Loss of microRNA targets in the 3′ untranslated region as a mechanism of retroviral insertional activation of growth factor independence 1

Journal of Virology

Volumn 83, Issue 16, 2009, Pages 8051-8061

  Dabrowska, Magdalena Julia ^a,b   Dybkaer, Karen ^a,b   Johnsen, Hans Erik ^a   Wang, Bruce ^c   Wabl, Matthias ^d   Pedersen, Finn Skou ^b  

^a AALBORG UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c Picobella   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; ONCOPROTEIN; PROTEIN GROWTH DIFFERENTIATION FACTOR 7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE INSERTION; GENE LOCUS; GENOME; HIGH THROUGHPUT SCREENING; LATENT PERIOD; MESENTERY LYMPH NODE; MOUSE; MURINE LEUKEMIA VIRUS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; RETROVIRUS; RNA SPLICING; SPLEEN CANCER; T CELL LYMPHOMA; THYMUS CANCER; TRANSCRIPTION INITIATION; UNTRANSLATED REGION; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; DNA-BINDING PROTEINS; LEUKEMIA VIRUS, MURINE; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; RETROVIRIDAE INFECTIONS; RNA SPLICING; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION; VIRUS INTEGRATION;

MURINE LEUKEMIA VIRUS; MUS;

EID: 67749106479     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00427-09     Document Type: Article

References (82)

1. Ben-David, Y., E. B. Giddens, K. Letwin, and A. Bernstein. 1991. Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes Dev. 6:908-918.
2. Brennecke, J., A. Stark, R. B. Russell, and S. M. Cohen. 2005. Principles of microRNA-target recognition. PLoS Biol. 3:e85-e99.
3. Celander, D., and W. A. Haseltine. 1987. Glucocorticoid regulation of murine leukemia virus transcription elements is specified by determinants within the viral enhancer region. J. Virol. 61:269-275.
4. Chakraborty, J., H. Okonta, H. Bagalb, S. J. Lee, B. Fink, R. Changanamkandat, and J. Duggan. 2008. Retroviral gene insertion in breast milk mediated lymphomagenesis. Virology 377:100-109.
5. Chatis, P. A., C. A. Holland, J. W. Hartley, W. P. Rowe, and N. Hopkins. 1983. Role for the 3′ end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses. Proc. Natl. Acad. Sci. USA 80:4408-4411.
6. Corcoran, L. M., J. M. Adams, A. R. Dunn, and S. Cory. 1984. Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion. Cell 37:113-122.
7. Costa, I. G., S. Roepcke, and A. Schliep. 2007. Gene expression trees in lymphoid development. BMC Immunol. 8:25-44.
8. Cuypers, H. T., G. Selten, W. Quint, M. Zijlstra, E. R. Maandag, W. Boelens, P. van Wezenbeek, C. Melief, and A. Berns. 1984. Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell 37:141-150.
9. DesGroseillers, L., and P. Jolicoeur. 1984. The tandem direct repeats within the long terminal repeat of murine leukemia viruses are primary determinant of their leukemogenic potential. J. Virol. 52:945-952.
10. Dickson, C., R. Smith, S. Brookes, and G. Peters. 1990. Proviral insertions within the int-2 gene can generate multiple anomalous transcripts but leave the protein-coding domain intact. J. Virol. 64:784-793.
11. Didiano, D., and O. Hobert. 2006. Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat. Struct. Mol. Biol. 13:849-851.
12. Didiano, D., and O. Hobert. 2008. Molecular architecture of a miRNA-regulated 3′UTR. RNA 14:1297-1317.
13. Doench, J. G., C. P. Petersen, and P. A. Sharp. 2003. siRNAs can function as miRNAs. Genes Dev. 17:438-442.
14. Doench, J. G., and P. A. Sharp. 2004. Specificity of microRNA target selection in translational repression. Genes Dev. 18:504-511.
15. Dwivedi, P. P., P. H. Anderson, J. L. Omdahl, H. L. Grimes, H. A. Morris, and B. K. May. 2005. Identification of growth factor independent-1 (GFI1) as a repressor of 25-hydroxyvitamin D 1-alpha hydroxylase (CYP27B1) gene expression in human prostate cancer cells. Endocrinol. Relat. Cancer 12:351-365.
