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A Feasibility Study of Oncogene Transgenic Mice As Therapeutic Models in Cytokine Research

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A Feasibility Study of Oncogene Transgenic Mice As Therapeutic Models in Cytokine Research A feasibility study of oncogene transgenic mice as therapeutic models in cytokine research Hilary Thomas A thesis submitted for the degree of Doctor of Philosophy in the University of London September 1996 Imperial Cancer Research Fund 44 Lincoln's Inn Fields London WC2A3PX ProQuest Number: 10055883 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. uest. ProQuest 10055883 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 Abstract Transgenic mice carrying the activated rat c-neu oncogene under transcriptional control of the MMTV promoter were backcrossed to BALB/c mice, with the aim of developing a model for cancer therapy. A total of 86 of 268 transgene positive mice in the first five generations developed 93 histologically diverse tumours (median age of onset 18 months). The cumulative incidence of breast tumours at 24 months was 18%, and overall tumour incidence 31%. As well as expected c-neii expressing breast cancers, lymphomas and Harderian gland carcinomas developed. All of the mammary carcinomas, Harderian gland carcinomas and lymphomas expressed c-erb B2. Virgin mice had fewer mammary tumours than those with two litters (p= 0.006), further litters did not affect tumour incidence. Breast carcinomas metastasised to the lungs, and lymphomas were widely disseminated. The tumours showed a range of architectural patterns which resembled human breast cancers or lymphomas. This diversity was reflected in S-phase fraction and aneuploidy. Mammary tumours transplanted to nude mice showed variable responses to IFN-a and -y. A tumour transplanted to BALB/c mice responded to IL- 12. Groups of mice treated prophytactically with IFN-a and -y, and IL-2 and IL-7 from the third and fourth generations respectively were studied for tumour development. No statistically significant differences were noted between the groups except an increased incidence of B-cell lymphomas in the IL-7 treated group. There was a significant decline in transgene positivity with successive generations (X^ test for trend p<0.001) but transmission of transgene, litter number and offspring viablity was not changed in homozygotes. The diversity, histologic and biologic resemblance to human cancer suggests the model has potential for evaluating novel therapies. Genetic and environmental manipulations are underway to increase tumour incidence and decrease age of onset. Acknowledgements I now understand that the development of an animal model is a lengthy and unpredictable process. Compounded by my return to a busy clinical post in November 1994 this has resulted in the elephantine gestation of this thesis. As a result many colleagues, particularly those in the Biological Therapy Lab, have had to bear with me in a protracted process. The brunt of this has been borne by my supervisor, Fran Balkwill, who has suffered the vagaries of this study throughout and has diligently honed each chapter. Thank you for your patience and tenacity. Peter Beverley, my second supervisor, has similarly had to tolerate the endless phone messages, and all with good grace. I am grateful to them both for the careful and helpful way in which they have shaped this project. I would like to thank Professor Paul Jolicouer of the Institut de Recherches, Montreal, for his generosity in providing the founder mice to establish the colony. I am greatly indebted to a large number of ICRF staff for advice both practical and academic. At 44 LIP - Clive Dickson, Ian Hart, Pei Juan, Mike Owen, Nigel Peat, Brendan de Souza, Joyce Taylor and Richard Whelan. Particular thanks are due to Vera Fantl for her patience on my steep molecular biology learning curve. At Clare Hall a large number of staff have been involved directly and indirectly - in particular Tracey Crafton, Peter Hagger, Gary Martin and Sue Northfield for the transgenic work and Nick East and Hazel Holdsworth for the nude mice experiments. Many thanks to George Elia and his staff in the I.C.R.F. Histopathology department, to Kirtika Patel who optimised the immunohistochemistry of the lymphomas and especially to Andrew Hanby for reviewing all the tumour and normal tissue pathology as well as his photographic skills. At the I.C.R.F. Medical Statistics Unit thanks are due to Sharon Love and Joanna Hadley for carrying out all the log rank tests and a wide range of statistical advice. To Dave Lawrence and Lorraine Beach in the print room and to George Holt and Bill Bessant