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Immunology of the Gray Short-Tailed Opossum During Pregnancy and Prenatal Development Victoria L

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Immunology of the Gray Short-Tailed Opossum During Pregnancy and Prenatal Development Victoria L University of New Mexico UNM Digital Repository Biology ETDs Electronic Theses and Dissertations Spring 5-13-2017 Immunology of the gray short-tailed opossum during pregnancy and prenatal development Victoria L. Hansen University of New Mexico Follow this and additional works at: https://digitalrepository.unm.edu/biol_etds Part of the Bioinformatics Commons, Biology Commons, Evolution Commons, Immunology and Infectious Disease Commons, and the Laboratory and Basic Science Research Commons Recommended Citation Hansen, Victoria L.. "Immunology of the gray short-tailed opossum during pregnancy and prenatal development." (2017). https://digitalrepository.unm.edu/biol_etds/203 This Dissertation is brought to you for free and open access by the Electronic Theses and Dissertations at UNM Digital Repository. It has been accepted for inclusion in Biology ETDs by an authorized administrator of UNM Digital Repository. For more information, please contact [email protected]. Victoria L. Hansen Candidate Biology Department This dissertation is approved, and it is acceptable in quality and form for publication: Approved by the Dissertation Committee: Robert Miller , Chairperson Paul Samollow Stephen Stricker Christina Vesbach i IMMUNOLOGY OF THE GRAY SHORT-TAILED OPOSSUM DURING PREGNANCY AND PRENATAL DEVELOPMENT BY VICTORIA L. HANSEN B.A., Biology, University of Puget Sound, 2007 DISSERTATION Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Biology The University of New Mexico Albuquerque, New Mexico May, 2017 ii DEDICATION This dissertation is dedicated to my parents, Jeanne and Walt, who are unconditionally supportive and loving. Thank you, Mommy and Daddy. iii ACKNOWLEDGEMENTS Thank you to my mentor and PhD advisor, Dr. Rob Miller, and to my committee members Drs Paul Samollow, Stephen Stricker, and Christina Vesbach. Thank you to my “lab sisters” Bethaney Fehrenkamp and Katina Krasnec. Thank you to my excellent student mentees Murtada Alsaadi, Lauren Faber, Abbie Reade, and Ali Salehpoor. Thank you to my family of friends who kept me sane throughout graduate school: Amanda, Cain, Cale, Chris, Dominique, Jane, Jason, Jim, Jona, Kira, Melissa, and Rowan. iv IMMUNOLOGY OF THE GRAY SHORT-TAILED OPOSSUM MONODELPHIS DOMESTICA DURING PREGNANCY AND PRENATAL DEVELOPMENT by Victoria L. Hansen B.S., Biology, University of Puget Sound, 2007 PhD, Biology, University of New Mexico, 2017 ABSTRACT Vertebrate species that bear live young have overcome the evolutionary challenge of maintaining both a functional adaptive immune system and viviparous life cycle. In normal pregnancy, viviparous mothers are able sustain and nourish a fetus that is genetically half non-self without mounting an immunological attack. In 1953 Sir Peter Medawar brought attention to the “enigma of the fetal graft” and immunologists have been puzzling out the intricacies of fetal tolerance ever since. Although viviparity has evolved in all jawed vertebrate lineages aside from Aves, the vast majority of reproductive immunology research has been limited to eutherian mammals. There are insights to be gained by examining the reproductive immunology of other viviparous lineages. Marsupials, which share a common viviparous ancestor with eutherians, could be key in highlighting the most ancestral of mammalian characteristics. v The gray short-tailed opossum, Monodelphis domestica, is a model marsupial species with a sequenced and well-annotated genome. Transcriptomes of pregnant and non- pregnant M. domestica uterine tissues were assessed by Next Generation RNA-Seq techniques. Global gene transcription profiles were generated for opossum uterine tissue from pregnant and control animals. Using multiple differential expression algorithms thousands of genes were determined to be differentially transcribed. Notable was the contribution of immune related genes to those most differentially abundant among the transcripts. Of particular interest were genes coding for pro-inflammatory cytokines and complement components, both known to be regulated in eutherian pregnancy. To extend the RNA-Seq results further, quantitative real-time PCR was used to assess transcript abundance of a subset of cytokines and complement components. The results revealed that the spike of increased inflammation is associated with parturition in the opossum consistent with its ancient role in birth in mammals. In addition, complement components were suppressed in the data set throughout pregnancy, consistent with regulation of this immune mechanism being critical for sustaining normal pregnancy in marsupials as it is in eutherians. Overall, the results presented support active regulation of some immune mechanisms during marsupial pregnancy and provide a basis for understanding the evolution of parturition mechanisms. vi TABLE OF CONTENTS LIST OF FIGURES .......................................................................................................xi LIST OF TABLES .........................................................................................................xii CHAPTER 1: Introduction ...........................................................................................1 Introduction to this dissertation ...........................................................................2 The evolution of live birth in jawed vertebrates ..................................................3 Mammalian relationships .....................................................................................4 Evolution of viviparity in mammals ....................................................................4 Placentation in mammals .....................................................................................6 Reproductive immunology of eutherians .............................................................8 Reproductive immunology of marsupials ............................................................9 A primer on mammalian complement .................................................................10 Monodelphis domestica: a model marsupial ........................................................13 The aims of this dissertation ................................................................................15 References ............................................................................................................18 CHAPTER 2: On the prenatal initiation of T cell development in the opossum Monodelphis domestica ..................................................................................................23 Abstract ................................................................................................................24 Introduction ..........................................................................................................25 Methods................................................................................................................26 Tissue collection and fixation ..................................................................26 Immunohistochemistry ............................................................................26 vii Imaging and quantification ......................................................................27 Results ..................................................................................................................28 Discussion ............................................................................................................33 Acknowledgements ..............................................................................................36 Author contributions ............................................................................................37 References ............................................................................................................38 CHAPTER 3: Transcriptomic changes associated with pregnancy in a marsupial, the gray short-tailed opossum Monodelphis domestica .....................................................41 Abstract ................................................................................................................42 Introduction ..........................................................................................................43 Results ..................................................................................................................46 Validation of differential gene transcript abundance ...............................49 Pregnancy-associated genes in the opossum ............................................51 Differential transcript abundance between pre- vs. post-estrus ...............51 Conservation of genes regulated during pregnancy .................................55 Discussion ............................................................................................................68 Materials and Methods .........................................................................................75 Animals and tissue collection ..................................................................75 RNA extraction ........................................................................................76 cDNA library synthesis and Illumina sequencing ...................................76 Data access ...............................................................................................78 Illumina read quality control, alignment, and quantification ...................78 Quantitative PCR .....................................................................................78 viii
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