16. Eis, P. S., W. Tam, L. Sun, A. Chadburn, Z. Li, M. F. Gomez, E. Lund, and J. E. Dahlberg. 2005. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. USA 102:3627-3632.
17. Ejegod, D., K. D. Sørensen, I. Mossbrugger, L. Quintanilla-Martinez, J. Schmidt, and F. S. Pedersen. 2009. Control of pathogenicity and disease specificity of a T-cell lymphomagenic gammaretrovirus by E-box motifs but not by an overlapping glucocorticoid response element. J. Virol. 83:336-346.
18. Ethelberg, S., B. Hallberg, J. Lovmand, J. Schmidt, A. Luz, T. Grundström, and F. S. Pedersen. 1997. Second-site proviral enhancer alterations in lymphomas induced by enhancer mutants of SL3-3 murine leukemia virus: negative effects of nuclear factor 1 binding site. J. Virol. 71:1196-1206.
19. Ethelberg, S., J. Lovmand, J. Schmidt, A. Luz, and F. S. Pedersen. 1997. Increased lymphomagenicity and restored disease specificity of AML1 site (core) mutant SL3-3 murine leukemia virus by a second-site enhancer variant evolved in vivo. J. Virol. 71:7273-7280.
20. Ethelberg, S., A. B. Sørensen, J. Schmidt, A. Luz, and F. S. Pedersen. 1997. An SL3-3 murine leukemia virus enhancer variant more pathogenic than the wild type obtained by assisted molecular evolution in vivo. J. Virol. 71:9796-9799.
21. Fan, H., B. K. Brightman, B. R. Davis, and Q. X. Li. 1991. Leukemogenesis by Moloney murine leukemia virus, p. 155-174. In H. Y. Fan et al. (ed.), Viruses that affect the immune system. American Society for Microbiology, Washington, DC.
22. Gilks, C. B., S. E. Bear, H. L. Grimes, and P. N. Tsichlis. 1993. Progression of interleukin-2 (IL-2)-dependent rat T-cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein. Mol. Cell. Biol. 13:1759-1768.
23. Gimbel, W., J. Schmidt, J. Barack-Werner, A. Luz, P. G. Strauss, V. Erfle, and T. Werner. 1996. Molecular and pathogenic characterization of the RFB osteoma virus: lack of oncogene and induction of osteoma, osteopetrosis and lymphoma. Virology 224:533-538.
24. Golemis, E. A., N. A. Speck, and N. Hopkins. 1990. Alignment of U3 region sequences of mammalian type C viruses: identification of highly conserved motifs and implications for enhancer design. J. Virol. 64:534-542.
25. Grimes, H. L., T. O. Chan, P. A. Zweidler-McKay, B. Tong, and P. N. Tsichlis. 1996. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16:6263-6272.
26. Grimes, H. L., C. B. Gilks, T. O. Chan, S. Porter, and P. N. Tsichlis. 1996. The Gfi-1 protooncoprotein represses Bax expression and inhibits T-cell death. Proc. Natl. Acad. Sci. USA 93:14569-14573.
27. Hallberg, B., J. Schmidt, A. Luz, F. S. Pedersen, and T. Grundström. 1991. SL3-3 enhancer factor I transcriptional activators are required for tumor formation by SL3-3 murine leukemia virus. J. Virol. 65:4177-4181.
28. Hayward, W. S., B. G. Neel, and S. M. Astrin. 1981. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290:475-480.
29. Hock, H., M. J. Hamblen, H. M. Rooke, J. W. Schindler, S. Saleque, Y. Fujiwara, and S. H. Orkin. 2004. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431:1002-1007.
30. Hwang, H. C., C. P. Martins, Y. Bronkhorst, E. Randel, A. Berns, M. Fero, and B. E. Clurman. 2002. Identification of oncogenes collaborating with p27kip1 loss by insertional mutagenesis and high-throughput insertion site analysis. Proc. Natl. Acad. Sci. USA 99:11293-11298.
31. Karsunky, H., H. Zeng, T. Schmidt, B. Zevnik, R. Kluge, K. W. Schmid, U. Dührsen, and T. Möröy. 2002. Inflamatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat. Genet. 30:295-300.
32. Kazanjian, A., D. Wallis, N. Au, R. Nigam, K. J. T. Venken, P. T. Cagle, B. F. Dickey, H. J. Bellen, C. B. Gilks, and H. L. Grimes. 2004. Growth factor independence-1 is expressed in primary human neuroendocrine lung carcinomas and mediates the differentiation of murine pulmonary neuroendocrine cells. Cancer Res. 64:6874-6882.
