Activation of gga-miR-155 by reticuloendotheliosis virus T strain and its contribution to transformation Open Access

Abstract

The v- oncoprotein encoded by reticuloendotheliosis virus T strain (Rev-T) is a member of the /NF-κB family of transcription factors capable of transformation of primary chicken spleen and bone marrow cells. Rapid transformation of avian haematopoietic cells by v- occurs through a process of deregulation of multiple protein-encoding genes through its direct effect on their promoters. More recently, upregulation of oncogenic miR-155 and its precursor pre-miR-155 was demonstrated in both Rev-T-infected chicken embryo fibroblast cultures and Rev-T-induced B-cell lymphomas. Through electrophoresis mobility shift assay and reporter analysis on the gga-miR-155 promoter, we showed that the v--induced miR-155 overexpression occurred by the direct binding to one of the putative NF-κB binding sites. Using the v--induced transformation model on chicken embryonic splenocyte cultures, we could demonstrate a dynamic increase in miR-155 levels during the transformation. Transcriptome profiles of lymphoid cells transformed by v- showed upregulation of miR-155 accompanied by downregulation of a number of putative miR-155 targets such as Pu.1 and CEBPβ. We also showed that v- could rescue the suppression of miR-155 expression observed in Marek’s disease virus (MDV)-transformed cell lines, where its functional viral homologue MDV-miR-M4 is overexpressed. Demonstration of gene expression changes affecting major molecular pathways, including organismal injury and cancer in avian macrophages transfected with synthetic mature miR-155, underlines its potential direct role in transformation. Our study suggests that v--induced transformation involves a complex set of events mediated by the direct activation of NF-κB targets, together with inhibitory effects on microRNA targets.

Keyword(s): miR-155 , NF-κB , transformation and v-rel
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2017-04-01
2024-03-29
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References

  1. Gilmore TD, Wolenski FS. NF-κB: where did it come from and why?. Immunol Rev 2012; 246:14–35 [View Article][PubMed]
    [Google Scholar]
  2. Gilmore TD, Gélinas C. Methods for assessing the in vitro transforming activity of NF-κB transcription factor c-Rel and related proteins. Methods Mol Biol 2015; 1280:427–446 [View Article][PubMed]
    [Google Scholar]
  3. Robinson FR, Twiehaus MJ. Isolation of tha avian reticuloendothelial virus (strain T). Avian Dis 1974; 18:278–288 [View Article][PubMed]
    [Google Scholar]
  4. Hunter JE, Leslie J, Perkins ND. c-Rel and its many roles in cancer: an old story with new twists. Br J Cancer 2016; 114:1–6 [View Article][PubMed]
    [Google Scholar]
  5. Chen IS, Mak TW, O'Rear JJ, Temin HM. Characterization of reticuloendotheliosis virus strain T DNA and isolation of a novel variant of reticuloendotheliosis virus strain T by molecular cloning. J Virol 1981; 40:800–811[PubMed]
    [Google Scholar]
  6. Stephens RM, Rice NR, Hiebsch RR, Bose HR Jr, Gilden RV. Nucleotide sequence of v-rel: the oncogene of reticuloendotheliosis virus. Proc Natl Acad Sci USA 1983; 80:6229–6233 [View Article][PubMed]
    [Google Scholar]
  7. Wilhelmsen KC, Eggleton K, Temin HM. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J Virol 1984; 52:172–182[PubMed]
    [Google Scholar]
  8. Bose HR Jr. The Rel family: models for transcriptional regulation and oncogenic transformation. Biochim Biophys Acta 1992; 1114:1–17 [View Article][PubMed]
    [Google Scholar]
  9. Gilmore TD, Kalaitzidis D, Liang MC, Starczynowski DT. The c-Rel transcription factor and B-cell proliferation: a deal with the devil. Oncogene 2004; 23:2275–2286 [View Article][PubMed]
    [Google Scholar]
  10. Sachdev S, Diehl JA, McKinsey TA, Hans A, Hannink M. A threshold nuclear level of the v-Rel oncoprotein is required for transformation of avian lymphocytes. Oncogene 1997; 14:2585–2594 [View Article][PubMed]
    [Google Scholar]
  11. Kralova J, Liss AS, Bargmann W, Bose HR Jr. AP-1 factors play an important role in transformation induced by the v-rel oncogene. Mol Cell Biol 1998; 18:2997–3009[PubMed] [Crossref]
    [Google Scholar]
  12. Liss AS, Tiwari R, Kralova J, Bose HR Jr. Cell transformation by v-Rel reveals distinct roles of AP-1 family members in Rel/NF-κB oncogenesis. Oncogene 2010; 29:4925–4937 [View Article][PubMed]
    [Google Scholar]
