Pattern of Circulation of Norovirus GII Strains during Natural Infection

Ayukekbong, James A; Fobisong, Cajetan; Tah, Ferdinand; Lindh, Magnus; Nkuo‐Akenji, Theresa; Bergström, Tomas

doi:10.1128/jcm.01896-14

Cited by 28 publications

(27 citation statements)

References 31 publications

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“…Second, the optimal HPP inactivation conditions and the uniformity of strain responses to those conditions for multiple HuNoVs have not been defined. In recent years, GII.6 and GII.1 have emerged worldwide and have caused many outbreaks (28,29). Therefore, there is an urgent need to determine whether HPP can effectively inactivate these newly emerged genotypes.…”

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confidence: 99%

Variable High-Pressure-Processing Sensitivities for Genogroup II Human Noroviruses

Lou

DiCaprio

et al. 2016

Appl Environ Microbiol

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Human norovirus (HuNoV) is a leading cause of foodborne diseases worldwide. High-pressure processing (HPP) is one of the most promising nonthermal technologies for the decontamination of viral pathogens in foods. However, the survival of HuNoVs after HPP is poorly understood because these viruses cannot be propagated in vitro. In this study, we estimated the survival of different HuNoV strains within genogroup II (GII) after HPP treatment using viral receptor-binding ability as an indicator. Four HuNoV strains (one GII genotype 1 [GII.1] strain, two GII.4 strains, and one GII.6 strain) were treated at high pressures ranging from 200 to 600 MPa. After treatment, the intact viral particles were captured by porcine gastric mucin-conjugated magnetic beads (PGM-MBs) that contained histo-blood group antigens, the functional receptors for HuNoVs. The genomic RNA copies of the captured HuNoVs were quantified by real-time reverse transcriptase PCR (RT-PCR). Two GII.4 HuNoVs had similar sensitivities to HPP. The resistance of HuNoV strains against HPP ranked as follows: GII.1 > GII.6 > GII.4, with GII.4 being the most sensitive. Evaluation of temperature and matrix effects on HPP-mediated inactivation of HuNoV GII.4, GII.1, and GII.6 strains showed that HuNoV was more easily inactivated at lower temperatures and at a neutral pH. In addition, phosphate-buffered saline (PBS) and minimal essential medium (MEM) can provide protective effects against HuNoV inactivation compared to H 2 O. Collectively, this study demonstrated that (i) different HuNoV strains within GII exhibited different sensitivities to high pressure, and (ii) HPP is capable of inactivating HuNoV GII strains by optimizing pressure parameters. IMPORTANCEHuman norovirus (HuNoV) is a leading cause of foodborne disease worldwide. Noroviruses are highly diverse, both antigenically and genetically. Genogroup II (GII) contains the majority of HuNoVs, with GII genotype 4 (GII.4) being the most prevalent. Recently, GII.1 and GII.6 have emerged and caused many outbreaks worldwide. However, the survival of these GII HuNoVs is poorly understood because they are uncultivable in vitro. Using a novel receptor-binding assay conjugated with real-time RT-PCR, we found that GII HuNoVs had variable susceptibilities to high-pressure processing (HPP), which is one of the most promising food-processing technologies. The resistance of HuNoV strains to HPP ranked as follows: GII.1 > GII.6 > GII.4. This study highlights the ability of HPP to inactivate HuNoV and the need to optimize processing conditions based on HuNoV strain variability and sample matrix.

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confidence: 99%

Variable High-Pressure-Processing Sensitivities for Genogroup II Human Noroviruses

Lou

DiCaprio

et al. 2016

Appl Environ Microbiol

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“…HBGAs are also found as soluble antigens in saliva and are expressed on epithelial cells. Genetic polymorphisms in genes that control their synthesis are known to provide intraspecies diversity (13). To date, based on the ABH and Lewis HBGA types, at least nine different HBGAs have been found to interact with human noroviruses.…”

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Human Noroviruses' Fondness for Histo-Blood Group Antigens

