C.Z. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 2008, 8:120-130.
4. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 2006, 103:12481-12486.
5. Ha T.Y. The role of microRNAs in regulatory T cells and in the immune response. Immune Netw. 2011, 11:11-41.
6. Fernando T.R., Rodriguez-Malave N., Rao D.S. MicroRNAs in B cell development and malignancy. J. Hematol. Oncol. 2012, 5:7.
7. Calin G.A., Liu C.G., Sevignani C., et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc. Natl. Acad. Sci. USA 2004, 101:11755-11760.
8. Calin G.A., Sevigniani C., Dumitru C.D., et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. USA 2004, 101:2999-3004.
9. Bandyopadhyay S., Mitra R., Maulik U., Zhang M.Q. Development of the human cancer microRNA network. Silence 2010, 1(6).
10. Li G., Wu Z., Peng Y., et al. MicroRNA-10b induced by Epstein-Barr virus-encoded latent membrane protein-1 promotes the metastasis of human nasopharyngeal carcinoma cells. Cancer Lett. 2010, 299:29-36.
11. Xu W.D., Lu M.M., Pan H.F., Ye D.Q. Association of microRNA-146a with autoimmune diseases. Inflammation 2012, 15:1525-1529.
12. Monticelli S., Ansel K.M., Xiao C., et al. MicroRNA profiling of the murine hematopoietic system. Genome Biol. 2005, 6:R71.
13. Peveling-Oberhag J., Crisman G., Schmidt A., et al. Dysregulation of global microRNA expression in splenic marginal zone lymphoma and influence of chronic hepatitis C virus infection. Leukemia 2012, 26:1654-1662.
14. Tomita M., Tanaka Y., Mori N. MicroRNA miR-146a is induced by HTLV-1 tax and increases the growth of HTLV-1-infected T-cells. Int. J. Cancer 2012, 130:2300-2309.
15. Zhong H., Xu L., Zhong J.H., et al. Clinical and prognostic significance of miR-155 and miR-146a expression levels in formalin-fixed/paraffin-embedded tissue of patients with diffuse large B-cell lymphoma. Exp. Ther. Med. 2012, 3:763-770.
16. Paik J.H., Jang J.Y., Jeon Y.K., et al. MicroRNA-146a downregulates NFκB activity via targeting TRAF6 and functions as a tumor suppressor having strong prognostic implications in NK/T cell lymphoma. Clin. Cancer Res. 2011, 17:4761-4771.
17. Cullen B.R. Viruses and microRNAs: RISCy interactions with serious consequences. Genes Dev. 2011, 25:1881-1894.
18. Motsch N., Pfuhl T., Mrazek J., et al. Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a. RNA Biol. 2007, 4:131-137.
19. Myklebust M.P., Bruland O., Fluge O., et al. MicroRNA-15b is induced with E2F-controlled genes in HPV-related cancer. Br. J. Cancer 2011, 105:1719-1725.
20. Wang Q., Li D.C., Liu C.X., et al. Upregulation of miR-27a contributes to the malignant transformation of human bronchial epithelial cells by SV40 small T antigen. Oncogene 2011, 30:3875-3886.
21. Wu Y.H., Hu T.F., Chen Y.C., et al. The manipulation of miRNA-gene regulatory networks by KSHV induces endothelial cell motility. Blood 2011, 118:2896-2905.
22. Zheng Z.M., Wang X. Regulation of cellular miRNA expression by human papillomaviruses. Biochem. Biophys. Acta 1809, 2011:668-677.
23. Cameron J.E., Yin Q., Fewell C., et al. Epstein-Barr virus latent membrane protein 1 induces celular microRNA miR-146a, a modulator of lymphocyte signaling pathways. J. Virol. 2008, 82:1946-1958.
24. Gatto G., Rossi A., Kroening S., et al. Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res. 2008, 36:6608-6619.
25. Rahadiani N., Takakuwa T., Tresnesari K., et al. Latent membrane protein-1 of Epstein-Barr virus induces the expression of B-cell integration cluster, a precursor fprm of microRNA-155, in B lymphoma cell lines. Biochem. Biophys. Res. Commun. 2008, 377:579-583.
26. Du Z.M., Hu L.F., Wang H.Y., et al. Upregulation of miR-155 in nasopharyngeal carcinoma is partly driven by LMP1 and LMP2A and downregulates a negative prognostic marker JMJD1A. PLoS One 2011, 6(4):e19137.
27. Anastasiodou E., Boccellato F., Vincenti S., et al. Epstein-Barr virus encoded LMP1 downregulates TCL1 oncogene through miR-29b. Oncogene 2010, 29:1316-1328.
28. Forte E., Salinas R.E., Chang C., et al. The Epstein-Barr virus (EBV)-induced tumor suppressor microRNA miR-34a is growth promoting in EBV-infected B cells. J. Virol. 2012, 86:6889-6898.
29. Yu H., Lu J., Zuo L., Yan Q., et al. Epstein-Barr virus downregulates microRNA 203 through the oncoprotein latent membrane protein 1: a contribution to increased tumor incidence in epithelial cells. J. Virol. 2012, 86:3088-3099.
