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De-Coding the Contributions of the Viral Rnas to Alphaviral Pathogenesis

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De-Coding the Contributions of the Viral Rnas to Alphaviral Pathogenesis pathogens Review De-Coding the Contributions of the Viral RNAs to Alphaviral Pathogenesis Autumn T. LaPointe 1 and Kevin J. Sokoloski 2,* 1 Department of Microbiology and Immunology, School of Medicine, University of Louisville, Louisville, KT 40202, USA; [email protected] 2 Center for Predictive Medicine and Emerging Infectious Diseases, University of Louisville, Louisville, KT 40202, USA * Correspondence: [email protected] Abstract: Alphaviruses are positive-sense RNA arboviruses that are capable of causing severe disease in otherwise healthy individuals. There are many aspects of viral infection that determine pathogen- esis and major efforts regarding the identification and characterization of virulence determinants have largely focused on the roles of the nonstructural and structural proteins. Nonetheless, the viral RNAs of the alphaviruses themselves play important roles in regard to virulence and pathogenesis. In particular, many sequences and secondary structures within the viral RNAs play an important part in the development of disease and may be considered important determinants of virulence. In this review article, we summarize the known RNA-based virulence traits and host:RNA interactions that influence alphaviral pathogenesis for each of the viral RNA species produced during infection. Overall, the viral RNAs produced during infection are important contributors to alphaviral patho- genesis and more research is needed to fully understand how each RNA species impacts the host response to infection as well as the development of disease. Citation: LaPointe, A.T.; Sokoloski, K.J. De-Coding the Contributions of the Viral RNAs to Alphaviral Keywords: alphavirus; virulence; viral pathogenesis; viral RNA Pathogenesis. Pathogens 2021, 10, 771. https://doi.org/10.3390/ pathogens10060771 1. Background Academic Editors: Tuli Mukhopadhyay Alphaviruses are single-stranded, positive-sense RNA viruses that are naturally trans- and Tem Morrison mitted between a mosquito vector and a vertebrate host. Epizootic spillover events result in the infection of humans and horses, potentially resulting in severe disease. Alphaviruses Received: 11 May 2021 are largely classified as either arthritogenic or encephalitic based on the symptoms of Accepted: 17 June 2021 infection. Arthritogenic alphaviral infection causes disease varying from mild to severe Published: 19 June 2021 multi-joint arthritis and can persist for several months to years past the acute phase of infection [1]. This includes Chikungunya (CHIKV) and Ross River Virus (RRV) which are Publisher’s Note: MDPI stays neutral capable of causing debilitating polyarthritis as well as the model alphavirus Sindbis virus with regard to jurisdictional claims in (SINV), which is the causative agent of rash-arthritic diseases like Pogosta disease, Ockelbo published maps and institutional affil- disease, and Karelian fever [2–5]. While not associated with high rates of mortality, the iations. high morbidity of arthritogenic alphaviral disease results in a high economic burden that is particularly damaging in regions where labor-intensive work is prevalent [6,7]. The encephalitic alphaviruses include Venezuelan, Eastern, and Western Equine Encephali- tis viruses (VEEV, EEEV, and WEEV) and are capable of causing severe meningitis and Copyright: © 2021 by the authors. encephalitis, as well as long-lasting sequelae such as seizures, paralysis, and cognitive Licensee MDPI, Basel, Switzerland. deficits in survivors [8–11]. These viruses, while comparatively rare in regards to their This article is an open access article incidence, typically have high mortality rates, especially in comparison to the arthritogenic distributed under the terms and alphaviruses, with viruses like EEEV having mortality rates as high as 70% in symptomatic conditions of the Creative Commons individuals [12]. Despite the threat that alphaviruses pose to public health, there are Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ no antiviral strategies or vaccines for preventing alphaviral infection or treating alphavi- 4.0/). ral disease. This deficit of viable therapeutics highlights the need to better understand Pathogens 2021, 10, 771. https://doi.org/10.3390/pathogens10060771 https://www.mdpi.com/journal/pathogens PathogensPathogens2021 202110, 10, x FOR PEER REVIEW 2 of 19 , , 771 2 of 18 phaviral disease. This deficit of viable therapeutics highlights the need to better under- the mechanisms behind alphaviral infection and pathogenesis in order to develop novel stand the mechanisms behind alphaviral infection and pathogenesis in order to develop antiviral strategies for the mitigation of alphaviral disease. novel antiviral strategies for the mitigation of alphaviral disease. 