Early Steps in Cell Infection by Parvoviruses: Host-Specific Differences in Cell Receptor Binding but Similar Endosomal Trafficking

Harbison, Carole; Lyi, Sangbom M.; Weichert, Wendy S.; Parrish, Colin R.

doi:10.1128/jvi.00295-09

Cited by 40 publications

(40 citation statements)

References 75 publications

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“…The 3-fold spikes are also the major antibody binding motif, and the antibody binding sites have been divided into two somewhat distinct groupings, which are termed the A and B sites (29,30). The modified sialic acid Neu5Gc binds to a site within the 2-fold dimple (31,32).…”

mentioning

confidence: 99%

Parvovirus Capsid Structures Required for Infection: Mutations Controlling Receptor Recognition and Protease Cleavages

Callaway

Feng

Lee

et al. 2017

J Virol

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Parvovirus capsids are small but complex molecular machines responsible for undertaking many of the steps of cell infection, genome packing, and cell-tocell as well as host-to-host transfer. The details of parvovirus infection of cells are still not fully understood, but the processes must involve small changes in the capsid structure that allow the endocytosed virus to escape from the endosome, pass through the cell cytoplasm, and deliver the single-stranded DNA (ssDNA) genome to the nucleus, where viral replication occurs. Here, we examine capsid substitutions that eliminate canine parvovirus (CPV) infectivity and identify how those mutations changed the capsid structure or altered interactions with the infectious pathway. Amino acid substitutions on the exterior surface of the capsid (Gly299Lys/Ala300Lys) altered the binding of the capsid to transferrin receptor type 1 (TfR), particularly during virus dissociation from the receptor, but still allowed efficient entry into both feline and canine cells without successful infection. These substitutions likely control specific capsid structural changes resulting from TfR binding required for infection. A second set of changes on the interior surface of the capsid reduced viral infectivity by Ͼ100-fold and included two cysteine residues and neighboring residues. One of these substitutions, Cys270Ser, modulates a VP2 cleavage event found in ϳ10% of the capsid proteins that also was shown to alter capsid stability. A neighboring substitution, Pro272Lys, significantly reduced capsid assembly, while a Cys273Ser change appeared to alter capsid transport from the nucleus. These mutants reveal additional structural details that explain cell infection processes of parvovirus capsids.IMPORTANCE Parvoviruses are commonly found in both vertebrate and invertebrate animals and cause widespread disease. They are also being developed as oncolytic therapeutics and as gene therapy vectors. Most functions involved in infection or transduction are mediated by the viral capsid, but the structure-function correlates of the capsids and their constituent proteins are still incompletely understood, especially in relation to identifying capsid processes responsible for infection and release from the cell. Here, we characterize the functional effects of capsid protein mutations that result in the loss of virus infectivity, giving a better understanding of the portions of the capsid that mediate essential steps in successful infection pathways and how they contribute to viral infectivity.

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confidence: 99%

Parvovirus Capsid Structures Required for Infection: Mutations Controlling Receptor Recognition and Protease Cleavages

Callaway

Feng

Lee

et al. 2017

J Virol

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“…Although a number of viruses traffic through the ERC during entry (55)(56)(57), their infection was not inhibited by Rab11-S25N, which is indicative of the Twenty-four hours later, the respective virus (at 100 TCID 50 /cell) was allowed to internalize for 60 min; unbound virus was washed away with cold PBSϩ containing 25 mM NH 4 Cl for 15 min, and replication was allowed to proceed for 6.5 h at 37°C in infection medium containing NH 4 Cl. Cells were fixed, quenched, permeabilized, and blocked, and de novo-synthesized viral protein was detected with the respective antibodies, followed by suitable fluorescent secondary antibodies.…”

Section: Pre-incubation Virus Internalization Cold Washmentioning

confidence: 99%

ICAM-1 Binding Rhinoviruses A89 and B14 Uncoat in Different Endosomal Compartments

Conzemius

Ganjian

Blaas

et al. 2016

J Virol

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Human rhinovirus A89 (HRV-A89) and HRV-B14 bind to and are internalized by intercellular adhesion molecule 1 (ICAM-1); as demonstrated earlier, the RNA genome of HRV-B14 penetrates into the cytoplasm from endosomal compartments of the lysosomal pathway. Here, we show by immunofluorescence microscopy that HRV-A89 but not HRV-B14 colocalizes with transferrin in the endocytic recycling compartment (ERC). Applying drugs differentially interfering with endosomal recycling and with the pathway to lysosomes, we demonstrate that these two major-group HRVs productively uncoat in distinct endosomal compartments. Overexpression of constitutively active (Rab11-GTP) and dominant negative (Rab11-GDP) mutants revealed that uncoating of HRV-A89 depends on functional Rab11. Thus, two ICAM-1 binding HRVs are routed into distinct endosomal compartments for productive uncoating. IMPORTANCEBased on similarity of their RNA genomic sequences, the more than 150 currently known common cold virus serotypes were classified as species A, B, and C. The majority of HRV-A viruses and all HRV-B viruses use ICAM-1 for cell attachment and entry. Our results highlight important differences of two ICAM-1 binding HRVs with respect to their intracellular trafficking and productive uncoating; they demonstrate that serotypes belonging to species A and B, but entering the cell via the same receptors, direct the endocytosis machinery to ferry them along distinct pathways toward different endocytic compartments for uncoating.

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“…In an earlier study on VPu of B19 virus, it was reported that the VPu motif is internally oriented but becomes exposed in heat-treated particles and in particles exposed to low pH . CPV capsids labeled with fluorescent markers were seen in Rab-5 positive endosomes within minutes of uptake (Harbison et al, 2009). Capsids were also seen in Rab7-and Rab11-positive endosomal compartments by 10-15 minutes after infection.…”

Section: Virus In the Early Endosomementioning

confidence: 81%

“…CPV binds to the filopodia of canine cells while FPV infects cats binding to the TfR on feline cells. FPV does not bind the canine TfR, does not infect dogs, or infect cultured canine cells (Harbison et al, 2009). Conversely, CPV can infect feline cells by binding to TfR on the cell body.…”

Section: Engulfmentmentioning

confidence: 99%

Clathrin-Associated Endocytosis as a Route of Entry into Cells for Parvoviruses

Johnson¹,

Dudleenamjil²

2012

Molecular Regulation of Endocytosis

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Early Steps in Cell Infection by Parvoviruses: Host-Specific Differences in Cell Receptor Binding but Similar Endosomal Trafficking

Cited by 40 publications

References 75 publications

Parvovirus Capsid Structures Required for Infection: Mutations Controlling Receptor Recognition and Protease Cleavages

Parvovirus Capsid Structures Required for Infection: Mutations Controlling Receptor Recognition and Protease Cleavages

ICAM-1 Binding Rhinoviruses A89 and B14 Uncoat in Different Endosomal Compartments

Clathrin-Associated Endocytosis as a Route of Entry into Cells for Parvoviruses

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