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Integrated Strategies for Investigating Endocrine Mechanisms in Biomphalaria Glabrata As a Test Organism for Androgenic Chemical Testing

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Integrated Strategies for Investigating Endocrine Mechanisms in Biomphalaria Glabrata As a Test Organism for Androgenic Chemical Testing INTEGRATED STRATEGIES FOR INVESTIGATING ENDOCRINE MECHANISMS IN BIOMPHALARIA GLABRATA AS A TEST ORGANISM FOR ANDROGENIC CHEMICAL TESTING A thesis submitted for the degree of Doctor of Philosophy By Satwant Kaur Institute for the Environment, Health and Societies Brunel University March 2015 DECLARATION The work submitted in this thesis was conducted between 2010 and 2014 at Brunel University (Uxbridge, West London, UK). This work was carried out independently and has not been submitted for any other degree. ii Abstract Endocrine and metabolic disease or dysfunctions are of growing concern in modern societies across the globe, underlining the need for continued focus on the development of pharmaceuticals. Subsequent scientific research has revealed a trend in the increase of such abnormalities and expansion of chemical industries, highlighting concerns that these disorders may, in part, be caused by exposure to environmental pollutants. This has led to changes in legislation concerning chemicals safety testing involving an increasing number of vertebrate animal tests as a part of environmental risk assessment process, at significant financial and ethical costs. A solution that is appropriate and aligned with the three R’s (reduction, refinement and replacement) in relation to animal research is to exploit the use of small invertebrate organisms as possible replacements for mammals. In line with the above approach/solution, this thesis is based on the null hypothesis that common genes, proteins and processes in gastropod molluscs and humans underlie the response of male reproductive organs to androgenic chemicals. Using a freshwater pulmonate snail, Biomphalaria glabrata, physiological effects of two steroid androgens on the development of mollusc secondary sexual organs were studied. Furthermore, an exhaustive investigation on the mollusc nuclear receptor repertoire and reproductive type neuropeptides was conducted. This also included the study of the evolutionary degree of conservation of these genes in non-model molluscs. The results obtained suggest that the snails did not respond to, and were not affected by exposure to the androgens. These results were supported by the absence of the members of subfamily 3C of nuclear receptors, which includes some of the “vertebrate” steroid hormone targets, suggesting that this mollusc may be an inappropriate model for steroid hormone mediated mammalian endocrine function. The nuclear receptor (NR) repertoire of B. glabrata comprised of 39 nuclear receptors representing all the known subfamilies of the NR superfamily. 21 reproductive type neuropeptide genes were identified encoding precursors that are predicted to release over 124 bioactive cleavage products. The consequence of these findings is significant in the context of the development of alternative model organisms for chemical testing as well as elucidating the taxonomic scope of nuclear receptor mediated endocrine disruption. iii Acknowledgement I take this opportunity to express my sincere gratitude towards my supervisors, Professor Susan Jobling and Dr Edwin Routledge to give me the opportunity to do research in their group, for their advice, support, motivation and encouragement throughout my work, and especially for the amount of time and dedication to discuss my work and beyond. I would also like to thanks all the students and members of staff of the Institute for the Environment (now Institute of Environment, Health and Societies) for creating such a friendly and supporting environment, helpful discussions, and pieces of advice and for just being great colleagues. Alice Baynes, Tamsin Runnalls, Catherine Harris, Margaret Town, Anne Lockyer, Erin Losty, Luigi Margiotta-Casaluci, Elizabeth Nicol, Elizabeth Lawton, Adam Lynch, Graham Harris, Nicola Beresford, Safeyeh Haghani, Lourdes Lopez-Merino and Alpa Patel. In particular I would like to thank Alice Baynes and Anne Lockyer for their incessant guidance and support, day to day assistance during my practical research help with proof reading of my chapters and keeping me sane with their words of encouragement. In addition to them I would also like to thank Elizabeth Lawton, Margaret Town and Richard Evans for proof reading of my thesis chapters. I would also like to thank Richard for helping me with my sudden computational doubts. Thanks are also due to the technical staff of the animal unit (Julie, Sue and Amy and Steve) and IFE’s admin crew (Anne Smith and Sue Maddix) for making things easier. I owe my gratitude to NC3Rs for their financial support. I would also like to take this opportunity to thanks my friends and family for all the good times, laughter, seamless support and little words of encouragement. In particular my parents for providing me financial and psychological support without which this dream would have been too difficult to pursue. iv Table of contents DECLARATION ........................................................................................................................................... II ABSTRACT .................................................................................................................................................. III ACKNOWLEDGEMENT ............................................................................................................................ IV TABLE OF CONTENTS ............................................................................................................................... V LIST OF FIGURES ........................................................................................................................................ X LIST OF TABLES ..................................................................................................................................... XIII 1 CHAPTER 1: GENERAL INTRODUCTION ................................................................................... 1 1.1 ENDOCRINE DISRUPTION AND ANIMAL TESTING .................................................................................. 2 1.2 THE VERTEBRATE ENDOCRINE SYSTEM ................................................................................................. 4 1.2.1 Endocrine glands...................................................................................................................................... 6 1.2.2 Hormones..................................................................................................................................................... 7 1.2.3 Hormone synthesis .................................................................................................................................. 8 1.2.4 Hormone action ........................................................................................................................................ 9 1.3 ENDOCRINE DISRUPTOR ACTION .......................................................................................................... 11 1.4 ENDOCRINE DISRUPTOR ANIMAL TESTING PROGRAMMES ............................................................. 13 1.5 THE 3RS (REPLACEMENT, REFINEMENT AND REDUCTION OF ANIMALS IN TESTING CHEMICALS) 18 1.6 INVERTEBRATES AS REPLACEMENTS FOR VERTEBRATES IN REPRODUCTIVE TOXICITY TESTING 19 1.7 MOLLUSCS AS PROPOSED TEST SYSTEMS FOR REPRODUCTIVE ENDOCRINE DISRUPTER TESTING 23 1.8 THE GASTROPOD NEURO-ENDOCRINE SYSTEM .................................................................................. 26 1.9 CONCLUSION ............................................................................................................................................ 29 1.10 AIM OF THE THESIS ................................................................................................................................. 30 2 CHAPTER 2: INTRODUCTION TO THE TEST SPECIES, BIOMPHALARIA GLABRATA AND PRELIMINARY WORK .................................................................................................................. 31 2.1 INTRODUCTION ........................................................................................................................................ 32 2.2 GASTROPODA ........................................................................................................................................... 32 2.2.1 Prosobranch ............................................................................................................................................ 32 2.2.1.1 Test species 1- Lottia gigantea (for computational purposes) ............................................................ 34 2.2.2 Pulmonates .............................................................................................................................................. 34 2.2.2.1 Test species 2-Biomphalaria glabrata .............................................................................................................. 36 2.2.2.1.1 General Anatomy ................................................................................................................................................. 37 2.2.2.1.2 Life cycle and reproduction ............................................................................................................................ 38 2.2.2.1.3 Molecular tools to study the biology of B. glabrata ............................................................................ 40 v 2.2.2.2 Preliminary work done on test species (B. glabrata) and optimization of techniques ............ 43 2.2.2.2.1 Sexual development in B. glabrata from day of
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