Heparan sulphate mediates swine vesicular disease virus attachment to the host cell

Escribano-Romero, Estela; Jiménez‐Clavero, Miguel Ángel; Gomes, Paula; Ranea, Juan A. G.; Ley, Victoria

doi:10.1099/vir.0.19603-0

Cited by 24 publications

(27 citation statements)

References 47 publications

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“…Therefore, the HS-virus interaction seen in this study is less likely to be originated from adaptation to cell culture. It can be thus proposed that cellular HS might mediate an early move for binding of the clinical isolate of EV71 to Vero cells, which could further assist recognition of other receptors, as shown for other HEV members such as SVDV [6]. These results can be also supported with the recent findings that a strain of EV71 was shown to use HS as an attachment receptor in RD cells [20].…”

Section: Discussionsupporting

confidence: 80%

“…This is also in agreement with a general fact that picornaviruses easily adapt to bind to different co-receptor(s) even in the same cell type due to having the flexibility in receptor usage [1,6,24]. Moreover, Vero cells, as an epithelial cell line, do not support EV71 replication through Human P-selectin Glycoprotein Ligand-1 (PSGL-1) that was reported to serve as an EV71 receptor primarily in leukocytes [13].…”

Section: Discussionsupporting

confidence: 64%

“…The possible role of cell surface HS in mediating infection of Human Enteroviruses (HEVs) has mostly been reported for serotypes of HEV group B, including Echovirus [8], Coxsackievirus B3 (CVB3) [24], swine vesicular disease virus (SVDV) [6], and Coxsackievirus A9 (CVA9) [11]. Recently, we demonstrated that several soluble HS mimetic compounds, including heparin (Hep), pentosan polysulphate (PPS) and HS, exhibited potent antiviral activities against a cloned strain of EV71 through interfering with the viral attachment in Vero cells [16] suggesting a role for cellular HS in mediating early move of the EV71 infection.…”

Section: Introductionmentioning

confidence: 99%

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Initial evidence on differences among Enterovirus 71, Coxsackievirus A16 and Coxsackievirus B4 in binding to cell surface heparan sulphate

2013

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Cell surface heparan sulphate (HS) mediates infection for many viruses from diverse families. We demonstrated significant antiviral potencies for a number of HS mimetics against a cloned strain of Enterovirus 71 (EV71) in a previous study. Thus, the involvement of HS in mediating viral infection of isolates of human enteroviruses was investigated in Vero and human neural cells in the present work. In both cell lines, heparin and pentosan polysulphate significantly inhibited both infection and attachment of low passage clinical isolates of EV71 and Coxsackievirus A16 (CVA16) but showed no affect on Coxsackievirus B4 (CVB4) (p \ 0.05). In addition, enzymatic removal of cell surface HS by heparinase I prevented binding of the clinical EV71 by nearly 50 % but failed to significantly inhibit CVA16 or CVB4 binding in Vero cells. Overall, the findings of this study provides evidence that whilst highly sulphated domains of HS serve as an essential attachment co-receptor for EV71, HS might be used as an alternative attachment receptor by the other member of Human Enterovirus group A, CVA16. In addition, HS may not mediate early infection in CVB4.

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Section: Discussionsupporting

confidence: 80%

Section: Discussionsupporting

confidence: 64%

Section: Introductionmentioning

confidence: 99%

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Initial evidence on differences among Enterovirus 71, Coxsackievirus A16 and Coxsackievirus B4 in binding to cell surface heparan sulphate

2013

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“…The resulting high molecular diversity of heparan sulfate (HS) chains enables many specific interactions with very different proteins and glycoproteins, e.g., growth factors, cytokines, and human pathogens, including enveloped viruses (13,22,36). Cell surface HS were also shown to bind nonenveloped viruses, e.g., a variant of human rhinovirus 89 (HRV89) (37), echoviruses (15), swine vesicular disease virus (11), and Theiler's murine encephalomyelitis virus (25), belonging, like CVB3 PD, to the picornavirus family. The sulfated structural motifs of HS mediating binding or entry of picornaviruses are poorly known.…”

mentioning

confidence: 99%

N- and 6-O-Sulfated Heparan Sulfates Mediate Internalization of Coxsackievirus B3 Variant PD into CHO-K1 Cells

