Shared and Group-Specific Features of the Rotavirus RNA Polymerase Reveal Potential Determinants of Gene Reassortment Restriction

McDonald, Sarah; Aguayo, Daniel; González‐Nilo, Fernando; Patton, John T.

doi:10.1128/jvi.00409-09

Cited by 45 publications

(68 citation statements)

References 44 publications

(74 reference statements)

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“…The RNA polymerase domain in VP1 and N-terminal RNA-binding domain in NSP3 are evidently conserved compared with other regions in individual proteins, as also found in cognate proteins of GAR (Rao et al, 1995;Heiman et al, 2008;McDonald et al, 2009). In these domains, some amino acids/motifs are commonly found among GAR, GBR and GCR, despite high sequence diversity among them.…”

Section: Discussionmentioning

confidence: 93%

“…The RNA polymerase domain of VP1 (finger I, II, palm I, II, and thumb) located in the central portion (469 aa) (McDonald et al, 2009), including functionally critical motifs shared by different rotavirus groups as well as other RNA viruses (Cohen et al, 1989;Nagashima et al, 2008), was highly conserved among GBRs (Fig. 2).…”

Section: Divergent Regions In Viral Proteinsmentioning

confidence: 99%

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Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments

Yamamoto

Ghosh

Ganesh

et al. 2010

Journal of General Virology

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Group B rotavirus (GBR) is a rare enteric pathogen that causes severe diarrhoea, primarily in adults. Nearly full-length sequences of all 11 RNA segments were determined for human GBRs detected recently in India (IDH-084 in 2007, IC-008 in 2008, Bangladesh (Bang117 in 2003) and Myanmar (MMR-B1 in 2007), and analysed phylogenetically with the sequence data of GBRs reported previously. All RNA segments of GBR strains from India, Bangladesh and Myanmar showed .95 % nucleotide sequence identities. Among the 11 RNA segments, the VP6 and NSP2 genes showed the highest identities (.98 %), whilst the lowest identities were observed in the NSP4 gene (96.1 %), NSP5 gene (95.6 %) and VP8*-encoding region of the VP4 gene (95.9 %). Divergent or conserved regions in the deduced amino acid sequences of GBR VP1-VP4 and NSP1-NSP5 were similar to those in group A rotaviruses (GARs), and the functionally important motifs and structural characteristics in viral proteins known for GAR were conserved in all of the human GBRs. These findings suggest that, whilst the degree of genetic evolution may be dependent on each RNA segment, human GBR may have been evolving in a similar manner to GAR, associated with the similar functional roles of individual viral proteins. INTRODUCTIONRotavirus, a member of the family Reoviridae, is the most important viral pathogen causing gastroenteritis in humans. Rotavirus has 11 segments of double-stranded RNA (dsRNA) as a genome, and the virus particle is composed of three concentric layers, i.e. the outer capsid, inner capsid and core (Estes & Kapikian, 2007). The outer capsid consists of two structural proteins, VP4 and VP7, which are neutralization antigens. The inner capsid consists of structural protein VP6. Rotavirus is classified into five groups (A-E) and two putative groups (F and G), based on the antigenicity of the inner capsid protein VP6 and genomic characteristics (Kapikian et al., 2001). In humans, groups A, B and C have so far been detected. Group A rotavirus (GAR) is the most prevalent throughout the world and is recognized as the leading viral pathogen of acute gastroenteritis in children.Group B rotavirus (GBR) is genetically and antigenically distinct from GAR and has been detected in humans, mice, calves, pigs and sheep. In humans, GBR has been noted because it causes severe, cholera-like diarrhoea, mostly in adults (Mackow, 1995). GBR was first identified as adult diarrhoea rotavirus (ADRV) in nationwide outbreaks in China in 1982-1983 (Hung et al., 1983, 1984Wang et al., 1985), and the detection of this virus has been limited to China (Dai et al., 1987; Fang et al., 1989). They were subsequently detected in sporadic cases in India in 1997 and in Bangladesh in 2000, demonstrating the distribution of GBRs in Asian countries outside China (Krishnan et al., 1999;Sanekata et al., 2003). Thereafter, GBRs have again been detected in these countries in sporadic cases of diarrhoea (Barman et al., 2006;Rahman et al., 2007). The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequen...

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Section: Discussionmentioning

confidence: 93%

Section: Divergent Regions In Viral Proteinsmentioning

confidence: 99%

Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments

Yamamoto

Ghosh

Ganesh

et al. 2010

Journal of General Virology

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“…Since the proposal that RV-A classification should be based on all 11 RV-A gene segments (Matthijnssens et al, 2008b), the number of studies reporting RV-A full genome sequences has increased Esona et al, 2010bMatthijnssens et al, 2008a;McDonald et al, 2009McDonald et al, , 2011MijatovicRustempasic et al, 2011). Previous studies have shown that the predominance of a specific G type is related to the emergence of atypical VP7 lineages Parra, 2009;Parra et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…The genetic variability of RV-A strains is the result of accumulation of single nucleotide mutations (genetic drift) and sudden changes in the RV-A genome (genetic shift), primarily by reassortment and recombination events (Estes and Kapikian, 2007;Matthijnssens et al, 2008c;McDonald et al, 2009;Ramig, 1997). Since the proposal that RV-A classification should be based on all 11 RV-A gene segments (Matthijnssens et al, 2008b), the number of studies reporting RV-A full genome sequences has increased Esona et al, 2010bMatthijnssens et al, 2008a;McDonald et al, 2009McDonald et al, , 2011MijatovicRustempasic et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Human G9P[8] rotavirus strains circulating in Cameroon, 1999–2000: Genetic relationships with other G9 strains and detection of a new G9 subtype

