An Atypical Parvovirus Drives Chronic Tubulointerstitial Nephropathy and Kidney Fibrosis

Roediger, Ben; Lee, Quintin; Tikoo, Shweta; Cobbin, Joanna C. A.; Henderson, James M.; Jormakka, Mika; O’Rourke, Matthew B.; Padula, Matthew P.; Pinello, Natalia; Henry, M. A. Coelho De Arruda; Wynne, Maria; Santagostino, Sara Francesca; Brayton, Cory; Rasmussen, Lorna; Lisowski, Leszek; Tay, Szun S.; Harris, David C.H.; Bertram, John F.; Dowling, John P.; Bertolino, Patrick; Lai, Jack H.; Wu, Wenwang; Bachovchin, William W.; Wong, Justin; Gorrell, Mark D.; Shaban, Babak; Holmes, Edward C.; Jolly, Christopher J.; Monette, Sébastien; Weninger, Wolfgang

doi:10.1016/j.cell.2018.08.013

Cited by 100 publications

(196 citation statements)

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“…For example, ambidensovirus-derived EPVs dominate invertebrate genomes (14), whereas vertebrate EPVs almost exclusively derive from dependoparvoviruses, protoparvoviruses, or viruses closely related to these two genera (12, 13, 25, 26). In this study we found no trace of ChPV-derived sequences in tetrapod genomes, despite recent evidence that ChPVs infect this host group (21). By contrast, ChPV-derived sequences are relatively common in arthropods, with the genomes of some species harboring multiple, independently acquired ChPVs ( Table 1 ).…”

Section: Discussioncontrasting

confidence: 94%

“…Our discovery of ChPV-derived elements in fish and arthropod genomes establishes that ChPVs can infect these species in addition to mammals (21). Moreover, it provides evidence that the ChPVs are probably an ancient lineage of parvoviruses.…”

Section: Discussionmentioning

confidence: 99%

“…Until relatively recently, evidence that the chapparvoviruses detected via sequencing actually infect vertebrate hosts has been lacking. However, a recent study has claimed to demonstrate that a chapparvovirus called ‘mouse kidney parvovirus’ (MKPV) circulates among laboratory mice populations, in which it causes a kidney disease known as ‘inclusion body nephropathy’ (21). These findings imply that chapparvoviruses represent a potential disease threat to humans and domestic species.…”

Section: Introductionmentioning

confidence: 99%

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An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

Pénzes

Souza

Agbandje‐McKenna

et al. 2019

Preprint

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2Chapparvoviruses are a highly divergent group of parvoviruses (family 3 Parvoviridae) first identified in 2013. Interest in these poorly characterized 4 viruses has been raised by recent studies indicating that they are the cause of 5 chronic kidney disease that arises spontaneously in laboratory mice. In this 6 study, we investigate the biological and evolutionary characteristics of 7 chapparvoviruses via comparative analysis of genome sequence data. Our 8 analysis, which incorporates sequences derived from endogenous viral 9 elements (EVEs) as well as exogenous viruses, reveals that 10 chapparvoviruses are an ancient lineage within the family Parvoviridae, 11 clustering separately from members of both currently established parvoviral 12 subfamilies. Consistent with this, they exhibit a number of characteristic 13 genomic and structural features, i.e. a large number of putative auxiliary 14 protein-encoding genes, capsid protein genes non-homologous to any hitherto 15 parvoviral cap, as well as a putative capsid structure lacking the canonical fifth 16 strand of the ABIDG sheet comprising the luminal side of the jelly roll. Our 17 findings demonstrate that the chapparvovirus lineage infects an exceptionally 18 broad range of host species, including both vertebrates and invertebrates.19Furthermore, we observe that chapparvoviruses found in fish are more closely 20 related to those from invertebrates than they are to those that infect amniote 21 vertebrates. This suggests that transmission between distantly related host 22 species may have occurred in the past. Our study provides the first integrated 23 overview of the chapparvovirus group, and revises current views of parvovirus 24 evolution 25 26 AUTHOR SUMMARY 27 Chapparvoviruses are a recently identified group of viruses about 28 which relatively little is known. However, recent studies have shown that these 29 viruses cause disease in laboratory mice and are prevalent in the fecal virome 30 of pigs and poultry, raising interest in their potential impact as pathogens, and 31 utility as experimental tools. We examined the genomes of chapparvoviruses 32 and endogenous viral elements ('fossilized' virus sequences derived from 33 ancestral viruses) using a variety of bioinformatics-based approaches. We 3 1 show that the chapparvoviruses have an ancient origin and are evolutionarily 2 distinct from all other related viruses. Accordingly, their genomes and virions 3 exhibit a range of distinct characteristic features. We examine the distribution 4 of these features in the light of chapparvovirus evolutionary history (which we 5 can also infer from genomic data), revealing new insights into chapparvovirus 6 biology. 7 8

