Gammaherpesvirus small noncoding RNAs are bifunctional elements that regulate infection and contribute to virulence in vivo

mBio

Volumn 6, Issue 1, 2015, Pages

  Diebel, Kevin W ^a   Oko, Lauren M ^a   Medina, Eva M ^a   Niemeyer, Brian F ^a   Warren, Cody J ^a   Claypool, David J ^a   Tibbetts, Scott A ^b   Cool, Carlyne D ^a   Clambey, Eric T ^a   van Dyk, Linda F ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; MICRORNA; SMALL UNTRANSLATED RNA; TRANSFER RNA; UNTRANSLATED RNA; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GAMMA HERPES VIRUS 68; GAMMAHERPESVIRINAE; GENE EXPRESSION; GENE LOCUS; HERPES VIRUS INFECTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TMER GENE; VIRUS GENE; VIRUS PATHOGENESIS; VIRUS PNEUMONIA; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; FIBROBLAST; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; RHADINOVIRUS; VIROLOGY; VIRULENCE;

ANIMALIA; HERPESVIRIDAE; HUMAN HERPESVIRUS 4; MURINAE; MUS;

ANIMALS; CELL LINE; FIBROBLASTS; GENE DELETION; GENE EXPRESSION REGULATION; HERPESVIRIDAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; MICE, INBRED BALB C; MICE, INBRED C57BL; RHADINOVIRUS; RNA, UNTRANSLATED; VIRULENCE; VIRULENCE FACTORS;

EID: 84924107201     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01670-14     Document Type: Article

References (49)

