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ICP8 Self Interactions Are Essential for HSV-1 Replication Compartment Formation Anthar Darwish University of Connecticut - Storrs, [email protected]

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ICP8 Self Interactions Are Essential for HSV-1 Replication Compartment Formation Anthar Darwish University of Connecticut - Storrs, Anthar.Darwish@Gmail.Com University of Connecticut OpenCommons@UConn Doctoral Dissertations University of Connecticut Graduate School 8-9-2018 ICP8 Self Interactions are Essential for HSV-1 Replication Compartment Formation Anthar Darwish University of Connecticut - Storrs, [email protected] Follow this and additional works at: https://opencommons.uconn.edu/dissertations Recommended Citation Darwish, Anthar, "ICP8 Self Interactions are Essential for HSV-1 Replication Compartment Formation" (2018). Doctoral Dissertations. 1940. https://opencommons.uconn.edu/dissertations/1940 ICP8 Self Interactions are Essential for HSV-1 Replication Compartment Formation Anthar S. Darwish, PhD University of Connecticut, 2018 ABSTRACT The objective of this thesis was to understand the ICP8 protein interactions involved during the formation of HSV-1 replication compartments. We focused our efforts on mapping the ICP8-ICP8 self-interactions that are involved in the formation of DNA independent filaments. We report here that the FNF motif (F1142, N1143 and F1144) and the FW motif (F843 and W844) are essential for ICP8 filament formation. Furthermore we observed a positive correlation between ICP8 filamentation and the formation of replication compartments. Mammalian expression plasmids bearing mutations in these motifs (FNF and FW) were unable to complement an ICP8 null virus for growth and replication compartment formation. We propose that filaments or other higher order structures of ICP8 may provide a scaffold onto which other proteins are recruited to form prereplicative sites and replication compartments. In an attempt to broaden our understanding of ICP8 self-interactions and its interactions with other essential viral proteins we searched for potential protein interaction sites on the surface of ICP8. Using the structural information of ICP8 and sequence comparison with homologous proteins, we identified conserved residues in the shoulder region (R262, H266, D270, E271, E274, Q706 and F707) of ICP8 that might function as protein interaction sites. The Q706A and F707A (QF) mutant protein was able to Anthar S. Darwish, University of Connecticut, 2018 form pre-replicative like sites and bind ssDNA but cannot complement ICP8 null virus for growth and replication compartment formation. Our analysis suggests that (QF) is involved in an important function or interaction that is required for the progression of mature replication compartments. ICP8 Self Interactions are Essential for HSV-1 Replication Compartment Formation Anthar S. Darwish B.S., Birzeit University, 2008 M.S., Al-Quds University, 2010 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy at the University of Connecticut 2018 i Copyright by Anthar S. Darwish 2018 ii APPROVAL PAGE Doctor of Philosophy Dissertation ICP8 Self Interactions are Essential for HSV-1 Replication Compartment Formation Presented by Anthar S. Darwish, B.Sc., M.Sc. Major Advisor ________________________________________________________________ Sandra K. Weller Associate Advisor ________________________________________________________________ Ann Cowan Associate Advisor ________________________________________________________________ John Carson Associate Advisor ________________________________________________________________ Christopher Heinen Associate Advisor ________________________________________________________________ Gordon Carmichael University of Connecticut 2018 iii Acknowledgments This thesis was completed because of the guidance, help and support of many remarkable people. The process of completing a doctoral degree requires a village of teachers, mentors, classmates, family and friends. I am tremendously grateful for this experience and all of the help and guidance that I received throughout this journey. I would like to thank the University of Connecticut for the opportunity to receive this training. I would also like to thank my advisor, Sandra Weller, for the opportunity to be a student in her lab. Thank you for all of your guidance, patience, support and help throughout the years. Thanks for always challenging and pushing us to be better scientists and thank you for your thoughtful revisions on my thesis. I would also like to thank my committee members Ann Cowan, John Cason, Chris Heinen, and Gordan Charmical for the helpful discussions, academic support, and guidance. I would like to additionally thank Ann Cowan for her personal support, revisions and suggestions during my thesis preparation. Furthermore, I am very grateful to have had such a thoughtful and caring Dean. Thank you Barbara Kream, for