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Gene Expression Profiling Reveals Novel Attributes of the Mouse Definitive Endoderm

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Gene Expression Profiling Reveals Novel Attributes of the Mouse Definitive Endoderm GENE EXPRESSION PROFILING REVEALS NOVEL ATTRIBUTES OF THE MOUSE DEFINITIVE ENDODERM by KRISTEN DAWN MCKNIGHT B.Sc. (Honors), Simon Fraser University, 2002 THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Genetics) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) December 2008 © Kristen Dawn McKnight, 2008 ABSTRACT Gastrulation is one of the most critical events of embryogenesis, generating the three primary germ layers (definitive endoderm, mesoderm, and ectoderm) and establishing the embryonic body plan. The definitive endoderm, which generates the lungs, liver, pancreas, and digestive tract, has become a tissue of particular interest in recent years. Understanding definitive endoderm formation and patterning will greatly aid progress in the in vitro differentiation of embryonic stem cells to definitive endoderm for use in treatment of diseases such as diabetes and hepatitis as an alternative for whole organ replacement. Gene targeting studies have demonstrated a critical role for the Nodal signaling pathway and the forkhead transcription factors Foxh1 and Foxa2 in specification of a group of cells referred to as the anterior primitive streak (APS). However, the transcriptional targets of Foxh1 and/or Foxa2 other than Nodal that regulate specification of this group of cells are currently unknown. Fate mapping and lineage tracing experiments have shown the APS to be the source of the definitive endoderm. However, many questions regarding specification and patterning of the definitive endoderm remain. The study of this tissue has been hampered by the lack of genetic markers specific for the definitive endoderm as many of the current markers, including Cerl, Foxa2, and Sox17, are also expressed in the visceral endoderm, an extraembryonic tissue. To further investigate the role of Foxh1 in specification of the anterior primitive streak and to address the lack of genetic markers for the definitive endoderm we performed expression profiling on post-implantation mouse embryos using Affymetrix™ GeneChips®. From this analysis we identified and characterized a novel marker of the mouse definitive endoderm. Examination of this, and other, novel endoderm markers in Foxh1 and Foxa2 deficient mouse ii embryos revealed that contrary to current models of definitive endoderm formation, we find some definitive endoderm is formed in these mutants. Specifically, specification of the midgut and hindgut definitive endoderm is largely unaffected, while foregut formation is severely affected. These results suggest that the formation of the midgut and hindgut definitive endoderm populations is independent of the anterior primitive streak and separate from the foregut definitive endoderm. This represents a major insight into the mechanisms regulating endoderm formation and patterning. iii TABLE OF CONTENTS ABSTRACT................................................................................................................................... ii TABLE OF CONTENTS ............................................................................................................ iv LIST OF TABLES ...................................................................................................................... vii LIST OF FIGURES .................................................................................................................... vii ACKNOWLEDGEMENTS ........................................................................................................ ix DEDICATION............................................................................................................................... x CO-AUTHORSHIP STATEMENT ........................................................................................... xi CHAPTER 1 INTRODUCTION................................................................................................. 1 1.1 GENERAL OVERVIEW OF THE EMBRYONIC DEVELOPMENT OF MUS MUSCULUS................................................................................................................................... 1 1.1.1 An introduction to the lineages constituting the mouse embryo ........................................ 1 1.1.1.1 The first lineages are specified during the pre-implantation stage............................... 4 1.1.1.2 The primary germ layers are formed during the post-implantation stage .................... 5 1.2 THE MOUSE GASTRULA ORGANIZER ............................................................................. 6 1.2.1 The mouse gastrula organizer is located at the anterior end of the primitive streak and contributes to the midline tissues of the embryo ......................................................................... 7 1.2.2 Tissues derived from the anterior primitive streak contribute to the patterning of all three body axes ..................................................................................................................................... 9 1.2.3 Specification of the anterior primitive streak ................................................................... 10 1.3 THE MOUSE DEFINITIVE ENDODERM........................................................................... 11 1.3.1 Formation and morphogenesis of the definitive endoderm.............................................. 12 1.3.2 Regulation of definitive endoderm cell fate ..................................................................... 15 1.3.3 Regionalization of the definitive endoderm ..................................................................... 17 1.4 THE NODAL SIGNALING PATHWAY.............................................................................. 18 1.4.1 Components of the Nodal signaling pathway................................................................... 19 1.4.2 Regulation of cell fate decisions in the mouse embryo by the Nodal pathway................ 23 1.4.2.1 There is a graded response to Nodal signaling within the primitive streak of the mouse embryo ........................................................................................................................ 23 1.5 THE FORKHEAD BOX PROTEINS FOXH1 AND FOXA2............................................... 28 1.5.1 Foxh1 and Foxa2 are winged helix transcription factors ................................................. 28 1.5.1.1 Foxh1.......................................................................................................................... 31 1.5.1.2 Foxa2.......................................................................................................................... 32 1.5.2 Roles of Foxh1 and Foxa2 in mouse embryogenesis....................................................... 34 1.5.2.1 Expression of Foxh1 and Foxa2 in the mouse embryo.............................................. 34 1.5.2.2 Foxh1 and Foxa2 are essential for specification of the anterior primitive streak and its derivative tissues ............................................................................................................... 35 1.5.2.3 Downstream targets of Foxh1 and Foxa2 in the mouse embryo................................ 39 1.6 AIM OF THE STUDY............................................................................................................ 41 1.7 REFERENCES ....................................................................................................................... 43 iv CHAPTER 2 A DIFFERENTIAL SCREEN FOR GENES INVOLVED IN SPECIFICATION OF THE ANTERIOR PRIMITIVE STREAK USING FOXH1 DEFICIENT EMBRYOS ........................................................................................................... 52 2.1 INTRODUCTION .................................................................................................................. 52 2.2 RESULTS ............................................................................................................................... 54 2.2.1 Identification of genes differentially expressed between E6.5 wild-type and Foxh1 null embryos using Affymetrix™ GeneChips® ................................................................................ 54 2.2.2 Assessment of microarray sensitivity and data quality .................................................... 58 2.2.3 Validation of microarray results by RT-PCR and qRT-PCR ........................................... 60 2.2.4 Analysis of BG078657, an uncharacterized expressed sequence tag, in E6.5 mouse embryos ..................................................................................................................................... 64 2.2.5 Characterization of Trh, a regulator of the hypothalamic-pituitary-thyroid axis, in E6.5 mouse embryos.......................................................................................................................... 66 2.3 DISCUSSION......................................................................................................................... 69 2.3.1 Multiple factors contributed to the discrepancies between the observed and expected results for control genes used to measure array quality and sensitivity .................................... 69 2.3.2 The gene expression profiles of E6.5 wild-type and Foxh1 null embryos are largely similar ........................................................................................................................................ 71 2.3.3 Contrary to its primary role as a transcriptional activator, loss of
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