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HSV-1 Reprogramming of the Host Transcriptional Environment By Title Page HSV-1 reprogramming of the host transcriptional environment by Sarah E. Dremel B.S., University of Minnesota Twin Cities, 2015 Submitted to the Graduate Faculty of the School of Medicine in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Pittsburgh 2020 Committee Page UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE This dissertation was presented by Sarah E. Dremel It was defended on March 20, 2020 and approved by Jennifer Bomberger, Associate Professor, Department of Microbiology and Molecular Genetics Fred Homa, Professor, Department of Microbiology and Molecular Genetics Nara Lee, Assistant Professor, Department of Microbiology and Molecular Genetics Martin Schmidt, Professor, Department of Microbiology and Molecular Genetics Dissertation Director: Neal DeLuca, Professor, Department of Microbiology and Molecular Genetics ii Copyright © by Sarah E. Dremel 2020 iii Abstract HSV-1 reprogramming of the host transcriptional environment Sarah E. Dremel, PhD University of Pittsburgh, 2020 Herpes Simplex Virus-1 (HSV-1) is a ubiquitous pathogen of the oral and genital mucosa. The 152 kilobase double stranded DNA virus employs a coordinated cascade of transcriptional events to efficiently generate progeny. Using Next Generation Sequencing (NGS) techniques we were able to determine a global, unbiased view of both the host and pathogen. We propose a model for how viral DNA replication results in the differential utilization of cellular factors that function in transcription initiation. Our work outlines the various cis- and trans- acting factors utilized by the virus for this complex transcriptional program. We further elucidated the critical role that the major viral transactivator, ICP4, plays throughout the life cycle. We found that ICP4 coated the viral genome early during infection, and that rather than occluding the genome, this dense binding was associated with recruitment of the Pol II machinery to viral promoters. ICP4 discriminately bound the viral genome due to the absence of cellular nucleosomes and high density of cognate binding sites. We posit that ICP4’s ability to recruit components of the Pol II machinery to the viral genome creates a competitive transcriptional environment. These distinguishing characteristics ultimately result in a rapid and efficient reprogramming of the host’s transcriptional machinery. iv Table of Contents 1.0 Introduction ............................................................................................................................. 1 1.1 Pathogenesis and Human Health .................................................................................. 1 1.1.1 Herpesvirales ........................................................................................................1 1.1.2 Pathogenesis ..........................................................................................................2 1.1.3 Treatment .............................................................................................................6 1.1.4 HSV Therapeutic Vectors ...................................................................................7 1.2 General Biology and HSV-1 Lifecycle .......................................................................... 8 1.2.1 Virion Structure ...................................................................................................8 1.2.2 Genome Structure ................................................................................................9 1.2.3 Productive Infection ...........................................................................................11 1.2.3.1 Viral Entry and Trafficking ................................................................. 12 1.2.3.2 Evasion of Nuclear Restriction Factors ............................................... 14 1.2.3.3 Overview of Pol II Transcription ......................................................... 15 1.2.3.4 Transcriptional Cascade ....................................................................... 16 1.2.3.5 VP16-Mediated Transcription .............................................................. 17 1.2.3.6 ICP4-Dependent Transcription ............................................................ 18 1.2.3.7 DNA Replication-Dependent Transcription ........................................ 18 1.2.3.8 Viral DNA Replication .......................................................................... 19 1.2.3.9 Packaging and Assembly ....................................................................... 22 1.3 Rationale ........................................................................................................................ 23 v 2.0 Genome replication affects transcription factor binding mediating the cascade of Herpes Simplex Virus transcription .......................................................................................... 25 2.1 Project Summary .......................................................................................................... 25 2.2 Importance .................................................................................................................... 26 2.3 Introduction .................................................................................................................. 27 2.4 Results ............................................................................................................................ 28 2.4.1 Dependence of Late Viral Transcription on Genome Replication ................28 2.4.2 Classification of Viral DNA Replication-Dependent Transcripts. ................30 2.4.3 Viral Replication Facilitates Preinitiation Complex Formation on Previously Silent Promoters. .........................................................................................................32 2.4.4 A Single Duplication Alters Genomic Accessibility. .......................................34 2.4.5 SP1 Preferentially Binds to the Viral Genome Pre-replication. ....................36 2.4.6 Differential TFIID Promoter Context Preferred After Replication. .............37 2.4.7 Continuous Requirement for ICP4 in Viral Transcription. ..........................39 2.5 Supplemental Figures ................................................................................................... 42 2.6 Discussion ...................................................................................................................... 48 2.7 Materials and Methods ................................................................................................ 50 3.0 Herpes simplex viral nucleoprotein creates a competitive transcriptional environment facilitating robust viral transcription and host shut off ................................... 56 3.1 Project Summary .......................................................................................................... 56 3.2 Importance .................................................................................................................... 57 3.3 Introduction .................................................................................................................. 57 3.4 Results ............................................................................................................................ 59 vi 3.4.1 ICP4 binding is altered by viral genome replication. .....................................59 3.4.2 ICP4 stabilizes GTF binding promoting cooperative preinitiation complex (PIC) assembly. ............................................................................................................62 3.4.3 Genome-bound ICP4 does not affect accessibility. .........................................65 3.4.4 ICP4 binds to cellular transcription start sites (TSS) early during infection. .......................................................................................................................................68 3.4.5 ICP4 binding is restricted to accessible regions of the cellular genome........70 3.4.6 ICP4 mediates depletion of Pol II on cellular promoters ...............................73 3.5 Supplemental Figures ................................................................................................... 76 3.6 Discussion ...................................................................................................................... 85 3.7 Materials and Methods ................................................................................................ 90 4.0 Summary and Discussion ..................................................................................................... 97 4.1 Summary of Thesis ....................................................................................................... 97 4.2 General Discussion ....................................................................................................... 98 5.0 Future Directions ................................................................................................................ 104 Bibliography .............................................................................................................................. 107 vii List of Tables Table 1 Classification of viral genes bases on DNA replication dependence ........................ 32 viii List of Figures Figure 1 Species tree of human herpesviruses ........................................................................... 1 Figure 2 Complications associated with HSV-1 infection and dissemination ......................... 2
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