always having an open door and for your countless support during my studies. I would also like to thank all of the past and present members of the Weller lab. I must start by acknowledging Ping Bai and Lorry Grady for their thoughtful collaborations on this study, it was a pleasure to work closely with both of you! We made a good team, iv thank you for sharing you expertise with me. I also had the wonderful opportunity of working with Jonathan Helmus, I would like to thank him for his significant contribution in helping to identify predicted protein interaction sites on ICP8. Furthermore, I would like to thank Renata Szczepaniak for her constant help with trouble shooting experiments and the valuable role she played in my lab training. I would also like to acknowledge Savithri Weerasooriya and Katherine DiScipio for their dedicated and fruitful continuation of this research project. Thank you for the great work you have done with ICP8! I was very lucky to have shared my time in the Weller lab with some amazing graduate students. I would like to start by thanking Mitali Adlakha for being a supportive, caring and wonderful lab mate. I enjoyed our discussions and teatime at Tisane. I would also like to thank Sam Smith for her constant support, encouragement and guidance through out my graduate studies! I consider myself immensely luck to have always had such a wonderful support system of classmates, friends and family. My parents Ghaziah and Saker are the most remarkable and selfless human beings I’ve ever met. Thank you for everything you have done for me and your endless support and constant belief in me! The greatest gift in life is wonderful siblings and I am very grateful for my brothers, Deya and Enar, and of course my sister and best friend, Esrar. Thank you for everything you have done for me! I love you guys! v Table of Contents Chapter 1. Introduction……………………………………………………………….………1 1.1 Human Herpesviridea Overview………………………………………………….......1 1.2 HSV-1 Virion……………………………………………………..……………………...3 HSV-1 Genome………………………………………………………………………….5 HSV-1 capsid……………………………………………………………………………7 Tegument……………………………………………………………………………...…8 Envelope……………………………………………………………………………...….8 1.3 HSV-1 pathogenesis and Life cycle overview………………………………………..9 1.4 HSV-1 DNA replication proteins……………..…………………………….…….12 A. Single strand DNA binding protein, ICP8…………………………………….…..12 Overview…………………………………………………………………………….12 ICP8 structure……………………………………………………………………....13 ssDNA binding and cooperativity…………………………………………………14 ICP8 filaments………………………………………………………………………16 B. UL9, origin-binding protein…………………………………………………………17 ICP8-UL9 interaction……………………………………………………………….18 C. UL5/8/52 Helicase-primase complex……………………………………………..19 ICP8-UL5/8/52 interaction………………………………………………………....20 D. UL30/42 DNA Polymerase Holoenzyme…………………………………………20 ICP8-UL30/42 interaction………………………………...………………………..21 1.5 Model for DNA replication………………….…………………………………………22 Initiation phase of DNA Replication………………………………………………23 vi Elongation phase of DNA replication……………………………………………..24 1.6 Replication Compartment Formation………………………………………………..25 1.7 Thesis Objectives……………………………………………………………………...28 Chapter 2. Material and Methods………………………………………………………….30 2.1 Cell culture and viruses……………………………………………………………….30 2.2 DNA constructs and mutagenesis…………………………………………………...30 2.3 Protein purification…………………………………………………………………….31 2.4 Electron microscopy…………………………………………………………………..32 2.5 Immunofluorescence (IF) analysis…………………………………………………..33 2.6 Transient complementation assays………………………………………………….33 2.7 Plaque reduction assay……………………………………………………………….34 2.8 ssDNA binding assay………………………………………………………………….34 2.9 Transfection assay…………………………………………………………………….35 2.10 Surface plasmon resonance (SPR)………………………………………………..35 2.11 Prediction of protein interaction sites………………………………………………36 Chapter 3. ICP8 Filament Formation is Essential for Replication Compartment Formation During Herpes Simplex Virus Infection…………………………………....37 Abstract…………………………………………………………………………………….38 Introduction…….…...…………………………………………………………………......39 vii Results………………………………………………………….……………………………...42 The FNF and FW motifs of ICP8 are required for filament formation………….42 ICP8 mutants that fail to form filaments are unable to complement the growth of an ICP8-null virus………………………………………………………………..…..44 FW and FNF exhibit a trans-dominant phenotype……………………..…………46 Mutant proteins retain ability to bind ss DNA with reduced cooperativity……...50 ICP8 mutants defective in filament formation are unable to generate replication compartments and PRS-like foci……………………………….…………………..52 HSV-1 helicase primase complex (UL5/8/52) interacts with ICP8 mutants.......55 Discussion………………………………………………..……………………….……….57 Chapter 4 -ICP8 Mutant Q706A-F707A Can Assemble Pre-replicative Like Site Although Fails to Form Replication Compartments……………………………….…..61 Abstract…………...………………..………………………………………………………62
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