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STUDY of the ROLE of MUTATIONS IDENTIFIED in the M27, M36, M139, M141, and M143 ORFS of the MURINE CYTOMEGALOVIRUS (MCMV) TEMPERATURE-SENSITIVE MUTANT TSM5

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STUDY of the ROLE of MUTATIONS IDENTIFIED in the M27, M36, M139, M141, and M143 ORFS of the MURINE CYTOMEGALOVIRUS (MCMV) TEMPERATURE-SENSITIVE MUTANT TSM5 STUDY OF THE ROLE OF MUTATIONS IDENTIFIED IN THE M27, M36, m139, m141, AND m143 ORFS OF THE MURINE CYTOMEGALOVIRUS (MCMV) TEMPERATURE-SENSITIVE MUTANT TSM5 By ABDULAZIZ TAHER ALALI A thesis submitted to The University of Birmingham for the degree of DOCTOR OF PHILOSOPHY School of Biosciences The University of Birmingham February, 2011 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Summary Infection with human cytomegalovirus (HCMV) is usually asymptomatic in normally healthy individuals although about 50-85% of adults are infected during their lifetime. However, it can cause severe or fatal disease in infants and immunocompromised patients. The generation of a potent protective vaccine is a necessity to protect vulnerable people. Because of host restriction, murine cytomegalovirus (MCMV) is used as a model for HCMV to study genes involved in pathogenicity. Previously, we have generated a temperature-sensitive mutant, tsm5, which failed to replicate to detectable levels in mice. Several mutations have been identified in this mutant. In a previous study in our laboratory, a mutation (C890Y) introduced into the M70 primase gene resulted in reduced viral replication at 40ºC in vitro and the mutant was severely attenuated in vivo. Two other previously identified mutations may also contribute to this lack of replication in vivo, namely an A658S mutation in a protein expressed by the M27 ORF, which is involved in interference with interferon- signalling, and a V54I mutation in the anti-apoptotic protein expressed by the M36 ORF. Further mutations have been identified in this study using Comparative Genome Sequencing (GCS) (Roche NimbleGen). A total of 10 synonymous and 15 non- synonymous single nucleotide polymorphisms (SNPs) have been identified in tsm5 and 14 of the non-synonymous mutations were confirmed by sequencing. Among these genes are m139 (Y565X) and m141 (V195M), which have been shown to be essential for replication in macrophages but not in fibroblasts, and m143 (M232I), shown to play an important role in the inhibition of the PKR-mediated host antiviral response. In the present study, the above mentioned mutations in M27, M36, m139, m141, and m143 were introduced individually into the MCMV K181 (Perth) variant bacterial artificial chromosome (BAC) using RecE/T homologous recombination. In addition, the M27 and M36 mutations were introduced together into the wt virus BAC. An in vitro phenotypical analysis revealed that, apart from the double mutant (Mt[M27A658SM36V54I]) and the m139 (Mt[m139Y565X]) mutant, the introduced mutations in the above mentioned genes did not show a temperature sensitive phenotype in MEF cells compared to their revertants or the wt virus. The M27 and M36 single mutants and the m141 and m143 mutants also showed similar growth kinetics to wt virus in Raw 264.7 macrophages. In contrast, replication of the M27/M36 double mutant was drastically reduced in MEFs at 40ºC and in macrophages at 37ºC. Replication of the m139 mutant was slightly reduced in MEF cells at 40ºC but not in macrophages. Interestingly, the attenuated replication of the M70 (Mt[M70C890Y]) mutant, previously noted only at 40oC in MEF cells, was also observed in Raw 264.7 macrophages at 37ºC. This M70 mutation however, was unstable. In an attempt to stabilise this mutation, many synonymous mutations have been introduced into this ORF by changing codon preferences that should reduce the efficiency of gene translation but not change protein structure. Two mutant BACs were constructed in which 403 of the 964 codons were changed to codons used less optimally in mouse cells but with either cysteine (BAC[M70SO403Cys]) or tyrosine (BAC[M70SO403Tyr] ) at residue 890. Another two BAC constructs were produced with only 155 codons (at the distal third of M70 gene) changed to mouse cell suboptimal codons and with either cysteine (BAC[M70SO155Cys]) or tyrosine (BAC[M70SO155Tyr]) at residue 890. Upon transfection of these BACs into MEF cells, none produced infectious progeny viruses except BAC[M70SO155Cys] which produced mutant Mt[M70SO155Cys] virus. In vitro, Mt[M70SO155Cys] replicated similarly to its revertant and the wt MCMV K181 (Perth) variant. DEDICATION This thesis is dedicated to my father, mother and wife for their love, support and encouragement. AKNOWLEDGEMENTS I would like to thank my