1. Speck SH, Virgin HW. 1999. Host and viral genetics of chronic infection: a mouse model of gamma-herpesvirus pathogenesis. Curr Opin Microbiol 2: 403-409. http://dx. doi. org/10. 1016/S1369-5274(99)80071-X.
2. Cesarman E. 2011. Gammaherpesvirus and lymphoproliferative disorders in immunocompromised patients. Cancer Lett 305: 163-174. http://dx. doi. org/10. 1016/j. canlet. 2011. 03. 003.
3. Conrad NK, Fok V, Cazalla D, Borah S, Steitz JA. 2006. The challenge of viral snRNPs. Cold Spring Harb Symp Quant Biol 71: 377-384. http://dx. doi. org/10. 1101/sqb. 2006. 71. 057.
4. Takada K. 2001. Role of Epstein-Barr virus in Burkitt's lymphoma. Curr Top Microbiol Immunol 258: 141-151. http://dx. doi. org/10. 1007/978-3-642-56515-1_9.
5. Sun R, Lin SF, Gradoville L, Miller G. 1996. Polyadenylylated nuclear RNA encoded by Kaposi sarcoma-associated herpesvirus. Proc Natl Acad Sci U S A 93: 11883-11888. http://dx. doi. org/10. 1073/pnas. 93. 21. 11883.
6. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grässer FA, van Dyk LF, Ho CK, Shuman S, Chien M, Russo JJ, Ju J, Randall G, Lindenbach BD, Rice CM, Simon V, Ho DD, Zavolan M, Tuschl T. 2005. Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276. http://dx. doi. org/10. 1038/nmeth746.
7. 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. http://dx. doi. org/10. 1128/JVI. 79. 14. 9301-9305. 2005.
8. Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, Cullen BR. 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. http://dx. doi. org/10. 1073/pnas. 0408192102.
9. Grundhoff A, Sullivan CS, Ganem D. 2006. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12: 733-750. http://dx. doi. org/10. 1261/rna. 2326106.
10. Zhu JY, Strehle M, Frohn A, Kremmer E, Höfig KP, Meister G, Adler H. 2010. Identification and analysis of expression of novel microRNAs of murine gammaherpesvirus 68. J Virol 84: 10266-10275. http://dx. doi. org/10. 1128/JVI. 01119-10.
11. Reese TA, Xia J, Johnson LS, Zhou X, Zhang W, Virgin HW. 2010. Identification of novel microRNA-like molecules generated from herpes-virus and host tRNA transcripts. J Virol 84: 10344-10353. http://dx. doi. org/10. 1128/JVI. 00707-10.
12. Zhu Y, Haecker I, Yang Y, Gao SJ, Renne R. 2013. Gamma-herpesvirusencoded miRNAs and their roles in viral biology and pathogenesis. Curr Opin Virol 3: 266-275. http://dx. doi. org/10. 1016/j. coviro. 2013. 05. 013.
13. Zhu Y, Huang Y, Jung JU, Lu C, Gao SJ. 2014. Viral miRNA targeting of bicistronic and polycistronic transcripts. Curr Opin Virol 7: 66-72. http://dx. doi. org/10. 1016/j. coviro. 2014. 04. 004.
14. Yajima M, Kanda T, Takada K. 2005. Critical role of Epstein-Barr virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation. J Virol 79: 4298-4307. http://dx. doi. org/10. 1128/JVI. 79. 7. 4298-4307. 2005.
15. Feederle R, Linnstaedt SD, Bannert H, Lips H, Bencun M, Cullen BR, Delecluse HJ. 2011. A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog. 7: e1001294. http://dx. doi. org/10. 1371/journal. ppat. 1001294.
16. Rossetto CC, Pari G. 2012. KSHV PAN RNA associates with demethylases UTX and JMJD3 to activate lytic replication through a physical interaction with the virus genome. PLoS Pathog. 8: e1002680. http://dx. doi. org/10. 1371/journal. ppat. 1002680.
17. Moody R, Zhu Y, Huang Y, Cui X, Jones T, Bedolla R, Lei X, Bai Z, Gao SJ. 2013. KSHV microRNAs mediate cellular transformation and tumorigenesis by redundantly targeting cell growth and survival pathways. PLoS Pathog. 9: e1003857. http://dx. doi. org/10. 1371/journal. ppat. 1003857.
18. Swaminathan S, Tomkinson B, Kieff E. 1991. Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro. Procee Natl Acad Sci U S A 88: 1546-1550. http://dx. doi. org/10. 1073/pnas. 88. 4. 1546.
19. Ensser A, Pfinder A, Müller-Fleckenstein I, Fleckenstein B. 1999. The URNA genes of herpesvirus saimiri (strain C488) are dispensable for transformation of human T cells in vitro. J Virol 73: 10551-10555.
20. Wahl A, Linnstaedt SD, Esoda C, Krisko JF, Martinez-Torres F, Delecluse HJ, Cullen BR, Garcia JV. 2013. A cluster of virus-encoded microRNAs accelerates acute systemic Epstein-Barr virus infection but does not significantly enhance virus-induced oncogenesis in vivo. J Virol 87: 5437-5446. http://dx. doi. org/10. 1128/JVI. 00281-13.
21. Barton E, Mandal P, Speck SH. 2011. Pathogenesis and host control of gammaherpesviruses: lessons from the mouse. Annu Rev Immunol 29: 351-397. http://dx. doi. org/10. 1146/annurev-immunol-072710-081639.
22. Bowden RJ, Simas JP, Davis AJ, Efstathiou S. 1997. Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J Gen Virol 78: 1675-1687.
23. Diebel KW, Smith AL, van Dyk LF. 2010. Mature and functional viral miRNAs transcribed from novel RNA polymerase III promoters. RNA 16: 170-185. http://dx. doi. org/10. 1261/rna. 1873910.
24. Diebel KW, Claypool DJ, van Dyk LF. 2014. A conserved RNA polymerase III promoter required for gammaherpesvirus TMER transcription and microRNA processing. Gene 544: 8-18. http://dx. doi. org/10. 1016/j. gene. 2014. 04. 026.
25. Bogerd HP, Karnowski HW, Cai X, Shin J, Pohlers M, Cullen BR. 2010. A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral microRNAs. Mol Cell 37: 135-142. http://dx. doi. org/10. 1016/j. molcel. 2009. 12. 016.
