A microRNA Encoded by Kaposi Sarcoma-Associated Herpesvirus Promotes B-Cell Expansion In Vivo

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Dahlke, Christine ^a   Maul, Katrin ^a   Christalla, Thomas ^a   Walz, Nicole ^a   Schult, Philipp ^a   Stocking, Carol ^a   Grundhoff, Adam ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; POLYCOMB GROUP PROTEIN; PROTEIN JARID2; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; GENE SEQUENCE; HEMATOPOIETIC STEM CELL; HUMAN HERPESVIRUS 8; IN VIVO STUDY; LYMPHOCYTE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

ANIMALS; B-LYMPHOCYTES; BONE MARROW CELLS; CELL PROLIFERATION; GENE TRANSFER TECHNIQUES; HEK293 CELLS; HEMATOPOIETIC STEM CELLS; HERPESVIRUS 8, HUMAN; HUMANS; MICE; MICE, INBRED C57BL; MICRORNAS; PLASMIDS; RNA, VIRAL; SARCOMA, KAPOSI;

HUMAN HERPESVIRUS 8; MUS;

EID: 84869856003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049435     Document Type: Article

References (88)

1. Cesarman E, Chang Y, Moore P, Said J, Knowles D, (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 18: 1186-1191.
2. Chang Y, Cesarman E, Pessin M, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science pp. 1865-1869.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
4. Grundhoff A, Ganem D, (2003) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids. J Virol 77: 2779-2783.
5. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, et al. (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A 93: 14862-14867.
6. Ballestas ME, Chatis PA, Kaye KM, (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641-644.
7. Grundhoff A, Ganem D, (2001) Mechanisms governing expression of the v-FLIP gene of Kaposi's sarcoma-associated herpesvirus. J Virol 75: 1857-1863.
8. Hu J, Garber AC, Renne R, (2002) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J Virol 76: 11677-11687.
9. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, et al. (1998) A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 72: 8309-8315.
10. Grundhoff A, Sullivan C, Ganem D, (2006) A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12: 733-750.
11. Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, et al. (2005) Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci U S A 102: 5570-5575.
12. Samols MA, Hu J, Skalsky RL, Renne R, (2005) Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J Virol 79: 9301-9305.
13. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, et al. (2005) Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
14. Pearce M, Matsumura S, Wilson AC, (2005) Transcripts encoding K12, v-FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcoma-associated herpesvirus originate from a common promoter. J Virol 79: 14457-14464.
15. Bartel D, (2004) MicroRNAs: Genomics, Biogenesis, Mechanism, and Function. Cell Press 116: 281-297.
16. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
17. Chi SW, Hannon GJ, Darnell RB, (2012) An alternative mode of microRNA target recognition. Nat Struct Mol Biol 19: 321-327.
18. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, et al. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
19. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, et al. (2011) Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10: 515-526.
20. Grundhoff A, Sullivan C, (2011) Virus-encoded microRNAs. Virology 411: 325-343.
21. Skalsky R, Samols M, Plaisance K, Boss I, Riva A, et al. (2007) Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81: 12836-12845.
22. Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, et al. (2006) Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2: e23.
23. Walz N, Christalla T, Tessmer U, Grundhoff A, (2010) A global analysis of evolutionary conservation among known and predicted gammaherpesvirus microRNAs. J Virol 84: 716-728.
24. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros W, et al. (2007) A viral microRNA functions as an ortholog of cellular miR-155. Nature 450: 1096-1099.
25. Thai T, Calado D, Casola S, Ansel K, Xiao C, et al. (2007) Regulation of the germinal center response by microRNA-155. Science 316: 604-608.
26. Rodriguez A, Vigorito E, Clare S, Warren M, Couttet P, et al. (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316: 608-611.
27. K. C, (2007) MicroRNA-155 function in B Cells. Immunity 6: 825-827.
28. O'Connell R, Rao D, Chaudhuri A, Boldin M, Taganov K, et al. (2008) Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 205: 585-594.
29. Eis P, Tam W, Sun L, Chadburn A, Li Z, et al. (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci 102: 3627-3632.
30. Volinia S, Calin G, Liu C, Ambs S, Cimmino A, et al. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci 103: 2257-2261.
