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Phd Thesis AML Final Insights into the host-pathogen interactions: Lagovirus in leporids Ana Margarida Lima Lopes Doutoramento em Biodiversidade, Genética e Evolução Departamento de Biologia 2016 Orientadora Joana Abrantes, PhD, Auxiliary Researcher CIBIO/InBIO, Laboratório Associado, Universidade do Porto Coorientador Jacques Le Pendu, PhD, DSc Institut de Recherche en Santé de l’Université de Nantes ii FCUP Insights into the host-pathogen interactions: Lagovirus in leporids FCUP iii Insights into the host-pathogen interactions: Lagovirus in leporids It would be possible to describe everything scientifically, but it would make no sense. It would be a description without meaning, as if you described a Beethoven symphony as a variation of wave pressure. Albert Eistein iv FCUP Insights into the host-pathogen interactions: Lagovirus in leporids FCUP v Insights into the host-pathogen interactions: Lagovirus in leporids Foreword In compliance with the no. 2 of article 4 of the General Regulation of Third Cycles of the University of Porto and with the article 31 of the Decree-Law no. 74/2006, of 24 March, with the alteration introduced by the Decree-Law no. 230/2009, of 14 September, the results of already published works were totally used and included in some of the chapters of this dissertation. As these works were performed in collaboration with other authors, the candidate clarifies that, in all these works, participated in obtaining, interpreting, analyzing and discussing the results, as well as in the writing of the published forms. This work was financially supported by Fundação para a Ciência e Tecnologia (FCT, Portugal) through the attribution of a PhD grant (ref.: SFRH/BD/78738/2011), and co- funded by Programa Operacional Potencial Humano (POPH) – Quadro de Referência Estratégico Nacional (QREN), financed by the European Union through the European Social Fund (ESF) and by the Portuguese government. vi FCUP Insights into the host-pathogen interactions: Lagovirus in leporids FCUP vii Insights into the host-pathogen interactions: Lagovirus in leporids Acknowledgments / Agradecimentos The work presented in this dissertation is the result of the efforts of so many people and institutions. Here I present my sincere thanks to all of them. À minha orientadora, Doutora Joana Abrantes, agradeço todo o apoio ao longo destes últimos quatro anos. Obrigada pela disponibilidade, pelo trabalho e pela dedicação a esta tese. Obrigada também por me teres mostrado Nantes e por me teres sempre acompanhado nessas estadias. São muitos os momentos que passámos juntas e que não esquecerei. To my co-supervisor, Dr. Jacques Le Pendu, I owe a special acknowledgement for accepting me as his student and for receiving me in his team in Nantes. Working there was undoubtedly a very fruitful experience and I thank you for sharing your vast experience in the glycobiology field with people that come from a totally different area of knowledge. Your encouraging ideas always kept me entusiastic after every failure. Ao Doutor Pedro J. Esteves, agradeço antes de mais ter-me acolhido no seu grupo de trabalho durante o meu estágio, pois sem essa oportunidade provavelmente o caminho trilhado seria outro. Obrigada por acreditares e me fazeres acreditar nas minhas capacidades para conduzir esta tese e pela abertura com que sempre nos ouves. Agradeço à Comissão Coordenadora e Científica do Programa Doutoral em Biodiversidade, Genética e Evolução, nas pessoas do Professor Doutor Nuno Ferrand de Almeida, do Professor Doutor Paulo Alexandrino (em memória) e do Professor Doutor Paulo Célio Alves, por me terem aceitado no Programa Doutoral e pela ajuda na resolução de questões burocráticas na Faculdade. Ao Professor Paulo Célio agradeço ainda ter-me “apresentado” o CIBIO e a cedência de amostras. À Fundação para a Ciência e Tecnologia agradeço a concessão da bolsa de doutoramento (ref.: SFRH/BD/78738/2011) e a atribuição de projetos de investigação (PTDC/CVT/108490/2008 e FCT-ANR/BIA-BIC/0043/2012) que permitiram subsidiar o trabalho desenvolvido no âmbito desta tese. viii FCUP Insights into the host-pathogen interactions: Lagovirus in leporids To Dr. Dolores Gavier-Widén and Dr. Ghislaine Le Gall-Reculé, for their kindness in providing us valuable samples to conduct our work and for their simplicity and loveliness. To Dr. Francisco Parra and Dr. Kevin P. Dalton for the Iberian collaboration and for sharing samples. To Dr. Edward C. Holmes for the huge knowledge that he brought to our work; his thorough revisions of our manuscripts greatly improved them. Uma palavra de agradecimento ao CTM, pela disponibilidade das instalações para a realização do trabalho laboratorial necessário à elaboração desta tese, e ao CIBIO, por me acolher também. Um obrigada especial ao pessoal do CIBIO, por sempre nos ajudarem com as questões burocráticas, e em especial ao Sr. Bernardino, pela sua dedicação ao centro e aos que aqui trabalham. Je remercie à tous les personnes qui ont fait part de ma vie quand j’étais à Nantes. À