2. The Contribution of Alphaviral RNAs to Pathogenesis, an Emerging Frontier 2. The Contribution of Alphaviral RNAs to Pathogenesis, an Emerging Frontier The primary purpose of this review is to summarize what is known about how The primary purpose of this review is to summarize what is known about how the the viral RNAs (vRNAs) produced during alphaviral infection influence pathogenesis viral RNAs (vRNAs) produced during alphaviral infection influence pathogenesis (Figure (Figure1). While much has been written about the role of viral RNA in translation, RNA 1). While much has been written about the role of viral RNA in translation, RNA synthesis, synthesis, and overall viral replication, relatively little is known about how the viral RNA and overall viral replication, relatively little is known about how the viral RNA influences influences alphaviral pathogenesis, and what information does exist on the topic has alphaviral pathogenesis, and what information does exist on the topic has never been for- never been formally summarized, leaving the current state of the field scattered. Thus, mally summarized, leaving the current state of the field scattered. Thus, the purpose of thethis purposereview isof to thisamass review what is known to amass about what alphaviral is known RNA about virulence alphaviral traits RNAand identify virulence traitswhat andis still identify unknown what regarding is still unknown the contribution regarding of the the viral contribution RNA to alphaviral of the viral patho- RNA to alphaviralgenesis. pathogenesis. FigureFigure 1.1. AlphaviralAlphaviral GeneticGenetic OrganizationOrganization andand RNARNA VirulenceVirulence Traits. Traits. Sequences Sequences and and secondary secondary RNA RNA structures in the genomic and subgenomic RNA known to impact virulence are indicated. structures in the genomic and subgenomic RNA known to impact virulence are indicated. Elements Elements that have only been shown to be present in a subset of alphaviruses have the specific vi- that have only been shown to be present in a subset of alphaviruses have the specific viruses listed in ruses listed in parentheses. sg 5′UTR = subgenomic 5′ UTR. parentheses. sg 50UTR = subgenomic 50 UTR. 3.3. AlphaviralAlphaviral RNA RNA Species Species and and Viral Viral Replication/Transcription Replication/Transcription Alphaviruses produce primarily three RNA species during viral replication: the ge- Alphaviruses produce primarily three RNA species during viral replication: the nome, which encodes the nonstructural proteins; the minus-strand RNA, which serves as genome, which encodes the nonstructural proteins; the minus-strand RNA, which serves the template for viral replication and transcription; and the subgenome, which encodes as the template for viral replication and transcription; and the subgenome, which encodes the structural proteins (Figure 2). The specific synthesis of the RNA species is in part de- the structural proteins (Figure2). The specific synthesis of the RNA species is in part termined by the processing of the nonstructural polyprotein and the promoter sequences determinedpresent on the by theviral processing RNAs. Translation of the nonstructural of the genomic polyprotein RNA produces and the the promoter nonstructural sequences presentpolyprotein on the P1234. viral To RNAs. form Translationthe initial viral of thereplicase genomic complex, RNA producesnsP4 is cleaved the nonstructural from the polyproteinpolyprotein by P1234. the proteolytic To form the activities initial of viral nsP2 replicase and associates complex, with nsP4 P123 is [13]. cleaved This initial from the polyproteincomplex then by uses the the proteolytic viral genome activities as a template of nsP2 and for the associates synthesis with of the P123 negative-sense [13]. This initial complexminus-strand then RNA. uses theThe viral nonstruc genometural aspolyprotein a template is forthen the furt synthesisher cleaved of theby nsP2 negative-sense to pro- minus-strandduce the individual RNA. nonstructural The nonstructural proteins, polyprotein nsP1-4 that is presumably then further in conjunction cleaved by with nsP2 to producehost factors, the form individual the fully nonstructural processed viral proteins, replicase nsP1-4 complex. that Once presumably fully processed, in conjunction the withreplicase host complex factors, formthen theuses fully the minus-strand processed viral RNA replicase as a template complex. to Oncesynthesize fully the processed, ge- thenomic replicase and subgenomic complex thenvRNAs. uses For the an minus-strand in-depth discussion RNA asof aalphaviral template replication, to synthesize see the genomicRupp et al., and 2015 subgenomic [14]. vRNAs. For an in-depth discussion of alphaviral replication,
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