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The Role of Rnai and Micrornas in Animal Virus Replication and Antiviral Immunity

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The Role of Rnai and Micrornas in Animal Virus Replication and Antiviral Immunity Downloaded from genesdev.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press REVIEW The role of RNAi and microRNAs in animal virus replication and antiviral immunity Jennifer L. Umbach and Bryan R. Cullen1 Department of Molecular Genetics and Microbiology and Center for Virology, Duke University Medical Center, Durham, North Carolina 27710, USA The closely related microRNA (miRNA) and RNAi path- enzyme, and its cofactor TRBP. Binding of Dicer/TRBP ways have emerged as important regulators of virus–host to the base of the pre-miRNA is followed by cleavage to cell interactions. Although both pathways are relatively release the terminal loop, yielding an RNA duplex of ;20 well conserved all the way from plants to invertebrates bp flanked by 2-nt 39 overhangs (Fig. 1A; Chendrimada to mammals, there are important differences between et al. 2005). The RNA strand that is less tightly base- these systems. A more complete understanding of these paired at the 59 end is loaded into the RNA-induced differences will be required to fully appreciate the re- silencing complex (RISC) and forms the mature miRNA lationship between these diverse host organisms and the (Khvorova et al. 2003; Schwarz et al. 2003). The miRNA various viruses that infect them. Insights derived from then guides RISC to mRNAs bearing complementary this research will facilitate a better understanding of target sites (Hammond et al. 2000). viral pathogenesis and the host innate immune response Although the vast majority of miRNAs are generated as to viral infection. described above, some exceptions exist. For example, some miRNAs are derived from short, excised introns, MicroRNAs (miRNAs) are small regulatory RNAs ;22 called mirtrons, which resemble pre-miRNA hairpins, nucleotides (nt) in length that are typically derived from bypassing the need for Drosha, and only require Dicer for a single arm of imperfect, ;80-nt long RNA hairpins maturation (Berezikov et al. 2007; Ruby et al. 2007). A located within polymerase II (pol II)-derived transcripts small number of miRNAs are transcribed as shRNAs referred to as primary miRNAs (pri-miRNAs) (Fig. 1A; with a 59 single-stranded tail (Babiarz et al. 2008). Sim- for review, see Bartel 2004; Cullen 2004). Pri-miRNAs ilar to mirtrons, these ‘‘tailed’’ pre-miRNAs are Drosha- are capped and polyadenylated and may be almost independent, but still require Dicer for final processing. any size, ranging from hundreds to thousands of nucleo- RISCs, which are minimally composed of a mature tides, and may encode a single miRNA or a cluster of miRNA and an Argonaute protein, usually, but not in- several miRNAs (Lagos-Quintana et al. 2001; Lim et al. variably, bind to the 39 untranslated region (UTR) of 2003). Pri-miRNA stem–loops, which consist of an ;32- targeted transcripts. Functional targets are generally fully base-pair (bp) imperfect stem and a $10-nt terminal loop, complementary to nucleotides 2–7, preferably 2–8, at the are cleaved by the RNase III enzyme Drosha, acting 59 end of the miRNA, referred to as the miRNA seed together with its cofactor DGCR8, ;22 bp from the (Bartel 2009). There are a few examples known, however, stem/loop junction (Han et al. 2004; Zeng et al. 2005), where base-pairing between the target transcript and the thereby excising the ;60-nt precursor miRNA (pre- 39 half of the miRNA can compensate for mismatches in miRNA) hairpin. Since the flanking 59 and 39 arms of the seed. Perhaps the best example of this phenomenon is the pri-miRNA are degraded following Drosha cleavage, provided by the miRNA lin-4 and a well-characterized pre-miRNAs are typically found within the exonic target mRNA encoding lin-14, where robust inhibition of regions of noncoding RNAs or in the introns of protein- lin-14 expression is conferred by target sites lacking full coding or noncoding transcripts (Fig. 1A). seed homology (Ha et al. 1996). Cleavage by Drosha leaves the pre-miRNA hairpin RISCs bound to partially complementary mRNA tar- with a 2-nt 39 overhang. This is recognized by Exportin gets induce the translational repression of that mRNA by 5, which transports the pre-miRNA to the cytoplasm (Yi a mechanism that remains to be fully defined (Fig. 1A; for et al. 2003; Lund et al. 2004). There, the same 2-nt 39 review, see Filipowicz et al. 2008). Translational repres- overhang is recognized by Dicer, another RNase III sion in turn often induces a modest destabilization of the target mRNA (Bagga et al. 2005). RISCs tend to function [Keywords: RNAi; innate immunity; microRNAs; viruses] in a cooperative manner; the greater the number of RISCs 1Corresponding author. E-MAIL [email protected]; FAX (919) 681-8979. bound to a target transcript, the greater the inhibitory Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.1793309. effect (Doench et al. 2003; Doench and Sharp 2004). GENES & DEVELOPMENT 23:1151–1164 Ó 2009 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/09; www.genesdev.org 1151 Downloaded from genesdev.