Esona

Mijatovic-Rustempasic

Foytich

et al. 2013

Infection, Genetics and Evolution

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Group A rotaviruses (RV-A) are the leading cause of viral gastroenteritis in children worldwide and genotype G9P[8] is one of the five most common genotypes detected in humans. In order to gain insight into the degree of genetic variability of G9P [8] HHS Public Access BackgroundChildhood mortality has been declining worldwide as a result of socioeconomic development and implementation of prevention and survival interventions (Claeson et al., 2000). Group A rotaviruses (RV-A) are the main etiologic agent of acute gastroenteritis in infants and young children worldwide (Estes and Kapikian, 2007) and an estimated 453,000 children aged <5 years die from rotavirus diarrhea each year, with >85% of these deaths occurring in low-income countries of Africa and Asia (Parashar et al., 2009;Tate et al., 2011). Rotaviruses belong to the family Reoviridae, and the rotavirus genome consists of 11 double-stranded RNA gene segments that encode six structural (VP) and six non-structural proteins (NSP). Based on the two genes that encode the outer capsid proteins, VP4 (P-type) and VP7 (G-type), a widely used binary classification system was established for RV-A (Estes and Kapikian, 2007). This system has been recently standardized and extended to all 11 genes (Matthijnssens et al., 2008b). To date, at least 27 G, 35 P, 16 I, 9 R, 9 C, 8 M, 16 A, 9 N, 12 T, 14 E and 11 H genotypes have been identified based on the eleven rotavirus A genes (Esona et al., 2010b;Matthijnssens et al., 2011). In humans, at least five RV-A G types (G1-G4 and G9), and two common P types (P[8] and P[4]) circulate worldwide (Banyai et al., 2012;Gentsch et al., 2005;Santos and Hoshino, 2005). G9 strains emerged in 1990s, and there has been a global description of the appearance and dominance of this genotype (Gentsch et al., 2005;Laird et al., 2003;Matthijnssens et al., 2009;Santos and Hoshino, 2005). Genotype G9 strains with a Wa-like or a DS-1-like genomic configuration or a mixture thereof have been detected sporadically in localized outbreaks (Page et al., 2010). In Cameroon, the first molecular identification of genotype G9 in human samples was reported in a study conducted by colleagues in 2003 (Steele andIvanoff, 2003). At least seven major phylogenetic lineages and eleven minor lineages within G9 VP7 genes have been described (Phan et al., 2007;Wu et al., 2011). A molecular evolutionary analysis study utilizing Bayesian inference supported the idea that one single sub-lineage introduced in the 1980s was responsible for all the worldwide spread of G9 in the 1990s .In order to gain insight into the degree of genetic variability of G9P [8] Viral RNA extraction, amplification, and sequencingViral RNA from each of the 15 specimens was extracted from a 10% stool suspension made from 0.1 g or 100 μl stool in 2 ml of a 1:1 Vertrel/Water solution using either a commercial RNA extraction kit (NucliSens automated extractor, BIOMERIEUX, Durham, NC) according to the protocol specified by the manufacturer or a silica binding method described pr...

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“…If complementarity is involved in the packaging mechanisms of RVA, co-evolution of complementary nucleotides may suppress reassortments between distantly related strains (Heiman et al, 2008;McDonald et al, 2009aMcDonald et al, , 2009bMcDonald and Patton, 2011;. Reassortment is known to occur within mammalian and avian RVA (Ward et al, 1990;Schumann et al, 2009).…”

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confidence: 99%

A possible packaging signal in the rotavirus genome

Suzuki

2014

Genes Genet. Syst.

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Group A rotavirus (RVA), an etiological agent of gastroenteritis in young mammals and birds, possesses a genome of 11 double-stranded RNA segments. Although it is believed that the RVA virion contains one copy of each genomic segment and that the positive-strand RNA (+RNA) is incorporated into the core shell, the packaging mechanisms of RVA are not well understood. Here, packaging signals of RVA were searched for by analyzing genomic sequences of mammalian and avian RVA, which are considered to have evolved independently without reassortment. Assuming that packaging is mediated by direct interaction between +RNA segments via base-pairing, co-evolving complementary nucleotide sites were identified within and between genomic segments. There were two pairs of co-evolving complementary sites within the segment encoding VP7 (the VP7 segment) and one pair between the NSP2 and NSP3 segments. In the VP7 segment, the co-evolving complementary sites appeared to form stem structures in both mammalian and avian RVA, supporting their functionality. In contrast, coevolving complementary sites between the NSP2 and NSP3 segments tended to be free from base-pairings and constituted loop structures, at least in avian RVA, suggesting that they are involved in a specific interaction between these segments as a packaging signal.

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Shared and Group-Specific Features of the Rotavirus RNA Polymerase Reveal Potential Determinants of Gene Reassortment Restriction

Cited by 45 publications

References 44 publications

Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments

Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments

Human G9P[8] rotavirus strains circulating in Cameroon, 1999–2000: Genetic relationships with other G9 strains and detection of a new G9 subtype

A possible packaging signal in the rotavirus genome

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