Antisense transcription in gammaretroviruses as a mechanism of insertional activation of host genes

Journal of Virology

Volumn 84, Issue 8, 2010, Pages 3780-3788

  Rasmussen, Mads Heilskov ^a   Ballarín González, Borja ^a   Liu, Jinghua ^a   Lassen, Louise Berkhoudt ^a   Füchtbauer, Annette ^a   Füchtbauer, Ernst Martin ^a   Nielsen, Anders Lade ^a   Pedersen, Finn Skou ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; COMPLEMENTARY RNA; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; B CELL LYMPHOMA; BACH2 GENE; GENE ACTIVATION; GENE AMPLIFICATION; GENE IDENTIFICATION; GENE INSERTION; GENE SEQUENCE; JDP2 GENE; MOUSE; MURINE LEUKEMIA VIRUS; NONHUMAN; NRAS GENE; PRIORITY JOURNAL; PROTO ONCOGENE; RETROVIRUS; T CELL LYMPHOMA; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; PROVIRUS; TRANSCRIPTION INITIATION SITE; VIRUS GENE;

EUKARYOTA; MURINE LEUKEMIA VIRUS;

ANIMALS; GENES, VIRAL; LEUKEMIA VIRUS, MURINE; MICE; MUTAGENESIS, INSERTIONAL; PROVIRUSES; RNA, ANTISENSE; RNA, VIRAL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 77950481763     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02088-09     Document Type: Article

References (53)