26. Orioli A, Pascali C, Quartararo J, Diebel KW, Praz V, Romascano D, Percudani R, van Dyk LF, Hernandez N, Teichmann M, Dieci G. 2011. Widespread occurrence of non-canonical transcription termination by human RNA polymerase III. Nucleic Acids Res 39: 5499-5512. http://dx. doi. org/10. 1093/nar/gkr074.
27. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerlessDNA manipulation in Escherichia coli. Biotechniques 40: 191-197. http://dx. doi. org/10. 2144/000112096.
28. Tischer BK, Smith GA, Osterrieder N. 2010. En passant mutagenesis: a two step markerless red recombination system. Methods Mol Biol 634: 421-430. http://dx. doi. org/10. 1007/978-1-60761-652-8_30.
29. Adler H, Messerle M, Wagner M, Koszinowski UH. 2000. Cloning and mutagenesis of the murine gammaherpesvirus 68 genome as an infectious bacterial artificial chromosome. J Virol 74: 6964-6974. http://dx. doi. org/10. 1128/JVI. 74. 15. 6964-6974. 2000.
30. Nealy MS, Coleman CB, Li H, Tibbetts SA. 2010. Use of a virus-encoded enzymatic marker reveals that a stable fraction of memory B cells expresses latency-associated nuclear antigen throughout chronic gammaherpesvirus infection. J Virol 84: 7523-7534. http://dx. doi. org/10. 1128/JVI. 02572-09.
31. Clambey ET, Virgin HW, Speck SH. 2002. Characterization of a spontaneous 9. 5-kilobase-deletion mutant of murine gammaherpesvirus 68 reveals tissue-specific genetic requirements for latency. J Virol 76: 6532-6544. http://dx. doi. org/10. 1128/JVI. 76. 13. 6532-6544. 2002.
32. Macrae AI, Dutia BM, Milligan S, Brownstein DG, Allen DJ, Mistrikova J, Davison AJ, Nash AA, Stewart JP. 2001. Analysis of a novel strain of murine gammaherpesvirus reveals a genomic locus important for acute pathogenesis. J Virol 75: 5315-5327. http://dx. doi. org/10. 1128/JVI. 75. 11. 5315-5327. 2001.
33. Flaño E, Kim IJ, Woodland DL, Blackman MA. 2002. Gammaherpesvirus latency is preferentially maintained in splenic germinal center and memory B cells. J Exp Med 196: 1363-1372. http://dx. doi. org/10. 1084/jem. 20020890.
34. Willer DO, Speck SH. 2003. Long-term latent murine gammaherpesvirus 68 infection is preferentially found within the surface immunoglobulin D-negative subset of splenic B cells in vivo. J Virol 77: 8310-8321. http://dx. doi. org/10. 1128/JVI. 77. 15. 8310-8321. 2003.
35. Lee KS, Cool CD, van Dyk LF. 2009. Murine gammaherpesvirus 68 infection of gamma interferon-deficient mice on a BALB/c background results in acute lethal pneumonia that is dependent on specific viral genes. J Virol 83: 11397-11401. http://dx. doi. org/10. 1128/JVI. 00989-09.
36. Cech TR, Steitz JA. 2014. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157: 77-94. http://dx. doi. org/10. 1016/j. cell. 2014. 03. 008.
37. Simas JP, Bowden RJ, Paige V, Efstathiou S. 1998. Four tRNA-like sequences and a serpin homologue encoded by murine gammaherpesvirus 68 are dispensable for lytic replication in vitro and latency in vivo. J Gen Virol 79: 149-153.
38. Feldman ER, Kara M, Coleman CB, Grau KR, Oko LM, Krueger BJ, Renne R, van Dyk LF, Tibbetts SA. 2014. Virus-encoded microRNAs facilitate gammaherpesvirus latency and pathogenesis in vivo. mBio 5: e00981-00914. http://dx. doi. org/10. 1128/mBio. 00981-14.
39. Dzananovic E, Patel TR, Deo S, McEleney K, Stetefeld J, McKenna SA. 2013. Recognition of viral RNA stem-loops by the tandem doublestranded RNA binding domains of PKR. RNA 19: 333-344. http://dx. doi. org/10. 1261/rna. 035931. 112.
40. Iwakiri D, Takada K. 2010. Role of EBERs in the pathogenesis of EBV infection. Adv Cancer Res 107: 119-136. http://dx. doi. org/10. 1016/S0065-230X(10)07004-1.
41. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K. 2002. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 21: 954-965. http://dx. doi. org/10. 1093/emboj/21. 5. 954.
42. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K. 2006. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 25: 4207-4214. http://dx. doi. org/10. 1038/sj. emboj. 7601314.
43. Iwakiri D, Zhou L, Samanta M, Matsumoto M, Ebihara T, Seya T, Imai S, Fujieda M, Kawa K, Takada K. 2009. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J Exp Med 206: 2091-2099. http://dx. doi. org/10. 1084/jem. 20081761.
44. Virgin HW, Latreille P, Wamsley P, Hallsworth K, Weck KE, Dal Canto AJ, Speck SH. 1997. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J Virol 71: 5894-5904.
45. Suárez AL, van Dyk LF. 2008. Endothelial cells support persistent gammaherpesvirus 68 infection. PLoS Pathog. 4: e1000152. http://dx. doi. org/10. 1371/journal. ppat. 1000152.
46. Lee KS, Suarez AL, Claypool DJ, Armstrong TK, Buckingham EM, van Dyk LF. 2012. Viral cyclins mediate separate phases of infection by integrating functions of distinct mammalian cyclins. PLoS Pathog. 8: e1002496. http://dx. doi. org/10. 1371/journal. ppat. 1002496.
47. van Dyk LF, Virgin HW, Speck SH. 2000. The murine gammaherpesvirus 68 v-cyclin is a critical regulator of reactivation from latency. J Virol 74: 7451-7461. http://dx. doi. org/10. 1128/JVI. 74. 16. 7451-7461. 2000.
48. Ehrentraut H, Westrich JA, Eltzschig HK, Clambey ET. 2012. Adora2b adenosine receptor engagement enhances regulatory T cell abundance during endotoxin-induced pulmonary inflammation. PLoS One 7: e32416. http://dx. doi. org/10. 1371/journal. pone. 0032416.
49. Kozomara A, Griffiths-Jones S. 2011. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-D157. http://dx. doi. org/10. 1093/nar/gkq1027.