Singh

Leuthold

Hansman

2015

J Virol

111

133

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IMPORTANCEOur data provide a comprehensive picture of GII.4 P domain and HBGA binding interactions. The exceptionally high resolutions of our X-ray crystal structures allowed us to accurately recognize novel GII.4 P domain interactions with numerous HBGA types. We showed that the GII.4 P domain-HBGA interactions involved complex binding mechanisms that were not previously observed in norovirus structural studies. Many of the GII.4 P domain-HBGA interactions we identified were negative in earlier enzyme-linked immunosorbent assay (ELISA)-based studies. Altogether, our data show that the GII.4 norovirus P domains can accommodate numerous HBGA types. Human noroviruses are responsible for most epidemic outbreaks of gastroenteritis. There are still no antivirals or vaccines approved, despite the discovery of these viruses over 4 decades ago (1). Noroviruses are genetically and antigenically diverse (2), yet a single genetic cluster (genogroup II, genotype 4 [GII.4]) has dominated over the past decade (3). The GII.4 noroviruses evolve ϳ5% every year and are believed to have a mechanism that allows them to evade the immune system or alter receptor binding profiles (4-6). However, immunity to noroviruses is still poorly understood (7).Human noroviruses interact with histo-blood group antigens (HBGAs), and this is thought to be important for viral infections (8-11). A recent report showed for the first time that human noroviruses infect B cells and that HBGAs (synthetic or from HBGAexpressing enteric bacteria) can enhance the infection (12). HBGAs are also found as soluble antigens in saliva and are expressed on epithelial cells. Genetic polymorphisms in genes that control their synthesis are known to provide intraspecies diversity (13). To date, based on the ABH and Lewis HBGA types, at least nine different HBGAs have been found to interact with human noroviruses. Individuals expressing the O type are thought to have a significantly higher infection rate than those for individuals with other blood types (11). The GII noroviruses are thought to have preferences for HBGAs in a strain-dependent manner (14)(15)(16)(17)(18)(19).Expression of the norovirus capsid protein in insect cells results in the formation of virus-like particles (VLPs) that are antigenically similar to native virions. The X-ray crystal structure of prototype (GI.1) norovirus VLPs identified two domains: the shell (S) and protruding (P) domains (20). The S domain forms a scaffold surrounding the viral RNA, whereas the P domain is thought to contain the determinants for cell attachment and strain diversity. The P domain can be further subdivided into P1 and P2 subdomains, and each subdomain likely has unique functions. In this study, we determined the X-ray crystal structures of P domains from three epidemic GII.4 variants, from 2004GII.4 variants, from , 2006GII.4 variants, from , and 2012, in complex with a panel of HBGAs in order to elucidate HBGA binding mechanisms. Our data showed that the GII.4 noroviruses bound numerous HBGA types and that bindi...

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“…RHDV was the first calicivirus shown to interact with HBGAs (22), followed by noroviruses (23,32). HBGAs can be subdivided into ABH and Lewis antigens (33), of which at least four were found to interact with RHDV (16). We determined the structures of the RHDVb P domain Le y -tetra and H2-tri complexes using X-ray crystallography (Table 1).…”

Section: Resultsmentioning

confidence: 99%

Structural Analysis of a Rabbit Hemorrhagic Disease Virus Binding to Histo-Blood Group Antigens

Leuthold

Dalton

Hansman

2015

J Virol

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Rabbit hemorrhagic disease virus (RHDV) is a member of the Caliciviridae family (Lagovirus genus). RHDV is highly contagious and attaches to epithelial cells in the digestive or respiratory tract, leading to massive lesions with high mortality rates. A new variant of RHDV (termed RHDVb) recently has emerged, and previously vaccinated rabbits appear to have little protection against this new strain. Similar to human norovirus (Caliciviridae, Norovirus genus), RHDV binds histo-blood group antigens (HBGAs), and this is thought to be important for infection. Here, we report the HBGA binding site on the RHDVb capsid-protruding domain (P domain) using X-ray crystallography. The HBGA binding pocket was located in a negatively charged patch on the side of the P domain and at a dimeric interface. Residues from both monomers contributed to the HBGA binding and involved a network of direct hydrogen bonds and water-mediated interactions. An amino acid sequence alignment of different RHDV strains indicated that the residues directly interacting with the ABH-fucose of the HBGAs (Asp472, Asn474, and Ser479) were highly conserved. This result suggested that different RHDV strains also could bind HBGAs at the equivalent pocket. Moreover, several HBGA binding characteristics between RHDVb and human genogroup II norovirus were similar, which indicated a possible convergent evolution of HBGA binding interactions. Further structural studies with other RHDV strains are needed in order to better understand the HBGA binding mechanisms among the diverse RHDV strains. IMPORTANCEWe identified, for the first time, the HBGA binding site on an RHDVb P domain using X-ray crystallography. Our results showed that RHDVb and human genogroup II noroviruses had similar HBGA binding interactions. Recently, it was discovered that synthetic HBGAs or HBGA-expressing enteric bacteria could enhance human genogroup II norovirus infection in B cells. Considering that RHDVb and genogroup II norovirus similarly interacted with HBGAs, it may be possible that a comparable cell culture system also could work with RHDVb. Taken together, these new findings will extend our understanding of calicivirus HBGA interactions and may help to elucidate the specific roles of HBGAs in calicivirus infections. Rabbit hemorrhagic disease (RHD) was first reported in China in 1984 (1), and the etiological agent, rabbit hemorrhagic disease virus (RHDV; Caliciviridae family, Lagovirus genus), was identified subsequently (2-4). RHDV is highly contagious and is endemic in several countries with wild rabbit populations. The virus attaches to epithelial cells in the digestive or respiratory tract and can lead to massive lesions in the liver, trachea, and lungs of adult rabbits. High mortality rates in the range of 90% can lead to a drastic decimation of rabbit populations (reviewed in reference 5), which is an ecological threat and economic burden. A vaccine for RHDV was introduced in the 1990s (6), and this provided good coverage for the strains circulating at that time and ...

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Pattern of Circulation of Norovirus GII Strains during Natural Infection

Cited by 28 publications

References 31 publications

Variable High-Pressure-Processing Sensitivities for Genogroup II Human Noroviruses

Variable High-Pressure-Processing Sensitivities for Genogroup II Human Noroviruses

Human Noroviruses' Fondness for Histo-Blood Group Antigens

Structural Analysis of a Rabbit Hemorrhagic Disease Virus Binding to Histo-Blood Group Antigens

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