mes collegues du labo: Mónica, Jézabel, Béatrice, Adrien, Allan et Laure. Je suis reconnaissante pour toute l’aide scientifique, les discussions animées, les petits- déjeuners au labo, etc. Un remerciement spécial aussi à Nathalie et sa fille Camille, pour me faire visiter un peu la région et pour me recevoir chez vous. To Sarah and Dan, thank you for sharing with me your time in Nantes, even for such short periods, unfortunately. À mes amies “latin-speakers” Marianna, Maria et Georgia. Le français était la raison pour laquelle je vous ai connu et grâce à ça j’ai fait des merveilleuses amies: merci pour tous les bons moments que nous avons passé ensemble! Agradeço de um modo muito especial a todos os colegas e amigos do CIBIO. Ao pessoal que partilhou espaço comigo (primeiro a “favela” e depois o “aquário”) e que, pelas parvoíces de alguns momentos, traz alegria ao trabalho. Assim vale a pena ir trabalhar! Aos companheiros das longas viagens de metro, que mais tarde foram substituídas pelas mui divertidas viagens de carro, especialmente à Soraia, ao Gui e à Fabiana, um obrigada. Obrigada Soraia pela ajuda nas figuras. Às “imídias”, pela imprescindível ajuda em momentos de aperto no trabalho, pelo companheirismo, pela amizade e pela dinâmica de um tão agradável grupo de trabalho. Aos amigos de sempre e aos mais recentes: Berta, Mariana, Daniel, Soni, Luís, Nandita, Raquel… O vosso contributo para este trabalho é maior do que possam imaginar! Porque uma chamada telefónica, uma mensagem, uma conversa, uma jantarada, fazem milagres e trazem novo ânimo quando as saudades apertam e quando o trabalho ocupa a nossa cabeça mais do que devia. Obrigada também a todos os meus meninos pelos vossos sorrisos e pela vossa alegria: continuam a ser pequeninos aos meus olhos e, no entanto, estão tão crescidos. Eduardo, obrigada também por acederes ao meu pedido de ajuda tão em cima da hora! FCUP ix Insights into the host-pathogen interactions: Lagovirus in leporids Porque a família é uma bagagem que nos acompanha desde o início da viagem, não podia deixar de lhes agradecer. Obrigada especialmente aos meus pais, que lá aprenderam a usar o Skype para não me deixar sozinha, e pelo quanto me mimam quando estou em casa. São os valores que me transmitiram que hão-de ter feito de mim melhor pessoa, colega e trabalhadora. À minha família alargada agradeço também, especialmente às minhas primas e aos meus pequeninos que, com os seus abraços gigantes de gente pequenina, trouxeram alegria ao nosso mundo. Foi também graças a esta família que fomos numa aventura até à Covilhã para um incrível trabalho de campo. Obrigada, Conceição e Barata, por nos terem recebido tão gentilmente em vossa casa. Finalmente, obrigada Hugo!, por teres acompanhado toda esta jornada aguentando os momentos de ausência, por trazeres a calma do oceano nos teus olhos e por seres uma luz que fusque sempre que eu preciso de me rir. x FCUP Insights into the host-pathogen interactions: Lagovirus in leporids FCUP xi Insights into the host-pathogen interactions: Lagovirus in leporids Summary The family Leporidae belongs to the order Lagomorpha and has 11 extant genera distributed worldwide. In Europe, two genera naturally occur: Lepus , originating from North America, and Oryctolagus , whose place of origin is Iberian Peninsula. Oryctolagus has a single extant taxon, the European rabbit ( Oryctolagus cuniculus ) and Lepus has six taxa inhabiting Europe, the most widespread being the European brown hare ( Lepus europaeus ). O. cuniculus and L. europaeus populations suffered severe declines in Europe. Along with other factors, the viral diseases rabbit hemorrhagic disease (RHD), affecting European rabbits, and European brown hare syndrome (EBHS), affecting hares, are responsible for these declines. The causative agents of RHD and EBHS are the rabbit hemorrhagic disease virus (RHDV) and the European brown hare syndrome virus (EBHSV), respectively. RHDV and EBHSV are single-stranded, positive-sense RNA viruses with ~ 7.4 kb in length, classified as Lagovirus from the family Caliciviridae . For RHDV, several genogroups (G1- G6) were identified, as well as non-pathogenic forms. The information available for the Iberian Peninsula until 2011 indicated the circulation of G1 in wild populations. In 2010, outbreaks of RHD with unique features were recorded in France, and a new RHDV variant was identified. The emergence of this new RHDV variant, related to, but highly distinct from the genogroups previously identified, triggered the study of the new RHDV variant within the scope of the host-pathogen interactions of lagoviruses. The first cases of the new RHDV variant in Portugal mainland date back to late 2012 in the north and early 2013 in the south. Analysis of a partial fragment of the capsid protein gene revealed 99 % of nucleotide identity with a strain of the new variant previously identified in Spain. Phylogenetic analysis positioned the new variant in an independent cluster in between non-pathogenic rabbit caliciviruses.
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