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Adaptive Strategies of African Horse Sickness Virus to Facilitate Vector Adaptive strategies of African horse sickness virus to facilitate vector transmission Anthony Wilson, Philip Scott Mellor, Camille Szmaragd, Peter Paul Clement Mertens To cite this version: Anthony Wilson, Philip Scott Mellor, Camille Szmaragd, Peter Paul Clement Mertens. Adaptive strategies of African horse sickness virus to facilitate vector transmission. Veterinary Research, BioMed Central, 2009, 40 (2), 10.1051/vetres:2008054. hal-00903094 HAL Id: hal-00903094 https://hal.archives-ouvertes.fr/hal-00903094 Submitted on 1 Jan 2009 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. (2009) 40:16 www.vetres.org DOI: 10.1051/vetres:2008054 Ó INRA, EDP Sciences, 2009 Review article Adaptive strategies of African horse sickness virus to facilitate vector transmission Anthony WILSON, Philip Scott MELLOR*, Camille SZMARAGD, Peter Paul Clement MERTENS Vector-Borne Disease Programme, Institute for Animal Health, Ash Road, Pirbright, Woking, Surrey, GU24 0NF, United Kingdom (Received 9 September 2008; accepted 16 December 2008) Abstract – African horse sickness virus (AHSV) is an orbivirus that is usually transmitted between its equid hosts by adult Culicoides midges. In this article, we review the ways in which AHSV may have adapted to this mode of transmission. The AHSV particle can be modified by the pH or proteolytic enzymes of its immediate environment, altering its ability to infect different cell types. The degree of pathogenesis in the host and vector may also represent adaptations maximising the likelihood of successful vectorial transmission. However, speculation upon several adaptations for vectorial transmission is based upon research on related viruses such as bluetongue virus (BTV), and further direct studies of AHSV are required in order to improve our understanding of this important virus. African horse sickness / AHSV / vector / Culicoides Table of contents 1. Introduction........................................................................................................................................... 2 2. The AHSV transmission cycle ............................................................................................................. 2 2.1. The transmission of vector-borne diseases.................................................................................. 2 2.2. Primary and secondary vector species ........................................................................................ 4 2.2.1. Culicoides vectors of AHSV........................................................................................... 4 2.2.2. Secondary vector species................................................................................................. 5 2.3. Primary and secondary host species............................................................................................ 5 2.4. Virus structure and protein function............................................................................................6 3. Adaptation for transmission from host to vector ................................................................................. 7 3.1. Generation of infectious sub-viral particles ................................................................................ 7 3.2. Adaptive role of clinical signs .................................................................................................... 8 4. Adaptation for dissemination within the vector................................................................................... 9 4.1. Role of nonstructural proteins in cell exit and cytopathogenesis............................................... 9 4.2. Effects of temperature on the replication of AHSV ................................................................... 9 5. Adaptation for transmission from vector to host................................................................................. 10 6. Adaptation to periods of vector absence.............................................................................................. 11 7. Potential effects of tissue culture attenuation on epidemiology.......................................................... 11 8. Conclusions........................................................................................................................................... 11 * Corresponding author: [email protected] Article published by EDP Sciences Vet. Res. (2009) 40:16 A. Wilson et al. 1. INTRODUCTION or AHSV-7 had been detected in West Africa. During 2007 the virus was also detected in African horse sickness virus (AHSV) is an Nigeria, Ghana, Mali and Mauritania. orbivirus transmitted between equid hosts by Orbiviruses have spread from West Africa to Culicoides midges (Diptera, Ceratopogonidae). the Iberian Peninsula on several occasions, The clinical signs of AHSV infection are rarely probably via the transportation of infected adult seen in zebras and donkeys, but mortality rates Culicoides on the wind [1, 95, 96]. The circula- can exceed 90% in horses. Although largely tion of AHSV in West Africa, combined with the restricted to sub-Saharan Africa, AHSV has rapid emergence of bluetongue virus (BTV) in expanded beyond this core region on several Europe since 1998, and particularly the damage occasions [24, 36], and has persisted for several caused by BTV-8 since 2006 [114], suggests that years on each, suggesting that the geographical the potential for Culicoides-borne orbiviruses to area that is potentially suitable for its transmis- spread in Europe may be greater than previously sion is considerably greater than that in which it appreciated. The recent spread of multiple currently occurs. As a consequence of its severity AHSV serotypes to West Africa has further in horses and its proven capacity for sudden and increased the risk of its introduction into Europe. rapid expansion, African horse sickness (AHS) is In light of both these developments, an listed by the OIE as a notifiable disease. improved understanding of factors that can Historical distribution and major outbreaks influence the distribution and spread of AHSV – Despite occasional small outbreaks in North is urgently required. This paper reviews the Africa and the Arabian Peninsula, prior to ways in which AHSV is adapted to vector-borne 1959 AHSV was thought to be effectively con- transmission. fined to sub-Saharan Africa [75, 91]. During that year, AHSV-9 emerged in the Middle East, spreading as far as Pakistan and India [29, 36, 2. THE AHSV TRANSMISSION CYCLE 37, 75, 91]. This devastating outbreak caused the deaths of over 300 000 equids before mas- 2.1. The transmission of vector-borne diseases sive vaccination and vector control efforts, combined with the virtual extinction of suscep- AHSV is a member of the genus Orbivirus in tible hosts in the region, brought it to a halt in the family Reoviridae [74, 98, 99, 108]. The 1961 [4, 64]. Another outbreak caused by the orbiviruses are predominantly transmitted via same serotype occurred in North Africa during the bites of haematophagous arthropods, the 1965, and is thought to have originated from main vectors being Culicoides midges, ticks, infected donkeys that were transported across phlebotomine sandflies and mosquitoes [17, the Sahara. This outbreak briefly spread as far 67], while their vertebrate hosts include bats, eq- north as southern Spain [23, 24, 43, 76]. In uids, primates, ruminants, lagomorphs, and birds 1987, AHSV-4 was accidentally introduced into [17, 30]. The biological transmission of AHSV central Spain when infected zebras were by Culicoides vectors is illustrated in Figure 1. imported for a safari park near Madrid [47], For biological transmission by haematopha- and remained active on the Iberian peninsula gous arthropods, the virus must be present in until 1990. More recently, in 2007, AHSV-4 peripheral blood vessels or in the skin tissues was detected in Kenya and AHSV-2 and of the vertebrate host, making it accessible to AHSV-7 were both detected in Senegal1,a blood-feeding arthropods. It must then survive country where serotype 9 has previously been in the environment of the arthropod gut long detected [82]. This was the first time AHSV-2 enough to penetrate and infect the cells of the gut wall. It must then finally spread through the internal environment of the arthropod to infect the salivary glands in order to be trans- 1 http://www.reoviridae.org/dsRNA_virus_proteins/ mitted back to the vertebrate host during sub- outbreaks.htm/ sequent blood-feeding. The time between Page 2 of 16 (page number not for citation purpose) AHSV adaptations for vector transmission Vet. Res. (2009) 40:16 Extrinsic incubation Host to vector Vector transmission to host transmission Intrinsic incubation Figure 1. The AHSV transmission cycle. (A color version of this figure is available at www.vetres.org.) ingestion and the insect being able to transmit being transmitted. This possibility is explored the virus to another vertebrate host is termed further in Section 3.2. the extrinsic incubation period (EIP), and is The infection
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