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Yellow Fever: Integrating Current Knowledge with Technological Innovations to Identify Strategies for Controlling a Re-Emerging Virus

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Yellow Fever: Integrating Current Knowledge with Technological Innovations to Identify Strategies for Controlling a Re-Emerging Virus viruses Review Yellow Fever: Integrating Current Knowledge with Technological Innovations to Identify Strategies for Controlling a Re-Emerging Virus 1, 1, 2, 3 Robin D.V. Kleinert y , Eduardo Montoya-Diaz y, Tanvi Khera y , Kathrin Welsch , Birthe Tegtmeyer 4 , Sebastian Hoehl 5 , Sandra Ciesek 5 and Richard J.P. Brown 1,* 1 Division of Veterinary Medicine, Paul-Ehrlich-Institute, 63225 Langen, Germany; [email protected] (R.D.V.K.); [email protected] (E.M.-D.) 2 Department of Gastroenterology and Hepatology, Faculty of Medicine, University Hospital Essen, University of Duisburg-Essen, 45147 Essen, Germany; [email protected] 3 University of Veterinary Medicine Hannover, 30559 Hannover, Germany; [email protected] 4 Institute for Experimental Virology, TWINCORE, Centre for Experimental and Clinical Infection Research; a joint venture between the Medical School Hannover (MHH) and the Helmholtz Centre for Infection Research (HZI), 30625 Hannover, Germany; [email protected] 5 Institute of Medical Virology, University Hospital Frankfurt, 60596 Frankfurt am Main, Germany; [email protected] (S.H.), [email protected] (S.C.) * Correspondence: [email protected]; Tel.: +49-6103-77-7441 These authors contributed equally to the work. y Received: 30 August 2019; Accepted: 11 October 2019; Published: 17 October 2019 Abstract: Yellow fever virus (YFV) represents a re-emerging zoonotic pathogen, transmitted by mosquito vectors to humans from primate reservoirs. Sporadic outbreaks of YFV occur in endemic tropical regions, causing a viral hemorrhagic fever (VHF) associated with high mortality rates. Despite a highly effective vaccine, no antiviral treatments currently exist. Therefore, YFV represents a neglected tropical disease and is chronically understudied, with many aspects of YFV biology incompletely defined including host range, host–virus interactions and correlates of host immunity and pathogenicity. In this article, we review the current state of YFV research, focusing on the viral lifecycle, host responses to infection, species tropism and the success and associated limitations of the YFV-17D vaccine. In addition, we highlight the current lack of available treatments and use publicly available sequence and structural data to assess global patterns of YFV sequence diversity and identify potential drug targets. Finally, we discuss how technological advances, including real-time epidemiological monitoring of outbreaks using next-generation sequencing and CRISPR/Cas9 modification of vector species, could be utilized in future battles against this re-emerging pathogen which continues to cause devastating disease. Keywords: yellow fever virus; flavivirus entry factor; global diversity; yellow fever virus tropism; animal models; transmission and vector control; vaccine; host immune response; E protein structure; re-emerging virus 1. General Introduction Yellow fever was historically the first described viral hemorrhagic fever (VHF) and its causative agent, the yellow fever virus (YFV), is the prototypic member of the family Flaviviridae. Pioneering experimental work in the 19th century identified the Aedes aegypti mosquitos as the vector responsible for transmission to humans, facilitating subsequent eradication from Europe and North America [1–4]. However, today, YFV remains prevalent in tropical regions of Africa and South America [4,5], with Viruses 2019, 11, 960; doi:10.3390/v11100960 www.mdpi.com/journal/viruses Viruses 2019, 11, 960 2 of 32 over 900 million people currently living in endemic areas, 500 million of whom reside in Africa [6]. YFV representsViruses 2019 a, zoonotic11, x FOR PEER pathogen REVIEW and complete eradication in tropical regions is2 not of 32 achievable due to rainforestresponsible circulation for transmission in primate to humans, reservoirs facilitating [4 subsequent,6,7]. A highly eradication effective from Europe live-attenuated and North vaccine, the 17D strain,America was [1–4]. developed However, intoday, the YFV 1930s remains and stillprevalent in use in today,tropical overregions 80 of years Africa later and [South3,6,8 ]. Indeed, vaccinationAmerica represents [4,5], with one over of the900 million core strategies people currently employed living in to endemic stop YFV areas, outbreaks 500 million orof whom minimize their reside in Africa [6]. YFV represents a zoonotic pathogen and complete eradication in tropical regions impact whenis not they achievable do occur due [ 9to]. rainforest circulation in primate reservoirs [4,6,7]. A highly effective The Flaviviridaelive-attenuatedis vaccine, a diverse the group17D