Host Glycobiology/Gut Microbiota in Rotavirus/Norovirus Infection

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1		Jesus Rodriguez Diaz	+ 2207 word(s)	2207	2021-12-21 09:52:53	\|
2	The format is correct	Lindsay Dong	Meta information modification	2207	2021-12-23 03:31:08	\|

This entry is adapted from the peer-reviewed paper 10.3390/ijms222413473

Rotavirus (RV) and norovirus (NoV) are the leading causes of acute gastroenteritis (AGE) worldwide. Histo-blood group antigens (HBGAs) have a role in NoV and RV infections since their presence on the gut epithelial surfaces is essential for the susceptibility to many NoV and RV genotypes. A second factor that influences enteric viral infections is the gut microbiota of the host. In vitro and animal studies have determined that the gut microbiota limits, but in some cases enhances enteric viral infection. The ways that microbiota can enhance NoV or RV infection include virion stabilization and promotion of virus attachment to host cells, whereas experiments with microbiota-depleted and germ-free animals point to immunoregulation as the mechanism by which the microbiota restrict infection.

rotavirus norovirus gut microbiota

1. Enteric Viruses and Their Impact on Human Health

Diarrheal disease was one of the top 10 global causes of death in 2016, being the second most common in low-income countries, as reported by the World Health Organization (WHO) ^[1]. Acute gastroenteritis (AGE) caused by viral infections is the most common type of diarrheal disease. Enteric viruses such as human noroviruses (NoVs) and rotaviruses (RVs) are one of the most important causes of AGE and are known to cause diarrhea, dehydration, or vomiting among other symptoms, leading to the death of patients in the worst cases. These infections have been associated with the consumption of contaminated food or water, person-to-person transmission via direct contact, exposure to aerosols, or the fecal–oral route ^[2].

2. Glycobiology Mediates Enteric Virus/Host Interactions

Carbohydrate binding is a common method many viruses and other microorganisms use to attach to their host cells. As for RV and NoV, several studies demonstrate that histo-blood group antigens (HBGAs) act as their receptors ^[3]^[4]. These complex carbohydrates are linked to proteins or lipids on the surface of red blood cells and mucosal epithelia of the respiratory, genitourinary, and digestive tracts, or as free oligosaccharides in biological fluids such as saliva ^[5]. HBGAs are synthesised from precursors by stepwise addition of monosaccharides, catalyzed by a set of glycosyltransferases coded by three major HBGA gene families: secretor, Lewis, and ABO ^[5]. The secretor gene codes for an α-1,2 fucosyltransferase (FUT2), the Lewis gene codes for an α-1,3 or α-1,4 fucosyltransferase (FUT3), while the ABO family codes for two glycosyltransferases (A and B enzymes) ^[6].

The type-1 (galactose-β-1→3-N-acetyl-glucosamine, lacto-N-biose) and the type-2 (galactose-β-1→4-N-acetyl-glucosamine, N-acetyl-lactosamine) precursors act as a substrate of the FUT2 enzyme, which modifies them by the addition of an L-fucose on the galactose moiety through an α-1→2 linkage, generating type-1 and type-2 H antigens, respectively. However, if it is the FUT3 enzyme that modifies the precursors, Le^a (type-1 precursor) and Le^x (type-2 precursor) antigens are generated. This modification consists of the addition of an L-fucose to N-acetyl-glucosamine with an α-1→4 linkage in the case of the type-1 precursor or an α-1→3 linkage in the case of the type-2 precursor. The FUT3 enzyme can also act on the H type-1 and -2 antigens generating Le^b and Le^y antigens, respectively. H type-1 and -2 antigens are also substrates of A and B enzymes, giving A and/or B blood groups as a result ^[5]^[6] (Figure 1).

Figure 1. Biosynthesis route for type-1 and -2 HBGAs. The type-1 and the type-2 precursors are further elongated by the fucosyltransferase-2 (FUT2) that adds fucose in α-1→2 to the galactose moiety and the fucosyltransferase-3 (FUT3) that adds fucose in α-1→3/4 to N-acetyl-glucosamine to produce H and Lewis antigens, respectively. Similarly, the A and B enzymes elongate the sugar chains by attaching an N-acetyl-galactosamine or galactose in α-1→3 to the galactose moiety, producing the A and B blood groups, respectively.

Several mutations in the FUT2 or FUT3 genes lead to a total absence or a decreased function of the corresponding fucosyltransferases. The absence of α-1→2- or α-1→3/4-fucosylated antigens in mucous surfaces and secretions determines the non-secretor and the Lewis negative phenotype, respectively ^[7]. Therefore, these genetic polymorphisms regulate the presence and absence of certain HBGAs, which in turn affects the interaction, susceptibility, or resistance to pathogens that recognize HBGAs as binding molecules ^[8]^[9].