supervisors Dr Clive Sweet and Dr Brian Martin for their guidance and the endless support during the course of these studies and for critical proof reading of this manuscript. I would not have wished better supervisors. I would also like to thank Professor David Blackbourn and Dr Simon Chanas for useful discussions in the meetings during the project and help in resolving the RFLP problems. I would like to thank Dr Olga Timoshenko and Dr Mohammad Ahasan for introducing me to the laboratory‟s techniques, guiding me through the early stage of my project and for being such nice colleagues who were always ready to help. I thank current and past members of S105 and S104, especially Debbie, Gemma, Dan, Rasha, Rob, Mala and Crystala and from cancer Research centre, Mark Beswick and Dr Annate Patchino for providing me with the HFFF cells. It is been a great pleasure working with them. A special thanks to Prof Charles Penn and Dr Lewis Begal for their useful discussions and all the help and support. I would like also to thank Miss Jennifer Cowan for her work and efforts in our work with the HCMV. A special thanks also to my best friends Dr. Ahmad Alwaimi, Naji Al-Ibrahim Abdullah Al-Musranda and Abdullah Al-Debasi for their help and support. I would like to thank Dr Alec Redwood for providing the MCMV K181 BAC and Simon Chanas for help and advice with RFLP. I would like to thank Dr Richard Stanton for his generosity in providing the HCMV Merlin BACand Professor Ulrich Koszinowski for providing us with the mouse macrophages cells. Table of Contents CHAPTER 1: INTRODUCTION ....................................................................................... 1 1.1 THE HERPESVIRIDAE: .............................................................................................. 1 1.2 CYTOMEGALOVIRUS: .............................................................................................. 4 1.2.1 Human Cytomegalovirus: .................................................................................. 4 1.3 GENETICS OF HUMAN CYTOMEGALOVIRUS: ................................................................. 12 1.4 THE VIRUS REPLICATION CYCLE, ENTRY: .................................................................... 15 1.4.1 Regulation of gene transcription: .................................................................... 19 1.4.2 DNA replication ............................................................................................... 23 1.4.3 Virion assembly, maturation, egress: .............................................................. 24 1.5 ACTIVATION OF IMMUNE RESPONSES: ...................................................................... 29 1.5.1 Activation of innate immunity: ........................................................................ 29 1.6 CYTOMEGALOVIRUS IMMUNE EVASION: .................................................................... 35 1.6.1 Interference with the induction of interferons: ............................................... 36 1.7 CONTROL OF APOPTOSIS: ....................................................................................... 41 1.8 LATENCY AND REACTIVATION: ................................................................................. 45 1.9 ANTIVIRAL TREATMENT OF CMV ............................................................................. 46 1.10 VACCINATION AGAINST HCMV ............................................................................... 48 1.10.1 Live attenuated HCMV vaccine........................................................................ 48 1.10.2 HCMV subunit vaccines ................................................................................... 49 1.10.3 Murine Cytomegalovirus: ................................................................................ 50 1.11 MUTAGENESIS: ................................................................................................... 52 1.11.1 BAC Technology: .............................................................................................. 53 1.11.2 BAC targeted mutagenesis by Red-mediated recombination: ........................ 54 1.12 BACKGROUND OF THE STUDY: ................................................................................. 58 1.12.1 Aim of the Study: ............................................................................................. 59 CHAPTER 2: MATERIALS AND METHODS ................................................................... 61 i 2.1 MAINTENANCE OF CELL LINES .................................................................................. 61 2.1.1 Mouse embryo fibroblasts ..............................................................................
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