Identification and potential function of viral microRNAs

doi:10.1017/CBO9780511541766.034

31 - Identification and potential function of viral microRNAs

from V - MicroRNAs in disease biology

Published online by Cambridge University Press: 22 August 2009

Finn Grey ,

Alec J. Hirsch and

Jay A. Nelson

Edited by

Krishnarao Appasani

Foreword by

Sidney Altman and

Victor R. Ambros

Show author details

Finn Grey: Affiliation:
Vaccine & Gene Therapy Institute Oregon Health & Sciences University Portland, OR 97201 USA
Alec J. Hirsch: Affiliation:
Vaccine & Gene Therapy Institute Oregon Health & Sciences University Portland, OR 97201 USA
Jay A. Nelson: Affiliation:
Vaccine & Gene Therapy Institute Oregon Health & Sciences University Portland, OR 97201 USA

Book contents

Get access

Summary

The discovery of RNA interference (RNAi) and microRNAs (miRNAs) is undoubtedly one of the most significant recent advances in the field of biology. miRNAs were initially identified in Caenorhabditis elegans with the discovery of a small RNA, lin-4, that was shown to regulate the heterochronic gene lin-14 (Lee et al., 1993; Wightman et al., 1993). Further investigations led to the identification of a second small RNA, let-7, that played a similar role in regulation of developmental genes (Reinhart et al., 2000). Subsequent studies using extensive cloning strategies and bioinformatics methods have identified hundreds of miRNA genes in plants and animals suggesting that post-transcriptional regulation through expression of small RNAs is an evolutionarily conserved and common mechanism of gene regulation (Bartel, 2004; Pfeffer et al., 2004; Pfeffer et al., 2005). More recent studies have revealed that a surprisingly large percentage of genes in higher organisms may be regulated by miRNAs (Brennecke et al., 2005; Grün et al., 2005; Krek et al., 2005; Lewis et al., 2005; Xie et al., 2005). Given the widespread prevalence and influential effects of miRNAs on gene expression it is unsurprising that viruses exploit RNAi pathways by expressing their own small RNAs. In this chapter we will review what is currently known about virally encoded miRNAs, including examination of their expression, genomic position and degree of evolutionary conservation between related viruses. We will also discuss the potential functions of viral miRNAs.

Type: Chapter
Information: MicroRNAs
From Basic Science to Disease Biology
, pp. 405 - 426

DOI: https://doi.org/10.1017/CBO9780511541766.034 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Book purchase

Temporarily unavailable

References

Andersson, M. G., Haasnoot, P. C., Xu, N.et al. (2005). Suppression of RNA interference by adenovirus virus-associated RNA. Journal of Virology, 79, 9556–9565.Google Scholar

Aparicio, O., Razquin, N., Zaratiegui, M., Narvaiza, I. and Fortes, P. (2006). Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. Journal of Virology, 80, 1376–1384.Google Scholar

Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.Google Scholar

Bennasser, Y., Le, S. Y., Benkirane, M. and Jeang, K. T. (2005). Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity, 22, 607–619.Google Scholar

Bentwich, I., Avniel, A., Karov, Y.et al. (2005). Identification of hundreds of conserved and nonconserved human microRNAs. Nature Genetics, 37, 766–770.Google Scholar

Berezikov, E., Guryev, V., Belt, J.et al. (2005). Phylogenetic shadowing and computational identification of human microRNA genes. Cell, 120, 21–24.Google Scholar

Bowden, R. J., Simas, J. P., Davis, A. J. and Efstathiou, S. (1997). Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. Journal of General Virology, 78, 1675–1687.Google Scholar

Branco, F. J. and Fraser, N. W. (2005). Herpes simplex virus type 1 latency-associated transcript expression protects trigeminal ganglion neurons from apoptosis. Journal of Virology, 79, 9019–9025.Google Scholar

Brennecke, J., Stark, A., Russell, R. B. and Cohen, S. M. (2005). Principles of microRNA-target recognition. Public Library of Science Biology, 3, e85.Google Scholar

Cai, X. and Cullen, B. R. (2006). Transcriptional origin of Kaposi's sarcoma-associated herpesvirus microRNAs. Journal of Virology, 80, 2234–2242.Google Scholar

Cai, X., Lu, S., Zhang, Z.et al. (2005). Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proceedings of the National Academy of Sciences USA, 102, 5570–5575.Google Scholar

Courcelle, C. T., Courcelle, J., Prichard, M. N. and Mocarski, E. S. (2001). Requirement for uracil-DNA glycosylase during the transition to late-phase cytomegalovirus DNA replication. Journal of Virology, 75, 7592–7601.Google Scholar

DeMarchi, J. M., Schmidt, C. A. and Kaplan, A. S. (1980). Patterns of transcription of human cytomegalovirus in permissively infected cells. Journal of Virology, 35, 277–286.Google Scholar

Dunn, W., Chou, C., Li, H.et al. (2003). Functional profiling of a human cytomegalovirus genome. Proceedings of the National Academy of Sciences USA, 100, 14 223–14 228.Google Scholar

Dunn, W., Trang, P., Zhong, Q.et al. (2005). Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cellular Microbiology, 7, 1684–1695.Google Scholar

Farh, K. K., Grimson, A., Jan, C.et al. (2005). The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science, 310, 1817–1821.Google Scholar

Furnari, F. B., Adams, M. D. and Pagano, J. S. (1992). Regulation of the Epstein–Barr virus DNA polymerase gene. Journal of Virology, 66, 2837–2845.Google Scholar

Goldmacher, V. S., Bartle, L. M., Skaletskaya, A.et al. (1999). A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proceedings of the National Academy of Sciences USA, 96, 12 536–12 541.Google Scholar

