Deep sequencing reveals abundant noncanonical retroviral microRNAs in B-cell leukemia/lymphoma

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 6, 2013, Pages 2306-2311

  Rosewick, Nicolas ^a,b,d   Momont, Mélanie ^a   Durkin, Keith ^a   Takeda, Haruko ^a   Caiment, Florian ^a,d   Cleuter, Yvette ^b   Vernin, Céline ^c   Mortreux, Franck ^c   Wattel, Eric ^c   Burny, Arsène ^b   Georges, Michel ^a   Van Den Broeke, Anne ^a,b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b JULES BORDET INSTITUTE   (Belgium)

^c UNIVERSITÉ DE LYON   (France)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

HTLV 1; Noncoding RNA; Oncogenesis; Retrovirus silencing

Indexed keywords

ARGONAUTE PROTEIN; DNA DIRECTED RNA POLYMERASE III; MICRORNA; UNTRANSLATED RNA; VIRUS RNA;

ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; B LYMPHOCYTE; BOVINE LEUKEMIA VIRUS; CANCER CELL; CARCINOGENESIS; CD4+ T LYMPHOCYTE; GENE SILENCING; HIGH THROUGHPUT SEQUENCING; HUMAN T CELL LEUKEMIA VIRUS 1; IN VIVO STUDY; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURIFYING SELECTION; REGULATOR GENE; RNA SEQUENCE; TUMOR GROWTH;

ANIMALS; ARGONAUTE PROTEINS; BASE SEQUENCE; CATTLE; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENZOOTIC BOVINE LEUKOSIS; GENE EXPRESSION; HIGH MOBILITY GROUP PROTEINS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA VIRUS, BOVINE; LEUKEMIA, B-CELL; LEUKEMIA-LYMPHOMA, ADULT T-CELL; LYMPHOMA, B-CELL; MICRORNAS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA POLYMERASE III; RNA, NEOPLASM; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SHEEP; SHEEP DISEASES; TERMINAL REPEAT SEQUENCES;

EID: 84873450117     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213842110     Document Type: Article

References (37)

