Glycosphingolipid Binding Specificities of Rotavirus: Identification of a Sialic Acid-Binding Epitope

Delorme, Cécile; Brüssow, Harald; Sidoti, Josette; Roche, Niamh; Karlsson, Karl‐Anders; Neeser, Jean‐Richard; Teneberg, Susann

doi:10.1128/jvi.75.5.2276-2287.2001

Cited by 127 publications

(155 citation statements)

References 66 publications

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“…Similarly, galactose is implicated in the entry process of rotavirus (52), yet its distribution on hSC was without effect on infectivity. Although present on hSC, the identity and spatial arrangement of glycans appear not to be optimal enough to permit interaction with rotavirus; this is consistent with the observation that specific rotavirus-glycan interaction is indeed highly constrained (53). Other milk proteins, including lactoferrin and lactadherin, appear to protect epithelial cells from rotavirus infection irrespective of the presence of carbohydrate residues (54 -56).…”

Section: Discussionsupporting

confidence: 66%

Glycans on Secretory Component Participate in Innate Protection against Mucosal Pathogens

Perrier

Sprenger

Corthésy

2006

Journal of Biological Chemistry

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In mucosal secretions, secretory component (SC) is found either free or bound to polymeric IgA within the secretory IgA complex. SC displays numerous and various glycans, which are potential ligands for bacterial compounds. We first established that human SC (hSC) purified from colostrum (hSCcol) or produced in Chinese hamster ovary cells (hSCrec) exhibits the same lectin reactivity. Both forms bind to Clostridium difficile toxin A and functionally protect polarized Caco-2 cell monolayers from the cytopathic effect of the toxin. The interaction is mediated by glycans present on hSC and involves galactose and sialic acid residues. hSCcol and hSCrec were also shown to bind enteropathogenic Escherichia coli adhesin intimin and to inhibit its infectivity on HEp-2 cells in a glycan-dependent manner as well. SC remained operative in the context of the whole secretory IgA molecule and can therefore enhance its Fabmediated neutralizing properties. On the contrary, hSC did not interact with three different strains of rotavirus (RF, RRV, and SA11). Accordingly, infection of target MA104 cells with these rotavirus strains was not reduced in the presence of either form of hSC tested. Although not a universal mechanism, these findings identify hSC as a microbial scavenger contributing to the antipathogenic arsenal that protects the body epithelial surfaces.

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Section: Discussionsupporting

confidence: 66%

Glycans on Secretory Component Participate in Innate Protection against Mucosal Pathogens

Perrier

Sprenger

Corthésy

2006

Journal of Biological Chemistry

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“…Model for involvement of ␣2␤1, ␣X␤2, and ␣V␤3 in early cellular interactions of integrin-using rotaviruses. Initial cell binding could be via low-affinity binding of VP8* to terminal or subterminal SA (and/or of VP4 to other sugars, such as galactose) on glycolipids or glycoproteins (14,16,22,26), including on integrins such as ␣2␤1. Terminal SA binding is not necessary for ␣2␤1 recognition, but SA binding could promote conformational change in VP4, exposing the VP5* DGE region, or could bring VP4 into closer proximity to the ␣2 I domain.…”

Section: Vol 77 2003 Rotaviruses Recognize Integrins Via Vp4 Dge Anmentioning

confidence: 99%

“…Terminal sialic acids (SA) can be used by a few animal strains, including SA11 and RRV (8), but are not essential for infection (55). Infection by the majority of rotaviruses is independent of terminal SA, but it might involve subterminal SA (14,22). SA11 binding to ␣2␤1 expressed on K562 cells as a result of transfection specifically resulted in increased infectivity, which was inhibited by cellular treatment with an anti-␣2 MAb (23).…”

mentioning

confidence: 99%

Integrin-Using Rotaviruses Bind α2β1 Integrin α2 I Domain via VP4 DGE Sequence and Recognize αXβ2 and αVβ3 by Using VP7 during Cell Entry

