Studies on the recombination between RNA genomes of poliovirus: The primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants

Tolskaya, Elena A.; Romanova, Lyudmila I.; Блинов, В. М.; Viktorova, Ekaterina G.; Sinyakov, A. N.; Kolesnikova, Marina S.; Agol, Vadim I.

doi:10.1016/0042-6822(87)90170-x

Cited by 81 publications

(78 citation statements)

References 24 publications

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“…Surprisingly, we found recombination to occur at a predominant site within the tested stretch of about 450 nt. This might support the view that RNA structures which favor template switching exist (45,54). Conceivably, other recombinants may develop outside of or within the VP1 region investigated, notably a possible reversed recombinant having an M1 5Ј and an S2 3Ј end.…”

Section: Discussionsupporting

confidence: 48%

“…Due to the small diameter of an RNA strand, even more than two RNA strands may be lying in parallel across a 50-nm-diameter area. The actual colinear alignment of those segments of the parental RNA strands involved in the switching process was proposed to be mediated by distinct secondary structures (45,54). In addition, it was recently suggested (36) that viral RNA synthesis takes place on the surfaces of two-dimensional viral polymerase lattices forming small tubules connected to the (36).…”

Section: Discussionmentioning

confidence: 99%

“…Its frequency is 10 to 20% of recombinants among progeny strands (33), and it may take place over the entire viral genome (for reviews, see references 1 and 57). Stem-loop structures were thought to promote recombination by allowing the alignment of the parental strands for the switching process (45,54). Recombination was considered to be important for both virus evolution and genome conservation (1), and it was found to happen in the human gut at rather high frequency after vaccination with trivalent oral polio vaccine (38).…”

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confidence: 99%

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Recombination of Poliovirus RNA Proceeds in Mixed Replication Complexes Originating from Distinct Replication Start Sites

Egger

Bienz

2002

J Virol

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Genetic recombination occurs frequently during replication of picornaviruses. To explore the intracellular site and structures involved in recombination, HeLa cells were infected with poliovirus type 1 Mahoney and type 2 Sabin. The two genomes were located by fluorescent in situ hybridization and confocal microscopy. For hybridization, type-specific fluorescent riboprobes were used to visualize the same genomic region where, in parallel, recombination was demonstrated with type-specific reverse transcription-PCR and sequencing. The hybridization analysis indicated that >85% of the replication complexes contained both type 1 and type 2 RNA sequences aligned at a lateral distance of 50 nm or less. Sequential infection of cells ruled out the possibility that the high percentage of mixed replication complexes was due to aggregation of input virus. Visualization of input genomic RNA over time showed that the viral genomes migrated to relatively few distinct, and thus presumably specific, perinuclear sites where replication started. The first recombinant RNA strands could be detected concomitantly with the onset of RNA replication. The limited number of start sites for replication may be the reason for the observed preferential formation of mixed replication complexes, each accommodating several parental RNA strands and thus allowing recombination.Poliovirus (PV), the prototype member of the family Picornaviridae, represents in many respects the paradigm for research on other plus-strand RNA viruses. Among the fundamental insights gained by PV research is the first discovery of recombination between viral RNA genomes (30, 35). Since then, some light has been thrown on mechanistic aspects of recombination (for a review see references 1 and 57); however, it is not clear in which context of the elaborate structures comprising the viral RNA replication machinery, i.e., the replication complex (4,6,9,12,21,22,51,52), recombination can occur.PV RNA replication is preceded by translation of the incoming viral genome. Translation, initiated at the internal ribosomal entry site (IRES) (42, 43), was reported to be enhanced by binding of the cellular poly(rC) binding protein (PCBP) to the IRES (10,11,25) and, additionally at early stages, by an interaction of eIF4G with the IRES and the poly(A)-bound poly(A) binding protein (PABP) (50). A transition from translation to transcription was thought to be mediated by the newly synthesized viral protein 3CD, which, together with PCBP, binds to the 5Ј cloverleaf of the viral mRNA (23,24,39). Poly(A)-bound PABP then would attach to this complex, leading (again) to a 5Ј-3Ј interaction in the viral plus-strand RNA (29). This interaction was proposed to be a prerequisite for minus-strand RNA synthesis, the first step in genome replication (3,29,53). The second step in viral genome replication is plus-strand RNA synthesis, which proceeds, after multiple initiations, in the partially doublestranded replicative intermediate. The primer for RNA synthesis is VPgpUpU (41), which was found to be ...