strain, of smallwas developed enveloped in the viruses 1930s and representing still in use today, over over 100 80 species [10]. Viral genomesyears later from [3,6,8].Flaviviridae Indeed, vaccinamemberstion represents are non-segmented one of the core positive-stranded strategies employed RNAsto stop YFV ranging from ~9 to ~13 kboutbreaks in length, or minimize and phylogenetic their impact when analyses they do of occur 125 family[9]. members revealed four well-supported The Flaviviridae is a diverse group of small enveloped viruses representing over 100 species [10]. genera: PestivirusViral genomes, Hepacivirus from Flaviviridae, Pegivirus membersand areFlavivirus non-segmented(Figure positive-stranded1 and [ 10]). Members RNAs ranging of thefromFlaviviridae which cause~9 ato significant~13 kb in diseaselength, and burden phylogenetic in humans analyses are highlightedof 125 family on members the tree revealed presented four in Figure1. Genome organizationwell-supported andgenera: cytoplasmic Pestivirus, Hepacivirus, replication Pegivirus on and endoplasmic Flavivirus (Figure reticulum 1 and [10]). (ER) Members membranes are conservedof between the Flaviviridae divergent whichFlaviviridae cause a significantmembers. disease However, burden in host-range,humans are highlighted tissue-tropism, on the pathogenicitytree presented in Figure 1. Genome organization and cytoplasmic replication on endoplasmic reticulum and modes(ER) of membranes transmission are conserved can differ between greatly divergent [10]. YFV Flaviviridae is a member members. of However, the Flavivirus host-range,genus, which is composedtissue-tropism, of arboviruses pathogenicity exhibiting and modes broad of transmis host rangession can which differ greatly can be [10]. transmitted YFV is a member to humans of from animal reservoirsthe Flavivirus via genus, insect which vectors. is composed This genus of arboviruses contains exhibiting a number broad of host important ranges which human can be pathogens which cantransmitted cause acute to humans infections, from animal including reservoirs dengue via insect virus vectors. (DENV), This Westgenus Nilecontains virus a number (WNV), of Japanese important human pathogens which can cause acute infections, including dengue virus (DENV), encephalitisWest virus Nile (JEV)virus (WNV), and Zika Japanese virus encephalitis (ZIKV) (Figure virus (JEV)1). Transmission and Zika virus is(ZIKV) mediated (Figure via 1). mosquito vectors andTransmission infection ofis mediated humans via can mosquito cause vectors a range and of infection clinical of outcomes, humans can ranging cause a range from ofasymptomatic clinical to encephalitisoutcomes, (WNV, ranging JEV and from ZIKV) asymptomatic or fatal to hemorrhagic encephalitis (WNV, fever JEV (YFV and andZIKV) DENV). or fatal hemorrhagic fever (YFV and DENV). Figure 1. Phylogenetic relationships within the Flaviviridae. The evolutionary tree presented was Figure 1. Phylogenetic relationships within the Flaviviridae. The evolutionary tree presented was generated using MEGA7 [11] from a conserved region of the viral RNA dependant RNA polymerase generated(RdRp: using NS5 MEGA7 or NS5B) [11 and] from represents a conserved n = 125 members region of of thethe viralFlaviviridae RNA. The dependant in-frame nucleotide RNA polymerase (RdRp: NS5alignment or NS5B) was downloaded and represents from https://talk.ictvonn = 125 membersline.org/, of theadjustedFlaviviridae manually,. Theand all in-frame positions nucleotide alignmentcontaining was downloaded gaps or missing from data https: were eliminated//talk.ictvonline.org prior to analyses/, adjusted(734 sites in manually,the final dataset). and The all positions containingresulting gaps orphylogeny missing was data inferred were via eliminated the Maximum prior Likelihood to analyses Composite (734 sitesmethod in under the finalthe dataset). The resulting phylogeny was inferred via the Maximum Likelihood Composite method under the GTR+I+G model of nucleotide substitution to account for evolutionary rate differences among sites. The genera Pegivirus, Hepacivirus, Pestivirus and Flavivirus are color-coded, in addition to distinct lineages within the genus Flavivirus. Statistical robustness of highlighted groupings was determined using the bootstrap approach and values assigned to these branches are percentages derived from 500 replications. Branch lengths are proportional to the scale bar (units: substitutions per site). Viruses 2019, 11, 960 3 of 32 YFV continues to pose a very real threat to public health, which has been starkly illustrated by recent outbreaks in Angola in 2015–2016 [1,12,13] and Brazil in 2016–2017 [14–16], and associated imports into non-endemic regions [15,17]. This is compounded by a limited vaccine production, which can easily be overwhelmed by a large YFV outbreak, and the collapse of vector control programs [1,14,15], coupled with
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