1. Akagi, K., T. Suzuki, R. M. Stephens, N. A. Jenkins, and N. G. Copeland. 2004. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 32: D523-D527.
2. Arnold, J., B. Yamamoto, M. Li, A. J. Phipps, I. Younis, M. D. Lairmore, and P. L. Green. 2006. Enhancement of infectivity and persistence in vivo by HBZ, a natural antisense coded protein of HTLV-1. Blood 107: 3976-3982.
3. Arnold, J., B. Zimmerman, M. Li, M. D. Lairmore, and P. L. Green. 2008. Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood 112: 3788-3797.
4. Audit, M., J. Dejardin, B. Hohl, C. Sidobre, T. J. Hope, M. Mougel, and M. Sitbon. 1999. Introduction of a cis-acting mutation in the capsid-coding gene of moloney murine leukemia virus extends its leukemogenic properties. J. Virol. 73: 10472-10479.
5. Birney, E., J. A. Stamatoyannopoulos, A. Dutta, R. Guigo, T. R. Gingeras, E. H. Margulies, Z. Weng, M. Snyder, E. T. Dermitzakis, R. E. Thurman, M. S. Kuehn, C. M. Taylor, S. Neph, C. M. Koch, S. Asthana, A. Malhotra, I. Adzhubei, J. A. Greenbaum, R. M. Andrews, P. Flicek, P. J. Boyle, H. Cao, N. P. Carter, G. K. Clelland, S. Davis, N. Day, P. Dhami, S. C. Dillon, M. O. Dorschner, H. Fiegler, P. G. Giresi, J. Goldy, M. Hawrylycz, A. Haydock, R. Humbert, K. D. James, B. E. Johnson, E. M. Johnson, T. T. Frum, E. R. Rosenzweig, N. Karnani, K. Lee, G. C. Lefebvre, P. A. Navas, F. Neri, S. C. Parker, P. J. Sabo, R. Sandstrom, A. Shafer, D. Vetrie, M. Weaver, S. Wilcox, M. Yu, F. S. Collins, J. Dekker, J. D. Lieb, T. D. Tullius, G. E. Crawford, S. Sunyaev, W. S. Noble, I. Dunham, F. Denoeud, A. Reymond, P. Kapranov, J. Rozowsky, D. Zheng, R. Castelo, A. Frankish, J. Harrow, S. Ghosh, A. Sandelin, I. L. Hofacker, R. Baertsch, D. Keefe, S. Dike, J. Cheng, H. A. Hirsch, E. A. Sekinger, J. Lagarde, J. F. Abril, A. Shahab, C. Flamm, C. Fried, J. Hackermuller, J. Hertel, M. Lindemeyer, K. Missal, A. Tanzer, S. Washietl, J. Korbel, O. Emanuelsson, J. S. Pedersen, N. Holroyd, R. Taylor, D. Swarbreck, N. Matthews, M. C. Dickson, D. J. Thomas, M. T. Weirauch, J. Gilbert, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
6. Briquet, S., J. Richardson, C. Vanhee-Brossollet, and C. Vaquero. 2001. Natural antisense transcripts are detected in different cell lines and tissues of cats infected with feline immunodeficiency virus. Gene 267: 157-164.
7. Carninci, P., A. Sandelin, B. Lenhard, S. Katayama, K. Shimokawa, J. Ponjavic, C. A. Semple, M. S. Taylor, P. G. Engstrom, M. C. Frith, A. R. Forrest, W. B. Alkema, S. L. Tan, C. Plessy, R. Kodzius, T. Ravasi, T. Kasukawa, S. Fukuda, M. Kanamori-Katayama, Y. Kitazume, H. Kawaji, C. Kai, M. Nakamura, H. Konno, K. Nakano, S. Mottagui-Tabar, P. Arner, A. Chesi, S. Gustincich, F. Persichetti, H. Suzuki, S. M. Grimmond, C. A. Wells, V. Orlando, C. Wahlestedt, E. T. Liu, M. Harbers, J. Kawai, V. B. Bajic, D. A. Hume, and Y. Hayashizaki. 2006. Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 38: 626-635.
8. Cavanagh, M. H., S. Landry, B. Audet, C. Arpin-Andre, P. Hivin, M. E. Pare, J. Thete, E. Wattel, S. J. Marriott, J. M. Mesnard, and B. Barbeau. 2006. HTLV-I antisense transcripts initiating in the 3'LTR are alternatively spliced and polyadenylated. Retrovirology 3: 15.
9. Choi, S. Y., and D. V. Faller. 1995. A transcript from the long terminal repeats of a murine retrovirus associated with trans activation of cellular genes. J. Virol. 69: 7054-7060.
10. Dabrowska, M. J., K. Dybkaer, H. E. Johnsen, B. Wang, M. Wabl, and F. S. Pedersen. 2009. Loss of microRNA targets in the 3'-untranslated region as a mechanism of retroviral insertional activation of growth factor independence 1. J. Virol. 83: 8051-8061.
11. Dejardin, J., G. Bompard-Marechal, M. Audit, T. J. Hope, M. Sitbon, and M. Mougel. 2000. A novel subgenomic murine leukemia virus RNA transcript results from alternative splicing. J. Virol. 74: 3709-3714.
12. Ejegod, D., K. D. Sorensen, I. Mossbrugger, L. Quintanilla-Martinez, J. Schmidt, and F. S. Pedersen. 2009. Control of pathogenicity and disease specificity of a T-lymphomagenic gammaretrovirus by E-box motifs but not by an overlapping glucocorticoid response element. J. Virol. 83: 336-346.
