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Developmental Regulation of Strongyloides Stercoralis Infectious Third-Stage Larvae by Canonical Dauer Pathways

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Developmental Regulation of Strongyloides Stercoralis Infectious Third-Stage Larvae by Canonical Dauer Pathways University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations 2013 Developmental Regulation of Strongyloides Stercoralis infectious Third-Stage Larvae by Canonical Dauer Pathways Jonathan David Chaffee Stoltzfus University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Cell Biology Commons, Molecular Biology Commons, and the Parasitology Commons Recommended Citation Stoltzfus, Jonathan David Chaffee, "Developmental Regulation of Strongyloides Stercoralis infectious Third-Stage Larvae by Canonical Dauer Pathways" (2013). Publicly Accessible Penn Dissertations. 806. https://repository.upenn.edu/edissertations/806 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/806 For more information, please contact [email protected]. Developmental Regulation of Strongyloides Stercoralis infectious Third-Stage Larvae by Canonical Dauer Pathways Abstract Parasitic nematodes inflict a vast global disease burden in humans as well as animals and plants of agricultural importance; understanding how these worms infect their hosts has significant health and economic implications. In humans, soil-transmitted parasitic nematodes cause hookworm disease and strongyloidiasis, and vector-transmitted parasitic nematodes cause filariasis. The infectious form of the species causing these diseases is a developmentally arrested third-stage larva (L3i). Molecular mechanisms governing L3i developmental arrest and activation within a host have been poorly understood. An analogous developmentally arrested third-stage larva--the dauer larva--forms during stressful environmental conditions in the free-living nematode Caenorhabditis elegans and is controlled by four cellular signaling pathways. The "dauer hypothesis" posits that similar mechanisms regulate dauer and L3i development. The parasitic nematode Strongyloides stercoralis was used to test the dauer hypothesis because its life cycle includes both parasitic and free-living forms. To investigate the role of canonical dauer pathway homologs in regulating L3i arrest and activation, this study utilized transcriptome sequencing (RNAseq), transgenesis, and pharmacological studies. Transcripts encoding cyclic guanosine monophosphate (cGMP) pathway components were coordinately up-regulated in L3i. Application of membrane-permeable 8-bromo-cGMP resulted in activation of L3i and modulation of ligand transcripts in other pathways. In comparison to C. elegans, S. stercoralis has few genes encoding insulin/ IGF-1 -like signaling (IIS) ligands, several of which have transcripts modulated during L3i development. Application of the phosphatidylinositol-3 kinase inhibitor, LY294002, prevented L3i activation in host-like conditions. The S. stercoralis transcriptome includes seven homologs of the single C. elegans dauer transforming growth factor &beta (TGF&beta) ligand, three of which are only expressed in L3i. Although the C. elegans nuclear hormone receptor ligand delta7-dafachronic acid (DA) stimulates L3i activation, putative DA biosynthetic genes were not coordinately regulated in L3i development. These data demonstrate that S. stercoralis has homologs for nearly every component in the four canonical dauer pathways, that cGMP signaling may transduce host cues during L3i activation, and that IIS regulates L3i arrest and activation. However, dauer TGF&beta signaling appears to function in L3i arrest, an opposite role than in C. elegans, and endogenous DA regulation of L3i development remains largely unexplored. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Cell & Molecular Biology First Advisor James B. Lok Keywords Caenorhabditis elegans, dauer, L3i, RNAseq, Strongyloides stercoralis Subject Categories Cell Biology | Molecular Biology | Parasitology This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/806 DEVELOPMENTAL REGULATION OF STRONGYLOIDES STERCORALIS INFECTIOUS THIRD-STAGE LARVAE BY CANONICAL DAUER PATHWAYS Jonathan David Chaffee Stoltzfus A DISSERTATION in Cell and Molecular Biology Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2013 Supervisor of Dissertation Dissertation Committee _____________________ David Abraham, Ph.D. Professor of Microbiology and Immunology James B. Lok, Ph.D. Professor of Parasitology Robert M. Greenberg, Ph.D. Research Associate Professor Graduate Group Chairperson S. Todd Lamitina, Ph.D. _______________________ Assistant Professor of Physiology Daniel S. Kessler, Ph.D. David S. Roos, Ph.D. (Chair) Associate