31. Kluiver J, Poppema S, de Jong D, Blokzijl T, Harms G, et al. (2005) BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol 207: 243-249.
32. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, et al. (2006) Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci 103: 7024-7029.
33. Zhao Y, Xu H, Yao Y, Smith L, Kgosana L, et al. (2011) Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek's disease lymphomas. PLoS Pathog 7.
34. Morgan R, Anderson A, Bernberg E, Kamboj S, Huang E, et al. (2008) Sequence conservation and differential expression of Marek's disease virus microRNAs. J Virol 82: 12213-12220.
35. Linnstaedt S, Gottwein E, Skalsky R, Luftig M, Cullen B, (2010) Virally Induced Cellular MicroRNA miR-155 Plays a Key Role in B-Cell Immortalization by Epstein-Barr Virus. J Virol 84: 11670-11678.
36. Cameron J, Fewell C, Yin Q, McBride J, Wang X, et al. (2008) Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382: 257-266.
37. Gatto G, Rossi A, Rossi D, Kroening S, Bonatti S, et al. (2008) Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res 36: 6608-6619.
38. Yin Q, McBride J, Fewell C, Lacey M, Wang X, et al. (2008) MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol 82: 5295-5306.
39. Bolisetty M, Dy G, Tam W, Beemon K, (2009) Reticuloendotheliosis virus strain T induces miR-155, which targets JARID2 and promotes cell survival. J Virol 83: 12009-12017.
40. Panning B, (2010) Fine-tuning silencing. Cell Stem Cell 6: 3-4.
41. Herz HM, Shilatifard A, (2010) The JARID2-PRC2 duality. Genes Dev 24: 857-861.
42. Boss I, Nadeau P, Abbott J, Yang Y, Mergia A, et al. (2011) A Kaposi's sarcoma-associated herpesvirus-encoded ortholog of microRNA miR-155 induces human splenic B-cell expansion in NOD/LtSz-scid IL2Rγnull mice. J Virol 85: 9877-9886.
43. Schwieger M, Löhler J, Friel J, Scheller M, Horak I, et al. (2002) AML1-ETO inhibits maturation of multiple lymphohematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency. J Exp Med 196: 1227-1240.
44. Renne R, Zhong W, Herndier B, McGrath M, Abbey N, et al. (1996) Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med 2: 342-346.
45. DeMars R, Chang CC, Shaw S, Reitnauer PJ, Sondel PM, (1984) Homozygous deletions that simultaneously eliminate expressions of class I and class II antigens of EBV-transformed B-lymphoblastoid cells. I. Reduced proliferative responses of autologous and allogeneic T cells to mutant cells that have decreased expression of class II antigens. Hum Immunol 11: 77-97.
46. Morita S, Kojima T, Kitamura T, (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 12: 1063-1066.
47. Beyer T, Kolowos W, Dumitriu I, Voll R, Heyder P, et al. (2002) Apoptosis of the teratocarcinoma cell line Tera-1 leads to the cleavage of HERV-K10gag proteins by caspases and/or granzyme B. Scand J Immunol 56: 303-309.
48. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
49. Chen C, Ridzon D, Broomer A, Zhou Z, Lee D, et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33.
50. Gatto G, Rossi A, Rossi D, Kroening S, Bonatti S, et al. (2008) Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappaB pathway. Nucleic Acids Res 36: 6608-6619.
51. Jiang J, Lee EJ, Schmittgen TD, (2006) Increased expression of microRNA-155 in Epstein-Barr virus transformed lymphoblastoid cell lines. Genes Chromosomes Cancer 45: 103-106.
52. Kluiver J, Haralambieva E, de Jong D, Blokzijl T, Jacobs S, et al. (2006) Lack of BIC and microRNA miR-155 expression in primary cases of Burkitt lymphoma. Genes Chromosomes Cancer 45: 147-153.
53. Kluiver J, van den Berg A, de Jong D, Blokzijl T, Harms G, et al. (2007) Regulation of pri-microRNA BIC transcription and processing in Burkitt lymphoma. Oncogene 26: 3769-3776.
54. Linnstaedt SD, Gottwein E, Skalsky RL, Luftig MA, Cullen BR, (2010) Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus. J Virol 84: 11670-11678.
55. Lu F, Weidmer A, Liu CG, Volinia S, Croce CM, et al. (2008) Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J Virol 82: 10436-10443.
56. Rahadiani N, Takakuwa T, Tresnasari K, Morii E, Aozasa K, (2008) Latent membrane protein-1 of Epstein-Barr virus induces the expression of B-cell integration cluster, a precursor form of microRNA-155, in B lymphoma cell lines. Biochem Biophys Res Commun 377: 579-583.
57. Xu G, Fewell C, Taylor C, Deng N, Hedges D, et al. (2010) Transcriptome and targetome analysis in MIR155 expressing cells using RNA-seq. RNA 16: 1610-1622.
58. Hardy R, Kincade P, Dorshkind K, (2007) The Protean Nature of Cells in the B Lymphocyte Lineage. Cell Press 26: 703-714.
