Molecular Characterization of the Alloherpesvirus Anguillid Herpesvirus 1
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Molecular characterization of the alloherpesvirus anguillid herpesvirus 1 Steven van Beurden 2012 The research described in this thesis was performed at the Central Veterinary Institute of Wageningen UR, Lelystad, the Netherlands, and was financially supported by the Dutch Ministry of Economic Affairs, Agriculture and Innovation. Printing of this thesis was financially supported by the Central Veterinary Institute of Wageningen UR, Lelystad, the Netherlands, and by Kees en Martha van Beurden. Cover illustration: Russell Kightley Lay-out: Steven van Beurden Printed by: Gildeprint Drukkerijen ISBN: 978-94-6108-325-8 Molecular characterization of the alloherpesvirus anguillid herpesvirus 1 Moleculaire karakterisering van het alloherpesvirus anguillid herpesvirus 1 (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof. dr. G.J. van der Zwaan, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op donderdag 30 augustus 2012 des middags te 12.45 uur door Stefanus Johannus van Beurden geboren op 20 september 1984 te Delfzijl Promotor: Prof. dr. P.J.M. Rottier Co-promotoren: Dr. ir. M.Y. Engelsma Dr. B.P.H. Peeters CONTENTS Chapter 1 General introduction 7 Chapter 2 Viral diseases of wild and farmed European eel (Anguilla anguilla) with 29 particular reference to the Netherlands Chapter 3 Development, optimization and validation of a TaqMan probe based 53 real-time PCR assay for the detection of anguillid herpesvirus 1 Chapter 4 Complete genome sequence and taxonomic position of anguillid 67 herpesvirus 1 Chapter 5 Anguillid herpesvirus 1 transcriptome 79 Chapter 6 Genome-wide gene expression analysis of anguillid herpesvirus 1 107 Chapter 7 Identification and localization of the structural proteins of anguillid 129 herpesvirus 1 Chapter 8 The alloherpesviral counterparts of interleukin 10 in European eel and 151 common carp Chapter 9 General discussion 165 Appendix New species Anguillid herpesvirus 1 in the genus Cyprinivirus, family 179 Alloherpesviridae, order Herpesvirales Samenvatting 185 Dankwoord 193 Curriculum vitae 201 General introduction Partially based on: Herpesviruses of fish, amphibians and invertebrates (2012) In Magel GM, Tyring S (eds). Herpesviridae – A look into this unique family of viruses. InTech, Rijeka Steven J van Beurden1,2 Marc Y Engelsma1 1 Central Veterinary Institute of Wageningen UR, Lelystad, The Netherlands 2 Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands Chapter 1 Herpesviruses are large DNA viruses with a distinctive virion morphology [1]. They have a long non- segmented linear double-stranded DNA genome. This genome is incorporated in an icosahedral nucleocapsid with a diameter of about 100 nm, made up of 162 hollow capsomers (T = 16). The nucleocapsid is surrounded by a proteinaceous layer called the tegument, which is surrounded in turn by a membrane envelope 120 to 260 nm in diameter. The envelope is host-derived and contains virus encoded glycoproteins. This constellation is distinctively different from that of any other animal virus. Herpesviruses infect a wide range of vertebrates and invertebrates, and are generally host-specific [2]. They belong to the taxonomic order Herpesvirales, which is subdivided into the families Herpesviridae, Alloherpesviridae and Malacoherpesviridae [3]. The family Herpesviridae comprises the herpesviruses infecting mammals, reptiles and birds. The family Alloherpesviridae contains the herpesviruses infecting amphibians and fish. The family Malacoherpesviridae comprises the herpesviruses infecting invertebrates. Herpesviruses have evolved with their respective hosts over long periods of time and are well adapted to them [4]. Molecular phylogenetic data and their generally modest pathogenicity in natural immunocompetent hosts support this view. Severe infections may occur when herpesviruses infect immunocompromised individuals or susceptible non-natural host species [1]. The viral diseases and cancers caused by human herpesviruses may be significant neveretheless, and specific herpesvirus infections in livestock may have serious economic consequences. Prevention and treatment of herpesvirus infections is complicated due to the ability of herpesviruses to persist as latent infections. In the last decades, several serious disease outbreaks in wild and cultured fish were found to be associated with herpesvirus infections [5-7]. In many of the major aquaculture species, such as carp, salmon, catfish, eel and sturgeon, herpesviruses have now been identified (Table 1). Preventive measures and management strategies are taken at fish farms to avoid and reduce the production losses