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Hélder José Martins Wlatato Mfcrotubule-ASSOCIATED Proteh KINETOCHORE FUNCTION and Spindle ASSEMBLY Instituto De Ciências

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Hélder José Martins Wlatato Mfcrotubule-ASSOCIATED Proteh KINETOCHORE FUNCTION and Spindle ASSEMBLY Instituto De Ciências Hélder José Martins Wlatato MfCROTUBULE-ASSOCIATED PROTEh KINETOCHORE FUNCTION AND SPiNDLE ASSEMBLY Instituto de Ciências Biomédicas de Abei Salazar Universidade do Porto PORTO, 2002 Hélder José Martins Maiato MICROTUBULE-ASSOCIATED PROTEINS IN KINETOCHORE FUNCTION AND SPINDLE ASSEMBLY Dissertação realizada para candidatura ao grau de Doutor em Ciências Biomédicas submetida ao Instituto de Ciências Biomédicas de Abel Salazar da Universidade do Porto Supervisor: Professor Claudio E. Sunkel, Universidade do Porto Co-Supervisor: Professor William C. Earnshaw, University of Edinburgh PORTO 2002 Dedicated to my wife and parents for their love and encouraging, to Claudio and Bill for giving me the opportunity to learn about cells, and to the memory of Theodor Boveri and Daniel Mazia, whose work has inspired me in the study of mitosis. Acknowledgements I would like to reserve this space to express my gratitude to the people that made this work possible. I start by thanking to the Gulbenkian PhD Programme in Biology and Medicine, namely to Prof. António Coutinho, for giving me and many others the opportunity to learn more about Biology and for the nobility to invest and form young scientists. Additionally, I would like to acknowledge the Programme and Fundação para a Ciência e Tecnologia for financial support during the last four years. I wish to address a very special thanks to Prof. Claudio Sunkel at the University of Porto, who always believed in this project, for allowing me to work in his lab, for giving me the freedom of experimentation and for his great encouraging and trust about my work. I would like to thank to Prof. Bill Earnshaw at the University of Edinburgh, the way he received me in his lab, for allowing me to bring my own project and for integrating me in the projects of his lab, for giving me the opportunity to learn about microscopy, and for his great influence in the way I think science. To all the people of the Sunkel and Earnshaw labs I want to share my gratitude for all the help and friendship. I wish to thank the personal involvement of Catarina Lemos and Dr. Paula Sampaio in the first part of this work, whose contribution was essential for the accurate understanding of MAST function. I also thank to John Findlay at the University of Edinburgh for technical help with EM and for his expertise about brewers, whiskeys and the real Scottish accent. To the Earnshaw lab members, I wish to thank the way they received me and made me feel at home. Among them, I must dedicate a very special thanks to Ana Carvalho, my closest friend while I was in Edinburgh, for sharing ideas, thoughts, relieves, joys, and solutions... To Dr. Conly Rieder at the Wadsworth Center, I must express my gratitude for receiving me in his lab during the last part of this work. It was a great privilege to work with someone that I personally admire and who has been a reference for me in the study of mitosis. From his lab, I thank Richard Cole, Grisel Casseis and Polla Hergert for technical help with live microscopy and EM. I would also like to thank Dr. Jason Swedlow at the University of Dundee, for receiving me in his lab and for teaching me how to study cells by 4-D restoration microscopy. I am indebt with Drs. Margarete Heck, Inke Nathke, Tim Yen, Takahiro Nagase, Kathryn Miller and Anna Akhmanova for the gift of reagents used in this work. I want to dedicate my most sincere gratitude to my parents for understanding why I had to leave and for their proud that fills up my heart. I am also proud of both of you! Finally, I thank to my wife, Marta, for your constant encouraging, for giving a sense to my dreams and for making me believe. Thank you for sharing the loneliness of the distance, the absence of our presence and the faith in our love. It had to be worthwhile and I am deeply convinced it was! The author of this Thesis declares that he was involved in the conception and execution of the experimental work, in the interpretation of the results and in the redaction of the published/submitted manuscripts or those that are currently in preparation described above, under the name of Maiato, H.: Maiato. H., Earnshaw, W.C, and Sunkel CE. Cell cycle analysis by RNAi in Drosophila tissue culture cells. (In preparation) Maiato. H„ Rieder, C.L., Swedlow, J., Cole, R.W., Sunkel, CE., and Earnshaw, W.C Human CLASP1 mediates kinetochore interactions with the plus-ends of dynamic microtubules. (Submitted) Maiato. H.. Sampaio, P., Lemos, CL., Findlay, J., Carmena, M., Earnshaw, W.C, and Sunkel, CE. (2002). MAST/Orbit has a role in microtubule-kinetochore attachment and is essential for chromosome alignment and maintenance of spindle bipolarity. J. Cell B/0/.157: 749-760. Adams, R.R., Maiato. H.. Earnshaw, W.C, and Carmena, M. (2001). Essential roles of Drosophila Inner Centromere Protein (INCENP) and Aurora B in Histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction and chromosome segregation. J. Cell Biol. 153: 865-879. Lemos, CL., Sampaio, P., Maiato. H.. Costa, M., Omel'yanchuk, L.V., Liberal, V., and Sunkel, CE. (2000). Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organisation. EMBO J., 19: 3668-3682. CONTENTS I. GENERAL INTRODUCTION 1. The Cell Cycle 1 2. Cell Cycle Regulation 1 3. Mitosis 3 4. Regulation of Mitosis 4 5. The Mitotic Apparatus 6 5.1. The Centrosome 6 5.1.1. Structure and Composition 6 5.1.2. The Centrosome Cycle 7 5.1.3. Microtubule Nucleation 9 5.2. Microtubules 11 5.2.1. Structure 11 5.2.2. Dynamics 11 5.3. MAPs and Molecular Motors 14 5.3.1. General Properties of MAPs 14 5.3.2. General Properties of Molecular Motors 14 5.3.3. Role in the Regulation of Microtubule Dynamics 15 5.4. The Mitotic Spindle 16 5.4.1. Structure 16 5.4.2. Role of MAPs and Molecular Motors in Spindle Assembly 17 5.4.3. Spindle Assembly without Centrosomes 19 5.5. The Kinetochore 20 5.5.1. Structure 20 5.5.2. Molecular Composition 20 6. Microtubule-Kinetochore Attachment 24 6.1. Properties of Kinetochore-Associated Microtubules 24 6.2. Chromosome Capture 25 6.3. Chromosome Congression and Polar Ejection Forces 26 6.4. Kinetochore Motion at the Met/Anaphase Transition 27 6.5. Role of Molecular Motors 28 6.6. Role of MAPs 30 7. The Spindle Assembly Checkpoint 31 7.1. Checkpoint Activation 31 7.2. Molecular Components 32 7.3. Checkpoint Mechanism and Kinetochore Function 33 7.4. Checkpoint Control of Anaphase Onset 35 7.5. Sister-Chromatid Separation 36 7.6. Control of Spindle Position and Exit from Mitosis 37 8. Microtubule-Plus-End-Tracking Proteins 38 8.1. CLIP and CLASP Families 3» 8.2. APCand EB1 Families 40 9. Objectives 42 II. EXPERIMENTAL WORK Chapter I. MAST is a Novel Evolutionary Conserved Protein Essential for Mitosis 1. Introduction 43 2. Results 45 2.1. Characterisation of the multiple asters (mast) Mutations 45 2.2. Molecular Cloning of the multiple asters gene 47 2.3. Evolutionary Conservation of MAST 48 3. Discussion 50 3.1. MAST is Essential for Mitosis in Drosophila 50 3.2. MAST and the Control of Mitotic Progression 51 3.3. MAST is Part of a New Family of Microtubule-Associated Proteins 52 4. Materials and Methods 53 Chapter II. MAST has a Role in Microtubule-Kinetochore Attachment and is 55 Essential for Chromosome Alignment and Spindle Bipolarity 1. Introduction 55 2. Results 56 2.1. Cell Cycle Progression after MAST RNAi 56 2.2. Organization of the Mitotic Apparatus in MAST RNAi Treated Cells 59 2.3. Characterisation of Microtubule-Kinetochore Attachment after MAST RNAi 61 2.4. Ultra-structural Analysis of MAST depleted S2 cells 62 2.5. Distribution of Zw10, Dynein and D-CLIP-190 in the absence of MAST 64 3. Discussion 66 3.1. Possible Roles for MAST in Microtubule-Kinetochore Attachment and Chromosome Congression 66 3.2. MAST Function is Required for Spindle Bipolarity 67 4. Materials and Methods 68 Chapter III. Absence of MAST Leads to an Abnormal Mitotic Exit 71 Independently of APC/Cyclosome Function 1. Introduction 71 2. Results 72 2.1. Analysis of Cell Cycle Progression after Prolonged Mitotic Block 72 2.2. Characterisation of Chromosome Behaviour after MAST RNAi 74 2.3. Characterisation of the Abnormal Mitotic Exit after MAST RNAi 76 3. Discussion 81 3.1. MAST-Depleted Cells Exit Mitosis via an APC/C Independent Pathway 81 3.2. MAST-Depleted Cells Become Polyploid after Initial Mitotic Block 82 4. Materials and Methods 83 Chapter IV. Molecular and Cellular Characterisation of CLASP1 and 85 CLASP2, Two Human Homologues of MAST 1. Introduction 85 2. Results 86 2.1. Molecular Cloning of Human CLASP1 and CLASP2 86 2.2. Sequence Analysis of Human CLASP1 and CLASP2 87 2.3. Expression Profile of CLASP 1 and CLASP2 in Human Tumour Cell Lines 89 2.4. Cellular Localization of Human CLASP1 During Mitosis 90 2.5. Cellular Localization of Human CLASP2 During Mitosis 91 3. Discussion 93 3.1. Human CLASPs Localise to Specific Mitotic Compartments 93 3.2. Possible Role for CLASPs During Mitosis 94 4. Materials and Methods 95 Chapter V. Human CLASP1 Mediates Kinetochore Interactions with Dynamic Microtubule-Plus-Ends and is Required for Mitotic Spindle Integrity 97 1. Introduction 97 2. Results 98 2.1. Cellular Localization of CLASP1 In Vivo During Mitosis and Cytokinesis 98 2.2.
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