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Hudish Thesis 12-14-15 MICRORNA CONTROL OF NEURAL PROGENITOR MAINTENANCE AND SPECIFICATION by LAURA IOANA HUDISH B.S., University of Denver, 2008 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirements for the degree of Doctor of Philosophy Molecular Biology Program 2016 This thesis for the Doctor of Philosophy degree by Laura Ioana Hudish has been approved for the Molecular Biology Program by Kristin Artinger, Chair Bruce Appel, Advisor Thomas Evans Wendy Macklin Lee Niswander Date: 05-20-2016 i Hudish, Laura Ioana (Ph.D., Molecular Biology) microRNA Control of Neural Progenitor Maintenance and Specification Thesis directed by Professor Bruce Appel ABSTRACT During neural development, progenitors both divide to expand the neural progenitor (NP) population and differentiate as neurons and glia. This balance of proliferation and differentiation is crucial to the proper development of the central nervous system (CNS). This balance appears to be regulated by multiple different mechanisms including apico- basal polarization by Partitioning defective proteins (Par) as well as Hedgehog signaling, which in addition to its role in dorso-ventral patterning also promotes progenitor proliferation. How both of these pathways are modulated at the end of neurogenesis remains poorly understood. Using bioinformatics we identified the polarity genes pard3 and prkci as candidate targets for microRNA-219 (miR-219). miR-219-deficient zebrafish embryos have a deficit of oligodendrocytes, the myelinating glial cells of the CNS. Because a disruption in polarity could affect the types of cell divisions that NPs undergo, thus altering the balance of cell types that arise, we hypothesized that neural precursor maintenance is regulated by modulation of polarity cues through miR-219. We found that miR-219 inhibited expression of pard3 and prkci mRNAs via target sites in the 3’ untranslated region. These data support the role of miR-219 in downregulating expression of Par polarity proteins at the end of neurogenesis. In addition, we also found that Sonic Hedgehog (Shh) signaling was significantly increased in miR-219 morphants, suggesting a role for miR-219 in regulating the levels of Shh. Using prkci mutant zebrafish embryos we found that reduction of apical Par proteins results in a reduction of Shh signaling. ii These data provide evidence for a new mechanism of NP regulation, in which miR-219 downregulates apical Par proteins and Shh at the end of neurogenesis. The form and content of this abstract are approved. I recommend its publication. Approved: Bruce Appel iii ACKNOWLEDGEMENTS I dedicate this thesis to the many people that were a part of this experience and helped me throughout this process. I’d like to thank Dr. Bruce Appel, my mentor. He really encompasses the true meaning of what a mentor is. He taught me not only how to be a better researcher, but how to be a good member of the research community, how to identify good questions and how to push through moments that seemed overwhelming. He leads by his example of hard work, resilience and creativity and I couldn’t be more thankful for all that he has taught me. Thank you to my committee, Kristin Artinger, Lee Niswander, Thomas Evans, Wendy Macklin and James DeGregori, who always supported me and pushed me to be better and to think outside the box. I’d also like to thank my mother, who is an extraordinarily strong, loving and resilient woman who gave up everything to move to the US for my sister and I. I could never thank her enough for all the sacrifices she has made so I could accomplish my dreams. She is a great rock I can always lean on, and one of my biggest supporters. I am truly only here because of everything she taught me. I also want to thank my sister, who always makes me laugh and listens to me. She has also given me the biggest gift, becoming an aunt to my precious and sweet nephew, Owen who always makes the hardest days better with his cute adorable smile. I am also very fortunate to have an amazing and supportive husband who is always ready to listen and help. He is also responsible for introducing me to many fun adventures. I wouldn’t be nearly as balanced and happy if he wasn’t a part of my life. Thank you! iv TABLE OF CONTENTS CHAPTER I. INTRODUCTION ........................................................................................................................ 1 The neural Epithelium and Neural Progenitor Behaviors .............................................. 2 Sonic Hedgehog Signaling in the Nervous System .......................................................... 3 The Primary Cilia and Hedgehog Signaling ........................................................................ 6 Apico-basal Polarity and the Role of Par complex Proteins ............................................ 9 The Polarization of the Epithelium ........................................................................................ 10 Polarity and Neural Development ......................................................................................... 11 Polarity and Primary Cilia Formation ................................................................................... 13 Discovery and Function of microRNAs .............................................................................. 14 microRNAs in Neural Development ..................................................................................... 17 Conclusions .................................................................................................................................. 18 II. MIR-219 REGULATES NEURAL PRECURSOR DIFFERENTIATION BY DIRECT INHIBITION OF APICAL PAR POLARITY PROTEINS ....................... 20 Abstract ......................................................................................................................................... 20 Introduction .................................................................................................................................. 21 Materials and Methods .............................................................................................................. 24 Zebrafish Husbandry ................................................................................................... 24 Immunohistochemistry ............................................................................................... 24 In situ RNA Hybridization ........................................................................................ 25 Luciferase Assay .......................................................................................................... 26 Morpholino Injections ................................................................................................. 26 BrdU and EdU Labeling ........................................................................................... 27 v GFP Injections and Quantification ......................................................................... 27 Tg(hsp70l:pard3-EGFP) construction and Heat Shock Procedure ............. 28 Quantitative PCR .......................................................................................................... 28 Quantification and Statistical Analysis ................................................................. 29 Results ............................................................................................................................................. 29 miR-219 Promotes Neural Precursor Exit from Proliferative Division ...... 29 miR-219 Regulates pard3 and prkci via 3’ UTR Target Sites ....................... 39 Discussion ...................................................................................................................................... 46 III. MIR-219 INITIATES NEURAL PROGENITOR DIFFERENTIATION BY DAMPENING APICAL PAR PROTEIN-DEPENDENT HEDGEHOG SIGNALING ................................................................................................................................. 54 Abstract ......................................................................................................................................... 54 Introduction .................................................................................................................................. 55 Materials and Methods .............................................................................................................. 57 Zebrafish Husbandry ................................................................................................... 57 Immunohistochemistry ............................................................................................... 58 In situ RNA Hybridization ........................................................................................ 58 Morpholino Injections ................................................................................................. 59 Plasmid injections and construction ....................................................................... 59 EdU Labeling ................................................................................................................ 60 Heat Shock Procedure ................................................................................................. 60 Quantitative PCR .......................................................................................................... 61 Quantification and Statistical Analysis ................................................................. 61 Cilia
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