30. Salamon D., Takacs M., Ujvari D., et al. Protein-DNA binding and CpG methylation at nucleotide resolution of latency-associated promoters Qp, Cp, and LMP1p of Epstein-Barr virus. J. Virol. 2001, 75:2584-2596.
31. Bakos A., Banati F., Koroknai A., et al. High-resolution analysis of CpG methylation and in vivo protein-DNA interactions at the alternative Epstein-Barr virus latency promoters Qp and C pin the nasopharyngeal carcinoma cell line C666-1. Virus Genes 2007, 35:195-202.
32. Patrone G., Puppo F., Cusano R., et al. Nuclear run-on assay using biotin labeling, magnetic bead capture and analysis by fluorescence-based RT-PCR. Biotechniques 2000, 29:1012-1017.
33. Szittya G., Molnár A., Silhavy D., et al. Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell 2002, 14:1-15.
34. Csorba T., Bovi A., Dalmay T., Burgyan J. The p122 subunit of tobacco mosaic virus replicase is a potent silencing suppressor and compromises both siRNA and miRNA mediated pathways. J. Virol. 2007, 81:11768-11780.
35. * and the C promoter of Epstein-Barr virus is unaffected by CpG methylation and does not correlate with Cp activity. J. Gen. Virol. 2009, 90:1183-1189.
36. Gerle B., Koroknai A., Fejer G., et al. Acetylated histone H3 and H4 mark the upregulated LMP2A promoter of Epstein-Barr virus in lymphoid cells. J. Virol. 2007, 81:13242-13247.
37. Fejer G., Koroknai A., Banati F., et al. Latency-type-specific distribution of epigenetic marks at the alternative promoters Cp and Qp of Epstein-Barr virus. J. Gen. Virol. 2008, 89:1364-1370.
38. Van Driel R., Fransz P. Nuclear architecture and genome functioning in plants and animals: what can we learn from both?. Exp. Cell Res. 2004, 296:86-90.
39. Wu Y., Kikuchi S., Yan H., et al. Euchromatic subdomains in rice centromers are associated with genes and transcription. Plant Cell 2011, 23:4054-4064.
40. Barski A., Jothi R., Cuddapah S., et al. Chromatin poises miRNA- and protein-coding genes for expression. Genome Res. 2009, 19:1742-1751.
41. Illingworth R.S., Bird A.P. CpG islands - 'a rough guide'. FEBS Lett. 2009, 583:1713-1720.
42. Takacs M., Banati F., Koroknai A., Segesdi J., et al. Epigenetic regulation of latent Epstein-Barr virus promoters. Biochim. Biophys. Acta 2010, 1799:228-235.
43. Pai S., O'Sullivan B.J., Cooper L., et al. RelB nuclear translocation mediated by C-terminal activator regions of Epstein-Barr virus-encoded latent membrane protein 1 and its effect on antigen-presenting function in B cells. J. Virol. 2002, 76:1914-1921.
44. Rosato T., Anastasiadou E., Garg N., et al. Differential regulation of miR-21 and miR-146a by Epstein-Barr virus-encoded EBNA2. Leukemia 2012, 10.1038/leu.2012.108.
45. Lenoir G.M., Vuillaume M., Bonnardel C. The use of lymphomatous and lymphoblastoid cell lines in the study of Burkitt's lymphoma. IARC Sci. Publ. 1985, 60:309-318.
46. Menezes J., Leibold W., Klein G., Clements G. Establishment and characterization of an Epstein-Barr virus (EBV)-negative lymphoblastoid B cell line (BJA-B) from an exceptional EBV-genome-negative African Burkitt's lymphoma. Biomedicine 1975, 22:276-284.
47. Ben-Bassat H., Goldblum N., Mitrani S., et al. Establishment in continuous culture of a new type of lymphocyte from a "Burkitt like" malignant lymphoma (line D.G.-75). Int. J. Cancer 1977, 19:27-33.
48. Ernberg I., Falk K., Minarovits J., et al. The role of methylation in the phenotype dependent modulation of Epstein-Barr nuclear antigen 2 and latent membrane protein genes in cells latently infected with Epstein-Barr virus. J. Gen. Virol. 1989, 70:2989-3002.
49. Altiok E., Minarovits J., Hu L.F., et al. Host-cell-phenotype-dependent control of the BCR2/BWR1 promoter complex regulates the expression of Epstein-Barr virus nuclear antigens 2-6. Proc. Natl. Acad. Sci. USA 1992, 89:905-909.
50. Hatfull G., Bankier A.T., Barrell B.G., Farrell P.J. Sequence analysis of Raji Epstein-Barr virus DNA. Virology 1988, 164:334-340.
51. Takada K., Horinouchi K., Ono Y., et al. An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 1991, 5:147-156.
52. Cheung S.T., Huang D.P., Hui A.B., et al. Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. Int. J. Cancer 1999, 83:121-126.
53. Wakisaka N., Kondo S., Yoshizaki T., Murono S., et al. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1 alpha. Mol. Cell. Biol. 2004, 24:5223-5234.