13. Fejes-Toth, K., V. Sotirova, R. Sachidanandam, G. Assaf, G. J. Hannon, P. Kapranov, S. Foissac, A. T. Willingham, R. Duttagupta, E. Dumais, T. R. Gingeras, et al. 2009. Post-transcriptional processing generates a diversity of 5'-modified long and short RNAs. Nature 457: 1028-1032.
14. Forman, L. W., R. Pal-Ghosh, R. A. Spanjaard, D. V. Faller, and S. K. Ghosh. 2009. Identification of LTR-specific small non-coding RNA in FeLV infected cells. FEBS Lett. 583: 1386-1390.
15. Gaudray, G., F. Gachon, J. Basbous, M. Biard-Piechaczyk, C. Devaux, and J. M. Mesnard. 2002. The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J. Virol. 76: 12813-12822.
16. Ghosh, S. K., and D. V. Faller. 1999. Feline leukemia virus long terminal repeat activates collagenase IV gene expression through AP-1. J. Virol. 73: 4931-4940.
17. Girard, L., Z. Hanna, N. Beaulieu, C. D. Hoemann, C. Simard, C. A. Kozak, and P. Jolicoeur. 1996. Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis. Genes Dev. 10: 1930-1944.
18. Gramberg, T., N. Sunseri, and N. R. Landau. 2009. Accessories to the crime: recent advances in HIV accessory protein biology. Curr. HIV/AIDS Rep. 6: 36-42.
19. Hallberg, B., J. Schmidt, A. Luz, F. S. Pedersen, and T. Grundstrom. 1991. SL3-3 enhancer factor 1 transcriptional activators are required for tumor formation by SL3-3 murine leukemia virus. J. Virol. 65: 4177-4181.
20. Kashanchi, F., and J. N. Brady. 2005. Transcriptional and post-transcriptional gene regulation of HTLV-1. Oncogene 24: 5938-5951.
21. Lakso, M., J. G. Pichel, J. R. Gorman, B. Sauer, Y. Okamoto, E. Lee, F. W. Alt, and H. Westphal. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U. S. A. 93: 5860-5865.
22. Landry, S., M. Halin, S. Lefort, B. Audet, C. Vaquero, J. M. Mesnard, and B. Barbeau. 2007. Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology 4: 71.
23. Larocca, D., L. A. Chao, M. H. Seto, and T. K. Brunck. 1989. Human T-cell leukemia virus minus strand transcription in infected T-cells. Biochem. Biophys. Res. Commun. 163: 1006-1013.
24. Lemasson, I., M. R. Lewis, N. Polakowski, P. Hivin, M. H. Cavanagh, S. Thebault, B. Barbeau, J. K. Nyborg, and J. M. Mesnard. 2007. HumanT-cell leukemia virus type 1 (HTLV-1) bZIP protein interacts with the cellular transcription factor CREB to inhibit HTLV-1 transcription. J. Virol. 81: 1543-1553.
25. Liu, J., A. B. Sorensen, B. Wang, M. Wabl, A. L. Nielsen, and F. S. Pedersen. 2009. Identification of novel Bach2 transcripts and protein isoforms through tagging analysis of retroviral integrations in B-cell lymphomas. BMC Mol. Biol. 10: 2.
26. Ludwig, L. B., J. L. Ambrus, Jr., K. A. Krawczyk, S. Sharma, S. Brooks, C. B. Hsiao, and S. A. Schwartz. 2006. Human Immunodeficiency Virus-Type 1 LTR DNA contains an intrinsic gene producing antisense RNA and protein products. Retrovirology 3: 80.
27. Martin-Hernandez, J., A. B. Sorensen, and F. S. Pedersen. 2001. Murine leukemia virus proviral insertions between the N-ras and unr genes in B-cell lymphoma DNA affect the expression of N-ras only. J. Virol. 75: 11907-11912.
28. Michael, N. L., M. T. Vahey, L. d'Arcy, P. K. Ehrenberg, J. D. Mosca, J. Rappaport, and R. R. Redfield. 1994. Negative-strand RNA transcripts are produced in human immunodeficiency virus type 1-infected cells and patients by a novel promoter downregulated by Tat. J. Virol. 68: 979-987.
29. Miller, R. H. 1988. Human immunodeficiency virus may encode a novel protein on the genomic DNA plus strand. Science 239: 1420-1422.
30. Moore, M. J., and N. J. Proudfoot. 2009. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136: 688-700.
31. Murata, K., T. Hayashibara, K. Sugahara, A. Uemura, T. Yamaguchi, H. Harasawa, H. Hasegawa, K. Tsuruda, T. Okazaki, T. Koji, T. Miyanishi, Y. Yamada, and S. Kamihira. 2006. A novel alternative splicing isoform of human T-cell leukemia virus type 1 bZIP factor (HBZ-SI) targets distinct subnuclear localization. J. Virol. 80: 2495-2505.
32. Neil, H., C. Malabat, Y. d'Aubenton-Carafa, Z. Xu, L. M. Steinmetz, and A. Jacquier. 2009. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457: 1038-1042.
33. Nieves, A., L. S. Levy, and J. Lenz. 1997. Importance ofa c-Myb binding site for lymphomagenesis by the retrovirus SL3-3. J. Virol. 71: 1213-1219.
