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The Role of Metastasis-Associated Proteins in Trophoblast Motility and Invasion

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The Role of Metastasis-Associated Proteins in Trophoblast Motility and Invasion Some pages of this thesis may have been removed for copyright restrictions. If you have discovered material in Aston Research Explorer which is unlawful e.g. breaches copyright, (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please read our Takedown policy and contact the service immediately ([email protected]) The Role of Metastasis- Associated Proteins in Trophoblast Motility and Invasion Maral Ebrahimzadeh Asl Tabrizi Doctor of Philosophy Aston University October 2020 © Maral Ebrahimzadeh Asl Tabrizi, 2020 Maral Ebrahimzadeh Asl Tabrizi asserts her moral right to be identified as the author of this thesis. This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with its author and that no quotation from the thesis and no information derived from it may be published without proper acknowledgement. The Role of Metastasis-Associated Proteins in Trophoblast Motility and Invasion Maral Ebrahimzadeh Asl Tabrizi For the degree of Doctor of Philosophy, 2020 Thesis Summary During placental development, the pathways that regulate the invasion of trophoblasts into the decidua will lead to remodelling the uterine vasculature and will eventually give rise to placenta formation. The same pathways get reactivated during cancer development and can lead to tumour cell invasion and the metastatic process. As a consequence, there are striking similarities between the behaviour of tumour cells and the trophoblasts, due to their similar gene expression pattern and protein profile and we set about to determine whether factors which have been shown to play important roles in cancer biology are also expressed and regulate trophoblast function. In this study we have focused on three different metastasis-associated proteins with well-defined roles in cancer progression, which have been closely linked with poor prognosis for cancer patients but have not been greatly studied in the context of placental development. The proteins are a small calcium-binding protein S100P, the ERM protein ezrin and the cytoskeleton- membrane linking protein, IQGAP1. After showing their expression and localisation pattern in human placental villi, we showed that these proteins are highly expressed during the earlier stages of the gestation, suggesting a potential role in early placenta development and implantation. We then studied their expression and localisation in trophoblast cell lines and primary trophoblasts. Using the trophoblast cell lines, through loss-of-function, and where relevant, gain of function studies, we showed that these three metastasis-associated proteins promote trophoblast motility and invasion. We also investigated some of the possible mechanisms that might have been involved in the mentioned pathways including changes in focal adhesions, protein localisation and phosphorylation. We have yet to investigate the underlying mechanisms that link these three proteins to trophoblast motility and invasion, and whether all or two of them work together to make these processes possible. [Keywords: placenta, S100P, ezrin, IQGAP1, focal adhesion] 1 Acknowledgements First of all, I would like to express my sincere gratitude to my first supervisor Dr Stephane Gross for letting me be a part of his lab as well as his continuous support during my research project and writing of this thesis, for his immense patience and motivation, as well as the invaluable knowledge he has impacted on me. I am also genuinely grateful for the insightful comments and encouragements of my second supervisor Prof. Asif Ahmed. I wish to express my gratitude to Dr Thamir Ismail from the University of Liverpool for making the S100P-expressing clones. I offer my appreciation to Prof. Melissa Westwood from the University of Manchester for supplying wax-embedded human placenta sections and for letting me work in their labs at Royal Manchester Children's Hospital. My gratitude goes as well to Prof. Janesh Gupta from the University of Birmingham, for providing us with human placenta samples. I also wish to thank the School of Life and Health Sciences at Aston University for awarding me with a scholarship, Charlotte Bland for kindly helping in microscopy, and Orianne Gru for helping me with my viability data, during her short stay at our lab. I thank my colleague Tara Lancaster and all past and present members of Lab MB331, who not only made my lab work time utterly pleasant but never hesitated to share their expertise generously. A big thank you to my beloved Mum and Dad for all their support, both emotionally and financially, and for making me believe in myself. To my lovely sisters Mahsa and Bita, and my dear Grandma who have always been there for me despite the distance between us, thanks a lot. Last (but certainly not least) I want to thank my best friend, soulmate and husband Mo, for putting up with me through the hard times and for sharing the happy times. 2 Contents List of publications ........................................................................................................................ 8 Abbreviations ................................................................................................................................ 9 List of Tables .............................................................................................................................. 13 List of Figures ............................................................................................................................. 15 Chapter 1. Introduction ......................................................................................................... 19 1.1. Placenta implantation .................................................................................................. 20 1.1.1. Placenta types ...................................................................................................... 20 1.1.2. Implantation ........................................................................................................ 21 1.1.3. Blastocyst formation ........................................................................................... 21 1.1.4. Placenta development .......................................................................................... 23 1.2. Cellular migration and invasion .................................................................................. 26 1.2.1. Migration ............................................................................................................. 26 1.2.2. Invasion ............................................................................................................... 29 1.3. Metastasis-associated proteins and implantation ........................................................ 30 1.3.1. Metastasis-associated proteins ............................................................................ 30 1.3.2. Tumour metastasis and implantation similarities ................................................ 32 1.3.3. Why study metastasis-associated proteins in implantation? ............................... 34 1.4. S100 family of proteins ............................................................................................... 35 1.4.1. Genetics ............................................................................................................... 35 1.4.2. Structure .............................................................................................................. 35 1.4.3. Function .............................................................................................................. 37 1.4.4. S100P .................................................................................................................. 38 1.5. ERM family of proteins .............................................................................................. 40 1.5.1. Genetics ............................................................................................................... 41 1.5.2. Structure .............................................................................................................. 41 1.5.3. Function .............................................................................................................. 43 3 1.5.4. Ezrin .................................................................................................................... 45 1.6. IQGAP family of proteins ........................................................................................... 49 1.6.1. Genetics ............................................................................................................... 49 1.6.2. Structure .............................................................................................................. 49 1.6.3. Function .............................................................................................................. 52 1.6.4. IQGAP1 .............................................................................................................. 54 1.7. Hypothesis ................................................................................................................... 58 1.7.1. Aims .................................................................................................................... 58 1.7.2. Objectives ...........................................................................................................
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