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Nuclear Receptors in Metazoan Lineages: the Cross-Talk Between Evolution and Endocrine Disruption

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Nuclear Receptors in Metazoan Lineages: the Cross-Talk Between Evolution and Endocrine Disruption Nuclear Receptors in Metazoan lineages: the cross -talk between Evolution and Endocrine Disruption Elza Sofia Silva Fonseca Tese de Doutoramento apresentada à Faculdade de Ciências da Universidade do Porto Biologia D 2020 Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption D Elza Sofia Silva Foseca Doutoramento em Biologia Departamento de Biologia 2020 Orientador Doutor Luís Filipe Costa Castro, Professor Auxiliar, Faculdade de Ciências da Universidade do Porto, Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR) Coorientador Professor Doutor Miguel Alberto Fernandes Machado e Santos, Professor Auxiliar, Faculdade de Ciências da Universidade do Porto Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR) FCUP i Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption This thesis was supported by FCT (ref: SFRH/BD/100262/2014), Norte2020 and FEDER (Coral – Sustainable Ocean Exploitation – Norte-01-0145-FEDER-000036 and EvoDis – Norte-01-0145-FEDER-031342). ii FCUP Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption The present thesis is organized into seven chapters. Chapter 1 consists of a general introduction, providing an overview on Metazoa definition, and a review on the current knowledge of evolution and function of nuclear receptors and their role in endocrine disruption processes. Chapters 2, 3, 4 and 6 correspond to several projects developed during the doctoral programme presented here as independent articles, listed below (three articles published in peer reviewed international journals and one article in final preparation for submission). Chapter 5 was adapted from an article published in a peer reviewed international journal (listed below), in which I executed the methodology regarding the structural and functional analyses of rotifer RXR and I contributed to the writing of the sections referring to these analyses (Material and Methods, Results and Discussion). Finally, Chapter 7 contains a general discussion, the main conclusions and the future challenges. I declare that I have totally or partially peformed the work included in this thesis, in close cooperation/co-authorships with supervisors and other researchers. I have total responsibiliy for the conception of Chapters 1, 5 and 7, with revisions from the supervising team. In the remaining chapters, I contributed significantly to the development of the research ideas, to produce and analyse the data presented and to the writing of all chapters. CHAPTER 2 Fonseca E*, Machado AM, Arrondo N, Gomes-dos-Santos A, Veríssimo A, Esteves P, Almeida T, Themudo G, Ruivo R, Román E, da Fonseca RR, Santos MM, Froufe E, Pérez M, Venkatesh B, Castro LFC. Chondrichthyes Offer Unique Insights into the Evolution of the Nuclear Receptor Gene Repertoire in Gnathostomes (In preparation). CHAPTER 3 Fonseca E*, Ruivo R*, Lopes-Marques M, Zhang H, Santos MM, Venkatesh B, Castro LF. 2017. LXRα and LXRβ Nuclear Receptors Evolved in the Common Ancestor of Gnathostomes.Genome Biol Evol. 9(1):222-230. doi: 10.1093/gbe/evw305. CHAPTER 4 Fonseca ESS*, Ruivo R, Machado AM, Conrado F, Tay BH, Venkatesh B, Santos MM, Castro LFC. 2019. Evolutionary Plasticity in Detoxification Gene Modules: The Preservation and Loss of the Pregnane X Receptor in Chondrichthyes Lineages. Int J Mol Sci. 20(9):E2331. doi: 10.3390/ijms20092331. CHAPTER 5 adapted from FCUP iii Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption Lee MC*, Fonseca E, Park JC, Yoon DS, Choi H, Kim M, Han J, Cho HS, Shin KH, Santos ML, Jung JH, Castro LFC, Lee JS. 2019. Tributyltin Affects Retinoid X Receptor-Mediated Lipid Metabolism in the Marine Rotifer Brachionus koreanus. Environ Sci Technol. 53(13):7830-7839. doi: 10.1021/acs.est.9b01359. CHAPTER 6 Fonseca ESS*, Hiromori Y*, Kaite Y, Ruivo R, Franco JN, Nakanishi T, Santos MM, Castro LFC. 2019. An Orthologue of the Retinoic Acid Receptor (RAR) Is Present in the Ecdysozoa Phylum Priapulida, Genes. 