Nucleotide sequences of normal and rearranged RNA segments 10 of human rotaviruses

Ballard, Anna; McCrae, Malcolm A.; Desselberger, Ulrich

doi:10.1099/0022-1317-73-3-633

Cited by 46 publications

(34 citation statements)

References 27 publications

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“…First, based on analysis of defective interfering segments and other naturally occurring rearrangements of genome segments, members of the Reoviridae have been shown to consistently retain the 59-and 39-end regions in their normal position (Ballard et al, 1992;Feenstra et al, 2014;Gault et al, 2001;González et al, 1989;Gorziglia et al, 1989;Hua & Patton, 1994;Hundley et al, 1985;Matsui et al, 1990;Méndez et al, 1992;Pedley et al, 1984;Scott et al, 1989;Tian et al, 1993). This indicates that these regions contain all the cis-acting sequences needed to regulate packaging, genome replication and transcription of the segment.…”

Section: Identification Of Potentially Functional Inter-segment Complmentioning

confidence: 99%

Inter-segment complementarity in orbiviruses: a driver for co-ordinated genome packaging in the Reoviridae?

Boyce

McCrae

Boyce

et al. 2016

Journal of General Virology

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The process by which eukaryotic viruses with segmented genomes select a complete set of genome segments for packaging into progeny virus particles is not understood. In this study a model based on the association of genome segments through specific RNA-RNA interactions driven by base pairing was formalized and tested in the Orbivirus genus of the Reoviridae family. A strategy combining screening of the genomic sequences for inter-segment complementarity with direct functional testing of inter-segment RNA-RNA interactions using reverse genetics is described in the type species of the Orbivirus genus, Bluetongue virus (BTV). Two examples, involving four of the ten BTV genomic segments, of specific intersegment interaction motifs whose maintenance is essential for the generation of infectious virus, were identified. Equivalent inter-segment complementarities were found between the identified regions of the orthologous genome segments of all orbiviruses, including phylogenetically distant species. Specific interaction of the participating RNA segments was confirmed in vitro using electrophoretic mobility shift assays, with the interactions inhibited using oligonucleotides complementary to the interaction motif of one of the interacting partners, and also through mutagenesis of the motifs. In each example, the base pairing rather than the absolute sequence was critical to the formation of a functional inter-segment interaction, with mutations only being tolerated in rescued virus if compensating changes were made in the interacting partner to restore uninterrupted base pairing. The absolute sequence of the complementarity motifs varied between species, indicating that this newly identified phenomenon may contribute to the observed lack of reassortment between Orbivirus species.

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Section: Identification Of Potentially Functional Inter-segment Complmentioning

confidence: 99%

Inter-segment complementarity in orbiviruses: a driver for co-ordinated genome packaging in the Reoviridae?

Boyce

McCrae

Boyce

et al. 2016

Journal of General Virology

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“…Defective interfering segments and other naturally occurring rearrangements of genome segments in members of the Reoviridae have been shown to consistently retain the 59 and the 39 end regions of the affected genome segment (Ballard et al, 1992;Desselberger, 1996;Feenstra et al, 2014;Gault et al, 2001;González et al, 1989;Gorziglia et al, 1989;Hua & Patton, 1994;Hundley et al, 1985;Matsui et al, 1990;Méndez et al, 1992;Palombo et al, 1998;Pedley et al, 1984;Scott et al, 1989;Shen et al, 1994;Tian et al, 1993). In each case the two regions are retained in their normal positions at the termini of the segment, indicating that they contain the cis-acting sequences which regulate transcription, genome replication and packaging of the segment.…”

Section: Introductionmentioning

confidence: 99%

Rapid mapping of functional cis-acting RNA elements by recovery of virus from a degenerate RNA population: application to genome segment 10 of bluetongue virus

Boyce

McCrae

2015

Journal of General Virology

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“…Current hypotheses suggest that the RNA-dependant RNA polymerase of the virus may jump back on its template during either the transcription (plus-strand synthesis) (20) or the replication (minus-strand synthesis) (9) step. Direct repeats that might favor the polymerase switch have been found close to the rearrangement site in some cases (3,13,20,38) but not in others (25,36).…”

mentioning

confidence: 99%

“…The duplication started from various positions after the stop codon and extended up to the 3Ј end, leading to a long 3Ј UTR (9). Thus, the rearranged gene expressed a normal protein product (3,27,38). However, Tian et al described two bovine rotavirus variants with rearrangements in the gene 5 that modified the ORF (42).…”

mentioning

confidence: 99%

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A Human Rotavirus with Rearranged Genes 7 and 11 Encodes a Modified NSP3 Protein and Suggests an Additional Mechanism for Gene Rearrangement

Gault

Schnepf

Poncet

et al. 2001

J Virol

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A human rotavirus (isolate M) with an atypical electropherotype with 14 apparent bands of double-stranded RNA was isolated from a chronically infected immunodeficient child. MA-104 cell culture adaptation showed that the M isolate was a mixture of viruses containing standard genes (M0) or rearranged genes: M1 (containing a rearranged gene 7) and M2 (containing rearranged genes 7 and 11). The rearranged gene 7 of virus M1 (gene 7R) was very unusual because it contained two complete open reading frames (ORF). Moreover, serial propagation of virus M1 in cell culture indicated that gene 7R rapidly evolved, leading to a virus with a deleted gene 7R (gene 7R⌬). Gene 7R⌬ coded for a modified NSP3 protein (NSP3m) of 599 amino acids (aa) containing a repetition of aa 8 to 296. The virus M3 (containing gene 7R⌬) was not defective in cell culture and actually produced NSP3m. The rearranged gene 11 (gene 11R) had a more usual pattern, with a partial duplication leading to a normal ORF followed by a long 3 untranslated region. The rearrangement in gene 11R was almost identical to some of those previously described, suggesting that there is a hot spot for gene rearrangements at a specific location on the sequence. It has been suggested that in some cases the existence of short direct repeats could favor the occurrence of rearrangement at a specific site. The computer modeling of gene 7 and 11 mRNAs led us to propose a new mechanism for gene rearrangements in which secondary structures, besides short direct repeats, might facilitate and direct the transfer of the RNA polymerase from the 5 to the 3 end of the plus-strand RNA template during the replication step.

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Nucleotide sequences of normal and rearranged RNA segments 10 of human rotaviruses

Cited by 46 publications

References 27 publications

Inter-segment complementarity in orbiviruses: a driver for co-ordinated genome packaging in the Reoviridae?

Inter-segment complementarity in orbiviruses: a driver for co-ordinated genome packaging in the Reoviridae?

Rapid mapping of functional cis-acting RNA elements by recovery of virus from a degenerate RNA population: application to genome segment 10 of bluetongue virus

A Human Rotavirus with Rearranged Genes 7 and 11 Encodes a Modified NSP3 Protein and Suggests an Additional Mechanism for Gene Rearrangement

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