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The Study of Nuclear Targets of Phosphatidylinositol-3 Kinase in Lymphocytes

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The Study of Nuclear Targets of Phosphatidylinositol-3 Kinase in Lymphocytes The study of nuclear targets of Phosphatidylinositol-3 Kinase in lymphocytes Angharad Mair Shore Department of Medical Biochemistry and Immunology Wales College of Medicine Cardiff University Supervisor: Dr. Paul Brennan A dissertation submitted to Wales College of Medicine, Cardiff University in candidature for the degree of Doctor of Philosophy September 2006 UMI Number: U584146 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U584146 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 SUMMARY Pathways regulated by Phosphotidylinositide-3-kinase (PI3K) have emerged as important mediators of cell proliferation and survival. When altered, several components of this pathway have been identified to contribute towards a wide range of human malignancies. PI3K has been implicated in the development of several EBV-associated malignancies of both lymphoid and epithelial origin. These include Burkitt’s lymphoma, Hodgkin’s disease and nasopharyngeal carcinoma. Although progress has been made in dissecting the pathways regulated by PI3K, the key components contributing to lymphocyte transformation have not been fully characterised. This study sought to investigate downstream targets of PI3K in lymphocytes in order to further our understanding of the contribution of PI3K signalling to lymphocyte proliferation and survival, particularly within the context of EBV-associated B-cell lymphomas. Initial work in this study revealed that a component of the mammalian ribosome, S6-ribosomal protein, is a major target for PI3K activation in transformed lymphocytes. In order to study PI3K and EBV regulated proteins on a larger scale, the technology of two-dimensional electrophoresis (2DE) was employed. The use of 2DE in combination with a PI3K inhibitor did not allow the identification of PI3K regulated proteins. However, three EBV regulated proteins were detected in the B-lymphocyte nucleus using this technology. The technology was further developed to study the post-translational modifications of DNA bound transcription factors. This detected multiple isoforms of the cAMP-response element binding protein (CREB), signal transducers and activators of transcription 1 (STAT1) and forkhead box O (FOXO) transcription factors in the nuclei of EBV immortalized lymphocytes. More detailed analysis of the PI3K regulated pro-apoptotic transcription factor, FOXOl, revealed that this protein is downregulated in EBV positive cells at both the transcriptional and translational levels. This downregulation was shown to directly correlate with the protein expression of a known target gene activated by FOXOl, Bcl-6, and to inversely correlate with protein levels of Cyclin D2, a target transcriptionally repressed by FOXOl. Further investigations into the mechanisms by which EBV downregulates FOXOl implicated a role for two EBV encoded proteins, Latent membrane protein-1 (LMP1) and LMP2A in the downregulation of both FOXOl, and its target gene, Bcl-6. In conclusion, this work has explored the use of antibody detection and proteomic techniques for the identification and analysis of nuclear proteins and transcription factors regulated by PI3K and EBV. Together, these investigations have deepened our understanding of the molecular changes that occur in lymphocytes in response to EBV infection, and how EBV may influence malignancy. DECLARATION This work has not previously been accepted in substance for any degree and is not being concurrently submitted in canditure for any degree. Signed . (Candidate) Date ..A p J .^ .lQ 3 ...................... STATEMENT 1 This thesis is the result of my own investigations, except where otherwise stated. Other sources are acknowledged by citations giving explicit references. A bibliography is appended. Signed ................... ............(Candidate) Date .. A .V?..! Q a ).................%............ Signed (Supervisor) Date ........ ............................. STATEMENT 2 I hereby give consent for my thesis, if accepted, to be available for photocopying and for interlibrary loan, and for the title and summary to be made available to outside organisations. Signed (Candidate) Date S?r. i. 5.. / 0.7? ....................... Acknowledgements Fisrtly, I would like to sincerely thank Dr. Paul Brennan for his excellent supervision and guidance throughout the last three years. I would also like to thank Professor Martin Rowe for his help with the manuscript and for all his good advice throughout my project. I thank all members of the lab, both past and present, Mat, James, Paul White, Ciaran, Elaine, Stefan, Isabel, David and Sam, and all members of the former Section of Infection and Immunity and the department of Medical Biochemistry and Immunology for their support, and for making the department a pleasant and excellent place to work. I thanks Dr. Ian Brewis for his help and advice with the protomics work. I would also like to acknowledge Professor Eric Lam and his group at the Division of Surgery and Oncology, imperial College London, for their contribution towards the manuscript. I wish to express my gratitude towards Tenovus, the Cancer Charity, for funding this project. I extend a special thanks to my family, Mam, Dad and Rhodri, for their support in everything that I do. Diolch am bob dim, rydach chi’n werth y byd. Finally, thanks to Sam for his patience throughout the last three years, encouragement always and for keeping me happy. ABBREVIATIONS 2DE Two-dimensional electrophoresis 4E-BP 4E-binding protein AGC cAMP-dependent protein kinase A/protein kinase G/protein kinase C AIDS Acquired immune deficiency syndrome AML Acute myeloblastic leukaemia AP Activating protein APA Alkaline phosphatase assay APS Ammonium perusulphate ARMS Alveolar rhabdomyosarcomas ATF Activator-transcription factor BART BamHI-A rightward transcript Bcl-6 B-cell lymphoma-6 BCR B-cell receptor BL Burkitt’s lymphoma BSA Bovine serum albumin ^ | CAM-KII Ca /calmodulin-dependent protein kinase II CDK Cyclin dependent kinase CDKI Cyclin dependent kinase inhibitor CHD Classic Hodgkin’s disease CRE Cyclic AMP-responsive element CREB Cyclic AMP responsive element binding protein CSK-1 Casein kinase-1 CTAR C-terminal activating regions CTL Cytotoxic T-lymphocyte DLBCL Diffuse large B-cell lymphoma DMSO Dimethyl sulfoxide DNA-AP DNA-affinity precipitation DTT Dithiothreitol DYRK-1 Dual tyrosine phosphorylated regulated kinase-1 EAP Epstein-Barr virus encoded RNA associated protein EBER Epstein-Barr virus encoded RNA EBNA Epstein-Barr virus nuclear antigen EBNA-LP Epstein-Barr virus nuclear antigen- leader protein EBV Epstein-Barr virus EDTA Ethylenediaminetetra acetic acid ERK Extracellular signal-regulated protein kinase Fas-L Fas-ligand FCS Foetal calf serum FOXO Forkhead box-0 GAB Growth factor receptor-bound protein-2 associated binding protein GC Germinal centre gp Glycoprotein GRB2 Growth factor receptor-bound protein-2 GSB Gel sample buffer GSK-3 Glycogen-synthase kinase 3 HD Hodgkin’s disease HHV Human herpesvirus HIV Human immunodeficiency virus HPV Human papilloma virus HRS Hodgkin and Reed-Sternberg HTLV-1 Human T-cell leukaemia virus 1 IARC International agency for research on cancer I k B IkappaB IKK IkappaB kinase ICAM Intercellular adhesion molecule ICAT Isotope Coded Affinity Tags IMAC Immobilized metal-affinity chromatography IEF Isolelectric focusing IFN Interferon Ig Immunoglobulin IL Interleukin ILK Integrin-linked kinase IM Infectious mononucleosis IPG Immobilized pH gradient IR Internal direct repeats ITAM Immunoreceptor tyrosine-based activation motif JAK Janus kinase JNK Jun N-terminal kinase Kb Kilobasepairs KSHV Kaposi’s sarcoma-associated herpesvirus LAR Luciferase assay reagent LB Luria-Bertani LCL Lymphoblatoid cell line LCV Lymphocryptoviridae LFA Lymphocyte-function-associated antigen LMP Latent membrane protein LUR Long unique region MAPK Mitogen-activated protein kinase MAPKAP Mitogen-activated protein kinase activated protein kinase MDM2 Murine double minute-2 MESNA 2-mercaptoethansulphonate MHC Major histocompatibility complex MLL Mixed lineage leukaemia Mr Molecular weight MS Mass spectrometry mTOR Mammalian target of rapamycin NES Nuclear export signal NFkB Nuclear factor-kappa B NHL Non-Hodgkin’s lymphoma NLPHD Nodular lymphocyte predominant hodgkin’s disease NLS Nuclear localization signal NPC Nasopharyngeal carcinoma OHL Oral hairy leukoplakia OriP Origin of replication p70S6K p70 ribosomal protein-S6 kinase PARP Poly-ADP-ribose polymerase PAX Paired box PBS Phosphate buffered saline PCR Polymerase chain reaction PKA Protein kinase A PKB Protein kinase B PKC Protein kinase C PKR Protein kinase R PH Pleckstrin-homolgy PHA Phytohaemagglutanin pi Isoelectric point PI3K Phosphotidylinositol-3-kinase PIP Phosphatidylinositol-phosphate PMSF Phenylmethylsulfonyl fluoride PTEN Phosphatase and tensin homologue deleted on chromosome ten PTK Protein tyrosine kinase PTLD Post-transplant lymphoproliferative disorder PTM Post-translational modification PVDF Polyvinylidene diflouride RB
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