Graham

Halász

Tan

et al. 2003

J Virol

141

186

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Integrins ␣2␤1, ␣X␤2, and ␣V␤3 have been implicated in rotavirus cell attachment and entry. The virus spike protein VP4 contains the ␣2␤1 ligand sequence DGE at amino acid positions 308 to 310, and the outer capsid protein VP7 contains the ␣X␤2 ligand sequence GPR. To determine the viral proteins and sequences involved and to define the roles of ␣2␤1, ␣X␤2, and ␣V␤3, we analyzed the ability of rotaviruses and their reassortants to use these integrins for cell binding and infection and the effect of peptides DGEA and GPRP on these events. Many laboratory-adapted human, monkey, and bovine viruses used integrins, whereas all porcine viruses were integrin independent. The integrin-using rotavirus strains each interacted with all three integrins. Integrin usage related to VP4 serotype independently of sialic acid usage. Analysis of rotavirus reassortants and assays of virus binding and infectivity in integrin-transfected cells showed that VP4 bound ␣2␤1, and VP7 interacted with ␣X␤2 and ␣V␤3 at a postbinding stage. DGEA inhibited rotavirus binding to ␣2␤1 and infectivity, whereas GPRP binding to ␣X␤2 inhibited infectivity but not binding. The truncated VP5* subunit of VP4, expressed as a glutathione S-transferase fusion protein, bound the expressed ␣2 I domain. Alanine mutagenesis of D308 and G309 in VP5* eliminated VP5* binding to the ␣2 I domain. In a novel process, integrin-using viruses bind the ␣2 I domain of ␣2␤1 via DGE in VP4 and interact with ␣X␤2 (via GPR) and ␣V␤3 by using VP7 to facilitate cell entry and infection.Rotaviruses are leading causes of acute gastroenteritis in human infants and young animals. Their restricted tropism suggests that very specific virus-host cell interactions are necessary to establish infection. The viral spike protein VP4, the major cell attachment protein, is cleaved by trypsin for enhanced infectivity into two subunits, VP5* (60 kDa) and VP8* (28 kDa). VP4 and the major outer capsid protein VP7 independently define serotype specificities. The inner capsid protein VP6 contains group-specific antigenic determinants. Reassortant rotaviruses containing combinations of the 11 double-stranded RNA genes from two parental viruses can be generated (27) which occasionally show unexpected phenotypes due to VP4-VP7 interactions (43).Integrins ␣2␤1, ␣X␤2, and ␣4␤1 were implicated in group A rotavirus cell attachment and entry (11, 23), and ␣V␤3 was proposed to mediate rotavirus cell entry (20). Integrin usage by rotaviruses was discovered when VP5* was shown to contain the type I collagen-derived, ␣2␤1 ligand sequence DGE at amino acids 308 to 310, and the fibrinogen-derived ␣X␤2 integrin ligand sequence GPR was identified in VP7 at amino acids 253 to 255 (11). Peptides containing these viral integrin ligand sequences (GPRP and RDGEE), monoclonal antibodies (MAbs) to ␣2␤1 and MAbs to ␤2, inhibited the infection of monolayers of MA104 and Caco-2 cells by simian rotavirus SA11 and/or human rotavirus RV-5 by 30 to 90% in additive fashion (9, 11). Infectivity blockade in MA104 cell monolayers...

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“…Some Sia-binding proteins can distinguish Neu5Gc from Neu5Ac. Thus, the CMAH mutation could have altered interactions involving endogenous human receptors such as sialoadhesin͞Siglec-1 (10) and myelin-associated glycoprotein͞Siglec-4a (11), as well as the binding of pathogenic microorganisms such as influenza A (12)(13)(14), rotaviruses (15), and Escherichia coli K99 (16). Such differences could have potentially affected human ontogeny, physiology, disease susceptibility, and͞or the ability of humans to domesticate livestock.…”

mentioning

confidence: 99%

Inactivation of CMP- N -acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution

Chou

Hayakawa

Díaz

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

319

236

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Humans are genetically deficient in the common mammalian sialic acid N-glycolylneuraminic acid (Neu5Gc) because of an Alu-mediated inactivating mutation of the gene encoding the enzyme CMP-N-acetylneuraminic acid (CMP-Neu5Ac) hydroxylase (CMAH). This mutation occurred after our last common ancestor with bonobos and chimpanzees, and before the origin of present-day humans. Here, we take multiple approaches to estimate the timing of this mutation in relationship to human evolutionary history. First, we have developed a method to extract and identify sialic acids from bones and bony fossils. Two Neandertal fossils studied had clearly detectable Neu5Ac but no Neu5Gc, indicating that the CMAH mutation predated the common ancestor of humans and Neandertals, Ϸ0.5-0.6 million years ago (mya). Second, we date the insertion event of the inactivating human-specific sahAluY element that replaced the ancestral AluSq element found adjacent to exon 6 of the CMAH gene in the chimpanzee genome. Assuming Alu source genes based on a phylogenetic tree of human-specific Alu elements, we estimate the sahAluY insertion time at Ϸ2.7 mya. Third, we apply molecular clock analysis to chimpanzee and other great ape CMAH genes and the corresponding human pseudogene to estimate an inactivation time of Ϸ2.8 mya. Taken together, these studies indicate that the CMAH gene was inactivated shortly before the time when brain expansion began in humankind's ancestry, Ϸ2.1-2.2 mya. In this regard, it is of interest that although Neu5Gc is the major sialic acid in most organs of the chimpanzee, its expression is selectively down-regulated in the brain, for as yet unknown reasons. hominid evolution ͉ sialic acids ͉ Alu sequences

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Glycosphingolipid Binding Specificities of Rotavirus: Identification of a Sialic Acid-Binding Epitope

Cited by 127 publications

References 66 publications

Glycans on Secretory Component Participate in Innate Protection against Mucosal Pathogens

Glycans on Secretory Component Participate in Innate Protection against Mucosal Pathogens

Integrin-Using Rotaviruses Bind α2β1 Integrin α2 I Domain via VP4 DGE Sequence and Recognize αXβ2 and αVβ3 by Using VP7 during Cell Entry

Inactivation of CMP- N -acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution

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