Insights into epigenetic regulation of microRNA-155 expression in multiple myeloma

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 3, 2015, Pages 353-366

  Krzeminski, Patryk ^a   Sarasquete, María E ^a   Misiewicz Krzeminska, Irena ^a,c   Corral, Rocío ^a   Corchete, Luis A ^a   Martín, Ana A ^a   García Sanz, Ramón ^a   San Miguel, Jesús F ^b   Gutiérrez, Norma C ^a  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

^c NATIONAL MEDICINES INSTITUTE   (Poland)

Author keywords

DNA methylation; LPS; MicroRNA; Multiple myeloma

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BISULFITE; DNA; LIPOPOLYSACCHARIDE; MAX PROTEIN; MICRORNA 155; PROTEIN MAD1; RNA; SMAD4 PROTEIN; TOLL LIKE RECEPTOR 4; MICRORNAS; MIRN155 MICRORNA, HUMAN;

ARTICLE; BINDING AFFINITY; CLINICAL ASSESSMENT; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; E BOX ELEMENT; EXON; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC REGULATION; HOST; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRON; LUCIFERASE ASSAY; MAJOR CLINICAL STUDY; MULTIPLE MYELOMA; MYELOMA CELL; ONCOGENE C MYC; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SURVIVAL RATE; TRANSCRIPTION INITIATION SITE; UPREGULATION; B-LYMPHOCYTES; BIOSYNTHESIS; CELL LINE, TUMOR; CPG ISLANDS; E-BOX ELEMENTS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETICS; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; PATHOLOGY; PROMOTER REGIONS, GENETIC;

B-LYMPHOCYTES; CELL LINE, TUMOR; CPG ISLANDS; DNA METHYLATION; E-BOX ELEMENTS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MICRORNAS; MULTIPLE MYELOMA; PROMOTER REGIONS, GENETIC;

EID: 84922967616     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.12.002     Document Type: Article

References (61)

1. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
2. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
3. de Yebenes V.G., Bartolome-Izquierdo N., Ramiro A.R. Regulation of B-cell development and function by microRNAs. Immunol. Rev. 2013, 253:25-39.
4. Spierings D.C., McGoldrick D., Hamilton-Easton A.M., Neale G., Murchison E.P., Hannon G.J., Green D.R., Withoff S. Ordered progression of stage-specific miRNA profiles in the mouse B2 B-cell lineage. Blood 2011, 117:5340-5349.
5. Teng G., Hakimpour P., Landgraf P., Rice A., Tuschl T., Casellas R., Papavasiliou F.N. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 2008, 28:621-629.
6. Vigorito E., Perks K.L., Abreu-Goodger C., Bunting S., Xiang Z., Kohlhaas S., Das P.P., Miska E.A., Rodriguez A., Bradley A., Smith K.G., Rada C., Enright A.J., Toellner K.M., Maclennan I.C., Turner M. MicroRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 2007, 27:847-859.
7. Dagan L.N., Jiang X., Bhatt S., Cubedo E., Rajewsky K., Lossos I.S. MiR-155 regulates HGAL expression and increases lymphoma cell motility. Blood 2013, 119:513-520.
8. Kong W., He L., Richards E.J., Challa S., Xu C.X., Permuth-Wey J., Lancaster J.M., Coppola D., Sellers T.A., Djeu J.Y., Cheng J.Q. Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene 2013, 33:679-689.
9. Tsitsiou E., Lindsay M.A. MicroRNAs and the immune response. Curr. Opin. Pharmacol. 2009, 9:514-520.
10. Zhang Y., Roccaro A.M., Rombaoa C., Flores L., Obad S., Fernandes S.M., Sacco A., Liu Y., Ngo H., Quang P., Azab A.K., Azab F., Maiso P., Reagan M., Brown J.R., Thai T.H., Kauppinen S., Ghobrial I.M. LNA-mediated anti-miR-155 silencing in low-grade B-cell lymphomas. Blood 2012, 120:1678-1686.
11. Tam W. Identification and characterization of human BIC, a gene on chromosome 21 that encodes a noncoding RNA. Gene 2001, 274:157-167.
12. Elton T.S., Selemon H., Elton S.M., Parinandi N.L. Regulation of the MIR155 host gene in physiological and pathological processes. Gene 2012, 532:1-12.
13. Gatto G., Rossi A., Rossi D., Kroening S., Bonatti S., Mallardo M. Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res. 2008, 36:6608-6619.
14. Kong W., Yang H., He L., Zhao J.J., Coppola D., Dalton W.S., Cheng J.Q. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol. Cell. Biol. 2008, 28:6773-6784.
15. Vargova K., Curik N., Burda P., Basova P., Kulvait V., Pospisil V., Savvulidi F., Kokavec J., Necas E., Berkova A., Obrtlikova P., Karban J., Mraz M., Pospisilova S., Mayer J., Trneny M., Zavadil J., Stopka T. MYB transcriptionally regulates the miR-155 host gene in chronic lymphocytic leukemia. Blood 2011, 117:3816-3825.
16. Yin Q., Wang X., McBride J., Fewell C., Flemington E. B-cell receptor activation induces BIC/miR-155 expression through a conserved AP-1 element. J. Biol. Chem. 2008, 283:2654-2662.
17. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011, 25:1010-1022.
18. Vu T.H., Li T., Nguyen D., Nguyen B.T., Yao X.M., Hu J.F., Hoffman A.R. Symmetric and asymmetric DNA methylation in the human IGF2-H19 imprinted region. Genomics 2000, 64:132-143.
19. Kluiver J., Haralambieva E., de Jong D., Blokzijl T., Jacobs S., Kroesen B.J., Poppema S., van den Berg A. Lack of BIC and microRNA miR-155 expression in primary cases of Burkitt lymphoma. Genes Chromosom. Cancer 2006, 45:147-153.
20. Tam W., Hughes S.H., Hayward W.S., Besmer P. Avian bic, a gene isolated from a common retroviral site in avian leukosis virus-induced lymphomas that encodes a noncoding RNA, cooperates with c-myc in lymphomagenesis and erythroleukemogenesis. J. Virol. 2002, 76:4275-4286.
21. Lorsbach R.B., Hsi E.D., Dogan A., Fend F. Plasma cell myeloma and related neoplasms. Am. J. Clin. Pathol. 2011, 136:168-182.
22. Gutierrez N.C., Sarasquete M.E., Misiewicz-Krzeminska I., Delgado M., De Las Rivas J., Ticona F.V., Ferminan E., Martin-Jimenez P., Chillon C., Risueno A., Hernandez J.M., Garcia-Sanz R., Gonzalez M., San Miguel J.F. Deregulation of microRNA expression in the different genetic subtypes of multiple myeloma and correlation with gene expression profiling. Leukemia 2010, 24:629-637.
23. Lionetti M., Biasiolo M., Agnelli L., Todoerti K., Mosca L., Fabris S., Sales G., Deliliers G.L., Bicciato S., Lombardi L., Bortoluzzi S., Neri A. Identification of microRNA expression patterns and definition of a microRNA/mRNA regulatory network in distinct molecular groups of multiple myeloma. Blood 2009, 114:e20-e26.
24. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132:365-386.
25. Li L.C., Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431.
26. Rohde C., Zhang Y., Jurkowski T.P., Stamerjohanns H., Reinhardt R., Jeltsch A. Bisulfite sequencing data presentation and compilation (BDPC) web server-a useful tool for DNA methylation analysis. Nucleic Acids Res. 2008, 36:e34.
27. Klug M., Rehli M. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 2006, 1:127-130.
28. Misiewicz-Krzeminska I., Sarasquete M.E., Quwaider D., Krzeminski P., Ticona F.V., Paino T., Delgado M., Aires A., Ocio E.M., Garcia-Sanz R., San Miguel J.F., Gutierrez N.C. Restoration of microRNA-214 expression reduces growth of myeloma cells through positive regulation of P53 and inhibition of DNA replication. Haematologica 2013, 98:640-648.
29. Nelson J.D., Denisenko O., Sova P., Bomsztyk K. Fast chromatin immunoprecipitation assay. Nucleic Acids Res. 2006, 34:e2.
