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Apoptosis As a Mechanism in Tri-N-Butyltin Mediated Thymocyte Cytotoxicity

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Apoptosis As a Mechanism in Tri-N-Butyltin Mediated Thymocyte Cytotoxicity Apoptosis as a mechanism in tri-n-butyltin mediated thymocyte cytotoxicity Mark Raffray Submitted to the University of London for examination for the degree of Doctor of Philosophy 1994 Toxicology Department, The School of Pharmacy, University of London, Brunswick Square, London WC IN lAX ProQuest Number: U075807 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 U075807 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 Tri-n-butyltin (TBT), an in]|)ortant environmental pollutant, is immunotoxic when administered to experimental animals. Thymic atrophy due to the depletion of cortical thymocytes has been shown to be central to this effect although the mechanism involved is currently undefined. The mode of cell death known as apoptosis has a key role in a number of physiological processes, including the regulation of the developing thymic T lynçhocyte repertoire, but can also be triggered in pathological states including toxic injury. This study investigated the effects of bis(tri-n-butyltin) oxide (TBTO) on rat thymocytes and conq>ared these findings to observations with other lymphotoxic model confounds. Exposure of thymocytes in vitro to low concentrations of TBTO resulted in delayed cell killing which bore many of the morphological and biochemical characteristics of apoptosis. Stereotypical intemucleosomal DNA cleavage preceded viabihty loss and both these processes were inhibited by intracellular Ca^"*" chelators, zinc, and agents expected to interfere with protein-DNA interactions. At tributyltin treatment levels less than an order of magnitude higher, cytolethahty by necrosis supervened. In contrast to thymocyte apoptosis caused by most other stimuli including glucocorticoids, that mediated by TBTO apparently did not require de novo protein synthesis. Thymocytes exposed to TBTO remained able to instigate apoptotic death although their ATP levels were severely depressed, indicating that the process was not dependent on fiiUy conserved cellular energetics fimction. In common with the microtubule assembly inhibitor nocodazole, tributyltin was very effective in disrupting the cellular microtuhule cytoskeleton. Though there was evidence that this effect may have been causal to nocodazole-mediated thymocyte apoptosis, a similar relationship was not apparent for TBTO. Apoptosis caused by TBTO was associated with nuclear hypodiploidy, but no overt disturbance of thymocyte cell cycle parameters occurred. In vivo studies indicated that thymocyte apoptosis contributed significantly to the cortical thymocyte deletion underlying the thymic involution provoked by administration of TBTO to immature rats. ACKNOWLEDGEMENTS This thesis is dedicated to Linda. Her love, patience and encouragement buoyed me up when a planned 'n=3' sometimes developed into 'n=33'. Luckily, her sense of humour outlasted my Invisible Man inq)ersonations. I am genuinely indebted to the many people who encouraged and assisted me during the course of this work. As a 'part-timer', I must sometimes have seemed a rather furtive figure, which given the nature of the process I was observing, may not have been entirely inappropriate: Now you see me.. .now you don't! Thanks are due to many people, but especially to the following: • Dr Gerry Cohen, my supervisor, for having sufficient faith to let me get started in the first place, and particularly for the way he always made time to enthusiastically discuss the latest riveting finding or hot new paper (sadly, these originated mainly from researchers other than myself) • Particularly to David McCarthy for microscopy sanq)le processing, expert microscopy involvements, and photography • Adrian Rodgers, whose encyclopaedic technical knowledge opened up new approaches and fixed the 'unfixable' • Fellow 'partners in crime' Adrian K, Mike, Winston, Jane, Cathy, Andy J, Phil, Michelle, Simon, Ruth, Vitor et al. ; I shall miss the scientific 'tea' club on Friday evenings. Surely you can't be serious! • Professor Andrew Wylhe and Dr Andre Penninks for making the subject area so magnetic during early discussions, and for strategic advice • Dr. Andreas Kortenkamp for further sage advice, and for not boasting about how much better his electrophoresis kit was than mine! • Roger Snowden of the MRC Toxicology Unit • Dr. Alan Crowe of the International Tin Research Institute Finally to my parents, Jean and Raff^ for their selfless devotion to the