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Understanding the Interaction Between Betanodavirus and Its Host for the Development of Prophylactic Measures for Viral Encephalopathy and Retinopathy

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Understanding the Interaction Between Betanodavirus and Its Host for the Development of Prophylactic Measures for Viral Encephalopathy and Retinopathy Fish & Shellfish Immunology 53 (2016) 35e49 Contents lists available at ScienceDirect Fish & Shellfish Immunology journal homepage: www.elsevier.com/locate/fsi Understanding the interaction between Betanodavirus and its host for the development of prophylactic measures for viral encephalopathy and retinopathy * Janina Z. Costa , Kim D. Thompson Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Scotland, EH26 0PZ, United Kingdom article info abstract Article history: Over the last three decades, the causative agent of viral encephalopathy and retinopathy (VER) disease Received 27 January 2016 has become a serious problem of marine finfish aquaculture, and more recently the disease has also been Received in revised form associated with farmed freshwater fish. The virus has been classified as a Betanodavirus within the family 4 March 2016 Nodaviridae, and the fact that Betanodaviruses are known to affect more than 120 different farmed and Accepted 15 March 2016 wild fish and invertebrate species, highlights the risk that Betanodaviruses pose to global aquaculture Available online 17 March 2016 production. Betanodaviruses have been clustered into four genotypes, based on the RNA sequence of the T4 var- Keywords: fi fi Betanodavirus iable region of their capsid protein, and are named after the sh species from which they were rst Viral encephalopathy and retinopathy derived i.e. Striped Jack nervous necrosis virus (SJNNV), Tiger puffer nervous necrosis virus (TPNNV), VER Barfin flounder nervous necrosis virus (BFNNV) and Red-spotted grouper nervous necrosis virus Viral characterisation (RGNNV), while an additional genotype turbot betanodavirus strain (TNV) has also been proposed. Vaccines However, these genotypes tend to be associated with a particular water temperature range rather than Disease control being species-specific. Larvae and juvenile fish are especially susceptible to VER, with up to 100% mortality resulting in these age groups during disease episodes, with vertical transmission of the virus increasing the disease problem in smaller fish. A number of vaccine preparations have been tested in the laboratory and in the field e.g. inactivated virus, recombinant proteins, virus-like particles and DNA based vaccines, and their efficacy, based on relative percentage survival, has ranged from medium to high levels of protection to little or no protection. Ultimately a combination of effective prophylactic measures, including vaccination, is needed to control VER, and should also target larvae and broodstock stages of production to help the industry deal with the problem of vertical transmission. As yet there are no commercial vaccines for VER and the aquaculture industry eagerly awaits such a product. In this review we provide an overview on the current state of knowledge of the disease, the pathogen, and interactions between betanodavirus and its host, to provide a greater understanding of the multiple factors involved in the disease process. Such knowledge is needed to develop effective methods for controlling VER in the field, to protect the various aquaculture species farmed globally from the different Betanodavirus genotypes to which they are susceptible. © 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Contents 1. Introduction . ................................................. 36 2. History of the disease . ................................................. 36 3. Pathogen.................................................................. ....... ................................................. 36 3.1. Characterisation of the virus . ........................36 * Corresponding author. E-mail address: [email protected] (J.Z. Costa). http://dx.doi.org/10.1016/j.fsi.2016.03.033 1050-4648/© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 36 J.Z. Costa, K.D. Thompson / Fish & Shellfish Immunology 53 (2016) 35e49 3.2. Phylogeny and serology . ........................................38 4. Thedisease................................................................. .................................. ..................... 38 4.1. Clinical signs and tissue distribution . ........................................38 4.2. Transmission . ...................................................39 4.3. Route of infection . ........................................39 5. Host-pathogen interactions . ..................... 40 5.1. The pathogen response . ........................................40 5.2. The host immune response . ........................................40 6. Control measures . ..................... 