2.1. HBGAs and RV

Despite the fact that a substantial amount of research has been carried out in the last few years on the RV mechanisms for host cell attachment, the process is still far from being understood. It is known that the VP4 spike protein (determining the viral P genotype) participates in the process and early studies with some P genotypes from animal origin revealed its interaction with sialic acid, whereas other animal and the human RV were sialic acid-independent and interacted with HBGAs ^[10]^[11]. VP4 from RV is post-translationally cleaved into VP8* (glycan-binding domain) and VP5* polypeptides, the VP8* portion being the one responsible for cellular attachment and entry, as well as HBGA binding ^[12]. The P genotypes would thus determine the pattern of genetic susceptibility. VP8* from P[8], P[4], P[6], P[14], P[11], and P[19] genotypes recognize the secretor HBGAs. Regarding P[8] and P[4] genotypes, there were controversial studies since some determined that they bind the Le^b and H type-1 ^[13]^[14]^[15]^[16], while others report no Le^b binding for these genotypes ^[17]^[18]. P[6] binds the H1 antigen but was reported not to bind Le^b ^[19], whereas P[19] binds mucin core glycans with the GlcNAc-β-1→6-GalNAc motif and the type-1 HBGA precursor ^[20]. Other studies also documented that P[9], P[14], and P[25] strains interact with the A antigen ^[12]^[21], whereas P[11] interacts with single and repeated N-acetyl-lactosamine, the type-2 precursor glycan ^[22]. The HBGAs interactions with VP8* have been investigated by X-ray crystallography in some cases, identifying sugar binding pockets which are different from the sialic acid binding site identified in animal RV ^[18]. The binding site for N-acetyl-lactosamine and A-antigen in P[11] and P[14] genotypes, respectively, is situated in a cleft between two twisted β-sheets of the typical galectin fold in VP8* ^[21]^[22]. A second pocket was identified in P[4], P[6], and P[19] genotypes for lacto-N-fucopentaose I (Fuc-α-1→2-Gal-β-1→3-GlcNAc-β-1→3-Gal-β-1→4-Glc) ^[18]^[23] and in P[8] for lacto-N-biose and H type-1 antigen binding ^[17], which is formed by one of the β-sheets and a C-terminal α-helix. This pocket is not able to accommodate the Le^b antigen, which contains an extra α-1→4-linked L-fucose. A second glycan-binding site for Le^b formed by the edges of two β-sheets in the VP8* structure has been identified in P[4] and P[8] genotypes and validated by crystallography and NMR techniques ^[15]. This provides evidence that classical techniques to identify the interactions between VP8* and HBGAs (e.g., glycan-binding assays in ELISA-like format) do not always give reliable results. Therefore, these two viral genotypes possess two glycan-binding sites which may reflect an adaptation to different host HBGAs polymorphisms.

2.2. HBGAs and NoV

The P2 subdomain found in the P-domain of the VP1 protein from NoVs interacts with HBGAs. Several studies have been made in order to elucidate the recognition pattern of NoVs. Some of them are based on the expression of the P-domain in vitro, which results in dimerization (P dimer) and the formation of P particles that retain HBGA-binding function, while others used virus-like particles (VLPs). These studies have utilized ELISA or haemagglutination-based assays using saliva, human milk, red blood cells, or synthetic oligosaccharides as HBGAs sources. The prototype Norwalk virus (GI.1) recognizes the type A and H secretors, but does not interact with type B secretors and non-secretors; Va387 (GII.4) binds to A, B, and O secretors; MOH (GII.5) and Hiro (GII.12) bind to A and B secretors; and Va207 (GII.9) recognizes Lewis positive secretors and non-secretors (Le^x and Le^y) ^[6]^[24]. As for the GII.4 strains Den Haag_2006b and Sydney_2012, Carmona et al. demonstrated that they did not recognize any HBGAs ^[25]. By contrast, these strains may recognize heparan sulphate or citrate since they are all capable of binding human NoV and may potentially play a role in NoV pathogenesis as cellular receptors/co-factors ^[26]. GI.3 NoV VLPs show strong binding to blood type A salivary HBGAs, slightly lower binding to blood type O salivary HBGAs, and weakly binding or none to blood type B and AB salivary HBGAs ^[27].

3. The Role of Bacteria in RVs and NoVs Infection

3.1. Bacteria against Enteric Viral Infections

Several studies demonstrate the beneficial effect of probiotic bacteria against enteric virus infections and many other diseases ^[28]^[29]^[30]^[31]. Probiotics protect the host from viral infection by modulating gut microbiota composition, enhancing intestinal barrier function, and promoting mucosal immunity ^[32]. Additionally, they interfere with the binding of the virus to their target cells by competitive exclusion by blocking viral receptors and binding viruses on the surface to promote their elimination in faeces ^[33].

