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Behavioural Characteristics of the Cells Which Form Epiretinal Membranes

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Behavioural Characteristics of the Cells Which Form Epiretinal Membranes BEHAVIOURAL CHARACTERISTICS OF THE CELLS WHICH FORM EPIRETINAL MEMBRANES PENELOPE ANN HOGG, BSc. Hons. Anat., MSc. (Lend.) Department of Clinical Science, Institute of Ophthalmology, University of London, Bath Street, London EClV 9EL. A thesis presented for the degree of Doctor of Philosophy in the University of London. April 1994 ProQuest Number: U085519 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 U085519 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 Epiretinal membranes are contractile cellular proliferations that form on the surfaces of the retina after trauma or insult to the posterior segment of the eye. Key cell types involved in membrane formation are retinal glia, retinal pigment epithelia and fibroblastic cells. A bovine tissue culture test system comprising bovine retinal glia, bovine retinal pigment epithelia and bovine scleral fibroblasts was employed in a series of behavioural studies to investigate the effect of soluble mediators and cell contact on migration, settlement and proliferation of the three key cell types in membrane formation. Migration was assessed in vitro in a modified 48-well Boyden chamber, employing a standard chemoattraction assay. The migration of all three test cell types was stimulated by a glycoprotein found abundantly in epiretinal membranes (fibronectin), samples of subretinal fluid and a retinal crude extract. Cells grown from epiretinal membranes removed during surgery for retinal detachment also migrated to fibronectin. Retinal pigment epithelial cells showed less aptitude for migration to soluble stimuli in a Boyden chamber than the other two cell types and when the cell types were labelled and migrated together, the retinal pigment epithelium still migrated less than the other two cell types. Retinal pigment epithelium were also less responsive to platelet derived growth factor. Static cell settlement studies demonstrated that retinal pigment epithelial cells showed more affinity for settlement onto plastic and in the presence of soluble fibronectin, than the other two cell types but the surface of a retinal glial monolayer appeared to be a less attractive substrate than serum coated plastic for the settlement of all three cell types. Video time- lapse microscopy was employed to monitor the settlement of retinal pigment epithelium onto glial and mixed cell layers. It revealed that the settlement process, in which distinct and reproducible stages could be identified, to be one of invasion and incorporation of the test cell types into the underlying cell layer. The fibroblasts entered a glial monolayer more rapidly than the pigment epithelia but the latter after entry, provoked a wave of glial mitotic activity. The results indicated that within the confines of the test system there was interaction between the cell types, both through cell contact and remotely via soluble mediators and these affected the behavioural responses of migration, settlement and proliferation. The findings when extrapolated to epiretinal membrane formation indicated thcLÜ the glia were not a particularly good substrate for either fibroblasts or retinal pigment epithelium. The glia secreted substances attractive for the settlement of the retinal pigment epithelium and for the migration of all three cell types and media collected from cultures of retinal pigment epithelial cells was stimulatory for a whole range of activities and provoked a powerful migratory response from the fibroblasts. So that the retinal pigment epithelium though possibly not the most important cell type in epiretinal membranes have an important role in membrane formation by releasing bioactive substances which attract and modify the behaviour of other cell types. ACKNOWLEDGEMENTS I am indebted to the Royal National Institute for the Blind for their generous financial support throughout this project. Also to Professor Alec Garner of Pathology and Professor Susan Lightman of Clinical Science for kindly allowing me to use the facilities in their departments. I would also like to thank Professor Ian Grierson for his support and supervision and his advice on settlement studies and video time-lapse microscopy. Many thanks to Dr. Felicity Savage and Mrs. Eileen Robbins for instructing me in tissue culture, Mrs. Joanne Willis for teaching me the Boyden chamber migration assay and to Miss Lynda Bradford for showing me the ELISA technique. I am also grateful to all the technical staff in the Department of Pathology for their support and guidance in the day to day