SPATIAL ORGANIZATION OF THE MITOTIC SPINDLE AND CHROMOSOME MOVEMENTS
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1 DISS. ETH NO SPATIAL ORGANIZATION OF THE MITOTIC SPINDLE AND CHROMOSOME MOVEMENTS A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by IVANA GASIC Graduate Molecular Biologist and Physiologist Born on Citizen of Serbia Accepted on the recommendation of Prof. Dr. Vikram Panse Prof. Dr. Patrick Meraldi Prof. Dr. Monica Gotta 2014
2 SUMMARY Mitosis is probably the most dramatic part of the cell cycle during which a dividing cell undergoes a complete structural re-arrangement: the condensed chromosomes are no longer protected by the nuclear envelope and they bind to the bipolar mitotic spindle. Numerous proteins bind to the mitotic spindle and the chromosomes to altogether coordinate chromosome alignment onto the metaphase plate and even partition between the two daughter cells in anaphase (Sharp 1934). It has been well established that the source of energy and force needed for chromosome movements during mitosis is the dynamic instability of the kinetochore-microtubules and kinetochore s microtubule depolymerizing activity (Mitchison et al. 1986; Hyman & Mitchison 1990; Grishchuk et al. 2005; Dumont et al. 2012). Based on this knowledge several models that explain chromosome movements were proposed (Hill 1985; Joglekar & Hunt 2002; Vladimirou et al. 2011; Civelekoglu-Scholey & Scholey 2010). Yet, none of the models could faithfully reproduce the pattern of chromosome movements observed in dividing cells. In fact, all those models reduce the mitotic spindle to microtubules, kinetochores and chromosomes as single units, neglecting the spatial organization of the mitotic spindle and its other numerous components. The aim of the study presented in this thesis was to elucidate how the spatial organization of the mitotic spindle contributes first to chromosome movements towards and on the spindle equator and subsequently to the two nascent daughter cells. In this thesis I show that chromosomes that are aligned on the metaphase plate undergo coordinated oscillatory motion, where neighboring chromosomes tend to move in the same direction. This coordinated movement is limited by the 5
3 motor activity of Eg5, which crosslinks neighboring kinetochore-microtubules. I further show that positioning the metaphase plate exactly in the middle of the mitotic spindle ensures symmetric partition of the cytoplasm between the two daughter cells in anaphase. Conversely, positioning every chromosome exactly in the middle of the mitotic spindle onto a narrow metaphase plate does not contribute to mitotic fidelity. Chromosome alignment, oscillations along the spindle axis and segregation into the two daughter cells, however, depend on the inner cellular environment as they are more robustly regulated in non-transformed than in transformed cells. Moreover, non-transformed cells are more tolerant to different perturbations, suggesting that the unity of all cellular components determines cellular behaviors. Finally, I show that cells have mechanisms to distinguish the attachment of chromosomes to the old and the young centrosome, which in the case of compromised chromosome segregation drives the bias in chromosome gain towards the cell that inherits the old centrosome. This bias is conserved from yeast to man and it depends on the higher stability of microtubules that emanate from the old centrosome. This difference in the stability of the microtubules also delays chromosome alignment at the half-spindle associated with the old centrosome. Together those data again suggest that information gathered from the cellular rather than subcellular context is integrated into the final chromosomal behavior. Taken together, the results of my PhD thesis reveal yet another layer of complexity in the regulation of chromosome movements during mitosis. This complexity involves communication between centrosomes, spindle microtubules, microtubule-associated proteins and chromosomes, the main goal of which is the birth of a healthy progeny. 6