3.2. Microbiota and Promotion of Enteric Viral Infections

Despite the significant evidence available about the role of intestinal-derived bacteria in the inhibition of viral infections, several investigations argued for a role of microbiota in promoting virus infection ^[34]. This was first demonstrated by Kuss et al. ^[35] and Kane et al. ^[36] when using poliovirus, reovirus, and mouse mammary tumour virus (MMTV) for infecting germ-free or antibiotic-treated mice. In these cases, it was observed that a substantial attenuation of infection occurred when compared to infection of microbially-colonized mice. Reconstitution of intestinal microorganisms into antibiotic-treated mice was enough to restore poliovirus pathogenesis ^[35]. Moreover, intestinal titres of reovirus were substantially reduced in antibiotic-treated, compared with control mice ^[36]. Similar findings were reported with RV and NoV when antibiotic-treated or germ-free mice were used ^[37]^[38], suggesting that microbiota enhances the pathogenesis of multiple families of enteric viruses.

3.3. Microbiota and Restriction of Enteric Viral Infections

Recently, it has been shown that microbiota ablation with antibiotics in mice allows for infection with the human RV strain Wa (G1P[8]), which replicates very inefficiently in animals with normal microbiota ^[39]. These results are in conflict with earlier experiments which demonstrated that microbiota eradication by antibiotics results in reduced infection of murine RV (EC strain), as shown by lower viral shedding in adult mice and diminished diarrhea incidence in mice pups ^[37]. Nevertheless, viral clearance lasted longer in this model. Furthermore, recent experiments with the murine EDIM strain confirmed that antibiotic treatment and the consequent decrease in intestinal bacterial loads or the use of germ-free mice results in increased RV infection ^[40], which argues against a positive effect of the microbiota in RV infection. In the experiments with the Wa strain, animals with ablated microbiota and subsequent subjection to self-transplantation of intestinal microbiota partially recovered the resistance to infection, which allowed the identification of bacterial taxa that likely participate indirectly or directly in the restriction of Wa infection in mice ^[39]. Thus, bacteria belonging to lactobacilli, Mucispirillum, Oscillospira, and Bilophila genera were negatively linked to RV infection in mice. Faecal material transplantation with infants as donors did not restrict infectivity in this model, suggesting that the microbiota from the donors was not able to control RV infection in this model and that mice autochthonous bacteria were needed for the process ^[39].

4. Microbiota and Enteric Viruses, Studies in Humans

Microbiota composition varies depending on the population ^[41] since it is affected by many factors including nutrition ^[42], sex, age, genetics, and health status ^[43], and these vary greatly between low-income and high-income countries. Such differences could be some of the reasons why RVVs have significantly lower efficacy in low-income countries ^[44]^[45].

A recent study evaluated whether microbiota modification by the use of broad- and narrow-spectrum antibiotics had an effect on immunization with Rotarix in adults ^[46]. Although the experimental groups did not differ in terms of total IgA produced, the narrow spectrum group showed a boost in IgA at day seven post-vaccination (basal levels of anti-RV IgA were high in the vaccination group) and the viral shedding was increased in both groups treated with antibiotics. Differences in the microbiota composition in faeces were evident between the groups and correlations between enrichment in Bacteroides populations at the boost at day seven were observed and several taxa (Prevotellaceae, Cloacibacillus everynsis, and Proteobacteria members such as Escherichia and Shigella) were associated with increased viral shedding. Antibiotic treatment had no effect on the immunogenicity of other systemic vaccines applied (pneumococcal and tetanus vaccine) ^[46]. These results highlight the fact that targeting the microbiota could be an alternative strategy to enhance RVVs efficacy, although the effectiveness in children still needs further investigation.

An ex vivo study analysed the bacterial groups that were interacting with RV in stool samples from children suffering RV (G1P[8]) diarrhea by flow cytometry followed by 16S rDNA sequencing ^[47]. This study also allowed the identification of Ruminococcus as RV-interacting bacteria. As already mentioned, a species of this group (R. gauvreauii) was shown to inhibit RV infection in vitro ^[47]. This, together with the correlation Ruminococcus-anti-RV IgA in humans and the fact that higher Ruminococcus numbers are found in healthy children compared to children with RV diarrhea ^[48], postulates these bacteria as likely players in the cross-talk bacteria-virus-host. Similar studies conducted with individuals suffering AGE caused by NoV will certainly aid in identifying bacterial taxons that interact with these viruses in stools. However, whether this interaction has some relevance in the infection process needs further investigation.

All these findings may help to improve RVVs performance in such a way that they have higher efficacy in low-income countries, preventing tens of thousands of RV-related deaths per year. However, differences in the conclusions drawn from the microbiota analyses are evident, and standardized and controlled methods (e.g., sampling and DNA extraction techniques, bacterial 16S rDNA sequencing platforms, microbial composition analysis methods, etc.) are needed to get a clearer picture.

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