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The Role of the Efflux Mechanisms in Multidrug Resistance In Universidade Nova de Lisboa Instituto de Higiene e Medicina Tropical The role of the efflux mechanisms in multidrug resistance in Mycobacterium tuberculosis Liliana Isabel Dias Rodrigues 2010 Universidade Nova de Lisboa Instituto de Higiene e Medicina Tropical The role of the efflux mechanisms in multidrug resistance in Mycobacterium tuberculosis Liliana Isabel Dias Rodrigues 2010 Thesis research submitted to Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa in partial fulfilment of the requirements for the granting of the degree of Doctor in Philosophy with specialization in the Biomedical science of Microbiology. The thesis research to be described was conducted at Unidade de Micobactérias at Instituto de Higiene e Medicina Tropical and supported by grant SFRH/BD/24931/2005 provided by Fundação para a Ciência e Tecnologia (FCT) of Portugal. Supervisor: Miguel Viveiros Bettencourt Tutorial Comission: Miguel Viveiros Bettencourt Leonard Amaral Filomena Pereira Na presente dissertação incluem-se resultados que foram ou estão a ser alvo de publicação em co-autoria. Os artigos publicados ou submetidos para publicação serão integralmente apresentados em anexo. Para efeitos do disposto no nº 1 do Despacho nº2303/2000 do regulamento de Programas de Doutoramento do Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa (Diário da República, 2ª série, nº 23, de 28 de Janeiro de 2000), o autor desta dissertação declara que interveio na concepção e execução do trabalho experimental, na interpretação dos resultados e na redacção dos manuscritos publicados, submetidos ou que aguardam submissão. Lisboa, Junho de 2010 ___________________________________ Liliana Isabel Dias Rodrigues To my parents ''Rich countries thought TB was a disease of the past ... a problem of the poorest. But it kills twice as many people as malaria and almost as many as AIDS. If you think this doesn't affect you, you are dead wrong'' Mario Raviglione Acknowledgments This PhD thesis wouldn't be possible without the help and support of several people. I would like to thank the ones that directly or indirectly have contributed for this work: Prof. Dr. Miguel Viveiros, my supervisor, thank you for giving me the opportunity to learn so much about efflux pumps and mycobacterial resistance and for teaching me how to become a scientist. Thank you for the orientation, incentive, dedication and friendship of the last five years. Prof. Dr. Leonard Amaral for his constant dedication to Science that inspire us to continue with our work and for pushing us to "think outside of the box", which allows us to grow up as scientists. Prof. Drª Isabel Couto for her friendship, support and "brainstorm" suggestions that have greatly improved this work and careful revisions of our papers and posters. Prof. Drª Filomena Pereira for accepting to be part of my tutorial comission and for her support and interest in my work and careful revisions of my reports. My colleagues of Unidade de Micobacterias, Marta Martins, Gabriella Spengler, Ana Martins, Sofia Costa, Diana Machado, Jorge Ramos, Susana Costa, Pedro Cerca, and Samuel Francisco thank you for your friendship and companionship. All the former Master's students at the Unidade de Micobacterias, Marta Costa, Ana Tavares, Maria João Caetano, Celeste Falcão, Ana Cardoso, Daniela Sampaio, Nadia Charepe, Laura Paixão, thank you all for your friendship and support. A special thank you to Daniela Sampaio and Laura Paixão, with whom I had the pleasure to work with, for their precious help that strongly contributed to the progress of this thesis. The members of Unidade de Virologia, Aida Esteves, João Piedade, Ricardo Parreira, Teresa Venenno, Sandra Videira e Castro, Cristina Branco, Ferdinando Freitas, and Unidade de Doenças Sexualmente Transmissiveis, Rita Castro and Emília Prieto, of the IHMT for their friendship and support. A special thank you to our present and former technicians Dª Fernanda, Dª Mariana, Dª Rosário, Dª Cidália, Dª Josefina for their precious help and support. Prof. Dr. Gabriel Monteiro, Prof. Dr. Pedro Fernandes and Drª Carla Carvalho, our colleagues of the Instituto Superior Técnico (IST), for helping us develop the ethidium bromide transport mathematical model described in Chapter III of this thesis. Dr. Filipe Sansonetty from Instituto de Patologia e Imunologia Molecular, Universidade do Porto (IPATIMUP), for helping us design our flow cytometry experiments used in the work described in Chapter III of this thesis. Prof. Dr. Winfried V. Kern, from the Centre of Infectious Diseases and Travel Medicine, Department of Medicine, University Hospital, Freiburg, Germany, for giving me the opportunity to do a training period of six weeks in his laboratory at the start