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Characterisation of Major Histocompatibility Complex Class I Genes in Japanese Ranidae Frogs

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Characterisation of Major Histocompatibility Complex Class I Genes in Japanese Ranidae Frogs Immunogenetics DOI 10.1007/s00251-016-0934-x ORIGINAL ARTICLE Characterisation of major histocompatibility complex class I genes in Japanese Ranidae frogs Quintin Lau1 & Takeshi Igawa 2 & Shohei Komaki3 & Yoko Satta1 Received: 21 April 2016 /Accepted: 23 June 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract The major histocompatibility complex (MHC) is a permits further exploration of the polygenetic factors associ- key component of adaptive immunity in all jawed vertebrates, ated with resistance to infectious diseases. and understanding the evolutionary mechanisms that have shaped these genes in amphibians, one of the earliest terrestrial Keywords Major histocompatibility complex . Selection . tetrapods, is important. We characterised MHC class I varia- Rana . Anura tion in three common Japanese Rana species (Rana japonica, Rana ornativentris and Rana tagoi tagoi) and identified a total of 60 variants from 21 individuals. We also found evolution- Introduction ary signatures of gene duplication, recombination and balancing selection (including trans-species polymorphism), Major histocompatibility complex (MHC) genes code for all of which drive increased MHC diversity. A unique feature membrane-bound glycoproteins that recognise, bind and pres- of MHC class I from these three Ranidae species includes low ent specific antigens to T lymphocytes and, thus, are important synonymous differences per site (dS) within species, which we components of adaptive immunity in jawed vertebrates. MHC attribute to a more recent diversification of these sequences or class I molecules bind endogenous antigenic peptides, pre- recent gene duplication. The resulting higher dN/dS ratio rela- senting them to cytotoxic Tcells, and comprised of an α heavy tive to other anurans studied could be related to stronger se- chain and β2m microglobulin chain. The α chain of MHC lection pressure at peptide binding sites. This is one of the first class I consists of three extracellular domains (α1, α2 and studies to investigate MHC in Japanese amphibians and α3) encoded by exons 2, 3 and 4, respectively. The anchor residues within the peptide binding groove, sometimes re- ferred to as peptide binding sites, are found in the α1 and α2 domains (Hughes and Yeager 1998). There are two groups Electronic supplementary material The online version of this article of class I genes based on functional differences: class Ia (doi:10.1007/s00251-016-0934-x) contains supplementary material, which is available to authorized users. (classical) genes which are highly polymorphic and expressed in all nucleated cells and class Ib (non-classical) that are less * Quintin Lau polymorphic and have variable expression across tissues [email protected] (Goyos et al. 2011; Hughes and Yeager 1998). Classical MHC genes are one of the most polymorphic genes of vertebrate genomes (Hedrick 1994), and they evolve 1 Department of Evolutionary Studies of Biosystems, Sokendai (The Graduate University for Advanced Studies), Kamiyamaguchi under a birth and death process (Nei and Rooney 2005), 1560-35, Hayama, Kanagawa 240-0193, Japan resulting in variation in MHC loci number between different 2 Global Career Design Center, Hiroshima University, 1-7-1, species. MHC variation is primarily maintained by pathogen- Higashi-Hiroshima, Hiroshima 739-8514, Japan mediated balancing selection (Bernatchez and Landry 2003; 3 Division of Developmental Science, Graduate School for Hughes and Yeager 1998). One of the characteristics of International Development and Cooperation, Hiroshima University, balancing selection is trans-species polymorphism, whereby 1-5-1, Higashi-Hiroshima, Hiroshima 739-8529, Japan alleles in different species are more closely related than Immunogenetics conspecific alleles (Klein et al. 1998), and this has been seen (green frog), Lithobates yavapaiensis (lowland leopard frog), in MHC genes (Wei et al. 2010; Jaratlerdsiri et al. 2014). As Lithobates pipiens (Northern leopard frog) and Rana the MHC is important for adaptive immunity, several studies temporaria (common frog), and signatures of balancing selec- in vertebrates have found associations with MHC variation tion have been detected (Flajnik et al. 1999;Kiemnec- and infectious diseases (summarised by Sommer 2005). In Tyburczy et al. 2012;Teacheretal.2009). Apart from particular, recent studies have identified MHC–disease asso- balancing selection, recombination and gene duplication also ciations in a number of amphibian species (Bataille et al. play a role in driving MHC diversity (Carrington 1999; 2015; Savage and Zamudio 2011; Teacher et al. 2009). Yeager and Hughes 