  13. Hrdlicková R, Nehyba J, Bose HR Jr. Interferon regulatory factor 4 contributes to transformation of v-Rel-expressing fibroblasts. Mol Cell Biol 2001; 21:6369–6386[PubMed] [Crossref]
    [Google Scholar]
  14. Majid SM, Liss AS, You M, Bose HR Jr. The suppression of SH3BGRL is important for v-Rel-mediated transformation. Oncogene 2006; 25:756–768 [View Article][PubMed]
    [Google Scholar]
  15. Tiwari R, Bargmann W, Bose HR Jr. Activation of the TGF-β/smad signaling pathway in oncogenic transformation by v-Rel. Virology 2011; 413:60–71 [View Article][PubMed]
    [Google Scholar]
  16. Hrdlicková R, Nehyba J, Liss AS, Bose HR Jr. Mechanism of telomerase activation by v-Rel and its contribution to transformation. J Virol 2006; 80:281–295 [View Article][PubMed]
    [Google Scholar]
  17. Gupta N, Delrow J, Drawid A, Sengupta AM, Fan G et al. Repression of B-cell linker (BLNK) and B-cell adaptor for phosphoinositide 3-kinase (BCAP) is important for lymphocyte transformation by rel proteins. Cancer Res 2008; 68:808–814 [View Article][PubMed]
    [Google Scholar]
  18. Dutta J, Fan G, Gélinas C. CAPERα is a novel Rel-TAD-interacting factor that inhibits lymphocyte transformation by the potent rel/NF-κB oncoprotein v-Rel. J Virol 2008; 82:10792–10802 [View Article][PubMed]
    [Google Scholar]
  19. Hwang HW, Mendell JT. MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 2006; 94:776–780 [View Article][PubMed]
    [Google Scholar]
  20. Miska EA. How microRNAs control cell division, differentiation and death. Curr Opin Genet Dev 2005; 15:563–568 [View Article][PubMed]
    [Google Scholar]
  21. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E et al. MicroRNA expression in zebrafish embryonic development. Science 2005; 309:310–311 [View Article][PubMed]
    [Google Scholar]
  22. Calame K. MicroRNA-155 function in B cells. Immunity 2007; 27:825–827 [View Article][PubMed]
    [Google Scholar]
  23. Teng G, Papavasiliou FN. Shhh! silencing by microRNA-155. Philos Trans R Soc Lond B Biol Sci 2009; 364:631–637 [View Article][PubMed]
    [Google Scholar]
  24. Mashima R. Physiological roles of miR-155. Immunology 2015; 145:323–333 [View Article][PubMed]
    [Google Scholar]
  25. Vigorito E, Kohlhaas S, Lu D, Leyland R. miR-155: an ancient regulator of the immune system. Immunol Rev 2013; 253:146–157 [View Article][PubMed]
    [Google Scholar]
  26. Clurman BE, Hayward WS. Multiple proto-oncogene activations in avian leukosis virus-induced lymphomas: evidence for stage-specific events. Mol Cell Biol 1989; 9:2657–2664 [View Article][PubMed]
    [Google Scholar]
  27. Tam W, Hughes SH, Hayward WS, 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 [View Article][PubMed]
    [Google Scholar]
  28. Huskova H, Korecka K, Karban J, Vargova J, Vargova K et al. Oncogenic microRNA-155 and its target PU.1: an integrative gene expression study in six of the most prevalent lymphomas. Int J Hematol 2015; 102:441–450 [View Article][PubMed]
    [Google Scholar]
  29. Justice J, Malhotra S, Ruano M, Li Y, Zavala G et al. The MET gene is a common integration target in avian leukosis virus subgroup J-induced chicken hemangiomas. J Virol 2015; 89:4712–4719 [View Article][PubMed]
    [Google Scholar]
  30. Salemi D, Cammarata G, Agueli C, Augugliaro L, Corrado C et al. miR-155 regulative network in FLT3 mutated acute myeloid leukemia. Leuk Res 2015; 39:883–896 [View Article][PubMed]
    [Google Scholar]
  31. Miao J, Bao Y, Ye J, Shao H, Qian K et al. Transcriptional profiling of host gene expression in chicken embryo fibroblasts infected with reticuloendotheliosis virus strain HA1101. PLoS One 2015; 10:e0126992 [View Article][PubMed]
    [Google Scholar]
  32. Yao Y, Zhao Y, Smith LP, Lawrie CH, Saunders NJ et al. Differential expression of microRNAs in Marek's disease virus-transformed T-lymphoma cell lines. J Gen Virol 2009; 90:1551–1559 [View Article][PubMed]
    [Google Scholar]
  33. Bolisetty MT, Dy G, Tam W, Beemon KL. Reticuloendotheliosis virus strain T induces miR-155, which targets JARID2 and promotes cell survival. J Virol 2009; 83:12009–12017 [View Article][PubMed]
    [Google Scholar]
  34. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE et al. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 1998; 26:362–367 [View Article][PubMed]
    [Google Scholar]
  35. Smyth GK. Limma: linear models for microarray data. In Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. et al (editors) Bioinformatics and Computational Biology Solutions Using R and Bioconductor New York: Springer; 2005 pp. 397–420 [Crossref]