and their colleagues in photography. Thanks also to Richard Camplejohn and Bhavna Raikundalia in the Richard Dimbleby Department of Cancer Research at St Thomas' Hospital for help with the Flow Cytometry. To the Haematology Laboratory at Hammersmith Hospital for carrying out the Coulter counts. For making my time at the Fund such a haven from the NHS thanks are owed to my friends and colleagues in the 'BT' Lab for their help and indulgence - individually Maureen Cobbing, Bernard Davies, Sergio Dias, Manos Karteris, Sylvie de Kossodo, Thomas Leber, Robert Moore, Saleem Malik, David Miles, Rupert Negus, Michelle Relf, RoseAnn Smith, Parames Thavasu and Lynn Turner. Special thanks are owed to Frances Burke and Stuart Naylor for e-mails, Sunday evening phonecalls, and helpful references and much constructive criticism-1 owe you. I would also like to thank my parents - it is only now that I appreciate the tabula rasa which I was given as a child. Never were my choices limited by you and your encouragement and support were always in abundance. Cancer, the disease, remains a source of continuing fascination for me. A number of members of my family have experienced it and sadly most have succumbed - 1 am grateful to them and my patients, for their courage as a continual reminder of the wonder of the human condition. Finally I must thank my 'family square' - Nick, Isobel and Phoebe - without whom this thesis would not have been possible or purposeful. This thesis is dedicated to Nick, Isobel and Phoebe Abbreviations bp base pair CD Control diluent CTL cytotoxic T Lymphocytes CO Corn Oil CSF Cerebrospinal fluid DCIS Ductal carcinoma in situ DEPC Diethylpyrocarbonate DMBA 7,12-dimethylbenzanthracene DMA Deoxyribonucleic acid ECM Extracellular matrix ECOG Eastern Cooperative Oncology Group EDTA Ethylenediaminetetracetic acid EGF Epidermal gorwth Factor EGFR Epidermal Growth Factor Receptor ER Oestrogen receptor EEC Friend Leukaemia cell GIT Guanidine isothiocyanate h hours HCl Hydrochloric acid HCL Hairy cell leukaemia IC Intermediate cell IFN Interferon Igh Immunoglobulin heavy chain IL-2 lnterleukin-2 IL-7 lnterleukin-7 IL-12 lnterleukin-12 ip intraperitoneal IRF insulin regulatory factor iv intravenous k kilobase kOa kilodalton LAK Lymphokine-activated killer LC Large cell LIE Leukaemia inhibitory factor LT Lymphotoxin LTR Long Terminal Repeat MCA 3-methylcholanthrene Kg microgrammes m g milligrammes MMP Matrix metalloproteinase MMTV Murine mammary tumour virus MTD maximum tolerated dose mRNA messenger ribonucleic acid MU M egaunits NC Negative control N IH National Institutes of Health NK Natural killer OD Optical Density PC Positive control PCR Polymerase chain reaction PEM Polymorphic epithelial mucin PK protein Kinase PR Progesterone Receptor Rb Retinoblastoma protein RNA Ribonucleic acid sc subcutaneous SCID Severe Combined Immunodeficiency SDS Sodium Dodecyl Sulphate SPF Specified Pathogen Free TBE Tris Borate EDTA buffer TBS Tris buffered saline TE Tris EDTA buffer TGF Transforming growth factor TNF Tumour necrosis factor WAP Whey Acidic Protein UICC International union against cancer uv ultraviolet Table of Contents Chapter One Introduction .....................................................................................................................................14 Cancer as a multistep process ...................................................................................... 14 The Problem of Breast Cancer ...................................................................................... 14 Epidemiology .................................................................................................... 14 Aetiology and Risk factors .............................................................................14 Natural History .................................................................................................16 Pathology ........................................................................................................... 17 Staging .................................................................................................................18 M anagem ent ...................................................................................................... 18 Surgery .................................................................................................18 Radiotherapy ..................................................................................... 18 Adjuvant therapy ..............................................................................18 Hormonal Therapy-T amoxifen ......................................................19
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