1. Burny A, et al. (1994) Bovine Leukemia Virus: Biology and mode of transformation. Viruses and Cancer, eds Minson AC, Neil JC, McRae MA (Cambridge Univ Press, Cambridge, UK), pp 313-334.
2. Gillet N, et al. (2007) Mechanisms of leukemogenesis induced by bovine leukemia virus: Prospects for novel anti-retroviral therapies in human. Retrovirology 4:18.
3. Mammerickx M, Palm R, Portetelle D, Burny A (1988) Experimental transmission of enzootic bovine leukosis to sheep: Latency period of the tumoral disease. Leukemia 2(2):103-107.
4. Matsuoka M, Jeang KT (2007) Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 7(4):270-280.
5. Moulés V, et al. (2005) Fate of premalignant clones during the asymptomatic phase preceding lymphoid malignancy. Cancer Res 65(4):1234-1243.
6. Willems L, et al. (1990) Cooperation between bovine leukaemia virus transactivator protein and Ha-ras oncogene product in cellular transformation. EMBO J 9(5):1577-1581.
7. Klener P, et al. (2006) Insights into gene expression changes impacting B-cell transformation: Cross-species microarray analysis of bovine leukemia virus tax-responsive genes in ovine B cells. J Virol 80(4):1922-1938.
8. Szynal M, et al. (2003) Disruption of B-cell homeostatic control mediated by the BLVTax oncoprotein: Association with the upregulation of Bcl-2 and signaling through NF-kappaB. Oncogene 22(29):4531-4542.
9. Kettmann R, et al. (1982) Leukemogenesis by bovine leukemia virus: Proviral DNA integration and lack of RNA expression of viral long terminal repeat and 3′ proximate cellular sequences. Proc Natl Acad Sci USA 79(8):2465-2469.
10. Van den Broeke A, et al. (1988) Even transcriptionally competent proviruses are silent in bovine leukemia virus-induced sheep tumor cells. Proc Natl Acad Sci USA 85(23): 9263-9267.
11. Van Den Broeke A, et al. (1999) In vivo rescue of a silent tax-deficient bovine leukemia virus from a tumor-derived ovine B-cell line by recombination with a retrovirally transduced wild-type tax gene. J Virol 73(2):1054-1065.
12. Merimi M, et al. (2007) Complete suppression of viral gene expression is associated with the onset and progression of lymphoid malignancy: Observations in bovine leukemia virus-infected sheep. Retrovirology 4:51.
13. Merimi M, et al. (2007) Suppression of viral gene expression in bovine leukemia virusassociated B-cell malignancy: Interplay of epigenetic modifications leading to chromatin with a repressive histone code. J Virol 81(11):5929-5939.
14. Colin L, et al. (2011) Chromatin disruption in the promoter of bovine leukemia virus during transcriptional activation. Nucleic Acids Res 39(22):9559-9573.
15. Willems L, et al. (1993) In vivo infection of sheep by bovine leukemia virus mutants. J Virol 67(7):4078-4085.
16. Florins A, et al. (2007) Even attenuated bovine leukemia virus proviruses can be pathogenic in sheep. J Virol 81(18):10195-10200.
17. Kincaid RP, Burke JM, Sullivan CS (2012) RNA virus microRNA that mimics a B-cell oncomiR. Proc Natl Acad Sci USA 109(8):3077-3082.
18. Ventura A, Jacks T (2009) MicroRNAs and cancer: Short RNAs go a long way. Cell 136(4):586-591.
19. Olive V, Jiang I, He L (2010) mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int J Biochem Cell Biol 42(8):1348-1354.
20. Ragan C, Zuker M, Ragan MA (2011) Quantitative prediction of miRNA-mRNA interaction based on equilibrium concentrations. PLoS Comput Biol 7(2):e1001090.
21. Bartel DP (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116(2):281-297.
22. Han J, et al. (2006) Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125(5):887-901.
23. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12(12):846-860.
24. Watashi K, Yeung ML, Starost MF, Hosmane RS, Jeang KT (2010) Identification of small molecules that suppress microRNA function and reverse tumorigenesis. J Biol Chem 285(32):24707-24716.
25. Hutvagner G, Simard MJ (2008) Argonaute proteins: Key players in RNA silencing. Nat Rev Mol Cell Biol 9(1):22-32.
26. Han YC, et al. (2010) microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 207(3):475-489.
27. Santanam U, et al. (2010) Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci USA 107(27):12210-12215.
28. Orioli A, Pascali C, Pagano A, Teichmann M, Dieci G (2012) RNA polymerase III transcription control elements: Themes and variations. Gene 493(2):185-194.
29. White RJ (2011) Transcription by RNA polymerase III: More complex than we thought. Nat Rev Genet 12(7):459-463.
30. Barski A, et al. (2010) Pol II and its associated epigenetic marks are present at Pol IIItranscribed noncoding RNA genes. Nat Struct Mol Biol 17(5):629-634.
31. Van den Broeke A, et al. (2010) Cytotoxic responses to BLV tax oncoprotein do not prevent leukemogenesis in sheep. Leuk Res 34(12):1663-1669.
32. Pekarsky Y, et al. (2006) Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res 66(24):11590-11593.
33. Cullen BR (2010) Five questions about viruses and microRNAs. PLoS Pathog 6(2): e1000787.
34. Umbach JL, et al. (2008) MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454(7205):780-783.
35. Grundhoff A, Sullivan CS (2011) Virus-encoded microRNAs. Virology 411(2):325-343.
36. Bogerd HP, et al. (2010) A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral microRNAs. Mol Cell 37(1):135-142.
37. Klase Z, et al. (2007) HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol Biol 8:63.