30. Qin J.Z., Dummer R., Burg G., Dobbeling U. Constitutive and interleukin-7/interleukin-15 stimulated DNA binding of Myc, Jun, and novel Myc-like proteins in cutaneous T-cell lymphoma cells. Blood 1999, 93:260-267.
31. Contal C.c., O'Quigley J. An application of changepoint methods in studying the effect of age on survival in breast cancer. Comput. Stat. Data Anal. 1999, 30:253-270.
32. Tili E., Michaille J.J., Cimino A., Costinean S., Dumitru C.D., Adair B., Fabbri M., Alder H., Liu C.G., Calin G.A., Croce C.M. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 2007, 179:5082-5089.
33. Gaubatz S., Meichle A., Eilers M. An E-box element localized in the first intron mediates regulation of the prothymosin alpha gene by c-myc. Mol. Cell. Biol. 1994, 14:3853-3862.
34. Luscher B. Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene 2001, 277:1-14.
35. Eis P.S., Tam W., Sun L., Chadburn A., Li Z., Gomez M.F., Lund E., Dahlberg J.E. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:3627-3632.
36. Faraoni I., Laterza S., Ardiri D., Ciardi C., Fazi F., Lo-Coco F. MiR-424 and miR-155 deregulated expression in cytogenetically normal acute myeloid leukaemia: correlation with NPM1 and FLT3 mutation status. J. Hematol. Oncol. 2012, 5:26.
37. Jardin F., Figeac M. MicroRNAs in lymphoma, from diagnosis to targeted therapy. Curr. Opin. Oncol. 2013, 25:480-486.
38. Kluiver J., Poppema S., de Jong D., Blokzijl T., Harms G., Jacobs S., Kroesen B.J., van den Berg A. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J. Pathol. 2005, 207:243-249.
39. Herman J.G., Graff J.R., Myohanen S., Nelkin B.D., Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9821-9826.
40. Kong J., Dougherty M.P., Perkins L.B., Camire M.E. Composition and consumer acceptability of a novel extrusion-cooked salmon snack. J. Food Sci. 2008, 73:S118-S123.
41. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
42. Kim D.W., Lassar A.B. Smad-dependent recruitment of a histone deacetylase/Sin3A complex modulates the bone morphogenetic protein-dependent transcriptional repressor activity of Nkx3.2. Mol. Cell. Biol. 2003, 23:8704-8717.
43. Wong K.Y., So C.C., Loong F., Chung L.P., Lam W.W., Liang R., Li G.K., Jin D.Y., Chim C.S. Epigenetic inactivation of the miR-124-1 in haematological malignancies. PLoS One 2011, 6:e19027.
44. Vesely J., Cihak A. 5-Aza-2'-deoxycytidine: preclinical studies in mice. Neoplasma 1980, 27:113-119.
45. Ortmann C.A., Burchert A., Holzle K., Nitsche A., Wittig B., Neubauer A., Schmidt M. Down-regulation of interferon regulatory factor 4 gene expression in leukemic cells due to hypermethylation of CpG motifs in the promoter region. Nucleic Acids Res. 2005, 33:6895-6905.
46. Tao L., Ge R., Xie M., Kramer P.M., Pereira M.A. Effect of trichloroethylene on DNA methylation and expression of early-intermediate protooncogenes in the liver of B6C3F1 mice. J. Biochem. Mol. Toxicol. 1999, 13:231-237.
47. Du H.L., Ren L.M., Chen H., Zhu Y., Qi Y. Re-expression of p16 gene in the myeloma cell line U266 induced by synergy of sodium butyrate and 5-Aza-2'-deoxycytidine. Di Yi Jun Yi Da Xue Xue Bao 2002, 22:981-984.
48. Galvao J., Davis B., Tilley M., Normando E., Duchen M.R., Cordeiro M.F. Unexpected low-dose toxicity of the universal solvent DMSO. FASEB J. 2014, 3:1317-1330.
49. Kawasaki H., Taira K. Induction of DNA methylation and gene silencing by short interfering RNAs in human cells. Nature 2004, 431:211-217.
50. Mathieu O., Bender J. RNA-directed DNA methylation. J. Cell Sci. 2004, 117:4881-4888.
51. Schmitz K.M., Mayer C., Postepska A., Grummt I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 2010, 24:2264-2269.
52. Husebye H., Halaas O., Stenmark H., Tunheim G., Sandanger O., Bogen B., Brech A., Latz E., Espevik T. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 2006, 25:683-692.
53. Morris M.C., Gilliam E.A., Button J., Li L. Dynamic modulation of innate immune response by varying dosages of LPS in human monocytic cells. J. Biol. Chem. 2014, 289:21584-21590.
54. Bala S., Marcos M., Kodys K., Csak T., Catalano D., Mandrekar P., Szabo G. Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor {alpha} (TNF{alpha}) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 2011, 286:1436-1444.
55. Cheung S.T., So E.Y., Chang D., Ming-Lum A., Mui A.L. Interleukin-10 inhibits lipopolysaccharide induced miR-155 precursor stability and maturation. PLoS One 2013, 8:e71336.
56. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12481-12486.
57. Prendergast G.C., Ziff E.B. Methylation-sensitive sequence-specific DNA binding by the c-Myc basic region. Science 1991, 251:186-189.
58. Swarnalatha M., Singh A.K., Kumar V. The epigenetic control of E-box and Myc-dependent chromatin modifications regulate the licensing of lamin B2 origin during cell cycle. Nucleic Acids Res. 2012, 40:9021-9035.
59. Walhout A.J., Gubbels J.M., Bernards R., van der Vliet P.C., Timmers H.T. c-Myc/Max heterodimers bind cooperatively to the E-box sequences located in the first intron of the rat ornithine decarboxylase (ODC) gene. Nucleic Acids Res. 1997, 25:1493-1501.
60. Horikawa I., Cable P.L., Mazur S.J., Appella E., Afshari C.A., Barrett J.C. Downstream E-box-mediated regulation of the human telomerase reverse transcriptase (hTERT) gene transcription: evidence for an endogenous mechanism of transcriptional repression. Mol. Biol. Cell 2002, 13:2585-2597.
61. Holien T., Vatsveen T.K., Hella H., Waage A., Sundan A. Addiction to c-MYC in multiple myeloma. Blood 2012, 120:2450-2453.