education of their three children, and for their wisdom and support whenever storm clouds gathered. The ninth visitor is life. The tenth visitor Is not usually named. Charles Causley. "The thymocyte, you see, is a large, ugly mystery to us. If you've ever studied thymocytes you'll know what I mean! Were pretty sure today that the thymocyte exists, and we have a fairly good idea of what it does whenever it's doing whatever it's supposed to be doing. Beyond that, we're really in the dark." With profiise apologies to Joseph Heller's Catch 22. CONTENTS Title page 1 Abstract 2 Acknowledgements 3 Contents 5 Abbreviations 10 Chapter 1. Introduction 12 1 INTRODUCTION 13 1.1 Modes of cell death 13 1.2 Necrosis 16 1.3 Cardinal operational aspects of apoptosis 17 1.4 Programmed cell death 18 1.5 The incidence of apoptosis and programmed cell death 19 1.6 The significance of apoptosis 24 2 MORPHOLOGICAL CHARACTERISTICS OF APOPTOSIS 25 2.1 Phase 1; early intraceUidar changes 27 2.2 Phase 2; apoptotic body formation 28 2.3 Phase 3; phagocytosis and resolution 30 3 THE MOLECULAR BIOLOGY OF APOPTOSIS 31 3.1 Regulation of apoptosis: gene level events 32 3.2 Signal transduction 35 3.3 Macromolecular synthesis 39 3.4 Chromatin organisation: relationship to DNA degradation in apoptosis 42 3.5 Nuclear enzyme involvement 43 3.6 Other aspects of the molecular biology of apoptosis 50 4 T LYMPHOCYTE ONTOGENY AND APOPTOSIS 51 4.1 The thymus; thymocytes and T cells 51 4.2 Thymocyte maturation (ontogeny) 53 4.3 Aspects of thymocyte negative selection and T cell apoptosis 55 5 CYTOTOXIC MODEL COMPOUNDS 57 5.1 Glucocorticoids 57 5.2 Divalent cation ionophores 59 5.3 Microtubule disrupting agents 60 6 TRIORGANOTINS 61 6 .1 Chemistry, physicochemical properties and apphcations 61 6.2 The growing problem of sub-mammalian ecotoxicity 62 6.3 Mammahan toxicity of the trisubstituted organotins 63 6.4 Effects of triorganotin compounds on lynq)hoid tissues and fimctions 64 7 SCOPE OF THIS THESIS 70 Chapter 2 Materials and methods 71 2.1.1 PREPARATION OF THYMOCYTES 72 2.1.2 Rationale for thymocyte derivation 72 2.1.3 Materials 72 2.1.4 Isolation media 73 2.1.5 hicubation media 73 2.1.6 Ancillary solutions 73 2.1.7 Preparation of thymocyte suspensions 74 2.1.8 Cell count 74 2.1.9 Primary cell culture 76 2.2.1 VIABILITY (DYE EXCLUSION) 76 2.2.2 Materials 77 2.2.3 Preparation of samples and determination of viability 77 2.2.4 Calculation of viability 78 2.3 CELL COUNTS 78 2.4.1 MORPHOLOGICAL STUDIES (LIGHT MICROSCOPY) 78 2.4.1.1 Resin embedded thymocyte sections 78 2.4.1.2 Materials 78 2.4.1.3 Preparation of samples 78 2.4.1.4 Sarq)le processing and staining 79 2.4.1.5 Evaluation and counting procedures 79 2.4.1.6 Calculation of the mcidence of apoptosis 79 2.4.2.1 Fluorescence microscopy 79 2.4.2.2 Materials 80 2.4.2.3 Sample preparation and visuabsation 80 2.42.4 Calculation of the incidence of apoptosis 80 2.5.1 MORPHOLOGICAL STUDIES (ELECTRON MICROSCOPY) 80 2.5.2 Materials 81 2.5.3 Preparation of samples 81 2.5.4 Sample processing 81 2.5.5 Evaluation and pbotomicrograpby 81 2.6.1 DNA FRAGMENTATION (COLORIMETRIC METHOD) 81 2.6.2 Materials 82 2.6.3 Differential centrifiigation 82 2.6.4 Assay 82 2.6.5 Calculation of results 83 2.7.1 DNA (FLUORIMETRIC METHOD) 83 2.7.2 Materials 83 2.7.3 Preparation of samples 83 2.7.4 Standards 83 2.7.5 Assay 83 2.7.6 Calculation of results 84 2.8 .1 GEL ELECTROPHORESIS 84 2.8.2 Materials 84 2.8.3 Preparation of sangles 84 2.8.4 Apparatus 85 2.8.5 Electrophoresis 85 2.8.6 Visuabsation and photography 8 6 2.9.1 PROTEIN SYNTHESIS 8 6 2.9.2 Materials 8 6 2.9.3 Assay 87 2.9.4 Calculation of results 87 2.10.1 ATP 87 2.10.2 Materials 8 8 2.10.3 Preparation of samples 8 8 2.10.4 Standards 88 2.10.5 Instrumentation 8 8 2.10.6 Assay 89 2.10.7 Calculation of results 89 2.11.1 FLOW CYTOMETRY/CYTOFLUOROGRAPHY 89 2.11.2 Materials 90 2.11.3 Preparation of samples 90 2.11.4 Instrumentation 90 2.11.5 Cytofluorimetric analysis 90 2.11.6 Data analysis 92 2.12 MICROTUBULAR CYTOSKELETON ASSESSMENT 92 2.13 IN VIVO STUDIES 92 2.14 ORGANOTIN COMPOUND PURIFICATION AND HANDLING 92 Chapter 3 Investigation of the modality and characteristics of cell killing caused by the in vitro exposure of rat thymocytes to tri-n-butyltin 93 ABSTRACT 94 3.1 INTRODUCTION 95 3.1.1 The thymocyte model of apoptosis 95 3.1.2 TBTO: An important environmental pollutant and immunotoxicant 95 3.1.3 Cytotoxic effects of TBT in vitro 96 3.1.4 Modes of toxicant-induced cell death 98 3.1.5 Aims of these studies 99 3.2 METHODS 1 0 0 3.2.1 Materials 100 3.2.2 Test compound handling 100 3.2.3 Experimental
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