of my PhD thesis, which has greatly improved my knowledge of the use of fluorometric techniques to detect efflux activity. The Freiburg team, in particular Dirk Wagner, Martina Vavra, Eva Fähnrich and Sabine Schuster for the warm welcome to their laboratory and for all their help and support during my stay there. Prof. Dr. Jean-Marie Pagès from UMR-MD-1, Transporteurs Membranaires, Chimiorésistance et Drug Design, Facultés de Médecine et de Pharmacie, Université de la Méditerranée, Marseille, France for helping us understand a little more about the mechanisms behind cellular permeability and how it correlates with efflux and for his valuable contribution for our studies, namely the work presented in chapter II of this thesis. Prof. Dr. Hiroshi Nikaido from Department of Molecular and Cell Biology, University of California, Berkeley, U.S.A., for kindly providing us the M. smegmatis mutant strains XZL1675 and XZL1720 used in Chapter IV of this thesis. Prof. Dr. Michael Niederweis from Department of Microbiology, University of Alabama at Birmingham, U.S.A. for kindly providing us the M. smegmatis strains mutants SMR5, MN01 and ML10 also used in Chapter IV of this thesis. Our international collaborators that integrate the COST Action BM0701 "Antibiotic Transport and Efflux: New Strategies to combat bacterial resistance" for their dedication to the study of efflux pumps and membrane transporters and incentive of younger scientists to pursue research in this area. My family, especially my parents, for their love and patience and for always believing in me. I thank you all and wish you the best for your life. ____________________________________________________________ Abstract The emergence of multi and extensively drug resistant tuberculosis (MDRTB and XDRTB) has increased the concern of public health authorities around the world. The World Health Organization has defined MDRTB as tuberculosis (TB) caused by organisms resistant to at least isoniazid and rifampicin, the main first-line drugs used in TB therapy, whereas XDRTB refers to TB resistant not only to isoniazid and rifampicin, but also to a fluoroquinolone and to at least one of the three injectable second-line drugs, kanamycin, amikacin and capreomycin. Resistance in Mycobacterium tuberculosis is mainly due to the occurrence of spontaneous mutations and followed by selection of mutants by subsequent treatment. However, some resistant clinical isolates do not present mutations in any genes associated with resistance to a given antibiotic, which suggests that other mechanism(s) are involved in the development of drug resistance, namely the presence of efflux pump systems that extrude the drug to the exterior of the cell, preventing access to its target. Increased efflux activity can occur in response to prolonged exposure to subinhibitory concentrations of anti-TB drugs, a situation that may result from inadequate TB therapy. The inhibition of efflux activity with a non-antibiotic inhibitor may restore activity of an antibiotic subject to efflux and thus provide a way to enhance the activity of current anti-TB drugs. The work described in this thesis foccus on the study of efflux mechanisms in the development of multidrug resistance in M. tuberculosis and how phenotypic resistance, mediated by efflux pumps, correlates with genetic resistance. In order to accomplish this goal, several experimental protocols were developed using biological models such as Escherichia coli , the fast growing mycobacteria Mycobacterium smegmatis , and Mycobacterium avium , before their application to M. tuberculosis . This approach allowed the study of the mechanisms that result in the physiological adaptation of E. coli to subinhibitory concentrations of tetracycline (Chapter II), the development of a fluorometric method that allows the detection and quantification of efflux of ethidium ____________________________________________________________ xiv ____________________________________________________________ bromide (Chapter III), the characterization of the ethidium bromide transport in M. smegmatis (Chapter IV) and the contribution of efflux activity to macrolide resistance in Mycobacterium avium complex (Chapter V). Finally, the methods developed allowed the study of the role of efflux pumps in M. tuberculosis strains induced to isoniazid resistance (Chapter VI). By this manner, in Chapter II it was possible to observe that the physiological adaptation of E. coli to tetracycline results from an interplay between events at the genetic level and protein folding that decrease permeability of the cell envelope and increase efflux pump activity. Furthermore, Chapter III describes the development of a semi-automated fluorometric method that allowed the correlation of this efflux activity with the
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