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Cell-Specific Gene Expression: Pylorus Morphogenesis and Hedgehog-Regulated Enhancers

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Cell-Specific Gene Expression: Pylorus Morphogenesis and Hedgehog-Regulated Enhancers CELL-SPECIFIC GENE EXPRESSION: PYLORUS MORPHOGENESIS AND HEDGEHOG-REGULATED ENHANCERS by Aaron Mark Udager A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Cell and Developmental Biology) in the University of Michigan 2010 Doctoral Committee: Professor Deborah L. Gumucio, Chair Professor Gregory R. Dressler Professor Ronald J. Koenig Professor Linda C. Samuelson Associate Professor Deneen M. Wellik Assistant Professor Scott E. Barolo © Aaron Mark Udager 2010 To my wife Kara and my parents Mark and Anita ii ACKNOWLEDGEMENTS First, I’d like to thank my mentor Deb Gumucio. Over the past four years, you have given me freedom to explore and opportunities to succeed (as well as fail). Without a doubt, these experiences have made me a better scientist. I’ll always admire your love of science and the dedication you show to teaching students, supporting your employees, and maintaining a family. I know we’ll remain good friends in the future. Second, I’d like to thank the members of my thesis committee. You challenged me when I needed to be and provided critical feedback at several key junctures in this project. Our meetings over the past several years have been an important part of my growth as a scientist. Third, I need to thank the extensive contributions made to this project by our collaborators, both here at the University and abroad. I’d like to thank Drs. Doug Engel and Kim-Chew Lim in this department for providing Gata3lacZ/+ mice and sharing a number of other resources. I’d also like to thank Dr. Richard Harvey of the Victor Chang Cardiac Research Institute in Australia for generously providing Nkx2-5lacZ/+ mice. A special thanks to Dr. Scott Barolo and his post-doc Dr. Dave Parker, of this department, for their critical work on the Topo-TX project (see Chapter IV). iii I’d like to thank the administrative staffs of the Department of Cell and Developmental Biology, the Center for Organogenesis, and the Medical Scientist Training Program (MSTP). In particular, I’d like to recognize Ellen Elkin, Penny Morris, Kristen Hug, and Becky Pintar. I’d also like to thank the technical staffs of the Microscopy and Image Analysis Laboratory and the Morphology Core. In particular, I’d like to recognize Shelley Almburg, Marta Dzaman, and Maria Ripberger. I’d like to thank past and present members of the Gumucio lab: Åsa Kolterud for your help with X-gal staining; Xing Li for teaching me everything I know about microarrays; Chunbo Hu for your help with in situ hybridizations; Tracy Xiao for your help with the border project; and Neil Richards for your help with RT-PCR and all things cloning. I’d also like to recognize Katherine Gurdziel and Mridula Jayaraman for your past (and future!) contributions to the Topo-TX project. And thank you to Jierong Lang for your tremendous work in maintaining the mouse room; the lab would not be the same without you. I’d like to thank all of our lab managers over the past four years: Kathleen Portman, Wendy McKimpson, Xueming Tang, and in particular, Mike Czerwinski. I’d also like to acknowledge the undergraduate students that have worked with me: Mikey Thomas and Vivek Mendiratta. Thank you to my fellow graduate students (and/or post-docs), Anne Grosse, Kate Walton, Andrea Waite, and Will Zacharias, for personal as well as scientific discussions. A special thanks to Ajay Prakash for all of your help with the Gata3 project. It’s been a blast. I couldn’t imagine being happier anywhere else. iv Lastly, I need to thank my family and friends. A special thank you to my MSTP classmates, Jae Lee, Steve Philips, and Dan Wahl, for our all too infrequent happy hour trips. To my sister Andrea, her husband Scott, and their two little girls, Annaleigh and Charlotte: I love you guys! To my in-laws, Gene and Lisa: thank you for your love and support and for being good role models for an academic career! To my grandparents, Gen, Hal, Wilbur, and Gladys: thank you for your love and support. I wish you were all around to share these important life moments with me! To my parents, Mark and Anita: thank you for recognizing what I needed to succeed and doing everything you could to provide it. To my mom: thank you for instilling in me the idea that nothing but my best is good enough. To my dad: thank you for reminding me the importance of taking time to enjoy life. Finally, to my wife Kara, who was born with Infantile Hypertrophic Pyloric Stenosis: Thank you. Thank you for listening to my rambling science discussions on our long runs. Thank you for helping me to be a better person. Thank you for making the last three and a half years the best of my life. I wouldn’t be the same without you and neither would this thesis! v TABLE OF CONTENTS DEDICATION................................................................................................................... ii ACKNOWLEDGEMENTS ............................................................................................ iii LIST OF FIGURES ......................................................................................................... ix LIST OF TABLES ........................................................................................................... xi ABSTRACT .................................................................................................................... xiii CHAPTER I. INTRODUCTION..................................................................................................1 I.1. Embryonic development of the early GI tract ........................................2 I.2. Establishing epithelial identity and morphology in the foregut .............6 I.3. Regulation of nutrient transport within the GI tract .............................11 I.4. Hh signaling in the late embryonic and adult GI tract .........................20 I.5. Hh regulation of gene expression ........................................................24 I.6. Summary and thesis outline .................................................................35 I.7. Attribution ............................................................................................37 I.8. Publication ...........................................................................................38 I.9. References ............................................................................................39 II. DYNAMIC PATTERNING AT THE PYLORUS: FORMATION OF AN EPITHELIAL INTESTINE-STOMACH BOUNDARY IN LATE FETAL LIFE .......................................................................................47 II.1. Introduction ..........................................................................................47 vi II.2. Materials and methods .........................................................................50 II.3. Results ..................................................................................................55 II.4. Discussion ............................................................................................67 II.5. Attribution ............................................................................................91 II.6. Publication ...........................................................................................92 II.7. References ............................................................................................93 III. GATA3 IS ESSENTIAL FOR SMOOTH MUSCLE STRUCTURES AT THE PYLORUS ............................................................99 III.1. Introduction ..........................................................................................99 III.2. Materials and methods .......................................................................102 III.3. Results ................................................................................................105 III.4. Discussion ..........................................................................................112 III.5. Attribution ..........................................................................................128 III.6. Publication .........................................................................................129 III.7. References ..........................................................................................130 IV. GENOME-WIDE CLUSTERING ANALYSIS OF GLI/CI BINDING SITES ACROSS DIVERGENT DROSOPHILA SPECIES REVEALS HEDGEHOG-REGULATED ENHANCERS .......134 IV.1. Introduction ........................................................................................135 IV.2. Materials and methods .......................................................................138 IV.3. Results ................................................................................................140 IV.4. Discussion ..........................................................................................148 IV.5. Attribution ..........................................................................................162 IV.6. Publication .........................................................................................163 IV.7. References ..........................................................................................164 V. CELL-SPECIFIC GENE EXPRESSION: MECHANISMS AND CONSEQUENCES ........................................................................................167 vii V.1. Evolutionary change and genetic redundancy in the GI tract ............167 V.2. The establishment and maintenance of differentiated gastric epithelium ..........................................................................................171
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