    [Google Scholar]
  36. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S et al. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in Eμ-miR155 transgenic mice. Proc Natl Acad Sci USA 2006; 103:7024–7029 [View Article][PubMed]
    [Google Scholar]
  37. Eis PS, Tam W, Sun L, Chadburn A, Li Z et al. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA 2005; 102:3627–3632 [View Article][PubMed]
    [Google Scholar]
  38. Lawrie CH, Soneji S, Marafioti T, Cooper CD, Palazzo S et al. MicroRNA expression distinguishes between germinal center B cell-like and activated B cell-like subtypes of diffuse large B cell lymphoma. Int J Cancer 2007; 121:1156–1161 [View Article][PubMed]
    [Google Scholar]
  39. van den Berg A, Kroesen BJ, Kooistra K, de Jong D, Briggs J et al. High expression of B-cell receptor inducible gene BIC in all subtypes of hodgkin lymphoma. Genes Chromosomes Cancer 2003; 37:20–28 [View Article][PubMed]
    [Google Scholar]
  40. Yin Q, McBride J, Fewell C, Lacey M, Wang X et al. MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol 2008; 82:5295–5306 [View Article][PubMed]
    [Google Scholar]
  41. Tam W, Dahlberg JE. miR-155/BIC as an oncogenic microRNA. Genes Chromosomes Cancer 2006; 45:211–212 [View Article][PubMed]
    [Google Scholar]
  42. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 2007; 104:1604–1609 [View Article][PubMed]
    [Google Scholar]
  43. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007; 316:608–611 [View Article][PubMed]
    [Google Scholar]
  44. Taganov KD, Boldin MP, Baltimore D. MicroRNAs and immunity: tiny players in a big field. Immunity 2007; 26:133–137 [View Article][PubMed]
    [Google Scholar]
  45. Thai TH, Calado DP, Casola S, Ansel KM, Xiao C et al. Regulation of the germinal center response by microRNA-155. Science 2007; 316:604–608 [View Article][PubMed]
    [Google Scholar]
  46. 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 [View Article][PubMed]
    [Google Scholar]
  47. Kong W, Yang H, He L, Zhao JJ, Coppola D et al. MicroRNA-155 is regulated by the transforming growth factor β/smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 2008; 28:6773–6784 [View Article][PubMed]
    [Google Scholar]
  48. Gatto G, Rossi A, Rossi D, Kroening S, Bonatti S et al. Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-κB pathway. Nucleic Acids Res 2008; 36:6608–6619 [View Article][PubMed]
    [Google Scholar]
  49. Lu F, Weidmer A, Liu CG, Volinia S, Croce CM et al. Epstein-Barr virus-induced miR-155 attenuates NF-κB signaling and stabilizes latent virus persistence. J Virol 2008; 82:10436–10443 [View Article][PubMed]
    [Google Scholar]
  50. Jiang J, Lee EJ, Schmittgen TD. Increased expression of microRNA-155 in Epstein-Barr virus transformed lymphoblastoid cell lines. Genes Chromosomes Cancer 2006; 45:103–106 [View Article][PubMed]
    [Google Scholar]
  51. Kluiver J, Haralambieva E, de Jong D, Blokzijl T, Jacobs S et al. Lack of BIC and microRNA miR-155 expression in primary cases of burkitt lymphoma. Genes Chromosomes Cancer 2006; 45:147–153 [View Article][PubMed]
    [Google Scholar]
  52. Yao Y, Zhao Y, Xu H, Smith LP, Lawrie CH et al. MicroRNA profile of Marek's disease virus-transformed T-cell line MSB-1: predominance of virus-encoded microRNAs. J Virol 2008; 82:4007–4015 [View Article][PubMed]
    [Google Scholar]
  53. Zhao Y, Yao Y, Xu H, Lambeth L, Smith LP et al. A functional MicroRNA-155 ortholog encoded by the oncogenic Marek's disease virus. J Virol 2009; 83:489–492 [View Article][PubMed]
    [Google Scholar]
  54. Woźniakowski G, Mamczur A, Samorek-Salamonowicz E. Common occurrence of gallid herpesvirus-2 with reticuloendotheliosis virus in chickens caused by possible contamination of vaccine stocks. J Appl Microbiol 2015; 118:803–808 [View Article][PubMed]
    [Google Scholar]
  55. Woźniakowski G, Samorek-Salamonowicz E, Kozdruń W. Molecular characteristics of Polish field strains of Marek's disease herpesvirus isolated from vaccinated chickens. Acta Vet Scand 2011; 53:10 [View Article][PubMed]
    [Google Scholar]
  56. Sun AJ, Xu XY, Petherbridge L, Zhao YG, Nair V et al. Functional evaluation of the role of reticuloendotheliosis virus long terminal repeat (LTR) integrated into the genome of a field strain of Marek's disease virus. Virology 2010; 397:270–276 [View Article][PubMed]
    [Google Scholar]
