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Methods to Record Transcription Factor Binding and Enhancer Activity Throughout Cellular Differentiation Zongtai Qi Washington University in St

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Methods to Record Transcription Factor Binding and Enhancer Activity Throughout Cellular Differentiation Zongtai Qi Washington University in St Washington University in St. Louis Washington University Open Scholarship Arts & Sciences Electronic Theses and Dissertations Arts & Sciences Summer 8-15-2018 Methods to Record Transcription Factor Binding and Enhancer Activity throughout Cellular Differentiation Zongtai Qi Washington University in St. Louis Follow this and additional works at: https://openscholarship.wustl.edu/art_sci_etds Part of the Bioinformatics Commons, and the Genetics Commons Recommended Citation Qi, Zongtai, "Methods to Record Transcription Factor Binding and Enhancer Activity throughout Cellular Differentiation" (2018). Arts & Sciences Electronic Theses and Dissertations. 1647. https://openscholarship.wustl.edu/art_sci_etds/1647 This Dissertation is brought to you for free and open access by the Arts & Sciences at Washington University Open Scholarship. It has been accepted for inclusion in Arts & Sciences Electronic Theses and Dissertations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. WASHINGTON UNIVERSITY IN ST. LOUIS Division of Biology and Biomedical Sciences Molecular Genetics and Genomics Dissertation Examination Committee: Robi Mitra, Chair Barak Cohen Joseph Dougherty Joshua Rubin Gray Stormo Andrew Yoo Methods to Record Transcription Factor Binding and Enhancer Activity throughout Cellular Differentiation. by Zongtai Qi A dissertation presented to The Graduate School of Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy August 2018 St. Louis, Missouri Table of Contents List of Figures ................................................................................................................................ v List of Tables ................................................................................................................................ vi Acknowledgments ....................................................................................................................... vii Abstract of the Dissertation ........................................................................................................ ix Chapter 1 ....................................................................................................................................... 1 Introduction ................................................................................................................................... 1 1.1 Development of an inducible transposon “Calling Card” method ........................................ 1 1.1.1 The transposon “Calling Card” method can record transcription factor binding. .......... 1 1.1.2 An “inducible” Calling Card method is useful in studying TF bindings underlying cell fate decisions. .......................................................................................................................... 2 1.1.3 Degradation domains allow a rapid post-translational induction system. ...................... 2 1.1.4 Degradation domains are utilized to develop an inducible transposon “Calling Card” method. .................................................................................................................................... 3 1.2 Application of the “Calling Card” method to study the role of Brd4-bound enhancers for sex differences in glioblastoma ................................................................................................... 4 1.2.1 Sex-dimorphism in glioblastoma is a cell-intrinsic property. ......................................... 4 1.2.2 Epigenetic regulatory mechanism may play a key role in establishing sex differences in GBM. ................................................................................................................................... 5 1.2.3 Epigenetic reader Brd4 establishes cell identity and regulates oncogenes. .................... 5 1.2.4 The “Calling Card” method is used to decipher the Brd4-bound enhancers. ................. 6 1.3 Development of a high-throughput functional identification of enhancers using a CRE recombinase mediated reporter assay .......................................................................................... 7 1.3.1 Enhancer and super enhancer play a fundamental role in cellular differentiation. ........ 7 1.3.2 Current methods have challenges for high-throughput identification of cell-specific enhancers in development. ...................................................................................................... 8 1.3.3 The CRE-mediated reporter assay allows a high-throughput functional identification of cell specific enhancers in development. ................................................................................ 10 Chapter 2 ..................................................................................................................................... 11 An optimized, broadly applicable piggyBac transposon induction system ............................ 11 2.1 Abstract ............................................................................................................................... 11 2.2 Introduction ......................................................................................................................... 12 2.3 Results ................................................................................................................................. 15 2.3.1 Overview ...................................................................................................................... 15 2.3.2 Evaluating the transposition efficiencies of inducible PBase ....................................... 18 2.3.3 The FKBP DD system achieved the highest fold-change between induced and uninduced states ..................................................................................................................... 20 2.3.4 HSP90 levels correlate with the dynamic range of the ERT2 system .......................... 21 2.3.5 There is a trade-off between maximal PBase activity and fold-induction ................... 22 2.3.6 Fusion protein levels can be tuned to achieve low background transposition and high inducibility ............................................................................................................................. 25 2.3.7 The FKBP-PBase-FKBP protein levels can be tuned post-transcriptionally ............... 27 2.3.8 The FKBP based PBase system is reversible ............................................................... 28 ii 2.3.9 Unlike 4OHT, Shld1 does not interfere with general cellular functions ...................... 31 2.4 Discussion ........................................................................................................................... 34 2.5 Method ................................................................................................................................ 36 2.5.1 Plasmid construction ..................................................................................................... 36 2.5.2 Cell culture and neural differentiation .......................................................................... 37 2.5.3 Cell transduction and transgenic cell line generation ................................................... 38 2.5.4 Cell transfection and drug administration .................................................................... 38 2.5.5 Cell colony staining and counting ................................................................................ 39 2.5.6 Imaging and flow cytometry ......................................................................................... 40 2.5.7 RNA extraction and sequencing ................................................................................... 40 2.5.8 Reads mapping and statistical analysis ......................................................................... 41 Chapter 3 ..................................................................................................................................... 42 Brd4-bound enhancers drive critical sex differences in glioblastoma ................................... 42 3.1 Abstract ............................................................................................................................... 42 3.2 Introduction ......................................................................................................................... 43 3.3 Results and discussion ......................................................................................................... 45 3.3.1 BET family protein (Brd4) inhibition has opposing effects on the tumorigenic phenotype in male and female GBM astrocytes .................................................................... 45 3.3.2 Male and female GBM cells utilize different sets of Brd4-bound enhancers .............. 48 3.3.3 Brd4-bound enhancers regulate sex differences in GBM ............................................. 52 3.5 Methods ............................................................................................................................... 59 3.3.1 RNA-sequencing .......................................................................................................... 59 3.3.2 Chromatin immunoprecipitation sequencing (ChIP-seq) for H3K27ac ....................... 60 3.3.3 Sequencing data alignment and analysis ...................................................................... 61 3.3.4 Pathway analysis ..........................................................................................................
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