41 6.1. Husbandry measures . ........................................41 6.2. Therapeutics . ...................................................41 6.3. Betanodavirus vaccines . ........................................42 7. Conclusion ................................................................. .................................. ..................... 44 Acknowledgements . ...................................................44 Supplementary data . ..................... 44 References . ...................................................44 1. Introduction 2. History of the disease Since its first outbreak in 1985, the disease Viral Encephalopathy Early studies described the agent of VER as a “picorna-like virus” and Retinopathy (VER) has been increasing in importance to the [7,8], but based on virion size and genome characteristics of Striped aquaculture industry, and is now recognised as a major problem in Jack (Pseudocaranx dentex) nervous necrosis virus (SJNNV), the Mediterranean and Asia marine aquaculture. Outbreaks of VER are pathogen was classified as a member of the Nodaviridae family [9]. associated with high levels of mortality, with up to 100% of fish A Nodaviridae virus was also identified as the pathogen involved in dying from the disease. In most cases of VER, the infection tends to VER outbreaks in European seabass (Dicentrarchus labrax) and be seen in post-hatch larvae, fingerlings and juvenile fish, and those Asian seabass (Lates calcarifer) [10]. In 2000, viruses within the surviving infection are inclined to perform poorly after recovering Nodaviridae family were re-classified into two genera, the Beta- from the disease [1,2]. nodavirus genus grouping the nodaviruses affecting fish, and the Because VER is caused by an RNA virus, which can be trans- genus Alphanodavirus that includes all the insect nodaviruses [11]. mitted both horizontally and vertically, the most sensible way of Betanodavirus is also referred to as NNV (Nervous Necrosis Virus). controlling this disease is to apply effective biosecurity and to Since 1985, VER has been reported worldwide, except for South vaccinate the fish. Although there are a number of promising America where no outbreaks of the disease have been reported studies in the literature focussing on different types of vaccines [12e16]. VER affects both farmed and wild fish, with more than 120 for VER (e.g. recombinant protein, DNA and inactivated vaccines), species belonging to 30 families from 11 different orders being there are still no commercial vaccines available for this disease. susceptible to infection (see supplementary Table 1). For more than This is possibly because the disease is associated with outbreaks a decade, VER was thought to be a problem solely of marine fish, in larvae and juvenile fish, prior to them becoming fully immu- but since 2000 the virus has also been reported in freshwater nocompetent, or perhaps other vaccine formulations/strategies species such as guppy (Poecilia reticulata), tilapia (Oreochromis are required to make the vaccines more efficacious in an aqua- niloticus), sturgeon (Acipenser gueldestaedi), Chinese catfish (Silurus culture setting. The lack of an effective commercial product asotus Linnaeus, 1758), Australian bass (Macquaria novemaculeata), highlights the need for a greater understanding of the interaction Nile tilapia (Oreochromis niloticus) and an endangered blenny spe- between the virus, the immune response of its host and the cies (Salaria fluviatilis) [17e22]. disease process that results. To be in a position to design a more VER is a neuropathogenic disease, and for this reason it was first effective vaccine against VER, we need a broader knowledge of: named sea bass viral encephalitis (SVE) [23]. The disease has also (a) the pathogen (e.g. its routes of infection, how it infects its been referred to as viral nervous necrosis (VNN) [24], fish viral host, how it manipulates the host's response to its own advantage encephalitis (FVE) [10] and viral encephalitis and retinitis [25]. The and evades the host's immune system, the role of the viral pro- disease is now officially named viral encephalopathy and retinop- _ teins in this process and what makes the virus temperature- and athy (VER) by the Office International des Epizooties (OIE), based on host-specific); (b) the host, (e.g. how it fights the viral infection, the histopathology that accompanies the infection [4]. the mechanisms involved and what makes some species sus- ceptible and others asymptomatic carriers) and (c) the disease (e.g. what are the clinical signs of the disease, how is it trans- 3. Pathogen mitted and how it can be managed though appropriate fish husbandry). Although a number of reviews are available 3.1. Characterisation of the virus providing an overview
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