1999). Recombination between exons at Anuran amphibians are ectothermic tetrapods with a a single locus has been identified in Xenopus laevis (African metamorphic life cycle, comprising a developing pre- clawed frog) and two Rhacophoridae species (Bos and metamorphic stage (tadpoles) inhabiting aqueous environ- Waldman 2006;Zhaoetal.2013). Whilst some model ments and a post-metamorphic stage occupying terrestrial Pipidae and Ranidae species express a single classical MHC and/or aquatic habitats. A change in morphology and class I locus (Flajnik et al. 1999; Goyos et al. 2011;Ohtaetal. environment during the life cycle presents the potential 2006; Teacher et al. 2009), copy number variation was for differential exposure to different pathogens during de- revealed following research across more expansive families velopment. There are reports that certain pathogens may and additional Ranidae species (Kiemnec-Tyburczy et al. have stronger impact on either pre- (Chambouvet et al. 2012;Lillieetal.2014;Zhaoetal.2013). The aim of this 2015; Haislip et al. 2011) or post-metamorphic life stages study was to characterise MHC class I genes in three (Blaustein et al. 2005), supporting that developmental and Japanese frog species from the Rana genus. In addition, we environmental changes could influence amphibian host wanted to investigate whether selective mechanisms and gene immunity. Many amphibian diseases caused by patho- duplication have shaped MHC variation. This will contribute gens, including bacteria, viruses, fungi and parasites, have to further understanding about the evolution of amphibian been reported (summarised by Densmore and Green MHC class I. 2007); one of the most commonly documented amphibian infectious diseases in recent times is chytridiomycosis. Chytridiomycosis is a serious disease in amphibians caused Methods by the chytrid fungus Batrachochytridium dendrobatidis, which was identified by Berger et al (1998) and characterised Sample collection and nucleic acid isolation by Longcore et al (1999). Many studies have attributed chytridiomycosis, which causes epidermal disruption, to the We selected three Rana frog species that are commonly found decrease in amphibian populations around the world (Daszak across Japan: the Japanese brown frog (Rana japonica), the et al. 2003; Longcore et al. 2007; Skerratt et al. 2007). In montane brown frog (Rana ornativentris) and Tago’sbrown Japan, several strains of B. dendrobatidis were frog (Rana tagoi tagoi). For genetic material, adult individuals characterised as either non-native or apparently endemic (n = 7 per species) originating from separate locations within strains, although low incidence (4.1 %) was found in free- Hiroshima prefecture, Japan, were used: R. japonica raised in ranging amphibians (Goka et al. 2009). Some amphibian captivity and originating from multiple egg clusters collected species in Japan where the fungus was detected include from an island population in Etajima (34°16′14″N, 132°28′ exotic species from the pet trade and the naturalised 37″E); R. ornativentris raised in captivity from tadpoles col- Lithobates (Rana) catesbeianus, a key carrier species at- lected from Yoshiwa (34°25′04″N, 132°05′15″E); and R. t. tributed with the spread of this global disease (Garner tagoi from adult frogs collected from Shobara (34°05′04″N, et al. 2006). It has been suggested that B. dendrobatidis 132°49′43″E). Adult frogs were euthanized by immersion in is endemic to Asia (Goka et al. 2009; Bataille et al. tricaine methanesulfonate (MS222, 0.5–3 g/L water) and 2013), implying the coexistence between Japanese (or spleen was collected. Total RNA was extracted using Asian) amphibians and B. dendrobatidis for a long time, ISOGEN (Nippon Gene, Tokyo, Japan) following the manu- which may have allowed the amphibians to evolve an facturer’s protocol, and first-strand complementary DNA was effective resistance against chytrid infection. This could synthesised using PrimeScriptTM RT reagent kit (Takara Bio explain the tolerance of endemic amphibians to the fungi Inc., Otsu, Japan). and the resulting low incidence in Japan (or Asia). Therefore, initiating the examination of immune genes of MHC class I PCR Japanese amphibian species will contribute to further un- derstanding amphibian host–disease dynamics. Primers were designed to amplify partial coding sequence of Within the family Ranidae, MHC class I has been studied MHC class I, spanning from exons 1 to 4, based on tran- in L. catesbeianus (American bullfrog), Lithobates clamitans scriptome data (T. Igawa, unpublished data) from skin Immunogenetics samples of R. japonica as well as several Ranidae species et al. 2013). For phylogenetic analyses, neighbour-joining from southern Japanese islands: Odorrana narina, trees (p distance) were constructed from amino acid align- Odorrana amamiensis, Odorrana supranarina,
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