Unraveling virus relationships by structure-based phylogenetic classification

Ng, Weng M; Stelfox, Alice J.; Bowden, Thomas A.

doi:10.1093/ve/veaa003

Cited by 26 publications

(24 citation statements)

References 159 publications

(191 reference statements)

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“…Recent structures of the attachment-mediating GP1 glycoprotein from the clade D WWAV have revealed structural diversity within the GP1 of TfR1-tropic viruses [ 25 , 66 ], principally within GP1 loop regions that are likely involved in TfR1 recognition [ 26 ]. Such structural variation across NW mammarenaviruses with shared receptor-tropism may indicate diverse modes of TfR1 recognition [ 67 ]. WWAV-AV96, which was associated with fatal human illness [ 20 ], utilizes hTfR1 for viral entry [ 25 , 51 ].…”

Section: Resultsmentioning

confidence: 99%

A novel circulating tamiami mammarenavirus shows potential for zoonotic spillover

et al. 2020

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A detailed understanding of the mechanisms underlying the capacity of a virus to break the species barrier is crucial for pathogen surveillance and control. New World (NW) mammarenaviruses constitute a diverse group of rodent-borne pathogens that includes several causative agents of severe viral hemorrhagic fever in humans. The ability of the NW mammarenaviral attachment glycoprotein (GP) to utilize human transferrin receptor 1 (hTfR1) as a primary entry receptor plays a key role in dictating zoonotic potential. The recent isolation of Tacaribe and lymphocytic choriominingitis mammarenaviruses from host-seeking ticks provided evidence for the presence of mammarenaviruses in arthropods, which are established vectors for numerous other viral pathogens. Here, using next generation sequencing to search for other mammarenaviruses in ticks, we identified a novel replication-competent strain of the NW mammarenavirus Tamiami (TAMV-FL), which we found capable of utilizing hTfR1 to enter mammalian cells. During isolation through serial passaging in mammalian immunocompetent cells, the quasispecies of TAMV-FL acquired and enriched mutations leading to the amino acid changes N151K and D156N, within GP. Cell entry studies revealed that both substitutions, N151K and D156N, increased dependence of the virus on hTfR1 and binding to heparan sulfate proteoglycans. Moreover, we show that the substituted residues likely map to the sterically constrained trimeric axis of GP, and facilitate viral fusion at a lower pH, resulting in viral egress from later endosomal compartments. In summary, we identify and characterize a naturally occurring TAMV strain (TAMV-FL) within ticks that is able to utilize hTfR1. The TAMV-FL significantly diverged from previous TAMV isolates, demonstrating that TAMV quasispecies exhibit striking genetic plasticity that may facilitate zoonotic spillover and rapid adaptation to new hosts.

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Section: Resultsmentioning

confidence: 99%

A novel circulating tamiami mammarenavirus shows potential for zoonotic spillover

et al. 2020

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“…Firstly, it has been shown that class II viral glycoproteins have counterparts in cellular proteins, demonstrating the possibility of horizontal gene exchange [ 70 ], and secondly, viral glycoproteins are under environmental selection pressure for the cellular receptors and thus inclined to higher sequence and/or structural variability. This is noticeable when comparing the available structures of the receptor-binding domain (RBD) within the spike glycoprotein S (a class I viral fusogen) across the members of the Coronaviridae family, as shown early this year [ 71 , 72 ].…”

Section: The Open Question Of a Structure-based Classification Of mentioning

confidence: 99%

Superimposition of Viral Protein Structures: A Means to Decipher the Phylogenies of Viruses

Ravantti

Martínez-Castillo

Abrescia

2020

Viruses

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Superimposition of protein structures is key in unravelling structural homology across proteins whose sequence similarity is lost. Structural comparison provides insights into protein function and evolution. Here, we review some of the original findings and thoughts that have led to the current established structure-based phylogeny of viruses: starting from the original observation that the major capsid proteins of plant and animal viruses possess similar folds, to the idea that each virus has an innate “self”. This latter idea fueled the conceptualization of the PRD1-adenovirus lineage whose members possess a major capsid protein (innate “self”) with a double jelly roll fold. Based on this approach, long-range viral evolutionary relationships can be detected allowing the virosphere to be classified in four structure-based lineages. However, this process is not without its challenges or limitations. As an example of these hurdles, we finally touch on the difficulty of establishing structural “self” traits for enveloped viruses showcasing the coronaviruses but also the power of structure-based analysis in the understanding of emerging viruses