4 ZUSAMMENFASSUNG Mitose ist wahrscheinlich der dramatischste Abschnitt des Zellzyklus bei dem sich die Zelle einer völligen strukturellen Umgestaltung unterzieht: die kondensierten Chromosomen sind nicht länger von der Kernhülle geschützt und binden an die bipolare mitotische Spindel. Zahlreiche Proteine binden die mitotische Spindel und die Chromosomen, um zusammen die Anordnung der Chromosomen in einer Metaphasenplatte und ihre gleichmässige Aufteilung auf die beiden Tochterzellen in Anaphase zu koordinieren (Sharp 1934). Es ist etabliert, dass die dynamische Instabilität der Kinetochor-Mikrotubuli und die Kinetochor-Mikrotubili-Depolymerisierungsaktivität die Quellen der Energie und Kraft sind, welche für die Chromosomen-bewegungen während der Mitose benötigt werden (Mitchison et al. 1986; Hyman & Mitchison 1990; Grishchuk et al. 2005; Dumont et al. 2012). Basierend auf diesem Wissen wurden mehrere Modelle, die die Chromosomenbewegungen erklären vorgeschlagen (Hill 1985; Joglekar & Hunt 2002; Vladimirou et al. 2011; Civelekoglu-Scholey & Scholey 2010). Dennoch, keines dieser Modelle kann das Muster der Chromosomenbewegungen einer sich teilenden Zellen zuverlässig darstellen. Vielmehr reduzieren alle Modelle die mitotische Spindel, Mikrotubuli, Kinetochore und Chromosomen auf Einheiten, die räumliche Organisation der mitotischen Spindel und ihrer zahlreichen Komponenten vernachlässigend. Das Ziel der vorgelegten Arbeit war es aufzuklären wie die räumliche Organisation der mitotischen Spindel erstens zur Bewegung der Chromosomen hin zum und innerhalb des Spindeläquators und folgend zu den entstehenden Tochterzellen beiträgt. In dieser Dissertation zeige ich, dass Chromosomen die in der Metaphasenplatte angeordnet sind einer koordinierten oszillatorischen Bewegung folgen, wo Nachbarchromosomen dazu tendieren sich in die gleiche Richtung zu 7
5 bewegen. Diese koordinierte Bewegung ist durch die Motoraktivität von Eg5 eingeschränkt, welche Kinetochor-Mikrotubuli-Nachbarn vernetzt. Weiterhin zeige ich, dass die Positionierung der Metaphasenplatte exakt in der Mitte der mitotischen Spindel die symmetrische Aufteilung des Zytoplasmas auf beide Tochterzellen in der Anaphase sicherstellt. Umgekehrt trägt die Positionierung der Chromosomen in der Mitte der mitotischen Spindel, in der schmalen Metaphasenplatte, nicht zur mitotischen Genauigkeit bei. Chromosomenanordnung, Oszillation entlang der Spindelachse und die Trennung in zwei Tochterzellen hängt vom inneren zellulären Milieu ab, denn diese sind in nicht-transformierten gegenüber transformierten Zellen enger reguliert. Darüber hinaus sind nicht transformierte Zellen toleranter gegenüber verschiedenen Einflüssen, was darauf hindeutet das die Einheit aller zellulären Komponenten das zelluläre Verhalten beeinflusst. Schliesslich zeige ich, dass Zellen über Mechanismen verfügen, die die Anbindung der Chromosomen an das alte oder das neue Zentrosom unterscheiden, welches im Falle einer beeinträchtigten Chromosomentrennung tendenziell zu einem Chromosomengewinn bei der Zelle mit dem alten Zentrosom führt. Dieser Trend ist von Hefe bis zum Menschen konserviert und hängt von einer höheren Stabilität der vom alten Zentrosom ausgehenden Mikrotubuli ab. Dieser Unterschied in der Mikrotubulistabilität verzögert ausserdem die Ausrichtung der Chromosomen in der mit dem alten Zentrosom assoziierten Halbspindel. Im Wesentlichen deuten diese Daten darauf hin, dass die Informationen welche aus dem zellulären weniger dem subzellulärem Kontext gewonnen werden in ein finales chromosomales Verhalten integriert werden. Zusammengefasst zeigen die Daten meiner Dissertation eine weitere Ebene der Regulation der Chromosomenbewegung während der Mitose. Diese Komplexität beinhaltet die Kommunikation zwischen Zentrosomen, Spindelmikrotubuli, mikrotubuli-assoziierten Proteinen und Chromosomen, mit dem Ziel einen gesunden Nachkommen hervorzubringen. 8
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