  57. Dorsett Y, McBride KM, Jankovic M, Gazumyan A, Thai TH et al. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 2008; 28:630–638 [View Article][PubMed]
    [Google Scholar]
  58. Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T et al. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 2008; 28:621–629 [View Article][PubMed]
    [Google Scholar]
  59. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 2007; 27:847–859 [View Article][PubMed]
    [Google Scholar]
  60. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 2009; 30:80–91 [View Article][PubMed]
    [Google Scholar]
  61. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci USA 2009; 106:2735–2740 [View Article][PubMed]
    [Google Scholar]
  62. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-α stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 2007; 179:5082–5089 [View Article][PubMed]
    [Google Scholar]
  63. Romania P, Lulli V, Pelosi E, Biffoni M, Peschle C et al. MicroRNA 155 modulates megakaryopoiesis at progenitor and precursor level by targeting Ets-1 and Meis1 transcription factors. Br J Haematol 2008; 143:570–580 [View Article][PubMed]
    [Google Scholar]
  64. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R et al. Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein β are targeted by miR-155 in B cells of Eμ-MiR-155 transgenic mice. Blood 2009; 114:1374–1382 [View Article][PubMed]
    [Google Scholar]
  65. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 2009; 106:7113–7118 [View Article][PubMed]
    [Google Scholar]
  66. Liu WH, Kang SG, Huang Z, Wu CJ, Jin HY et al. A miR-155-Peli1-c-Rel pathway controls the generation and function of T follicular helper cells. J Exp Med 2016; 213:1901–1919 [View Article][PubMed]
    [Google Scholar]
  67. Gironella M, Seux M, Xie MJ, Cano C, Tomasini R et al. Tumor protein 53-induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development. Proc Natl Acad Sci USA 2007; 104:16170–16175 [View Article][PubMed]
    [Google Scholar]
  68. Yang J, Zhang P, Krishna S, Wang J, Lin X et al. Unexpected positive control of NFκB and miR-155 by DGKα and ζ ensures effector and memory CD8+ T Cell differentiation. Oncotarget 2016; 7:33744–33764 [View Article][PubMed]
    [Google Scholar]
  69. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65:9628–9632 [View Article][PubMed]
    [Google Scholar]
  70. Mu P, Han YC, Betel D, Yao E, Squatrito M et al. Genetic dissection of the miR-17~92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev 2009; 23:2806–2811 [View Article][PubMed]
    [Google Scholar]
  71. van Haaften G, Agami R. Tumorigenicity of the miR-17-92 cluster distilled. Genes Dev 2010; 24:1–4 [View Article][PubMed]
    [Google Scholar]
  72. Olive V, Jiang I, He L. mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int J Biochem Cell Biol 2010; 42:1348–1354 [View Article][PubMed]
    [Google Scholar]
  73. Nazerian K. An updated list of avian cell lines and transplantable tumours. Avian Pathol 1987; 16:527–544 [View Article][PubMed]
    [Google Scholar]
  74. Akiyama Y, Kato S. Two cell lines from lymphomas of Marek's disease. Biken J 1974; 17:105–116[PubMed]
    [Google Scholar]
  75. Himly M, Foster DN, Bottoli I, Iacovoni JS, Vogt PK. The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 1998; 248:295–304 [View Article][PubMed]
    [Google Scholar]
  76. Hughes SH. The RCAS vector system. Folia Biol 2004; 50:107–119[PubMed]
    [Google Scholar]
  77. Hrdlicková R, Nehyba J, Humphries EH. v-rel induces expression of three avian immunoregulatory surface receptors more efficiently than c-rel. J Virol 1994; 68:308–319[PubMed]
    [Google Scholar]
  78. Yao Y, Zhao Y, Xu H, Smith LP, Lawrie CH et al. Marek's disease virus type 2 (MDV-2)-encoded microRNAs show no sequence conservation with those encoded by MDV-1. J Virol 2007; 81:7164–7170 [View Article][PubMed]
    [Google Scholar]
  79. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004; 20:307–315 [View Article][PubMed]
    [Google Scholar]
  80. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008; 36:D154–D158 [View Article][PubMed]
    [Google Scholar]
  81. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 1995; 57:289–300
    [Google Scholar]
  82. Wu X, Watson M. CORNA: testing gene lists for regulation by microRNAs. Bioinformatics 2009; 25:832–833 [View Article][PubMed]
    [Google Scholar]
  83. Team RC R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria 2014
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