33. Kertesz, M., N. Iovino, U. Unnerstall, U. Gaul, and E. Segal. 2007. The role of site accessibility in miRNA target recognition. Nat. Genet. 39:1278-1284.
34. Kim, R., A. Trubetskoy, T. Suzuki, N. A. Jenkins, N. G. Copeland, and J. Lenz. 2003. Genome-based identification of cancer genes by proviral tagging in mouse retrovirus-induced T-cell lymphomas. J. Virol. 77:2056-2062.
35. Landais, S., S. Landry, P. Legault, and E. Rassart. 2007. Oncogenic potential of the miR-106-363 cluster and its implication in human T-cell leukemia. Cancer Res. 67:5699-5707.
36. Lee, R. C., R. L. Feinbaum, and V. Ambros. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843-854.
37. Lenz, J., D. Celander, R. L. Crowther, R. Patarca, D. W. Perkins, and W. A. Haseltine. 1984. Determination of the leukaemogenicity of a murine retrovirus by sequences within the long terminal repeat. Nature 308:467-470.
38. Lewis, A. F., T. Stacy, W. R. Green, L. Taddesse-Heath, J. W. Hartley, and N. A. Speck. 1999. Core-binding factor influences the disease specificity of Moloney murine leukemia virus. J. Virol. 73:5535-5547.
39. Lewis, B. P., C. B. Burge, and D. P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
40. Liao, X., A. M. Buchberg, N. A. Jenkins, and N. G. Copeland. 1995. Evi-5, a common site of retroviral integration in AKXD T-cell lymphomas, maps near Gfi1 on mouse chromosome 5. J. Virol. 69:7132-7137.
41. Lim, L. P., N. C. Lau, P. Garrett-Engele, A. Grimson, J. M. Schelter, J. Castle, D. P. Bartel, P. S. Linsley, and J. M. Johnson. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769-773.
42. Long, D., R. Lee, P. Williams, C. Y. Chan, V. Ambros, and Y. Ding. 2007. Potent effect of target structure on microRNA function. Nat. Struct. Mol. Biol. 14:287-294.
43. Lovmand, J., A. B. Sørensen, J. Schmidt, M. ∅stergaard, A. Luz, and F. S. Pedersen. 1998. B-cell lymphoma induction by Akv murine leukemia viruses harboring one or both copies of the tandem repeat in the U3 enhancer. J. Virol. 72:5745-5756.
44. Lund, A. H., G. Turner, A. Trubetskoy, E. Verhoeven, E. Wientjens, D. Hulsman, R. Russell, R. A. DePinho, J. Lenz, and M. van Lohuizen. 2002. Genome-wide retroviral insertional tagging of genes involved in cancer in Cdkn2a-deficient mice. Nat. Genet. 32:160-165.
45. Ma, S. L., J. Lovmand, A. B. Sørensen, A. Luz, J. Schmidt, and F. S. Pedersen. 2003. Triple basepair changes within and adjacent to the conserved YY1 motif upstream of the U3 enhancer repeats of SL3-3 murine leukemia virus cause a small but significant shortening of latency of T-lymphoma induction. Virology 313:638-644.
46. Mead, R. S., and J. K. Cowell. 1995. Molecular characterization of a (1; 10)(p22;q21) constitutional translocation from a patient with neuroblastoma. Cancer Genet. Cytogenet. 81:151-157.
47. Merkerova, M., M. Belickova, and H. Bruchova. 2008. Differential expression of microRNA in hematopoietic cell lineages. Eur. J. Haematol. 81:304-310.
48. Mikkers, H., J. Allen, P. Knipscheer, L. Romeijn, A. Hart, E. Vink, and A. Berns. 2002. High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat. Genet. 32:153-159.
49. Morse, H. C., III, M. R. Anver, T. N. Fredrickson, D. C. Haines, A. W. Harris, N. L. Harris, E. S. Jaffe, S. C. Kogan, I. C. MacLennan, P. K. Pattengale, and J. M. Ward. 2002. Hematopathology subcommittee of the Mouse Models of Human Cancers Consortium. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 100:246-258.