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Section: Discussioncontrasting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

Pénzes

Souza

Agbandje‐McKenna

et al. 2019

Preprint

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“…The Shelduck parvovirus described here is of particular interest as it is a member of the genus Chapparvovirus. Metagenomic analyses have recently identified members of this genus in a large number of vertebrates [55], and are known agents of severe disease [56].…”

Section: Discussionmentioning

confidence: 99%

Virome heterogeneity and connectivity in waterfowl and shorebird communities

et al. 2019

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Models of host-microbe dynamics typically assume a single-host population infected by a single pathogen. In reality, many hosts form multi-species aggregations and may be infected with an assemblage of pathogens. We used a meta-transcriptomic approach to characterize the viromes of nine avian species in the Anseriformes (ducks) and Charadriiformes (shorebirds). This revealed the presence of 27 viral species, of which 24 were novel, including double-stranded RNA viruses (Picobirnaviridae and Reoviridae), single-stranded RNA viruses (Astroviridae, Caliciviridae, Picornaviridae), a retro-transcribing DNA virus (Hepadnaviridae), and a single-stranded DNA virus (Parvoviridae). These viruses comprise multi-host generalist viruses and those that are host-specific, indicative of both virome connectivity (host sharing) and heterogeneity (host specificity). Virome connectivity was apparent in two well described multi-host virus species -avian coronavirus and influenza A virus- and a novel Rotavirus species that were shared among some Anseriform species, while virome heterogeneity was reflected in the absence of viruses shared between Anseriformes and Charadriiformes, as well as differences in viral abundance and alpha diversity among species. Overall, we demonstrate complex virome structures across host species that co-exist in multi-species aggregations.

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“…Chapparvoviruses are being increasingly identified in metagenomic studies, and seemingly have a wide host range (42), including bats (43), and the feces of turkeys (44), red-crowned cranes (45), wild rats (46) and pigs (47). Importantly, a murine kidney parvovirus was recently found in immunodeficient laboratory mice strains, causing renal failure and kidney fibrosis (48), indicating that some chapparvoviruses are associated with highly virulent infections.…”

Section: Discussionmentioning

confidence: 99%

Meta-transcriptomic analysis of virus diversity in urban wild birds with paretic disease

Chang

Eden

Hall

et al. 2020

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29Wild birds are major natural reservoirs and potential dispersers of a variety of infectious 30 diseases. As such, it is important to determine the diversity of viruses they carry and use this 31 information to help understand the potential risks of spill-over to humans, domestic animals, and 32 other wildlife. We investigated the potential viral causes of paresis in long-standing, but 33 undiagnosed disease syndromes in wild Australian birds. RNA from diseased birds was extracted 34 and pooled based on tissue type, host species and clinical manifestation for metagenomic 35 sequencing. Using a bulk and unbiased meta-transcriptomic approach, combined with careful 36 clinical investigation and histopathology, we identified a number of novel viruses from the 37 families Astroviridae, Picornaviridae, Polyomaviridae, Paramyxoviridae, Parvoviridae, 38 Flaviviridae, and Circoviridae in common urban wild birds including Australian magpies, 39 magpie lark, pied currawongs, Australian ravens, and rainbow lorikeets. In each case the 40 presence of the virus was confirmed by RT-PCR. These data revealed a number of candidate 41 viral pathogens that may contribute to coronary, skeletal muscle, vascular and neuropathology in 42 birds of the Corvidae and Artamidae families, and neuropathology in members of the 43 Psittaculidae. The existence of such a diverse virome in urban avian species highlights the 44 importance and challenges in elucidating the etiology and ecology of wildlife pathogens in urban 45 environments. This information will be increasingly important for managing disease risks and 46 conducting surveillance for potential viral threats to wildlife, livestock and human health. More 47

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An Atypical Parvovirus Drives Chronic Tubulointerstitial Nephropathy and Kidney Fibrosis

Cited by 100 publications

References 60 publications

An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

Virome heterogeneity and connectivity in waterfowl and shorebird communities

Meta-transcriptomic analysis of virus diversity in urban wild birds with paretic disease

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