Grey, F., Antoniewicz, A., Allen, E.et al. (2005). Identification and characterization of human cytomegalovirus-encoded microRNAs. Journal of Virology, 79, 12 095–12 099.Google Scholar

Grun, D., Wang, Y. L., Langenberger, D., Gunsalus, K. C. and Rajewsky, N. (2005). MicroRNA target predictions across seven Drosophila species and comparison to mammalian targets. Public Library of Science Computer Biology, 1, e13.Google Scholar

Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M. and Sarnow, P. (2005). Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science, 309, 1577–1581.Google Scholar

Krek, A., Grun, D., Poy, M. N.et al. (2005). Combinatorial microRNA target predictions. Nature Genetics, 37, 495–500.Google Scholar

Lecellier, C. H., Dunoyer, P., Arar, K.et al. (2005). A cellular microRNA mediates antiviral defense in human cells. Science, 308, 557–560.Google Scholar

Lee, R. C., Feinbaum, R. L. and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.Google Scholar

Lewis, B. P., Burge, C. B. and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15–20.Google Scholar

Lim, L. P., Lau, N. C., Weinstein, E. G.et al. (2003). The microRNAs of Caenorhabditis elegans. Genes & Development, 17, 991–1008.Google Scholar

Lu, S. and Cullen, B. R. (2004). Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. Journal of Virology, 78, 12 868–12 876.Google Scholar

McCormick, C. and Ganem, D. (2005). The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science, 307, 739–741.Google Scholar

Moore, P. and Chang, Y. (2001). Kaposi's sarcoma-associated Herpesvirus. Fields Virology, 2, 2803–2831.Google Scholar

Omoto, S. and Fujii, Y. R. (2005). Regulation of human immunodeficiency virus 1 transcription by nef microRNA. Journal of General Virology, 86, 751–755.Google Scholar

Omoto, S., Ito, M., Tsutsumi, Y.et al. (2004). HIV-1 nef suppression by virally encoded microRNA. Retrovirology, 1, 44.Google Scholar

Pasquinelli, A. E., Reinhart, B. J., Slack, F.et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature, 408, 86–89.Google Scholar

Patterson, C. E. and Shenk, T. (1999). Human cytomegalovirus UL36 protein is dispensable for viral replication in cultured cells. Journal of Virology, 73, 7126–7131.Google Scholar

Pearce, M., Matsumura, S. and Wilson, A. C. (2005). Transcripts encoding K12, v-FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcoma-associated herpesvirus originate from a common promoter. Journal of Virology, 79, 14 457–14 464.Google Scholar

Pfeffer, S., Zavolan, M., Grasser, F. A.et al. (2004). Identification of virus-encoded microRNAs. Science, 304, 734–736.Google Scholar

Pfeffer, S., Sewer, A., Lagos-Quintana, M.et al. (2005). Identification of microRNAs of the herpesvirus family. Nature Methods, 2, 269–276.Google Scholar

Prichard, M. N., Duke, G. M. and Mocarski, E. S. (1996). Human cytomegalovirus uracil DNA glycosylase is required for the normal temporal regulation of both DNA synthesis and viral replication. Journal of Virology, 70, 3018–3025.Google Scholar

Reinhart, B. J., Slack, F. J., Basson, M.et al. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901–906.Google Scholar

Roizman, B. and Pellet, E. (2001). The family Herpesviridae: a brief introduction. Fields Virology, 2, 2381–2397.Google Scholar

Samols, M. A., Hu, J., Skalsky, R. L. and Renne, R. (2005). Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. Journal of Virology, 79, 9301–9305.Google Scholar

Sano, M., Kato, Y. and Taira, K. (2006). Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. Federation of European Biological Sciences Letters, 580, 1553–1564.Google Scholar

Shenk, T. (2001). Adenoviridae: the viruses and their replication. Fields Virology, 2, 2265–2326.Google Scholar

Simas, J. P., Bowden, R. J., Paige, V. and 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. Journal of General Virology, 79, 149–153.Google Scholar

Skaletskaya, A., Bartle, L. M., Chittenden, T.et al. (2001). A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proceedings of the National Academy of Sciences USA, 98, 7829–7834.Google Scholar

Smith, P. R., Jesus, O., Turner, D.et al. (2000). Structure and coding content of CST (BART) family RNAs of Epstein–Barr virus. Journal of Virology, 74, 3082–3092.Google Scholar

Stark, A., Brennecke, J., Bushati, N., Russell, R. B. and Cohen, S. M. (2005). Animal microRNAs confer robustness to gene expression and have a significant impact on 3′ UTR evolution. Cell, 123, 1133–1146.Google Scholar

Sullivan, C. S. and Ganem, D. (2005). MicroRNAs and viral infection. Molecular Cell, 20, 3–7.Google Scholar

Sullivan, C. S., Grundhoff, A. T., Tevethia, S., Pipas, J. M. and Ganem, D. (2005). SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature, 435, 682–686.Google Scholar

Thompson, R. L. and Sawtell, N. M. (2001). Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. Journal of Virology, 75, 6660–6675.Google Scholar

Wathen, M. W. and Stinski, M. F. (1982). Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. Journal of Virology, 41, 462–477.Google Scholar

Wightman, B., Ha, I. and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell, 75, 855–862.Google Scholar

Xie, X., Lu, J., Kulbokas, E. J.et al. (2005). Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature, 434, 338–345.Google Scholar

Yu, D., Silva, M. C. and Shenk, T. (2003). Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proceedings of the National Academy of Sciences USA, 100, 12 396–12 401.Google Scholar