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Lineage Specification of Ovarian Theca Cells Requires Multi- Cellular Interactions Via Oocyte and Granulosa Cells

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Lineage Specification of Ovarian Theca Cells Requires Multi- Cellular Interactions Via Oocyte and Granulosa Cells LINEAGE SPECIFICATION OF OVARIAN THECA CELLS REQUIRES MULTI- CELLULAR INTERACTIONS VIA OOCYTE AND GRANULOSA CELLS BY CHANG LIU DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Animal Sciences in the Graduate College of the University of Illinois at Urbana-Champaign, 2015 Urbana, Illinois Doctoral Committee: Professor Janice M. Bahr, Chair Professor David J. Miller Professor Romana A. Nowak Principle Investigator Humphrey H.-C. Yao, National Institute of Environmental Health Sciences ABSTRACT Organogenesis of the ovary is a highly orchestrated process involving multiple lineage determinations of ovarian surface epithelium, granulosa cells, and theca cells. While the sources of ovarian surface epithelium and granulosa cells are known, the embryonic origin(s) of theca stem/progenitor cells have not been definitively identified. Here I show that theca cells derive from two sources: Wt1‐positive cells indigenous to the ovary and Gli1‐positive mesenchymal cells that migrate from the mesonephros. These two theca progenitor populations are distinct in their cell lineage contributions, relative proximity to granulosa cells, and their gene expression profiles. The two sources of theca progenitors acquire theca lineage marker Gli1 in the ovary soon after birth, in response to paracrine signals Desert hedgehog (Dhh) and Indian hedgehog (Ihh) from granulosa cells. Ovaries lacking Dhh/Ihh exhibited a loss of theca layer, blunted steroid production, arrested folliculogenesis, and failure to form corpora lutea. Production of Dhh/Ihh in granulosa cells requires growth differentiation factor 9 (GDF9) from the oocyte. Gdf9 ablation resulted in diminished expression of Dhh, Ihh, and theca cell‐specific Gli1. Conversely, supplementation of GDF9 to oocyte‐depleted ovaries reactivated Dhh/Ihh production and subsequent expression of Gli1. My studies provide the first genetic evidence for the origins of theca cells and reveal a novel multicellular interaction via GDF9 and Hedgehog signaling critical for ovarian folliculogenesis and formation of a functional theca. ii To my wife Yanzhen Li iii ACKNOWLEDGEMENTS I own a great debt of gratitude to my mentor Dr. Humphrey Yao for his guidance, training, support, generosity and friendship. He is my mentor for life. Words cannot express my appreciation to him. I want to thank all the members of the Yao lab including Karina Rodriguez, Paula Brown, Erica Ungewitter, Barbara Nicol and Fei Zhao as well as former lab members Heather Franco, Denise Archambeault, Jeff Chen‐Che Huang, Chia‐ Feng Liu for all your support and help over the years. I feel extremely blessed to have such a wonderful “family” and it is you all who have made my everyday work in the lab full of joy. It is my great honor to have worked with each and every one of you. I would like to thank all my committee members including Dr. Janice Bahr, Dr. Romana Nowak, and Dr. David Miller for their advice, encouragement and availability especially during the years I am doing my PhD thesis at NIEHS in NC. Not to mention that many of them also served my committee during my Master’s study. I cannot come to this far without all your support. I want to particularly thank my scientific grandma Dr. Janice Bahr for her loving kindness, advice and support throughout my graduate study. I am also thankful for all the support that I received from Reproductive and Development Biology Laboratory at NIEHS. I thank Dr. Ken Korach, Dr. Mitch Eddy, Dr. Carmen Williams and Dr. Masahiko Negishi for their advice and suggestions on my research projects and my career as well as our secretaries Juanita Roman and Marsha Johnston who had made my life so much easier here at NIEHS. Finally, I would like to acknowledge my family and friends for their care and prayers over the years. I love you all. iv Table of Contents CHAPTER 1: Literature Review .......................................................................................................................... 1 1.1 Overview of ovarian organogenesis ..................................................................................................... 1 1.2 Current understanding of the establishment of the ovarian somatic cell lineages ......... 3 1.3 Current understanding of the establishment of the female germline ................................... 6 1.4 Regulation of folliculogenesis .............................................................................................................. 11 1.5 Theca cells and ovarian diseases ........................................................................................................ 21 1.6 The Hedgehog signaling Pathway in mammalian gonad development ............................. 24 1.7 Summary ....................................................................................................................................................... 26 CHAPTER 2: The Origins of Theca Cells: Divergent Sources to a Convergent End ................... 28 2.1 Abstract ......................................................................................................................................................... 28 2.2 Introduction ................................................................................................................................................ 29 2.3 Materials and Methods ........................................................................................................................... 31 2.4 Results ............................................................................................................................................................ 36 2.5 Discussion..................................................................................................................................................... 43 2.6 Figures and Tables .................................................................................................................................... 50 CHAPTER 3: Role of Desert/Indian Hedgehog Signaling in Theca Cell Development in the Murine Ovary ........................................................................................................................................................... 70 3.1 Abstract ......................................................................................................................................................... 70 3.2 Introduction ................................................................................................................................................ 72 3.3 Materials and Methods ........................................................................................................................... 74 3.4 Results ............................................................................................................................................................ 80 3.5 Discussion..................................................................................................................................................... 84 3.6 Figures and Tables .................................................................................................................................... 90 CHAPTER 4: Expression of Theca Cell‐Specific Gli1 Requires Oocyte‐Derived GDF9 through Hedgehog Signaling from Granulosa Cells ................................................................................................ 103 4.1 Abstract ....................................................................................................................................................... 103 v 4.2 Introduction .............................................................................................................................................. 105 4.3 Material and Methods ........................................................................................................................... 108 4.4 Results .......................................................................................................................................................... 111 4.5 Discussion................................................................................................................................................... 114 4.6 Figures ......................................................................................................................................................... 118 CHAPTER 5: Conclusions and Future Directions ................................................................................... 124 5.1 Figures ......................................................................................................................................................... 130 BIBLIOGRAPHY .................................................................................................................................................... 131 vi CHAPTER 1: Literature Review 1.1 Overview of ovarian organogenesis The word “ovary” derives from the Latin word “ovarium”, literally “egg” or “nut”. The mammalian ovary plays two central roles in female reproduction by acting as both gonads and reproductive glands. As gonads, the ovary supplies germ cells to produce the next generation. While acting as glands, the ovary produces hormones controlling a variety of aspects of female development and physiology. The structural precursor of the ovary is the genital ridge (or gonadal primordium). Genital ridges emerge as paired thickenings of the epithelial layer, the coelomic
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