50. Nielsen, A. L., P. L. Nørby, F. S. Pedersen, and P. J.ørgensen. 1996. Various models of basic helix-loop-helix protein-mediated regulation of murine leukemia virus transcription in lymphoid cells. J. Virol. 70:5893-5901.
51. Nielsen, A. A., A. B. Sørensen, J. Schmidt, and F. S. Pedersen. 2005. Analysis of wild-type and mutant SL3-3 murine leukemia virus insertions in the c-myc promoter during lymphomagenesis reveals target site hot spots, virus-dependent patterns, and frequent error-prone gap repair. J. Virol. 79:67-78.
52. Nieves, A., L. S. Levy, and J. Lenz. 1997. Importance of a c-Myb binding site for lymphomagenesis by the retrovirus SL3-3. J. Virol. 71:1213-1219.
53. Nusse, R., and H. E. Varmus. 1982. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31:99-109.
54. + T lymphocyte function. Eur. J. Immunol. 37:3551-3563.
55. Rasmussen, M. H., A. B. Sørensen, D. W. Morris, J. C. Dutra, E. K. Engelhard, C. L. Wang, J. Schmidt, and F. S. Pedersen. 2005. Tumor model-specific proviral insertional mutagenesis of the Fos/Jdp2/Batf locus. Virology 337:353-364.
56. Rathinam, C., H. Lassmann, M. Mengel, and C. Klein. 2008. Transcription factor Gfi1 restricts B-cell mediated autoimmunity. J. Immunol. 181:6222-6229.
57. Rathinam, C., and C. Klein. 2007. Transcriptional repressor Gfi1 integrates cytokine-receptor signals controlling B-cell differentiation. PLoS ONE 2:e306-e317.
58. Roberts, T., and J. K. Cowell. 1997. Cloning of the human Gfi-1 gene and its mapping to chromosome region 1p22. Oncogene 14:1003-1005.
59. Sakai, I., H. Yamauchi, M. Yasukawa, H. Kohno, and S. Fujita. 2001. Expression of the Gfi-1 gene in HTLV-I-transformed T cells. Int. J. Hematol. 73:507-516.
60. Salaverria, I., B. Espinet, A. Carrió, D, Costa, L, Astier, J. Slotta-Huspenina, L, Quintanilla-Martinez, F. Fend, F. Solé, D. Colomer, S. Serrano, R. Miró, S. Beà, and E. Campo. 2008. Multiple recurrent chromosomal breakpoints in mantle cell lymphoma revealed by a combination of molecular cytogenetic techniques. Genes Chromosomes Cancer 47:1086-1097.
61. Sander, S., L. Bullinger, E. Leupolt, A. Benner, D. Kienle, T. Katzenberger, J. Kalla, G. Ott, H. K. Müller-Hermelink, T. F. Barth, P. Möller, P. Lichter, H. Döhner, and S. Stilgenbauer. 2008. Genomic aberrations in mantle cell lymphoma detected by interphase fluorescence in situ hybridization. Incidence and clinicopathological correlations. Haematologica 93:680-687.
62. Scheijen, B., J. Jonkers, D. Acton, and A. Berns. 1997. Characterization of pal-1, a common proviral insertion site in murine leukemia virus-induced lymphomas of c-myc and pim-1 transgenic mice. J. Virol. 71:9-16.
63. Schmidt, J., K. Lumniczky, B. D. Tzschaschel, H. L. Guenther, A. Luz, S. Riemann, W. Gimbel, V. Erfle, and R. G. Erben. 1999. Onset and dynamics of osteosclerosis in mice induced by Reilly-Finkel-Biskis (RFB) murine leukemia virus. Am. J. Pathol. 155:557-570.
64. Schmidt, T., H. Karsunky, B. Rödel, B. Zevnik, H-P. Elsässer, and T. Möröy. 1998. Evidence implicating Gfi-1 and Pim-1 in pre-T-cell differentiation steps associated with β-selection. EMBO J. 17:5349-5359.
65. Schmidt, T., M. Zörnig, R. Benke, and T. Möröy. 1996. MoMuLV proviral integrations identified by Sup-F selection in tumors from infected myc/pim bitransgenic mice correlate with activation of the gfi-1 gene. Nucleic Acids Res. 24:2528-2534.
66. Selten, G. H., H. T. Cuypers, and A. Berns. 1985. Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J. 4:1793-1798.
