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(Herpetosoma) Rangeli (Kinetoplastida 1 Molecular Epidemiology of Trypanosoma (Herpetosoma) rangeli (Kinetoplastida: Trypanosomatidae) in Ecuador, South America, and Study of the Parasite Cell Invasion Mechanism in vitro A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Segundo Mauricio Lascano November 2009 © 2009 Segundo Mauricio Lascano. All Rights Reserved. 2 This dissertation titled Molecular Epidemiology of Trypanosoma (Herpetosoma) rangeli (Kinetoplastida: Trypanosomatidae) in Ecuador, South America, and Study of the Parasite Cell Invasion Mechanism in vitro by SEGUNDO MAURICIO LASCANO has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Mario J. Grijalva Associate Professor of Biomedical Sciences Benjamin M. Ogles Dean, College of Arts and Sciences 3 ABSTRACT LASCANO, SEGUNDO M., Ph.D., November 2009, Biological Sciences Molecular Epidemiology of Trypanosoma (Herpetosoma) rangeli (Kinetoplastida: Trypanosomatidae) in Ecuador, South America, and Study of the Parasite Cell Invasion Mechanism in vitro. (154 pp.) Director of Dissertation: Mario J. Grijalva Trypanosoma rangeli is a protozoan hemoflagellate able to infect insects of the subfamily Triatominae (Hemiptera: Reduviidae), mammals, and humans in the American continent. Although the human infection by T. rangeli is non-pathogenic, the importance of the study of this parasite resides in the fact that it shares the same vectors and mammal reservoirs with T. cruzi, the pathogenic parasite causative of Chagas disease. This situation commonly results in misdiagnosis of Chagas disease in patients living in areas where the two parasites overlap spatially and temporarily. The occurrence of T. rangeli in Ecuador had not been documented prior to this study and only sporadic reports of T. rangeli-like organisms had been published. This study was divided in two sections: the objective of the first was to establish the presence of T. rangeli in Ecuador and to carry out an investigation of the relationship of the parasite with its Triatominae vectors and mammal hosts in two regions of the country. Rhodnius ecuadoriensis, Panstrongylus howardi, and Triatoma carrioni were found naturally infected with T. rangeli. Mixed infections with T. rangeli and T. cruzi were also observed in those vectors. Analysis of host preferences for blood meal revealed that 4 the triatomines analyzed had fed on several species of mammals (common rat, mice, dog, cat, goat, guinea pig, human) and an avian species (chicken). The identification of the blood meal sources can contribute to the understanding of the epidemiology of T. cruzi and T. rangeli transmission cycles. The objective of the second part of the study was to investigate the mechanism that T. rangeli uses to invade mammalian cells. Immunofluorescence assays were used for this purpose. The Choachi strain of T. rangeli and BALB/c fibroblasts were chosen to evaluate the cell invasion process. T. rangeli invades cells primarily by a lysosome- dependent fashion similar to that of T. cruzi, although T. rangeli seems to lack the alternative lysosome-independent pathway that has been described for T. cruzi. Cells infected with T. rangeli did not show signs of intracellular division up to 288 hours post- infection and parasitemia in BALB/c mice was transient and declined rapidly overtime. Approved: _____________________________________________________________ Mario J. Grijalva Associate Professor of Biomedical Sciences 5 ACKNOWLEDGMENTS I am indebted to a number of people who helped me during the dissertation process. Without them, I could not have completed this project. I would like to acknowledge: My advisor, Dr. Mario Grijalva, who introduced me to the world of Chagas disease and trypanosomiasis, for his support, guidance, friendship, and patience, and also for encouraging and challenging me throughout my academic career. Dr. Edwin Rowland, for his continued academic support, technical advice, and guidance. The members of my dissertation committee: Dr. Calvin James and Dr. Sarah Wyatt, for their help, advice, and constructive criticism. Dr. Edmundo C. Grisard, for his valuable advice and support, and the kind donation of culture stocks of trypanosomes. Dr. Jaime Costales, for his friendship and technical advice. The technicians and students at the Center for Infectious Disease Research at Catholic University of Ecuador for their help during various stages of the process. Christian Stork, MSc, for his willingness to help and guide me through the process of getting acquainted with fluorescence and confocal microscopy. Dr. William Romoser, for his selfless support, advice, guidance, and sincere friendship. 6 Abbey Wojno, MA, for all her loyal support and understanding throughout the completion of this dissertation. The Graduate Student Senate and the Student Enhancement Award Program of Ohio University for the financial support provided to carry out different sections of this dissertation. 7 DEDICATION To my parents 8 TABLE OF CONTENTS Page Abstract ............................................................................................................................... 3 Acknowledgments............................................................................................................... 5 Dedication ........................................................................................................................... 7 List of Tables .................................................................................................................... 12 List of Figures ................................................................................................................... 13 List of Abbreviations ........................................................................................................ 15 Introduction ................................................................................................................... 16 Taxonomic position .................................................................................................. 17 Biology of Trypanosoma rangeli .............................................................................. 19 Vectors of T. rangeli ................................................................................................. 20 Reservoirs of T. rangeli ............................................................................................ 21 Life cycle in the vertebrate host ................................................................................ 22 Life cycle in the invertebrate host ............................................................................. 23 Pathogenicity to the insect vector ............................................................................. 27 Biochemistry and Molecular Biology ....................................................................... 30 Lysis by complement ................................................................................................ 31 Lectin discrimination of cell surface carbohydrates ................................................. 31 Neuraminidase production ........................................................................................ 33 Antigenic characterization ........................................................................................ 33 9 Isoenzyme analysis ................................................................................................... 34 DNA analysis ............................................................................................................ 36 Epidemiology ............................................................................................................ 39 Specific Aims ................................................................................................................ 41 Materials and Methods .................................................................................................. 43 Study areas ................................................................................................................ 43 Informed consent ...................................................................................................... 44 Insect collection ........................................................................................................ 44 Taxonomic identification and entomological indexes .............................................. 45 Insect samples collection .......................................................................................... 46 Blood source identification ....................................................................................... 49 Parasite controls ........................................................................................................ 52 Molecular characterization algorithm ....................................................................... 53 DNA sequencing for confirmation of parasite identity ............................................. 56 Cell culture maintenance ........................................................................................... 56 Parasite culture maintenance ..................................................................................... 57 DNA Polyacrylamide Gel Electrophoresis (PAGE) ................................................. 59 Polyclonal antibody production in mice ..................................................................
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