due to these viruses. In addition, several other less-pathogenic fish herpesviruses, some of which induce skin tumours and tumour-like proliferations [8], have been identified. The course of infection of both the high pathogenic and tumour-inducing alloherpesviruses seems to be dependent on host age and ambient water temperature. In this chapter an overview will be given on the biology of alloherpesviruses, the classification and taxonomy of the order Herpesvirales, the genome organization and gene conservation within the family Alloherpesviridae, the current knowledge on gene expression of alloherpesviruses, and the conservation of herpesvirus virion structure, as well as a brief introduction into herpesvirus immune evasion. 8 General introduction Table 1. Classified, unclassified and uncharacterized fish and amphibian herpesviruses of the family Alloherpesviridae. Genus Virus name Common name Natural host(s) Reference Batrachovirus Ranid herpesvirus 1 Lucké tumour herpesvirus Leopard frog (R. pipiens) [9] Ranid herpesvirus 2 Frog virus 4 Leopard frog (R. pipiens) [9] Cyprinivirus Cyprinid herpesvirus 1 Carp pox Common carp (C. carpio) [10] Cyprinid herpesvirus 2 Goldfish hematopoietic Goldfish (C. auratus) [10] necrosis virus Cyprinid herpesvirus 3 Koi herpesvirus Common carp (C. carpio carpio) & [10] Koi (C. carpio koi) Anguillid herpesvirus 1 Eel herpesvirus European eel (A. anguilla) & This Japanese eel (A. japonica) thesis Ictalurivirus Acipenserid herpesvirus 2 White sturgeon herpesvirus 2 White sturgeon (A. ransmontatus) [11] Ictalurid herpesvirus 1 Channel catfish virus Channel catfish (I. punctatus) [12] Ictalurid herpesvirus 2 Ictalurus melas herpesvirus Black bullhead (A. melas) & [13] Channel catfish (I. punctatus) Salmonivirus Salmonid herpesvirus 1 Herpesvirus salmonis Rainbow trout (O. mykiss) [14] Salmonid herpesvirus 2 Coho salmon herpesvirus Salmon spp. (Oncorhynchus spp.) [14] Salmonid herpesvirus 3 Epizootic epitheliotrophic Lake trout (S. namaycush) [14] disease virus Unclassified Acipenserid herpesvirus 1 White sturgeon herpesvirus 1 Sturgeon spp. (Acipenser spp.) [11] alloherpesviruses - Pilchard herpesvirus Pacific sardine (S. sagax) [15] Uncharacterized Esocid herpesvirus 1 Blue spot disease virus Northern pike (E. Lucius) & - alloherpesviruses Muskellunge (E. masquinongy) Percid herpesvirus 1 Herpesvirus vitreum Walleye (S. vitreum) - Pleuronectid herpesvirus 1 Herpesvirus scophthalami Turbot (S. maximus) - - Atlantic salmon Atlantic salmon (S. salar) - papillomatosis virus - Herpesvirus of osmerus European smelt (O. eperlanus) & - eperlanus 1 Rainbow smelt (O. mordax) - Tilapia larvae encephalitis Tilapia (Oreochromis spp.) - virus - Viral epidermal Japanese flounder (P. esus) - hyperplasia/necrosis - - Angelfish (P. altum) - - - Golden ide (L. ide) - - - Red striped rockfish (S. proriger) - - - Smooth dogfish (M. canis) - 9 Chapter 1 BIOLOGY OF THE ALLOHERPESVIRUSES Frog herpesviruses The North American leopard frog (Rana pipiens) is occasionally affected by a renal adenocarcinoma known as the Lucké tumour. A viral aetiology was proposed based on the presence of acidophilic inclusions in tumour cell nuclei and on transmission experiments [16, 17]. Viral particles were observed by electron microscopy (EM) about 20 years later [18]. Yet another decade later, the virus was characterized as a herpes-type virus [19], later designated Ranid herpesvirus 1 (RaHV1). Tumour formation could be induced by injection with purified RaHV1 [20], and Koch-Henle’s postulates were fulfilled [21]. Virus replication is promoted by low temperature [22], whereas induction of metastasis is promoted by high temperature [23, 24]. Although RaHV1 cannot be cultured in cell lines, it was the first amphibian herpesvirus subjected to extensive genomic studies [25]. During an attempt to isolate the causative agent of the Lucké tumour from pooled urine of tumour- bearing frogs, another virus – designated frog virus 4 – was isolated using a frog embryo cell line [26]. The virus was shown to possess the morphological characteristics of a herpesvirus [27], but appeared to be clearly distinctive from the Lucké tumour herpesvirus with regard to its in vitro propagation and genomic properties [28]. In addition, frog virus 4 has no oncogenic potential, although it infects leopard frog embryos and larvae effectively [22]. Frog virus 4 was later designated Ranid herpesvirus 2 (RaHV2). Catfish herpesviruses In the United States, during the rapid expansion of the pond-cultured channel catfish (Ictalurus punctatus) industry in the late 1960s, high mortalities were reported in fingerlings and fry shortly after transfer from the hatchery to the fry ponds [7]. Moribund fish showed behavioural