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1.4. Shear-Stress Sensing of Vascular Endothelial Cells

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1.4. Shear-Stress Sensing of Vascular Endothelial Cells Mechanisms of Ca2+ entry and mechanical sensation in the vasculature Bing Hou Submitted in accordance with the requirements for the Degree of Doctor of Philosophy The University of Leeds School of Biomedical Sciences September 2014 Funded by CSC and the University of Leeds The candidate confirms that the work submitted is his own and that appropriate credit has been given where reference has been made to the work of others. This copy has been submitted on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. 2 Acknowledgements I would like to express my sincerest gratitude to my supervisor Professor David Beech for all his support and guidance throughout my PhD. I came as a foreigner with English as my second language. However with his patience and help, I quickly found my feet and have learnt a great amount over the last 4 years. I am really grateful for his understanding and backing up during my PhD. I have really enjoyed my life at Leeds, and have been feeling proud to be a member in the Beech lab. I would also like to thank my co-supervisor Dr. Lin- Hua Jiang and my assessor Prof. Asipu Sivaprasadarao for all their assistance throughout my PhD. I have learnt a lot from all of the Beech lab members who helped and supported during my PhD, for which I am really grateful. I would like to express my special thanks to Jing, who not only taught me many experimental techniques but also helped me a lot in my life. Also special thanks to Sarka Tumova for teaching me all about Western blotting and the proofreading of my thesis, and to Lynn and Amer for teaching me immunostaining and Ca2+ imaging. I would also like to thank all my good friends for their friendship and support. I would like to thank China Scholarship Council, the University of Leeds, and the Beech lab for funding my PhD study. Especially, I would like to thank my mum and dad for their love and support through my life. I would like to express a huge thank you to my wonderful wife Xin, who has been looking after our 1-year-old son, Chenbei, by herself. I want to thank her for her supports, encouragement and love throughout. Thanks are also to my lovely son, Chenbei, for bringing me so much happiness. Finally, a special thanks to my late grandfather. He was always so proud of me. I hope I am still making him proud. 3 Abstract Both Ca2+ entry and shear stress sensation of vascular cells play important roles not only in vascular physiology, but also pathology. Therefore, understanding the mechanism of these processes could greatly help the therapeutic strategies to treat vascular diseases like atherosclerosis. The overall aim of this research was to develop a better understanding of molecular mechanisms of Ca2+ entry and shear stress sensation in the vasculature. Transient Receptor Potential Canonical (TRPC) proteins assemble to form channels for calcium and sodium ion entry. TRPC5 readily forms functional homomers, whereas TRPC1 forms functional heteromers with TRPC5 but has weak or no channel function on its own. In this study, impact of cholesterol on these proteins was investigated, because it is an important membrane constituent and driver of cardiovascular and other diseases. I found that TRPC5-mediated calcium entry is suppressed by cholesterol due to internalization of TRPC5 via the caveolin-1-dependent retraction mechanism but that TRPC1 prevents the internalization by heteromerising with TRPC5 and causing segregation to a membrane raft rich in GM1 ganglioside and dissociated from caveolin-1. Endogenous TRPC5 containing channels of vascular smooth muscle cells are stimulated by exogenous GM1 gangliosides and resistant to inhibition by cholesterol. The data suggest that a previously unrecognized purpose of incorporating a subunit in a heteromer is to segregate the protein complex to a membrane raft that is protected against cholesterol- evoked internalization. Force sensors used by endothelial cells to detect fluid shear stress are pivotal in vascular physiology and disease but there is lack of clarity about their identity. Here I show that a recently-discovered calcium-permeable channel formed by Piezo1 is important in sensing physiological shear stress and in driving a key downstream functional event. Calcium influx evoked by physiological shear stress depended on endogenous Piezo1. Exogenous Piezo1 confers sensitivity to shear stress on otherwise resistant cells. Real-time subcellular tracking 4 studies showed accumulation of Piezo1 at the endothelial cell leading edge. Depletion of endogenous Piezo1 prevented endothelial cell alignment to shear stress. Calpain activation and focal adhesion is the mechanism of Piezo1- dependent alignment of endothelial cells to shear stress. Piezo1 also crosstalks with CD31, which is a component of a known shear stress sensory complex. The data suggest that Piezo1 has the dual function of sensing physiological shear stress and driving downstream endothelial cell alignment through calcium ion entry and a calpain-focal adhesion mechanism. Alignment of endothelial cells has major roles in physiology and various disease processes which include protection against atherosclerosis. In summary, this research has generated new knowledge and hypotheses about molecular mechanism of Ca2+ entry and mechanical sensation of vascular cells under physiological and pathological conditions, which may help generate new strategies to treat cardiovascular diseases such as atherosclerosis. 5 Table of Contents Acknowledgements .......................................................................................... 2 Abstract ............................................................................................................. 3 Table of Contents .............................................................................................. 5 List of Figures ................................................................................................... 9 List of Tables ................................................................................................... 12 List of Abbreviations ...................................................................................... 13 Publications and Communications ............................................................... 16 Chapter 1. Introduction .................................................................................. 18 1.1. Cardiovascular system............................................................................18 1.2. Cardiovascular disease: Atherosclerosis................................................19 1.2.1. Pathogenesis of atherosclerosis ...................................................... 20 1.2.2. Ca2+ in atherosclerosis ..................................................................... 23 1.2.3. Shear stress in atherosclerosis ........................................................ 23 1.3. Ca2+ signalling in the vascular system....................................................24 1.3.1. Ca2+ entry mechanism ..................................................................... 27 1.3.2. Intracellular Ca2+ release and uptake mechanisms .......................... 31 1.3.3. Ca2+ extrusion mechanism ............................................................. 32 1.3.4. TRP Channels ................................................................................. 34 1.4. Shear-stress sensing of vascular endothelial cells..................................39 1.4.1. Ion Channels in shear stress sensing .............................................. 41 1.4.2. CD31/VE-cadherin/VEGFR2 mechanosensory complex ................. 43 1.4.3. Integrins ........................................................................................... 44 1.4.4. Caveolae ......................................................................................... 45 1.4.5. G proteins and GPCRs .................................................................... 45 1.4.6. The Glycocalyx ................................................................................ 46 1.4.7. The Cytoskeleton ............................................................................. 46 1.5. Aims of the study.....................................................................................48 Chapter 2. Materials and Methods ................................................................. 49 2.1. Cells........................................................................................................49 6 2.2. Ionic solutions..........................................................................................50 2.3. Reagents and chemicals.........................................................................51 2.4. Cell culture..............................................................................................53 2.5. Cell transfection.......................................................................................54 2.5.1. LipofectamineTM 2000 ...................................................................... 54 2.5.2. FuGene HD transfection reagent ..................................................... 54 2.5.3. NucleofectorTM ................................................................................. 55 2.5.4. DNA constructs ................................................................................ 55 2.5.5. Short interfering (si) RNAs ............................................................... 56 2.6. Membrane cholesterol depletion and loading..........................................56
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