10(12):985. doi: 10.3390/genes10120985. *First author or joint first authors iv FCUP Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption Ao astro que me guiou, Ao anjo que me aconselhou, Ao lar que me acolheu. Não são os Lusíadas de Camões Tão pouco a Odisseia de Homero, Mas é parte da minha vida que vingou. Elza Fonseca “If I have the belief that I can do it, I shall surely acquire the capacity to do it even if I may not have it at the beginning.” Mahatma Gandhi FCUP v Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption Agradecimentos Em primeiro lugar, tenho a agradecer à Fundação para a Ciências e a Tecnologias (FCT), à Faculdade de Ciências da Universidade do Porto (FCUP) e ao Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR) pelo financiamento e disponivbilização de infraestruturas necessários para a realização deste trabalho. Em segundo lugar, agradeço ao meu orientador Doutor Filipe Castro e ao meu coorientador Doutor Miguel Santos pela receção e integração nas suas equipas, bem como, por todo apoio prestado desde a conceção de todos os trabalhos, ao apoio psicológico e emocional que foram imperativos para a conclusão deste meu percurso. Um especial agradecimento a Filipe Castro, mais do que o orientador da minha tese de doutoramento, foi um conselheiro e amigo que levarei para toda a vida como exemplo a nível profissional e pessoal. Não poderia deixar de agradecer a todos os meus colegas de laboratório pelo apoio dado tanto a nível da conceção e da execução dos trabalhos, como pelos bons momentos passados nas memoráveis pausas para almoço. Muitos tornaram-se amigos que nunca esquecerei, pois ficarão com um lugar especial no meu coração. Teresa Neuparth, Raquel Ruivo, Ana André, Ana Capitão, Joana Soares, Rita Mendes, Inês Páscoa, André Machado, Susana Barros, Mónica Lopes e Patrícia Ferreira, mais do que colegas de trabalho, são pessoas excecionais com as quais tive o privilégio de trabalhar e com as quais pude partilhar todas as minhas frustrações e desabafos. Um grande obrigada pela vossa, disponibilidade, paciência, amizade e por devolverem à humanidade alguns dos seus valores perdidos. Não poderia deixar de agradecer a todos os membros integrantes do CIIMAR. Convosco sinto-me em família. Por último, mas não menos importante, agradeço à minha família, pais, irmã e sobrinho, que estiveram sempre dispostos a ajudar-me a superar todas as dificuldades que foram surgindo. A todos um enorme obrigada e a vós tudo devo. vi FCUP Nuclear Receptors in Metazoan lineages: the cross-talk between Evolution and Endocrine Disruption Resumo A multicelularidade é uma caraterística definidora dos metazoários. Neste contexto, o sistema endócrino desempenha um papel essencial na comunicação célula a célula e, consequentemente, na homeostasia destes organismos. Assim, a evolução e diversificação dos sistemas endócrinos dos metazoários representam um tópico fundamental de investigação em biologia. O sistema endócrino opera como uma rede altamente regulada, na qual os recetores nucleares (RNs) constituem componentes críticos. Os RNs são a superfamília de fatores de transcrição intracelulares mais abundante nos genomas dos metazoários. Têm como principal função a regulação da expressão de genes a jusante, normalmente após ativação por ligação específica a um ligando, modulando múltiplos processos biológicos como por exemplo a reprodução e o desenvolvimento embrionário, no seu conjunto definindo o “anel de fisiologia dos RNs”. Nos últimos anos, tornou-se evidente que existem diferenças cruciais entre os repertórios genéticos de RNs de vertebrados e invertebrados. Essas diferenças derivam em parte de processos genómicos, tais como, a duplicação em tandem, a perda secundária de genes, mutações na região codificante ou reguladora, e duplicações do genoma (DG) que ocorreram em momentos específicos da evolução dos metazoários (ex.: transição invertebrados/vertebrados), contribuindo para a evolução e diversificação dos RNs. Adicionalmente, tem-se verificado uma plasticidade estrutural de RNs ortólogos na acomodação de ligandos. Além disso, tal como as hormonas e os metabolitos resultantes da dieta, os xenobióticos podem também interagir com os RNs, mimetizando ligandos naturais. Desse modo, este grupo alargado de compostos tem a capacidade de bloquear a ação dos RNs, ou promover ora ativação ora repressão da transcrição de genes. Como são conhecidos por causar desequilíbrios fisiológicos nos metazoários, estes compostos são chamados de disruptores endócrinos (DEs). Por conseguinte, a persistência de DEs e de poluentes emergentes no meio ambiente, especialmente em ecossistemas aquáticos, tornou-se num assunto de preocupação global. Assim, de forma a esclarecer os mecanismos de disrupção endócrina por DEs que atuam via RNs em linhagens de metazoários e para evitar efeitos adversos na saúde humana e na fauna selvagem, é necessário investigar a evolução e a função dos RNs em linhagens com importantes posições filogenéticas (ex.: invertebrados vs. vertebrados, lofotrocozoários vs. ecdisozoários). Neste contexto, os repertórios de genes de RNs, a sua caraterização funcional e exploração por DEs foram investigados em linhagens filogeneticamente informativas para determinar a história evolutiva dos RNs no sistema endócrino dos metazoários. FCUP vii Nuclear Receptors in Metazoan lineages: the cross-talk
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