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Expression and Functional Sialome of Triatomines, Insect Vectors of Chagas Disease

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Expression and Functional Sialome of Triatomines, Insect Vectors of Chagas Disease University of Texas at El Paso ScholarWorks@UTEP Open Access Theses & Dissertations 2020-01-01 Expression And Functional Sialome Of Triatomines, Insect Vectors Of Chagas Disease Maria Tays Mendes University of Texas at El Paso Follow this and additional works at: https://scholarworks.utep.edu/open_etd Part of the Allergy and Immunology Commons, Medical Immunology Commons, and the Parasitology Commons Recommended Citation Mendes, Maria Tays, "Expression And Functional Sialome Of Triatomines, Insect Vectors Of Chagas Disease" (2020). Open Access Theses & Dissertations. 3005. https://scholarworks.utep.edu/open_etd/3005 This is brought to you for free and open access by ScholarWorks@UTEP. It has been accepted for inclusion in Open Access Theses & Dissertations by an authorized administrator of ScholarWorks@UTEP. For more information, please contact [email protected]. EXPRESSION AND FUNCTIONAL SIALOME OF TRIATOMINES, INSECT VECTORS OF CHAGAS DISEASE MARIA TAYS MENDES Doctoral Program in Bioscience APPROVED: Igor C. Almeida, D.Sc., Chair Douglas Watts, Ph.D. Katja Michael, Ph.D. __________________________________________ Siddhartha Das, Ph.D. __________________________________________ Rosa A. Maldonado, D.Sc., Advocate Stephen L. Crites, Jr., Ph.D. Dean of the Graduate School Copyright © by Maria Tays Mendes 2020 Dedication To my family, especially to my husband, Leandro, my kids Luis and Emily, and to my grandmother (in memoriam). Before I left my country to start this journey, my grandmother gave me some money, which I refused at first because I knew it would be more useful for her. She made me accept it anyways, and told me it would mean a lot to her because once I reached the end, she could tell everyone that she helped me get there. Unfortunately, she passed away a year before that. Thank you “vó Quinquinha”, I dedicate this work to you. I will love you forever. EXPRESSION AND FUNCTIONAL SIALOME OF TRIATOMINES, INSECT VECTORS OF CHAGAS DISEASE by MARIA TAYS MENDES, M.Sc. DISSERTATION Presented to the Faculty of the Graduate School of The University of Texas at El Paso in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Department of Biological Sciences THE UNIVERSITY OF TEXAS AT EL PASO May 2020 Acknowledgements My sincere thanks: To my mentor Dr. Igor Almeida for giving me the opportunity to be part of his group and for all the support he has given to me so far. To my committee members Dr. Siddhartha Das, Dr. Katja Michael, and Dr. Douglas Watts for their support and insights into my project. To my advocate Dr. Rosa Maldonado for her encouragement and kind words. To all the present and past Almeida’s lab members, faculty, staff and core facilities for their assistance along the years. Specially thanks to Nasim Karimi, Susana Portillo, Brian Grajeda, Igor Estevao, Cameron Ellis, Uriel Ortega, Nuria Cortes, Brenda Zepeda, Gloria Polanco, Ramon Brito, and Emanuella Fajardo. To all the professors of the Department of Biological Sciences for all the teachings and experiences transmitted. To colleagues and former colleagues of the Graduate School for their excellent coexistence, for their help during the disciplines, for the moments of relaxation, for the scientific discussions and exchange of experiences. Special thanks to those who helped me to correct this dissertation. To my former advisor Dr. Carlo José Freire de Oliveira for the trust placed in me and for the help not only in my scientific development but also in my personal growth. To the collaborations made so far: Dr. Carlo José Freire de Oliveira and his lab members for providing the saliva samples; Dr. José Marcos Ribeiro for sharing the P. herreri database; Dr. Luis Fabiano Oliveira, for the BLAST analysis; Dr. Laura-Isobel for the metabolomic analysis; Dr. Alan Carneiro for teaching me the Toll-like receptors assays; Dr. Douglas Watts, Dr. Belkisyolé Alarcón De Noya, Dr. Oscar Noya, Dr. Iliana R. Malo, Dr. Janine M. Ramsey, Dr. Léa v S. Soussumi, Dr. Faustino Torrico, Dr. Maria Paola Zago, Dr. Julio Alonso-Padilla, Dr. Luis Izquierdo, Dr. Maria-Jesus Pinazo, Dr. Joaquim Gascon for providing the human sera pools from Chagas disease patients (ChHSP) and normal human sera pool (NHSP). To my dear friends Sol (Soraia), Monica, and Luciene for the great moments lived together. Additionally, to my friends in Brazil Tamires, Marcos, Monique, and Lara for the comfort given by the long Skype talks. Thank you for allowing me to be a part of your lives. To all my family members for their encouragement and understanding. In particular, to my parents, Terezinha and João Pedro, for always supporting and believing in me. To my husband, Leandro and