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Faculdade De Medicina Veterinária UNIVERSIDADE DE LISBOA Faculdade de Medicina Veterinária BESNOITIA BESNOITI AND TOXOPLASMA GONDII INVASION: THE ROLE OF THE PARASITE´S TUBULIN FOLDING PATHWAY AND MANIPULATION OF HOST CELL ORGANIZATION Rita Isabel de Amorim Cardoso CONSTITUIÇÃO DO JÚRI ORIENTADOR Doutor Andrew Edward Hemphill Doutor José Alexandre da Costa Doutora Isabel Maria Soares Pereira da Fonseca de Perdigão e Cameira Leitão Sampaio Doutora Maria Helena Antunes Soares CO-ORIENTADORA Doutor José Augusto Farraia e Silva Meireles Doutora Maria Helena Antunes Soares Doutor Helder Carola Espiguinha Cortes Doutor José Alexandre da Costa Perdigão e Cameira Leitão 2014 LISBOA UNIVERSIDADE DE LISBOA Faculdade de Medicina Veterinária BESNOITIA BESNOITI AND TOXOPLASMA GONDII INVASION: THE ROLE OF THE PARASITE´S TUBULIN FOLDING PATHWAY AND MANIPULATION OF HOST CELL ORGANIZATION Rita Isabel de Amorim Cardoso TESE DE DOUTORAMENTO EM CIÊNCIAS VETERINÁRIAS ESPECIALIDADE DE CIÊNCIAS BIOLÓGICAS E BIOMÉDICAS CONSTITUIÇÃO DO JÚRI ORIENTADOR Doutor Andrew Edward Hemphill Doutor José Alexandre da Costa Doutora Isabel Maria Soares Pereira da Fonseca de Perdigão e Cameira Leitão Sampaio Doutora Maria Helena Antunes Soares CO-ORIENTADORA Doutor José Augusto Farraia e Silva Meireles Doutora Maria Helena Antunes Soares Doutor Helder Carola Espiguinha Cortes Doutor José Alexandre da Costa Perdigão e Cameira Leitão 2014 LISBOA Acknowledgments I would like to thank my supervisor, Alexandre Leitão, for helping me to overcome all the challenges presented to me during the course of this work, from little to fundamental things you have always supported me, and I am truly thankful. Working with you brought me a great amount of knowledge, and important new perspectives, and I sincerely hope to be able to continue having your support and advice. I cannot end without recognizing your infinite patience when dealing with me and my (sometimes) ‘idiosyncratic behavior’. I would also like to thank my co-supervisor, Helena Soares, for all the support and scientific knowledge, and for always being prepared with new ideas to new problems, which helped me to circumvent many obstacles. My special thanks to Helder Cortes, for believing in me, in my work, and for being a good friend. Thank you also for all the knowledge about B. besnoiti. Thank you, my colleagues and friends at the bench: Afonso Basto, Alexandra Tavares, Dulce Santos, Eduardo Marcelino, Joana Morais, João Gonçalves, Rúben Ramalho, Rodrigo Cunha, Samuel Francisco, Sara Zúquete and Sofia Nolasco. All of you taught me how to work around the lab, helped me when I needed, and were always available for a conversation. You were able to turn serious work into laughing moments (particularly you, Sara and Samuel). I would like to give special thanks to Sofia Nolasco, for the help and knowledge about cell culture and immunofluorescence. I am thankful to Silvia Almeida, for the knowledge and help on real time PCR. To Helga Waap, for being a good colleague and friend, and for defying me to work on other projects. I would like to thank Doutor Carlos Novo, for the INETI facilities where the anti B. besnoiti CCTα antibody was produced, and for the provided help when producing it. I would also like to thank Professor Doutor Carlos Martins for letting me use the infectious diseases facilities. i A special thank you to Professora Doutora Conceição Peleteiro for allowing me to use the pathological anatomy facilities, and to D. Maria Augusta, D. Rosário, Sandra Carvalho, and Rute Noiva, for their friendly support. I am also thankful to Faculdade de Medicina Veterinária de Lisboa (FMV) and Centro de Investigação Interdisciplinar em Sanidade Animal (CIISA), in the persons of Professor Doutor Luís Tavares and Professor Doutor Luís Costa, for all the support since I have initiated my work. Thank you, my close friends, Aldina Almeida, Maria Matos, and Susana Cruz. I truly think you believe more in my success than I do. Thank you for that. I would also like to thanks Maria Matos for the help in editing the images. Finally, my family that has always supported and provided me in many ways. A special word to my mother, for her generosity, and for making it easier for me to choose my own path. ii Financial Support This study was supported by: FCT - Fundação para a Ciência e Tecnologia (FCT), through the fellowship SFRH/BD/38122/2007 and project grants PTDC/CVT/71630/2006; PTDC/CVT/105470/2008. Centro de Investigação Interdisciplinar em Sanidade Animal (CIISA), Faculdade de Medicina Veterinária de Lisboa, Universidade de Lisboa (FMV-UL). iii Besnoitia besnoiti and Toxoplasma gondii invasion: the role of the parasite´s tubulin folding pathway and manipulation of host cell organization Abstract Besnoitia besnoiti and Toxoplasma gondii, the etiological agents of besnoitiosis and