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Section: Discussionsupporting

confidence: 48%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Recombination of Poliovirus RNA Proceeds in Mixed Replication Complexes Originating from Distinct Replication Start Sites

Egger

Bienz

2002

J Virol

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“…The findings from the PCM analysis provide little support for the existence of specifically favored sites of recombination in enteroviruses. Sites of RNA secondary structure formation have been previously shown to promote recombination in copy-choice mechanisms of RNA recombination (20,35,42), in contrast to premature termination (32) and nonreplicative models (10,11). However, there is no evidence from the PCM that recombination was specifically favored at sites of RNA structure, such as the conserved cis-replicating element (alignment positions 4439 to 4493; Fig.…”

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confidence: 67%

Frequency and Dynamics of Recombination within Different Species of Human Enteroviruses

Simmonds

Welch

2006

J Virol

239

230

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Enteroviruses are members of the family Picornaviridae that cause widespread infections in human and other mammalian populations. Enteroviruses are genetically and antigenically highly variable, and recombination within and between serotypes contributes to their genetic diversity. To investigate the dynamics of the recombination process, sequence phylogenies between three regions of the genome (VP4, VP1, and 3Dpol) were compared among species A and B enterovirus variants detected in a human population-based survey in Scotland between 2000 and 2001, along with contemporary virus isolates collected in the same geographical region. This analysis used novel bioinformatic methods to quantify phylogenetic compatibility and correlations with serotype assignments of evolutionary trees constructed for different regions of the enterovirus genome. Species B enteroviruses showed much more frequent, time-correlated recombination events than those found for species A, despite the equivalence in population sampling, concordant with a linkage analysis of previously characterized enterovirus sequences obtained over longer collection periods. An analysis of recombination among complete genome sequences by computation of a phylogenetic compatibility matrix (PCM) demonstrated sharply defined boundaries between the VP2/VP3/VP1 block and sequences to either side in phylogenetic compatibility. The PCM also revealed equivalent or frequently greater degrees of incompatibility between different parts within the nonstructural region (2A-3D), indicating the occurrence of extensive recombination events in the past evolution of this part of the genome. Together, these findings provide new insights into the dynamics of species A and B enterovirus recombination and evolution and into the contribution of structured sampling to documenting reservoirs, emergence, and spread of novel recombinant forms in human populations.The genus Enterovirus in the family Picornaviridae is a group of nonenveloped RNA viruses that cause a wide range of diseases in humans and other mammals. The enterovirus genome is a single strand of positive-sense RNA of approximately 7,500 nucleotides (nt) comprising a long open reading frame flanked 5Ј and 3Ј by untranslated regions (UTRs). The encoded polyprotein is subsequently cleaved to produce structural (capsid proteins VP1 to VP4) and nonstructural (2A and 3D) proteins. Primary infection with an enterovirus leads to viral replication in the tissue around the gastrointestinal tract, followed by a transient viremia and sometimes migration into other tissues (2, 34). Although infection in immunocompetent individuals is often asymptomatic or causes mild febrile illness, a persistent or widely disseminated, systemic infection associated with severe disease outcomes is observed in highly immunosuppressed individuals and neonates (6, 13, 18).Enteroviruses were originally classified as polioviruses, coxsackie type A or B viruses (CVA and CVB), or echoviruses (enteric cytopathic human orphan viruses), depending on the infectious...

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“…There is no evidence that such alignment may actually occur, although a somewhat similar idea-for example, formation of heteroduplexes involving short inverted repeats present in any RNA molecule-has been considered as a factor contributing to the choice of crossover sites during replicative recombination (Romanova et al 1986;Tolskaya et al 1987;Nagy and Bujarski 1993;Figlerowicz 2000). (2) Another way to obtain precise recombinants is to allow (nearly) promiscuous covalent interactions between any nucleotides, internal or terminal, in the pool of viral fragments, followed by selection of viable, that is precise or nearly so, genomes.…”

Section: Does Precision Reflect Promiscuity?mentioning

confidence: 99%

Nonreplicative homologous RNA recombination: Promiscuous joining of RNA pieces?

Gmyl¹,

Korshenko²,

Belousov³

et al. 2003

RNA

Self Cite

104

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Biologically important joining of RNA pieces in cells, as exemplified by splicing and some classes of RNA editing, is posttranscriptional, whereas in RNA viruses it is generally believed to occur during viral RNA polymerase-dependent RNA synthesis. Here, we demonstrate the assembly of precise genome of an RNA virus (poliovirus) from its cotransfected fragments, which does not require specific RNA sequences, takes place before generation of the viral RNA polymerase, and occurs in different ways: Apparently unrestricted ligation of the terminal nucleotides, joining of any one of the two entire fragments with the relevant internal nucleotide of its partner, or internal crossovers within the overlapping sequence. Incorporation of the entire 5 or 3 partners into the recombinant RNA is activated by the presence of terminal 3-phosphate and 5-OH, respectively. Such postreplicative reactions, fundamentally differing from the known site-specific and structurally demanding cellular RNA rearrangements, might contribute to the origin and evolution of RNA viruses and could generate new RNA species during all stages of biological evolution.

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Studies on the recombination between RNA genomes of poliovirus: The primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants

Cited by 81 publications

References 24 publications

Recombination of Poliovirus RNA Proceeds in Mixed Replication Complexes Originating from Distinct Replication Start Sites

Recombination of Poliovirus RNA Proceeds in Mixed Replication Complexes Originating from Distinct Replication Start Sites

Frequency and Dynamics of Recombination within Different Species of Human Enteroviruses

Nonreplicative homologous RNA recombination: Promiscuous joining of RNA pieces?

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