Frequent Cross-Species Transmission of Parvoviruses among Diverse Carnivore Hosts

Allison, Andrew B.; Köhler, D; Fox, Karen A.; Brown, Justin D.; Gerhold, Richard W.; Shearn-Bochsler, Valerie I.; Dubovi, Edward J.; Parrish, Colin R.; Holmes, Edward C.

doi:10.1128/jvi.02428-12

Cited by 129 publications

(148 citation statements)

References 24 publications

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“…It is possible that these residues are equally efficacious in allowing cell infection and replication or that they are being maintained by alternative receptor interactions, perhaps by variations in the canine TfR sequence (e.g., different isoforms that exist in carnivore TfRs) or by differential expression of glycans. Although variation of position 301 has not been observed in viruses from domestic dogs, we previously identified a 301-Ser residue in viruses from wild coyotes (which have a TfR sequence identical to that of the domestic dog) (15,17), suggesting that such variability may exist in nature.…”

Section: Discussionmentioning

confidence: 99%

“…For example, all FPV isolates from cats have a 300-Ala residue, as did the first strains of CPV in dogs (CPV-2), whereas all recent isolates of CPV from dogs (CPV-2a and its variants) collected worldwide have a 300-Gly residue. In contrast, all recently identified CPV raccoon isolates contain a 300-Asp residue, which was the only mutation common to all raccoon viruses analyzed (15)(16)(17). Although a number of additional VP2 mutations were observed in raccoon isolates compared to dog viruses (e.g., at VP2 residues 190, 224, 232, and 305), the change of residue 300 was the only capsid mutation needed for that virus to gain the dog host range in vitro (15).…”

mentioning

confidence: 89%

“…It was later demonstrated that a unique glycosylation site found only in the TfRs of dogs and very closely related canids (coyotes [Canis latrans] and gray wolves [Canis lupus]) was a primary determinant blocking binding and infection of FPV-like viruses in these species and that this barrier was overcome by CPV (11)(12)(13)(14)(15). Since its emergence, CPV not only has continued to circulate worldwide in domestic dogs and cats but is also endemic in sylvatic cycles among various wild carnivore species, such as raccoons (Procyon lotor), pumas (Puma concolor), fishers (Martes pennanti), coyotes, and wolves, which in turn suggests that cross-species transmission events between domestic and nondomestic carnivores have played a major role in CPV evolution (15)(16)(17).…”

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confidence: 99%

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Single Mutations in the VP2 300 Loop Region of the Three-Fold Spike of the Carnivore Parvovirus Capsid Can Determine Host Range

Allison

Organtini

Zhang

et al. 2016

J Virol

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Sylvatic carnivores, such as raccoons, have recently been recognized as important hosts in the evolution of canine parvovirus (CPV), a pandemic pathogen of domestic dogs. Although viruses from raccoons do not efficiently bind the dog transferrin receptor (TfR) or infect dog cells, a single mutation changing an aspartic acid to a glycine at capsid (VP2) position 300 in the prototype raccoon CPV allows dog cell infection. Because VP2 position 300 exhibits extensive amino acid variation among the carnivore parvoviruses, we further investigated its role in determining host range by analyzing its diversity and evolution in nature and by creating a comprehensive set of VP2 position 300 mutants in infectious clones. Notably, some position 300 residues rendered CPV noninfectious for dog, but not cat or fox, cells. Changes of adjacent residues (residues 299 and 301) were also observed often after cell culture passage in different hosts, and some of the mutations mimicked changes seen in viruses recovered from natural infections of alternative hosts, suggesting that compensatory mutations were selected to accommodate the new residue at position 300. Analysis of the TfRs of carnivore hosts used in the experimental evolution studies demonstrated that their glycosylation patterns varied, including a glycan present only on the domestic dog TfR that dictates susceptibility to parvoviruses. Overall, there were significant differences in the abilities of viruses with alternative position 300 residues to bind TfRs and infect different carnivore hosts, demonstrating that the process of infection is highly host dependent and that VP2 position 300 is a key determinant of host range. IMPORTANCEAlthough the emergence and pandemic spread of canine parvovirus (CPV) are well documented, the carnivore hosts and evolutionary pathways involved in its emergence remain enigmatic. We recently demonstrated that a region in the capsid structure of CPV, centered around VP2 position 300, varies after transfer to alternative carnivore hosts and may allow infection of previously nonsusceptible hosts in vitro. Here we show that VP2 position 300 is the most variable residue in the parvovirus capsid in nature, suggesting that it is a critical determinant in the cross-species transfer of viruses between different carnivores due to its interactions with the transferrin receptor to mediate infection. To this end, we demonstrated that there are substantial differences in receptor binding and infectivity of various VP2 position 300 mutants for different carnivore species and that single mutations in this region can influence whether a host is susceptible or refractory to virus infection.T he emergence of viruses to cause epidemic or pandemic disease in new hosts is a continual threat to human and animal health. However, the viral and host mechanisms that control such events are often poorly understood. Although there are constant viral exposures occurring between many different species, most viruses do not infect or achieve sustained onward transmis...

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Section: Discussionmentioning

confidence: 99%

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confidence: 89%

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confidence: 99%

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Single Mutations in the VP2 300 Loop Region of the Three-Fold Spike of the Carnivore Parvovirus Capsid Can Determine Host Range

Allison

Organtini

Zhang

et al. 2016

J Virol

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“…The phylogenetic relationships between CPV-2 isolates from dogs and the viruses from cats (FPV), mink (MEV), raccoon (RPV), raccoon dog (Raccoon dog parvovirus, RDPV) and blue fox (Blue fox parvovirus, BFPV) showed that all CPVs derived from a single common ancestor, and that the strains were mostly similar to viruses from different wildlife animals including raccoons and foxes (Allison et al, 2012(Allison et al, , 2013. CPV was shown to be related to a virus similar to the long recognized FPV, but likely not from cats (Truyen et al, 1995).…”

Section: Originmentioning

confidence: 99%

“…In Italy, four isolates from wolves analysed by Battilani et al (2001) were antigenically and genetically identified as CPV-2b. The phylogenetic analysis from several non-domestic animals, such as, raccoon (Procyon lotor), coyote (Canis latrans), grey wolf (Canis lupus baileyi/nubilus/occidentalis), puma (Puma concolor), striped skunk (Mephitis mephitis) and bobcat (Lynx rufus) (Allison et al, 2012(Allison et al, , 2013 revealed the presence of the three CPV variants. A recent study by Filipov et al (2014) detected two wild carnivores parvovirus positive, a wolf (Canis lupus) and a red fox (Vulpes vulpes), both being infected by CPV-2a strains.…”

Section: Wild Animalsmentioning

confidence: 99%