my kids, Luis Felipe and Emily for their patience and love. To my parents-in-law, Susana and Edson, and my sister-in-law Thamyres for making this journey happier. To my whole family in Brazil who despite the distance did not stop supporting me. To the funding agencies, the Science Without Borders program by the Coordination for the Improvement of Higher Education Personnel (CAPES), Brazil, the Border Biomedical Research Center (BBRC), and the National Institutes of Health (NIH). To everyone who directly or indirectly helped in the execution of this work. Finally, to God, for the gift of life and the opportunities offered. vi Abstract Triatomines are blood-sucking arthropods that transmit Trypanosoma cruzi, the etiologic agent of Chagas disease (ChD). Triatomines use bioactive molecules in the saliva for successful blood feeding and to evade the hemostatic and immune defense system of the hosts. Knowing the saliva composition could be useful for a better understanding which and how insect-derived molecules might influence host-parasite interactions. Previous studies have shown that some saliva-derived proteins and lipids can modulate the host immune system and increase T. cruzi infection. We hypothesize that the triatomine saliva contains a great diversity of lipids and proteins that can modulate the mammalian host immune response favoring blood-feeding and pathogen transmission. Moreover, these molecules could be used as biomarker of vector bite. Thus, the main purpose of this work is to conduct an omics (proteomic, lipidomic, and metabolomic) analysis on the saliva of different species of triatomines and identify these potential molecules. To address our hypothesis, we first identified the proteins, lipids, and metabolites (Specific Aim 1), and then tested the immunoreactivity against sera of negative or positive ChD patients (Specific Aim 2). Saliva of two species from North America, Meccus pallidipennis and Triatoma lecticularia, and two from South America, Panstrongylus herreri and Rhodnius prolixus, were obtained by dissection of the triatomine salivary glands. The proteins were digested using a Filter-Aided Sample Prep (FASP) kit. Extracellular vesicles (EVs) were recovered in the triatomine saliva after ultrafiltration. The lipids and metabolites were extracted by Folch’s partition. Resulting peptides, lipids and metabolites were analyzed by high-resolution liquid chromatography-tandem mass spectrometry (HR-LC-MS/MS) in a QE-Plus Orbitrap mass spectrometer. Immunoreactivity against sera of negative or positive ChD patients was screened by chemiluminescent enzyme-linked immunosorbent assay (CL-ELISA). Significant qualitative and quantitative differences were vii observed at protein, lipid, and metabolite levels between the four-triatomine species. No clustering regarding geographical origin was noticed; however, considerable differences were observed regarding the tribes of the four triatomine species analyzed. The most abundant proteins in triatomine saliva belong to the lipocalin group. EVs were found for the first time in the triatomine saliva. Different immunoreactivity against salivary antigens with ChD sera from different countries was found. Eighteen lipid classes were identified in the triatomine saliva, including the lyso-phosphatidylcholine (LPC)-C16:0 previously described. Arachidonic acid (C20:4), the precursor of prostaglandins, and some purines such as adenosine, were also detected. In conclusion, our findings will further our understanding of potential effects of triatomine saliva in the establishment and long-term maintenance of T. cruzi infection within the mammalian host. Keywords: Triatomines; Saliva; Proteomics; Lipidomics; Metabolomics, Chagas Disease. viii Table of contents Acknowledgements ..........................................................................................................................v Abstract ......................................................................................................................................... vii Table of contents ............................................................................................................................ ix List of tables ................................................................................................................................... xi List of figures ................................................................................................................................ xii Chapter 1: General introduction.......................................................................................................1 1.1 Chagas disease and Trypanosoma cruzi ........................................................................1 1.2 Triatomines ....................................................................................................................3 1.3
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