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Chapter 15 : Picornaviruses as a Model for Studying the Nature of RNA Recombination

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Abstract:

The possibility of recombination should obviously depend on the fate and status of the viral RNA in the infected cell. Two fundamentally different but not mutually exclusive mechanisms of RNA recombination were proposed at an early step of investigation of this phenomenon. The preciseness of recombination may also be interpreted in favor of the replicative model. Perhaps the most formidable problem of replicative RNA recombination is finding the proper anchoring site on the secondary template. The crossovers during RNA recombination can be distributed over the whole viral genome, indicating that no specific sequences or structures are required. Numerous examples of natural interserotype picornavirus recombinants have been described in this chapter. The chapter focuses on an aspect especially important from the evolutionary perspective, namely, the possible role of RNA recombination in viral speciation. Remarkably, IRESs of some picornaviruses exhibit marked structural similarities to respective -elements of viruses belonging to other families of RNA viruses, e.g., . In addition to picornaviruses, it is very common in nidoviruses, in particular, coronaviruses and toroviruses. It should be noted that mechanisms of RNA recombination other than the aforementioned classical template switch and apparently host protein-dependent nonreplicative mode have been proposed to occur in some systems. Another promising approach consists of using small interfering RNA to identify host genes involved in RNA recombination, a technique not yet attempted for picornaviruses.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Figures

Image of Figure 1.
Figure 1.

Replicative and nonreplicative models of RNA recombination. Note that the primary recombinant molecule generated by the replicative (template switch) mechanism corresponds to the complements of portions of the parental molecules, whereas that generated by the nonreplicative mechanism has the polarity of the parental molecules.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 2.
Figure 2.

A model implicating “supporting” sequences to keep two parental templates in close proximity. Such proximity has been suggested ( ) to allow a “smooth” template switch during the generation of a recombinant molecule.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 3.
Figure 3.

Hypothetical ( ) heteroduplex intermediate of replicative RNA recombination. Two viral genomic RNA molecules possessing similar hairpin structures (a and a′) anneal with one another, generating a heteroduplex (step 1). Synthesis of a complementary strand is initiated at the 3′ terminus of one of the parental molecules (step 2). The template switch takes place at a homologous site in the base-paired region (step 3). Synthesis of the nascent complementary strand is completed using the second parental molecule as a template (step 4).

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 4.
Figure 4.

Schematic (not to scale) of the poliovirus genome and the RNA partners used in experiments ( ) demonstrating nonhomologous nonreplicative RNA recombination targeted at the 5′ UTR. The major components of poliovirus RNA are indicated: VPg; the 5′ UTR with its replicative oriL and translational IRES, -elements; a promiscuous region between nucleotides 588 and 743; polyprotein-coding region; the 3′ UTR with its replicative -element oriR; poly(A). The 5′ partners are represented by truncated poliovirus 5′ UTR RNA containing an intact oriL and IRES, and also a portion of the promiscuous spacer, whereas these two essential -elements are either inactivated or deleted in the full-length 3′ partners. Cotransfection of susceptible cells with the two partners readily generated infectious recombinant progeny.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 5.
Figure 5.

Distribution of crossovers upon nonhomologous RNA recombination between the pair of partners shown in Fig. 4 (also based on reference and unpublished observations). Dotted lines correspond to identical portions of the promiscuous regions of the two partners. Recombination events within these portions did occur, but they are not depicted in the figure due to the impossibility of precisely mapping crossovers. Other portions of the promiscuous region were engineered to be specific for each partner. Arrows correspond to clusters of crossovers (“hot spots”).

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 6.
Figure 6.

Schematic representation of partners used in experiments ( ) demonstrating homologous nonreplicative RNA recombination targeted at the sequence encoding viral RNA polymerase 3D. The partners correspond, respectively, to 3′-truncated and 5′-truncated pieces of the poliovirus RNA with an overlap within the 3D-coding sequence.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 7.
Figure 7.

Dependence of the structure of a recombinant genome on the chemical nature of the partners’ termini ( ). Circles, full and striped, denote the 3′-terminal nucleotide of the 5′ partner and 5′-terminal nucleotide of the 3′ partner, respectively. The presence of a 3′-terminal phosphate on the 5′ partner or 5′-terminal OH group on the 3′ partner promotes incorporation of the entire respective partner into the recombinant molecule. The absence of the above functional groups on the terminal nucleotides results in predominantly internal crossovers (i.e., occurring within the overlap).

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 8.
Figure 8.

Schematic and simplified representation of the genomes of several picornavirus genera. The lengths of the UTRs and protein-coding regions are not drawn to scale. Identical shading signifies a marked similarity, rather than identity, of the respective nucleotide and amino acid sequences. Variability of the 3′ UTR is not shown because there is essentially no similarity of this genomic part in the different picornavirus genera. Empty spaces denote the absence of L protein. Evidently, there is no strict correlation between the structures of the 5′ UTR, L (or even its presence or absence), and 2A (and 3′ UTR, also). The actual mosaic situation is even more complex because (i) differences in the 5′-end-adjacent replicative -elements (oriL) are not shown, and (ii) different representatives of a given genus may have structurally and functionally different 5′ UTRs ( ) and 2A proteins, and some picornaviruses have more than one 2A protein ( ).

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 9.
Figure 9.

Schematic representation of generation of interspecies recombinants between poliovirus and CVB3 with the crossovers in the 5′ UTR/VP4 regions (Gmyl et al., unpublished). CVB3-N70 stands for CVB3 with a randomized 3′ UTR ( ). In poliovirus-Cp148/2A, the IRES was replaced by a 148-nucleotide sequence derived from a plant virus RNA; in addition, a poliovirus 2A-recognizable cleavage site was engineered just before the start of the VP4-coding sequence. (A) Generation of homologous recombinants with crossovers within the VP4 gene. (B) Generation of nonhomologous recombinants acquiring a novel “leader” protein encoded in part by sequences derived from a 5′-terminal portion of the CVB3 VP4-coding sequence and 5′ UTR of the poliovirus-Cp148/2A RNA.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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Image of Figure 10.
Figure 10.

Schematic representation of generation of interspecies recombinants between poliovirus and CVB3 with crossovers in the 3D/3′ UTR (Gmyl et al., unpublished). The recombinants possess an extended 3′ UTR, composed of portions of randomized CVB3-N70-derived sequence and poliovirus 3D-coding sequence as well as the intact poliovirus 3′ UTR.

Citation: Agol V. 2010. Picornaviruses as a Model for Studying the Nature of RNA Recombination, p 239-252. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch15
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