running of my project, especially Mr. John Peacock, Mr. Robert Alexander, Mr. Gas Sheridah, Mr. Melville Matheson, Mr. Robin Howes and Mrs. Irene Dray. My thanks go to Mr. David McLeod and Mr. Robert Cooling who provided the surgical specimens and Mr. Graham Nunn who supervised their safe collection and delivery. To Mr. David Johnson, Miss Susan Wilson and Mr. Bernie Harper of the Central Television and Photographic Services, Liverpool University for help with editing the time-lapse video microscopy material and the technical staff of Becton and Dickinson for their assistance with the flow cytometry. I would also like to thank Dr. Paul Hiscott for his advice on the clinical and pathological aspects of the project and to Dr. William Unger for reading the manuscript and making many helpful recommendations. Lastly, to Dr. Geoffry Bourne and Dr. Nelly Golarz for their support and encouragement. To my mother and father and my brother, without whose help this would not have been possible. Thank you. PUBLICATIONS ARISING FROM THE WORK CONTAINED IN THIS THESIS Savage, F.J., Day, J.E., Hogg, P. and Grierson, I., Characterisation and use of cultured retinal glial cells. Invest. Ophth. Vis. Sci., 1988, Suppl., 29, 244. Savage, F.J., Day, J.E., Hogg, P. and Grierson, I., Tissue culture of retinal glial cells. Eye, 1982, Suppl., 1, 164-179. Hogg, P. and Grierson, I., Model for the simultaneous migration of the three cell types in epiretinal membrane formation. Invest. Ophth. Vis. Sci., 1991, Suppl., 32, 767. Grierson, I., Hiscott, P., Hogg, P., Robey, H., Mazure, A., Larkin, G., Development, repair and regeneration of the retinal pigment epithelium. Eye, 1994, 8, in press. CONTENTS TITLE PAGE 1 ABSTRACT 2 ACKNOWLEDGEMENTS 4 PUBLICATIONS ARISING FROM THE WORK CONTAINED 5 IN THIS THESIS CONTENTS 6 ILLUSTRATIONS 13 LIST OF ABBREVIATIONS 23 Chapter 1. INTRODUCTION 25 1.1 Anatomy and Pathology 25 1.1.1. The Posterior Segment of the Eye 25 1.1.2. The Retina 25 1.1.3. The Vitreoretinal Interface and Vitreous 31 1.1.4. Epiretinal Membrane Formation and Proliferatiye 33 Vitreoretinopathy 1.1.5. A Comparison of Complex Epiretinal Membrane 38 Formation with Wound Healing 1.2. Cell Types found in Complex Epiretinal Membranes 39 1.2.1. Inflammatory Cells 40 1.2.2. Glial Cells 41 1.2.3. The Retinal Pigment Epithelium 42 1.2.4. Fibroblasts and Fibroblastic Cells 45 1.3. Cell Behaviour in Epiretinal Membrane Formation 48 1.3.1. Activation 49 1.3.2. Migration 49 1.3.3. Adhesion, Settlement and Invasion 55 1.3.4. Proliferation 59 1.3.5. Contraction 61 1.3.6. Synthesis 63 1.3.7. Remodelling 66 1.4. Factors Influencing Cell Behaviour in Complex 68 Epiretinal Membrane Formation 1.4.1. Direct Signalling: Cell-cell Contact 68 1.4.2. Indirect Signalling: Factors in the External 69 Environment 1.5. Aims and Purpose of Studv 77 Chapter 2. MATERIALS AND METHODS 79 2.1. Tissue Culture I; Isolation of Primary Cultures 79 2.1.1. Culture Media 79 2.1.2. Bovine Retinal Glia 79 2.1.3. Bovine Retinal Pigment Epithelium 81 2.1.4. Bovine Scleral Fibroblasts 84 2.1.5. Epiretinal Membranes 85 2.2 Tissue Culture 11; General Techniques 90 2.2.1. Subculture 90 2.2.2. Freeze Storage in Liquid Nitrogen and Thawing 90 for Regrowth 2.3. Migration 94 2.3.1. Micro Chemoattraction Assay 94 2.3.2. Chemoattractants 100 2.3.3. Zigmond Hirsch Chequerboard Analysis of the 105 Migratory response 2.3.4. Mixed Labelled Migration of the Three Cell Types 106 2.4. Cell Migration. Settlement and Proliferation 110 in the Presence of Medium Harvested from Cultures of the Bovine Test Cells 2.4.1. Preparation of Cell Conditioned Media 110 2.4.2. Migration, Settlement and Proliferation 111 2.5. Cell Settlement 113 2.5.1. Static Settlement Evaluation; Cellular Substrates 114 2.5.2. Static Settlement Evaluation: Plastic Substrates 118 2.5.3. Kinetic Evaluation of Cell Settlement onto 120 Cellular Monolayers: Video Time-Lapse Phase Contrast Microscopy 2.5.4. Presentation and Statistical Analysis of Data 122 Chapter 3. RESULTS 123 3.1. Behavioural Comparisons Relating to Relative 123 Migratory Abilitv 3.1.1. Migration of Single Cell Types: I Dose Response 123 Curves to Fibronectin 3.1.2. Migration of Single Cell Types: II Zigmond Hirsch 125 Analysis of the Migratory Response 3.1.3. Migration of the Test Cells in Mixed Populations 125 Labelled with Latex Microspheres 3.1.4. Migration of the Test Cells in Mixed Populations 135 Labelled with Carmine and Latex Beads 3.2. Behavioural Comparison of the Migration of the 142 Three Cell Tvoes to Samples of Subretinal Fluid and a Retinal Crude Extract 3.2.1. Migration to Subretinal Fluid 151 3.2.2. Migration to a Bovine Retinal Crude Extract 152 3.3. Behavioural Comparisons Relating to Migration.
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