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“…CoV S protein is a key viral factor that primarily shoulders the host cell and species tropism, one of the critical viral properties, and thus, its biologically significant variations would influence much the viral phenotype. Of note here, the structure-based phylogenetic analysis of the receptor-binding S1 domain ( Forni et al, 2017 ; Ng et al, 2020 ) and also the extensive systemic study on the receptor-usage and infection ability to cell types of different species ( Letko et al, 2020a ) have suggested the presence of an unknown receptor(s) for HCoVs. The current seven species of HCoVs are most likely to have appeared through evolution via multiple complicated receptor switching events.…”

Section: Integrative Virology Of Hcovsmentioning

confidence: 99%

“…Many CoVs utilize peptidases as the cellular receptor, despite that their enzymatic domains are not required for the viral entry process ( Fehr and Perlman, 2015 ). It has been reported that the receptor-specific clustering for viral receptor-binding proteins from the family Coronaviridae is absent ( Ng et al, 2020 ), and that there exist many HCoV receptors other than ACE2 ( Fehr and Perlman, 2015 ; de Wilde et al, 2018 ; Ye et al, 2020 ). These reports suggest a complicated evolutionary pathway for HCoVs, which may include the switch to the same receptor on multiple occasions ( Li F. et al, 2005 ; Wu et al, 2009 ; Song et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Toward Understanding Molecular Bases for Biological Diversification of Human Coronaviruses: Present Status and Future Perspectives

et al. 2020

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Human coronaviruses (HCoVs) are of zoonotic origins, and seven distinct HCoVs are currently known to infect humans. While the four seasonal HCoVs appear to be mildly pathogenic and circulate among human populations, the other three designated SARS-CoV, MERS-CoV, and SARS-CoV-2 can cause severe diseases in some cases. The newly identified SARS-CoV-2, a causative virus of COVID-19 that can be deadly, is now spreading worldwide much more efficiently than the other two pathogenic viruses. Despite evident differences in these properties, all HCoVs commonly have an exceptionally large genomic RNA with a rather peculiar gene organization and have the potential to readily alter their biological properties. CoVs are characterized by their biological diversifications, high recombination, and efficient adaptive evolution. We are particularly concerned about the high replication and transmission nature of SARS-CoV-2, which may lead to the emergence of more transmissible and/or pathogenic viruses than ever before. Furthermore, novel variant viruses may appear at any time from the CoV pools actively circulating or persistently being maintained in the animal reservoirs, and from the CoVs in infected human individuals. In this review, we describe knowns of the CoVs and then mention their unknowns to clarify the major issues to be addressed. Genome organizations and sequences of numerous CoVs have been determined, and the viruses are presently classified into separate phylogenetic groups. Functional roles in the viral replication cycle in vitro of non-structural and structural proteins are also quite well understood or suggested. In contrast, those in the in vitro and in vivo replication for various accessory proteins encoded by the variable 3′ one-third portion of the CoV genome mostly remain to be determined. Importantly, the genomic sequences/structures closely linked to the high CoV recombination are poorly investigated and elucidated. Also, determinants for adaptation and pathogenicity have not been systematically investigated. We summarize here these research situations. Among conceivable projects, we are especially interested in the underlying molecular mechanism by which the observed CoV diversification is generated. Finally, as virologists, we discuss how we handle the present difficulties and propose possible research directions in the medium or long term.

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Unraveling virus relationships by structure-based phylogenetic classification

Cited by 26 publications

References 159 publications

A novel circulating tamiami mammarenavirus shows potential for zoonotic spillover

A novel circulating tamiami mammarenavirus shows potential for zoonotic spillover

Superimposition of Viral Protein Structures: A Means to Decipher the Phylogenies of Viruses

Toward Understanding Molecular Bases for Biological Diversification of Human Coronaviruses: Present Status and Future Perspectives

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