67. Selten, G. H., H. T. Cuypers, M. Zijlstra, C. Melief, and A. Berns. 1984. Involvement of c-Myc in T cell lymphomas in mice: frequency and mechanism of activation. EMBO J. 3:3215-3222.
68. Shin, M. S., T. N. Fredrickson, J. W. Hartley, T. Suzuki, K. Akagi, and H. C. Morse III. 2004. High-throughput retroviral tagging for identification of genes involved in initiation and progression of mouse splenic marginal zone lymphomas. Cancer Res. 64:4419-4427.
69. Sørensen, K. D., S. Kunder, L. Quintanilla-Martinez, J. Sørensen, J. Schmidt, and F. S. Pedersen. 2007. Enhancer mutations of Akv murine leukemia virus inhibit the induction of mature B-cell lymphomas and shift disease specificity towards the more differentiated plasma cell stage. Virology 362:179-191.
70. Sørensen, K. D., L. Quintanilla-Martinez, S. Kunder, J. Schmidt, and F. S. Pedersen. 2004. Mutation of all Runx (AML1/core) sites in the enhancer of T-lymphomagenic SL3-3 murine leukemia virus unmasks a significant potential for myeloid leukemia induction and favors enhancer evolution toward induction of other disease patterns. J. Virol. 78:13216-13231.
71. Speck, N. A., B. Renjifo, E. Golemis, T. N. Fredrickson, J. W. Hartley, and N. Hopkins. 1990. Mutation of the core or adjacent LVb elements of the Moloney murine leukemia virus enhancer alters disease specificity. Genes Dev. 4:233-242.
72. Suzuki, T., K. Minehata, K. Agaki, N. A. Jenkins, and N. G. Copeland. 2006. Tumor suppressor gene identification using retroviral insertional mutagenesis in Blm-deficient mice. EMBO J. 25:3422-3431.
73. Suzuki, T., H. Shen, K. Akagi, H. C. Morse, J. D. Malley, D. Q. Naiman, N. A. Jenkins, and N. G. Copeland. 2002. New genes involved in cancer identified by retroviral tagging. Nat. Genet. 32:166-174.
74. Tam, W., D. Ben-Yehuda, and W. S. Hayward. 1997. bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Mol. Cell. Biol. 17:1490-1502.
75. Tsichlis, P. N., and P. A. Lazo. 1991. Virus-host interactions and the pathogenesis of murine and human oncogenic retroviruses. Curr. Top. Microbiol. Immunol. 171:95-173.
76. Uren, A. G., J. Kool, K. Matentzoglu, J. de Ridder, J. Mattison, M. van Uitert, W. Lagcher, D. Sie, E. Tanger, T. Cox, M. Reinders, T. J. Hubbard, J. Rogers, J. Jonkers, L. Wessels, D. J. Adams, M. van Lohuizen, and A. Berns. 1998. Large-scale mutagenesis in p19ARF- and p53-deficient mice identifies cancer genes and their collaborative networks. Cell 133:727-741.
77. Vega, F., and L. J. Medeiros. 2001. Marginal-zone B-cell lymphoma of extranodal mucosa-associated lymphoid tissue type: molecular genetics provides new insights into pathogenesis. Adv. Anat. Pathol. 8:313-326.
78. Wang, C. L., B. B. Wang, G. Bartha, L. Li, N. Channa, M. Klinger, N. Killeen, and M. Wabl. 2006. Activation of an oncogenic microRNA cistron by provirus integration. Proc. Natl. Acad. Sci. USA 103:18680-18684.
79. Wingett, D., R. Reeves, and N. S. Magnuson. 1992. Characterization of the testes-specific pim-1 transcript in rat. Nucleic Acids Res. 20:3183-3189.
80. Yücel, R., H. Karsunky, L. Klein-Hitpass, and T. Möröy. 2003. The transcriptional repressor Gfi1 affects development of early uncommitted c-kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J. Exp. Med. 197:831-844.
81. Yücel, R., C. Kosan, F. Heyd, and T. Möröy. 2004. Gfi1:Green fluorescent protein knock-in mutant reveals different expression and autoregulation of the growth factor independence 1 (Gfi1) gene during lymphocyte development. J. Biol. Chem. 279:40906-40917.
82. Zeng, H., R. Yücel, C. Kosan, L. Klein-Hitpass, and T. Möröy. 2004. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO J. 23:4116-4125.