34. Peeters, A., P. F. Lambert, and N. J. Deacon. 1996. A fourth Sp1 site in the human immunodeficiency virus type 1 long terminal repeat is essential for negative-sense transcription. J. Virol. 70: 6665-6672.
35. Preker, P., J. Nielsen, S. Kammler, S. Lykke-Andersen, M. S. Christensen, C. K. Mapendano, M. H. Schierup, and T. H. Jensen. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
36. Prescott, E. M., and N. J. Proudfoot. 2002. Transcriptional collision between convergent genes in budding yeast. Proc. Natl. Acad. Sci. U. S. A. 99: 8796-8801.
37. Rasmussen, M. H., A. B. Sorensen, D. W. Morris, J. C. Dutra, E. K. Engelhard, C. L. Wang, J. Schmidt, and F. S. Pedersen. 2005. Tumor modelspecific proviral insertional mutagenesis of the Fos/Jdp2/Batf locus. Virology 337: 353-364.
38. Rasmussen, M. H., B. Wang, M. Wabl, A. L. Nielsen, and F. S. Pedersen. 2009. Activation of alternative Jdp2 promoters and functional protein isoforms in T-cell lymphomas by retroviral insertion mutagenesis. Nucleic Acids Res. 37: 4657-4671.
39. Saito, M., T. Matsuzaki, Y. Satou, J. Yasunaga, K. Saito, K. Arimura, M. Matsuoka, and Y. Ohara. 2009. In vivo expression of the HBZ gene of HTLV-1 correlates with proviral load, inflammatory markers and disease severity in HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP). Retrovirology 6: 19.
40. Satou, Y., J. Yasunaga, M. Yoshida, and M. Matsuoka. 2006. HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 103: 720-725.
41. Shearwin, K. E., B. P. Callen, and J. B. Egan. 2005. Transcriptional interference-a crash course. Trends Genet. 21: 339-345.
42. Sneppen, K., I. B. Dodd, K. E. Shearwin, A. C. Palmer, R. A. Schubert, B. P. Callen, and J. B. Egan. 2005. A mathematical model for transcriptional interference by RNA polymerase traffic in Escherichia coli. J. Mol. Biol. 346: 399-409.
43. Sorensen, A. B., M. Duch, H. W. Amtoft, P. Jorgensen, and F. S. Pedersen. 1996. Sequence tags of provirus integration sites in DNAs of tumors induced by the murine retrovirus SL3-3. J. Virol. 70: 4063-4070.
44. Sorensen, A. B., A. H. Lund, S. Ethelberg, N. G. Copeland, N. A. Jenkins, and F. S. Pedersen. 2000. Sint1, a common integration site in SL3-3-induced T-cell lymphomas, harbors a putative proto-oncogene with homology to the septin gene family. J. Virol. 74: 2161-2168.
45. Sorensen, A. B., A. H. Lund, S. Kunder, L. Quintanilla-Martinez, J. Schmidt, B. Wang, M. Wabl, and F. S. Pedersen. 2007. Impairment of alternative splice sites defining a novel gammaretroviral exon within gag modifies the oncogenic properties of Akv murine leukemia virus. Retrovirology 4: 46.
46. Sorensen, K. D., S. Kunder, L. Quintanilla-Martinez, J. Sorensen, 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.
47. Stewart, M., N. Mackay, L. Hanlon, K. Blyth, L. Scobie, E. Cameron, and J. C. Neil. 2007. Insertional mutagenesis reveals progression genes and checkpoints in MYC/Runx2 lymphomas. Cancer Res. 67: 5126-5133.
48. Swiatek, P. J., and T. Gridley. 1993. Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev. 7: 2071-2084.
49. Uren, A. G., J. Kool, A. Berns, and M. van Lohuizen. 2005. Retroviral insertional mutagenesis: past, present and future. Oncogene 24: 7656-7672.
50. Vanhee-Brossollet, C., H. Thoreau, N. Serpente, L. D'Auriol, J. P. Levy, and C. Vaquero. 1995. A natural antisense RNA derived from the HIV-1 env gene encodes a protein which is recognized by circulating antibodies of HIV+ individuals. Virology 206: 196-202.
51. Weinberg, M. S., L. M. Villeneuve, A. Ehsani, M. Amarzguioui, L. Aagaard, Z. X. Chen, A. D. Riggs, J. J. Rossi, and K. V. Morris. 2006. The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 12: 256-262.
52. Xu, Z., W. Wei, J. Gagneur, F. Perocchi, S. Clauder-Munster, J. Camblong, E. Guffanti, F. Stutz, W. Huber, and L. M. Steinmetz. 2009. Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033-1037.
53. Zhao, T., J. Yasunaga, Y. Satou, M. Nakao, M. Takahashi, M. Fujii, and M. Matsuoka. 2009. Human T-cell leukemia virus type 1 bZIP factor selectively suppresses the classical pathway of NF-kappaB. Blood 113: 2755-2764.