59. Liu J, van Mil A, Vrijsen K, Zhao J, Gao L, et al. (2011) MicroRNA-155 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J Cell Mol Med 15: 1474-1482.
60. Burnside J, Morgan R, (2011) Emerging roles of chicken and viral microRNAs in avian disease. BMC Proc 5.
61. Thorley-Lawson DA, (2001) Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75-82.
62. Kalla M, Hammerschmidt W, (2012) Human B cells on their route to latent infection-early but transient expression of lytic genes of Epstein-Barr virus. Eur J Cell Biol 91: 65-69.
63. Roughan JE, Thorley-Lawson DA, (2009) The intersection of Epstein-Barr virus with the germinal center. J Virol 83: 3968-3976.
64. Vrazo AC, Chauchard M, Raab-Traub N, Longnecker R, (2012) Epstein-Barr virus LMP2A reduces hyperactivation induced by LMP1 to restore normal B cell phenotype in transgenic mice. PLoS Pathog 8: e1002662.
65. Yin Q, McBride J, Fewell C, Lacey M, Wang X, et al. (2008) MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol 82: 5295-5306.
66. Vigorito E, Perks K, Abreu-Goodger C, Bunting S, Xiang Z, et al. (2007) microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27.
67. Bender T, Thompson C, Kuehl W, (1987) Differential expression of c-myb mRNA in murine B lymphomas by a block to transcription elongation. Science 237: 1473-1476.
68. Thomas MD, Kremer CS, Ravichandran KS, Rajewsky K, Bender TP, (2005) c-Myb is critical for B cell development and maintenance of follicular B cells. Immunity 23: 275-286.
69. Liebermann DA, Hoffman B, (1994) Differentiation primary response genes and proto-oncogenes as positive and negative regulators of terminal hematopoietic cell differentiation. Stem Cells 12: 352-369.
70. Gonda TJ, Metcalf D, (1984) Expression of myb, myc and fos proto-oncogenes during the differentiation of a murine myeloid leukaemia. Nature 310: 249-251.
71. Greig KT, de Graaf CA, Murphy JM, Carpinelli MR, Pang SH, et al. (2010) Critical roles for c-Myb in lymphoid priming and early B-cell development. Blood 115: 2796-2805.
72. Imig J, Motsch N, Zhu J, Barth S, Okoniewski M, et al. (2011) microRNA profiling in Epstein-Barr virus-associated B-cell lymphoma. Nucleic Acids Res 39: 1880-1893.
73. Zhang Z, Jones A, Sun C, Li C, Chang C, et al. (2011) PRC2 complexes with JARID2, MTF2, and esPRC2p48 in ES cells to modulate ES cell pluripotency and somatic cell reprogramming. Stem Cells 29: 229-240.
74. Li G, Margueron R, Ku M, Chambon P, Bernstein B, et al. (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev pp. 368-380.
75. Majewski IJ, Ritchie ME, Phipson B, Corbin J, Pakusch M, et al. (2010) Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells. Blood 116: 731-739.
76. Richie ER, Schumacher A, Angel JM, Holloway M, Rinchik EM, et al. (2002) The Polycomb-group gene eed regulates thymocyte differentiation and suppresses the development of carcinogen-induced T-cell lymphomas. Oncogene 21: 299-306.
77. Lessard J, Schumacher A, Thorsteinsdottir U, van Lohuizen M, Magnuson T, et al. (1999) Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation. Genes Dev 13: 2691-2703.
78. Martin-Perez D, Piris MA, Sanchez-Beato M, (2010) Polycomb proteins in hematologic malignancies. Blood 116: 5465-5475.
79. Margueron R, Reinberg D, (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
80. Richly H, Aloia L, Di Croce L, (2011) Roles of the Polycomb group proteins in stem cells and cancer. Cell Death Dis 2: e204.
81. Gunther T, Grundhoff A, (2010) The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog 6: e1000935.
82. Herz HM, Mohan M, Garrett AS, Miller C, Casto D, et al. (2012) Polycomb repressive complex 2-dependent and-independent functions of Jarid2 in transcriptional regulation in Drosophila. Mol Cell Biol 32: 1683-1693.
83. Peng JC, Valouev A, Swigut T, Zhang J, Zhao Y, et al. (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139: 1290-1302.
84. Shen X, Kim W, Fujiwara Y, Simon MD, Liu Y, et al. (2009) Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139: 1303-1314.
85. Li G, Margueron R, Ku M, Chambon P, Bernstein BE, et al. (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev 24: 368-380.
86. Puda A, Milosevic JD, Berg T, Klampfl T, Harutyunyan AS, et al. (2012) Frequent deletions of JARID2 in leukemic transformation of chronic myeloid malignancies. Am J Hematol 87: 245-250.
87. Score J, Hidalgo-Curtis C, Jones AV, Winkelmann N, Skinner A, et al. (2012) Inactivation of polycomb repressive complex 2 components in myeloproliferative and myelodysplastic/myeloproliferative neoplasms. Blood 119: 1208-1213.
88. Toyoda M, Kojima M, Takeuchi T, (2000) Jumonji is a nuclear protein that participates in the negative regulation of cell growth. Biochem Biophys Res Commun 274: 332-336.