Professor of Cell and Developmental Biology E. Otis Kendall Professor of Biology DEVELOPMENTAL REGULATION OF STRONGYLOIDES STERCORALIS INFECTIOUS THIRD-STAGE LARVAE BY CANONICAL DAUER PATHWAYS COPYRIGHT 2013 Jonathan David Chaffee Stoltzfus This work is licensed under the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/ ACKNOWLEDGMENT As with any significant undertaking, this thesis would not have been possible without a great deal of encouragement. First, I have appreciated the generous support of my thesis committee, including David Abraham, Robert Greenberg, Todd Lamitina, and David Roos. Additionally, I would like to thank my friends and colleagues in the Cell and Molecular Biology Graduate Group for their camaraderie. To my dear friends Christie Helfer, Stacey Lehman, and Keeley Mui - thank you for always being willing to try a new restaurant, commiserate with my failed experiments, and share the experience of graduate school with me. You all really helped to make these four years enjoyable. A special "thank you" to my family for encouraging my exploration of the natural world and helping foster my sense of curiosity as to how things work. Your tolerance of my experiments, which often involved explosions, is truly unsurpassed. Likewise, to my many science professors throughout my undergraduate studies - thank you for teaching and challenging me to think critically and carefully about the world! I am additionally grateful for all the technical assistance, conversations about worms, and support from Tom Nolan and members of the Lok lab. The assistance of other friends and colleagues, particularly Sam Minot, has greatly facilitated this thesis project. I owe a debt of gratitude to two people in particular, without whom this thesis would never have been completed. To my thesis advisor Sparky Lok - thank you for your guidance and patience in teaching me the ways of the worms, for always being available to answer my questions, and for your willingness to let me explore all manner of scientific questions. To my partner Kristina Lewis - thank you for listening to my science banter for so many years, for your endless encouragement during the many dark days, and for allowing me to share this journey with you. Your support is sincerely appreciated. Last, but certainly not least, I wish to thank the worms and the research animals that hosted them. iii ABSTRACT DEVELOPMENTAL REGULATION OF STRONGYLOIDES STERCORALIS INFECTIOUS THIRD-STAGE LARVAE BY CANONICAL DAUER PATHWAYS Jonathan David Chaffee Stoltzfus James Barron Lok Parasitic nematodes inflict a vast global disease burden in humans as well as animals and plants of agricultural importance; understanding how these worms infect their hosts has significant health and economic implications. In humans, soil-transmitted parasitic nematodes cause hookworm disease and strongyloidiasis, and vector-transmitted parasitic nematodes cause filariasis. The infectious form of the species causing these diseases is a developmentally arrested third-stage larva (L3i). Molecular mechanisms governing L3i developmental arrest and activation within a host have been poorly understood. An analogous developmentally arrested third-stage larva—the dauer larva—forms during stressful environmental conditions in the free- living nematode Caenorhabditis elegans and is controlled by four cellular signaling pathways. The "dauer hypothesis" posits that similar mechanisms regulate dauer and L3i development. The parasitic nematode Strongyloides stercoralis was used to test the dauer hypothesis because its life cycle includes both parasitic and free-living forms. To investigate the role of canonical dauer pathway homologs in regulating L3i arrest and activation, this study utilized transcriptome sequencing (RNAseq), transgenesis, and pharmacological studies. Transcripts encoding cyclic guanosine monophosphate (cGMP) pathway components were coordinately up-regulated in L3i. Application of membrane-permeable 8-bromo-cGMP resulted in activation of L3i and modulation of ligand transcripts in other pathways. In comparison to C. elegans, S. stercoralis has few genes encoding insulin/IGF-1 -like signaling (IIS) ligands, several of which have transcripts modulated during L3i development. Application of the phosphatidylinositol-3 kinase inhibitor, LY294002, prevented L3i activation in host-like conditions. The S. stercoralis transcriptome includes seven homologs of the single C. elegans dauer transforming growth factor β (TGFβ) ligand, three of which are only expressed in L3i. Although the C. elegans nuclear hormone receptor ligand Δ7- dafachronic acid (DA) stimulates L3i activation, putative DA biosynthetic genes were not coordinately regulated in L3i
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