Zautner

Jahn

Hammerschmidt

et al. 2006

J Virol

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Group B coxsackieviruses (CVB) belonging to the family of nonenveloped picornaviruses utilize the coxsackievirus-adenovirus receptor (CAR) to bind to and enter into host cells (5). Small depressions surrounding the fivefold axis, the so-called canyons formed by the viral capsid proteins VP1, VP2, and VP3, bind the CAR (24). Receptor binding induces conformational changes which facilitate the internalization of viral RNA into host cells (18,26). Additionally, human decay accelerating factor (hDAF/CD55) functions as an attachment but not an entry receptor for CVB1, -3, and -5 (6, 32). Recently, cell surface heparan sulfate proteoglycans (HSPG) were identified as additional receptors for the CVB3 variant PD (CVB PD) (38). Using HSPG for infection, CVB3 PD also replicates in CAR-lacking cell lines, e.g., CHO-K1, BHK-21, RD, and L929 (29).HSPG consist of a polydisaccharide chain tethered to serine residues of defined core proteins by a linking tetrasaccharide composed of xylose-galactose-galactose-glucuronic acid (12). NAcetyl-D-glucosamine (GlcNAc) and D-glucuronic acid (GlcA) residues are added alternatingly to the linker tetrasaccharide. Several steps of modifications of GlcNAc and GlcA then follow, including N-deacetylation and N-sulfation of GlcNAc, C-5 epimerization of GlcA to L-idoronic acid (IdoA), 2-O-sulfation of the uronic acid, and 6-O-and 3-O-sulfation of D-glucosamine (GlcN) residues. The resulting high molecular diversity of heparan sulfate (HS) chains enables many specific interactions with very different proteins and glycoproteins, e.g., growth factors, cytokines, and human pathogens, including enveloped viruses (13,22,36). Cell surface HS were also shown to bind nonenveloped viruses, e.g., a variant of human rhinovirus 89 (HRV89) (37), echoviruses (15), swine vesicular disease virus (11), and Theiler's murine encephalomyelitis virus (25), belonging, like CVB3 PD, to the picornavirus family. The sulfated structural motifs of HS mediating binding or entry of picornaviruses are poorly known. Strong differences in viral replication in CHO cell mutants with different defects in heparan sulfate synthesis led to the assumption that CVB3 PD binds to specifically sulfated HS moieties.During this study, the following tasks were performed: (i) the structural requirements, especially the sulfation pattern of HS necessary for CVB3 PD entry, were examined by using competition assays with growth factors binding to specifically sulfated HS sequences as well as with specifically desulfated heparins; (ii) the entry pathway of CVB3 PD while using HS was studied; and (iii) the kinetics of viral entry and the viral life cycle depending on the presence of CAR or HS as the receptor were investigated. MATERIALS AND METHODSCell lines and viruses. Chinese hamster ovary cells (CHO-K1; German Collection of Microorganism and Cell Cultures no. ACC-110) and heparan sulfatenegative, human CAR-transfected pgsD-677-hCAR cells (38) were grown in Dulbecco's modified Eagle's medium (Cambrex, Belgium) supplemented with 10% fetal bovine...

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“…Recently, it has been found that many viruses can use cell surface HS proteoglycans for attachment and entry. Among the family Picornaviridae, footand-mouth disease virus, swine vesicular disease virus, coxsackievirus B3, Theiler's murine encephalomyelitis virus, some echoviruses, and variants of HRV89 have been shown to in-teract with HS for cell attachment and entry, especially in the absence of their classic receptors (4,6,11,23,35,37). Having seen that HRV54 can infect the ICAM-1-negative RD cells but is not inhibited by the recombinant VLDLR derivative, we set out to identify the receptor used in addition to ICAM-1.…”

mentioning

confidence: 99%

Human Rhinovirus Type 54 Infection via Heparan Sulfate Is Less Efficient and Strictly Dependent on Low Endosomal pH

Khan

Pichler

Rosemann

et al. 2007

J Virol

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K-type major-group human rhinoviruses (HRVs) (including HRV54) share a prominent lysine residue in the HI surface loop of VP1 with all minor-group HRVs. Despite the presence of this residue, they cannot use members of the low-density lipoprotein receptor family for productive infection. Reexamining all K-type viruses for receptor usage, we noticed that HRV54 is able to replicate in RD cells that lack the major-group receptor intercellular adhesion molecule 1 (ICAM-1). By using receptor blocking assays, inhibition of sulfation, enzymatic digestion, and proteoglycan-deficient cell lines, we show here that wild-type HRV54, without any adaptation, uses heparan sulfate (HS) proteoglycan as an alternate receptor. However, infection via HS is less efficient than infection via ICAM-1. Moreover, HRV54 has an acid lability profile similar to that of the minor-group virus HRV2. In ICAM-1-deficient cells its replication is completely blocked by the H ؉ -ATPase inhibitor bafilomycin A1, whereas in ICAM-1-expressing cells it replicates in the presence of the drug. Thus, use of a "noncatalytic" receptor requires the virus to be highly unstable at low pH.

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Heparan sulphate mediates swine vesicular disease virus attachment to the host cell

Cited by 24 publications

References 47 publications

Initial evidence on differences among Enterovirus 71, Coxsackievirus A16 and Coxsackievirus B4 in binding to cell surface heparan sulphate

Initial evidence on differences among Enterovirus 71, Coxsackievirus A16 and Coxsackievirus B4 in binding to cell surface heparan sulphate

N- and 6-O-Sulfated Heparan Sulfates Mediate Internalization of Coxsackievirus B3 Variant PD into CHO-K1 Cells

Human Rhinovirus Type 54 Infection via Heparan Sulfate Is Less Efficient and Strictly Dependent on Low Endosomal pH

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