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Umbach and Cullen Figure 1. Schematic outline of miRNA and siRNA biogenesis. (A) miRNAs are transcribed as long pri-mRNAs and may be located in either noncoding RNAs or, as shown here, in an intron. After excision by Drosha, the pre-miRNA hairpin is exported to the cytoplasm for further processing by Dicer. One strand of the resulting miRNA duplex intermediate is incorporated into RISC, where it acts as a guide RNA to target RISC to either partially or fully complementary mRNAs. This primarily results in translational inhibition or mRNA degradation, respectively. (B) The antiviral RNAi pathway in plants and invertebrates is triggered by long, perfect dsRNAs that are generated by viral replication. These dsRNAs are cleaved by Dicer to generate siRNA duplexes, one strand of which is incorporated into RISC either directly or after being used as a primer by cellular RdRP to generate additional dsRNA substrates. When targeted to a viral mRNA, these viral siRNAs induce transcript cleavage and degradation. Viral dsRNAs may also be actively or passively released by virus-infected cells to induce a systemic antiviral state after capture by other, noninfected cells. While RISCs bound to partially complementary mRNA DNA viruses also produce dsRNAs by convergent tran- targets primarily induce translational inhibition, mRNAs scription of their compact viral genomes. Unlike the short, bearing perfectly complementary miRNA targets are imperfectly base-paired RNA stem–loop structures typi- cleaved by RISC and degraded in a process referred to as cally found in cellular transcripts, viral dsRNAs are gen- RNAi (Fig. 1A; Hutvagner and Zamore 2002; Zeng et al. erally both long and perfectly complementary. In plants 2003). Unlike translational inhibition, which requires and invertebrates, Dicer cleavage of such dsRNAs gen- stable binding of RISC to its target mRNA, RNAi permits erates a pool of ;22 bp dsRNAs, called siRNA duplexes, a single RISC to act enzymatically to irreversibly inhibit that are structurally similar to the miRNA duplex inter- the expression of multiple mRNA molecules. mediate described above (Fig. 1A,B). As with miRNAs, one miRNAs are expressed by plants and metazoans (Bartel strand of the siRNA duplex is loaded into RISC, where it 2004), where they have been found to play a role in a wide is used to guide RISC to complementary mRNAs. In this variety of cellular processes including cellular prolifera- context, the relevant targets are viral mRNAs and geno- tion, regulation of development, apoptosis, homeostasis, mic RNAs. As these are fully complementary to any viral and tumor formation (Ambros 2004; He and Hannon siRNAs, RISC binding results in their cleavage and 2004; Lai 2005). Humans encode >500 different miRNAs degradation (Fig. 1B), thus potently inhibiting virus rep- (Griffiths-Jones et al. 2008), which tend to be expressed in lication. In plants and nematodes, this antiviral response a developmental or tissue-specific manner (Landgraf et al. is further amplified through a secondary wave of siRNAs 2007). It has been demonstrated that individual miRNAs generated by RNA-dependent RNA polymerases (RdRPs), are capable of directly down-regulating the expression of which greatly increases the pool of siRNAs available to hundreds of different mRNAs, and >30% of all mamma- RISC (Aoki et al. 2007; Diaz-Pendon et al. 2007). Al- lian mRNAs are thought to be regulated by miRNAs though insects do not share the ability of plants and (Lewis et al. 2005). nematodes to amplify the antiviral siRNA response using RdRPs, all of these organisms do mount systemic antivi- ral RNAi responses that are critical for effective antiviral RNAi as an innate antiviral mechanism immunity through uptake of viral dsRNAs either se- Infection by all RNA viruses, except retroviruses, leads to creted or released by virus-infected cells (Feinberg and the generation of long dsRNAs during the virus life cycle. Hunter 2003; Saleh et al. 2009). 1152 GENES & DEVELOPMENT Downloaded from genesdev.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Viruses, microRNAs, and RNAi Plant and invertebrate viruses can block antiviral RNAi within their insect vectors is limited. In contrast, and as discussed in more detail below, there is currently no The generation of antiviral siRNAs has been observed evidence supporting the hypothesis that arboviruses, during viral infection in several plant and invertebrate such as yellow fever virus (YFV), induce a protective systems (Hamilton and Baulcombe 1999; Zamore et al. RNAi response in mammalian cells (Pfeffer et al. 2005), 2000). To counter antiviral RNAi responses, many plant and the lack of an SRS would therefore not prevent high- and invertebrate viruses have evolved proteins that act as level replication and pathogenicity in these hosts.
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