toxoplasmosis, respectively, are two apicomplexan parasites unable to replicate outside the host cell. In order to survive inside the host cell, these parasites have developed strategies to subvert the cytoskeleton and the endomembrane system of the host cell. In this work, the strategies used by B. besnoiti and T. gondii to manipulate the cytoskeleton, remodeling microtubules (MTs), and interfering with the centrosome and Golgi apparatus of the host cell are studied. We observed that the parasitophorous vacuole (PV) of both parasites is surrounded by host MTs, but only T. gondii recruits the host cell centrosome towards the PV. However, the host Golgi apparatus is recruited to the PV by both parasites but its organization is affected in different ways. The differences found between these two parasites are most likely a result of two distinct evolutionary mechanisms and might reflect the different tissue tropism and pathogeny. Since not only the host cell cytoskeleton, but also the cytoskeleton of the parasite, participate in the establishment of infection, this work also addresses the role of the parasite cytoskeleton during entry and development inside the host cell. For this we propose that components of the tubulin folding pathway are good candidates to regulate cytoskeleton dynamics and reorganization during host invasion. Thus, we started the characterization of the gene structure and expression patterns of the components of tubulin folding pathway (CCTα, TBCB, TBCE and α-tubulin). These studies suggest that these proteins have an important role in parasite replication. Overall, our results contribute to the present knowledge of the mechanisms underlying host cell invasion by these parasites, which might be important for the definition of future therapeutic strategies. Keywords: Besnoitia besnoiti, Toxoplasma gondii, microtubule cytoskeleleton, Golgi apparatus, centrosome, tubulin folding pathway. iv Estudo da invasão por Besnoitia besnoiti e Toxoplasma gondii: papel de componentes da via de aquisição da estrutura tridimensional nativa da tubulina do parasita e manipulação da organização da célula hospedeira Resumo Besnoitia besnoiti e Toxoplasma gondii, agentes etiológicos da besnoitiose e toxoplasmose, respetivamente, são dois parasitas do filo Apicomplexa incapazes de se replicarem fora da célula hospedeira. De forma a sobreviver dentro da célula hospedeira estes parasitas desenvolveram estratégias para subverter o citoesqueleto e sistema endomembranar da célula. Neste trabalho são estudadas as estratégias utilizadas por B. besnoiti e T. gondii para manipular o citoesqueleto, remodelar microtúbulos (MTs), e interferir com o centrossoma e o aparelho de Golgi da célula hospedeira. Observámos que o vacúolo parasitóforo (VP) dos dois parasitas está rodeado de MTs da célula hospedeira, mas apenas T.gondii desloca o centrossoma para o VP. No entanto, o aparelho de Golgi é recrutado para próximo do VP por ambos os parasitas, sendo a sua organização afetada de forma diferente. As diferenças encontradas entre os dois parasitas são provavelmente o resultado de evoluções diferentes, podendo isto refletir o seu diferente tropismo e patogenicidade. Visto que para além do citoesqueleto da célula hospedeira, também o citoesqueleto do parasita participa no desenvolvimento da infeção, este trabalho também se destina a estudar o papel do citoesqueleto do parasita durante a entrada e multiplicação dentro da célula hospedeira. Desta forma propomos que os componentes da via de aquisição da estrutura tridimensional nativa da tubulina são bons candidatos para regular a dinâmica e reorganização do citoesqueleto durante a invasão. Assim, caracterizámos a estrutura dos genes CCTα, cofator B, cofator E e α-tubulina, e o seu padrão de expressão, obtendo dados que sugerem que estas proteínas poderão ter um importante papel na replicação do parasita. Globalmente, os nossos resultados contribuem para o conhecimento dos mecanismos subjacentes à invasão da célula hospedeira por estes parasitas, o que poderá ser importante no futuro para a definição de estratégias terapêuticas. Palavras chave: Besnoitia besnoiti, Toxoplasma gondii, citoesqueleto de microtúbulos, aparelho de Golgi, centrossoma, via de aquisição da estrutura tridimensional nativa da tubulina. v Table of Contents Chapter 1: Introduction ............................................................................................................... 1 1.1 - Bovine besnoitiosis ........................................................................................................ 3 1.1.1 History ........................................................................................................................ 3 1.1.2 - The genus Besnoitia ................................................................................................
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