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Characterization of Microtubule Organizing Center Associated Proteins in Aspergillus Nidulans

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Characterization of Microtubule Organizing Center Associated Proteins in Aspergillus Nidulans Characterization of microtubule organizing center associated proteins in Aspergillus nidulans Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT) - Universitätsbereich genehmigte DISSERTATION von Ying Zhang aus Weifang, China Dekan: Prof. Dr. Peter Roesky Referent: Prof. Dr. Reinhard Fischer Korreferent: Prof. Dr. Peter Nick Tag der mündlichen Prüfung: 18.12.2015 Erklärung Ich erkläre, dass ich die Doktorarbeit selbständig angefertigt und keine anderen als die angegebenen Quellen und Hilfsmittel benutzt sowie die wörtlich oder inhaltlich übernommenen Stellen als solche kenntlich gemacht und die Satzung des Karlsruher Institut für Technologie (KIT) zur Sicherung guter wissenschaftlicher Praxis in der jeweils gültigen Fassung beachtet hat. Karlsruhe, den 3.11.2015 ___________________ Ying Zhang Publikationsliste Im Rahmen dieser Arbeit konnten folgende Publikationen angefertigt oder vorbereitet werden: Zhang, Y., Teichert, I., Kück, U. & Fischer, R. (2015). Laser capture microdissection to identify septum-associated proteins in Aspergillus nidulans. Mycologia, in revision. Zhang, Y., Schmid, M., Osmani, S. & Fischer, R. (2015). Functional analysis of a microtubule organizing center associated protein SPA18 and characterization of the different MTOCs in Aspergillus nidulans. In preparation. Weitere Publikationen, die nicht direkt mit dem Thema dieser Arbeit verknüpft sind: Cai M.*, Zhang Y.*, Hu W., Shen W., Yu Z., Zhou W., Jiang T., Zhou X. & Zhang Y. (2014). Genetically shaping morphology of the filamentous fungus Aspergillus glaucus for production of antitumor polyketide aspergiolide A. Microb Cell Fact 13, 73-83. Fang Z., Zhang Y., Cai M., Zhang J., Zhang Y. & Zhou X. (2012). Improved gene targeting frequency in marine-derived filamentous fungus Aspergillus glaucus by disrupting ligD. J Appl Genet 53, 355-362. Yu Z., Cai M., Hu W., Zhang Y., Zhou J., Zhou X. & Zhang Y. (2014). A cyclin-like protein, ClgA, regulates development in Aspergillus nidulans. Res Microbiol 165, 462-467. * Autoren haben in gleichem Maße zu der Arbeit beigetragen. Contents I Abbreviations ................................................................................................................................. 1 II Summary ......................................................................................................................................... 2 II Zusammenfassung ....................................................................................................................... 4 III Introduction .................................................................................................................................... 6 1 The microtubule cytoskeleton ................................................................................................... 6 1.1 On the role of the microtubule cytoskeleton in polar growth ................................... 6 1.2 Microtubule nucleation ........................................................................................................ 7 2 Microtubule organizing center ................................................................................................... 8 2.1 The γ-tubulin complex ......................................................................................................... 9 2.2 Targeting of γ-Tubulin complexes to multiple distinct cellular locations ............14 2.2.1 The basic MT organization system in budding yeast ......................................... 14 2.2.2 Increased complexity of MT nucleation in fission yeast ................................... 15 2.2.3 Emergence of paralogs in higher eukaryotes ...................................................... 16 2.2.4 MTOC associated proteins in A. nidulans ............................................................. 18 2.3 Non-centrosomal MTOCs ..................................................................................................18 2.3.1 Golgi apparatus ............................................................................................................ 18 2.3.2 Nuclear membrane ...................................................................................................... 19 2.3.3 Chromatin and kinetochores .................................................................................... 19 2.3.4 Microtubules branching on pre-existing MTs ....................................................... 20 2.4 The spindle pole body in budding yeast .......................................................................21 3 Aim of this work ..........................................................................................................................24 IV Results ...........................................................................................................................................26 1 Characterization of the role of ApsB at septal MTOCs .....................................................26 1.1 Deletion of apsB4.7 ...............................................................................................................26 1.2 Localization of ApsB4.7 .......................................................................................................26 1.3 The N-terminal 523 aa are functionally important ......................................................27 2 Characterization of SPA18 ........................................................................................................28 2.1 Bioinformatic analysis of SPA18 .....................................................................................28 2.2 Localization of SPA18 ........................................................................................................29 2.3 Double deletion of apsB and SPA18 ..............................................................................29 3 The interaction and interdependence between ApsB and SPA18 .................................30 3.1 Co-localization of ApsB and SPA18 ...............................................................................30 3.2 Bimolecular Fluorescence Complementation assay .................................................31 3.3 Yeast two Hybrid .................................................................................................................31 3.4 Localization of ApsB and SPA18 to different MTOCs do not completely depend on each other ..................................................................................................................................32 4 The role of ApsB and SPA18 on microtubule organization .............................................33 4.1 The ApsB/SPA18 complex is essential for sMTOC formation.................................33 4.2 The activity of SPBs and sMTOCs in the absence of ApsB or SPA18 ..................34 4.3 The number of cytoplasmic MT bundles and astral MTs in the absence of ApsB or SPA18 ..........................................................................................................................................34 4.4 Nuclear migration in the absence of ApsB or SPA18 ................................................35 5 Domain analysis of ApsB ..........................................................................................................37 5.1 The CM1 motif is responsible for recruitment of γ-TuRCs to MTOCs ...................37 5.2 ApsB targeting to multiple distinct MTOCs via the MASC domain and the SMB domain ..............................................................................................................................................37 6 Localization of ApsB and SPA18 to septa requires SPA10 .............................................40 7 Preliminarily differentiation of SPB and sMTOC ................................................................41 7.1 SepK is the ApsB receptor at SPBs ...............................................................................41 7.2 PcpA is an SPB-specific protein .....................................................................................43 7.3 A novel γ-TuRC component MztA ...................................................................................44 7.4 SPB duplication associated proteins SfiA and centrin/Cdc31 ................................44 8 The role of peroxisomes in microtubule organization ......................................................45 9 S-tag affinity purification to identify interaction partners of ApsB ...............................48 10 Laser capture microdissection and mass spectrometry to indentify septum-associated proteins ...........................................................................................................48 V Discussion ....................................................................................................................................51 1 How are ApsB and SPA18 targeted to SPBs and sMTOCs? ...........................................51 1.1 SepK is not the sole receptor of ApsB to SPBs ..........................................................51 1.2 SPA10 recruits both ApsB and SPA18 to septa ..........................................................52 1.3 Interdependence between ApsB and SPA18 ...............................................................52 2 Recruitment of γ-TuRCs to different MTOCs .......................................................................53 2.1 γ-Tubulin complexs are targeted to distinct MT nucleation
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