Kinetochores prevent repair of UV damage in Saccharomyces cerevisiae centromeres
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1 Research Collection Doctoral Thesis Kinetochores prevent repair of UV damage in Saccharomyces cerevisiae centromeres Author(s): Capiaghi, Christoph Othmar Publication Date: 2006 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 DISS. ETH NO KINETOCHORES PREVENT REPAIR OF UV DAMAGE IN SACCHAROMYCES CEREVISIAE CENTROMERES A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH (ETH ZURICH) for the degree of Doctor of Natural Sciences presented by CHRISTOPH OTHMAR CAPIAGHI Dipl. Natw. ETH, ETH Zürich born April 16, 1975 citizen of Uznach, SG accepted on the recommendation of Prof. Dr. Fritz Thoma, examiner Prof. Dr. Ueli Suter, co-examiner Prof. Dr. Josef Jiricny, co-examiner 2006
3 Summary Chromatin is the complex of DNA and proteins, in which the genetic material is packaged inside the nucleus. A specialized chromatin structure, termed kinetochore, is required for accurate segregation of chromosomes. The kinetochore contains centromeric DNA and proteins, which are required for the attachment of the spindle microtubules to the chromosomes. In Saccharomyces cerevisiae, the centromeric sequence is about 125 bp long and very short compared with the several Mbp long centromeres of higher eukaryotes. Mutations in the centromeric DNA and centromere associated proteins may result in chromosome instability and missegregation. In living cells, DNA is continuously damaged by intra- and extracellular DNAdamaging agents. DNA-lesions may affect cell cycle progression, block transcription and replication, and eventually lead to cell death, mutations and cancer. Cyclobutane pyrimidine dimers (CPDs) and pyrimidine (6-4) pyrimidone photoproducts (6-4-PPs) are two major classes of stable DNA-lesions generated by ultraviolet (UV) light. In yeast, those UV lesions are repaired by nucleotide excision repair (NER), a ubiquitous multienzyme pathway, or by CPD-specifi c photolyase in a light-dependent reaction (photoreactivation, PR). Since UV lesions can disrupt protein-dna interactions, DNAlesions in centromeric DNA represent a unique type of damage, as loss of function could result in catastrophic loss of the genetic material of an entire chromosome. We investigated how UV lesions are repaired in yeast centromeres. A suspension of cells was irradiated with UV light (254 nm) and incubated in the dark for NER or exposed to photoreactivating light (366 nm) for DNA repair by photolyase. DNA was purifi ed, cut at CPDs by T4-endonucleaseV and the cutting sites were measured in the centromere and fl anking regions. We show that yeast centromeres are heavily resistant to the removal of UV-induced DNA-lesions by both photolyase and nucleotide excision repair. Repair resistance persists in G1- and G2/M-arrested cells. Effi cient repair was obtained only by disruption of the kinetochore structure in a ndc10-1 mutant, but not in cse4-1 and cbf1 mutants. Thus, UV lesions do not appear to disrupt protein-dna interactions in the centromere. Maintaining a stable kinetochore structure seems to be more important for the cell than an immediate removal of DNAlesions. Structural models of yeast kinetochores were based on the observation of low 7
4 resolution footprints that varied from 150 to 250 bp. To address this topic in detail with a different approach, we applied UV photofootprinting and DNA repair footprinting at nucleotide resolution. Our results show that centromere proteins cover about 120 bp of the centromere elements CDEII and CDEIII, including 20 bp of the fl anking CDEIII, which is consistent with a very small and tight kinetochore structure. Additional experiments with UV doses from 5 to 150 J/m 2 indicate that at a low UV dose, a fraction of cells overcomes the damage-induced cell cycle arrest and resumes proliferation. A reduction of CPDs observed under those conditions suggests that centromeres may be repaired by postreplication repair pathways. The major results of this work were published in Capiaghi, C., T.V. Ho, and F. Thoma Kinetochores Prevent Repair of UV Damage in Saccharomyces cerevisiae Centromeres. Mol Cell Biol 24:
5 Zusammenfassung Chromatin ist die organisierte und verpackte Form der DNA im Zellkern. Die DNA liegt als Komplex mit Histon und Nicht-Histon Proteinen vor. Eine spezialisierte Struktur des Chromatins ist das Kinetochor, welches für die fehlerfreie Trennung von Chromosomen benötigt wird. Das Kinetochor, das aus Zentromer-DNA und Proteinen besteht, gewährleistet die Bindung der Spindelmikrotubuli an das Chromosom. In Saccharomyces cerevisiae ist die Zentromer-DNA ungefähr 125 bp lang und verglichen mit den mehreren Mbp langen Zentromeren der höheren Eukaryoten sehr kurz. Mutationen in der Zentromer-DNA oder in Zentromer-assoziierten Proteinen führen zu Chromosomeninstabilität und zu Misssegregation. In lebenden Zellen wird die DNA fortlaufend durch intra- und extrazelluläre Ereignisse geschädigt. DNA-Schäden hemmen den Zellzyklusverlauf, die Transkription und die Replikation und können schliesslich zu Zelltod, zu Mutationen und zu Krebs führen. UV Licht erzeugt hauptsächlich zwei Klassen von stabilen DNA-Schäden: Cyclobutan Pyrimidin Dimere (CPD) und Pyrimidin (6-4) Pyrimidon Photoprodukte. In Hefe werden diese UV-Schäden durch ein Multienzymreparaturweg (Nukleotid Exzisions Reparatur; NER), oder durch CPD-spezifi sche Photolyase in einer lichtabhängigen Reaktion (Photoreaktivierung; PR) repariert. UV-Schäden können die Wechselwirkung von Protein-DNA-Komplexen unterbrechen. Daher könnten UV- Schäden im Zentromer zu einem katastrophalen Verlust eines ganzen Chromosoms führen. In dieser Arbeit wurde die Reparatur von UV-Schäden durch NER und Photolyase in der Zentromer-DNA der Hefe Saccharomyces cerevisiae untersucht. Für die Schadensinduktion wurde eine Suspension von Hefezellen mit 150J/m 2 UV-Licht (254nm) bestrahlt. Zur anschliessenden NER Messung wurden die Proben nach der Bestrahlung im Dunkeln inkubiert. Um die Reparatur durch Photolyase zu erfassen, wurden die Hefezellen nach der UV Bestrahlung im Photoreaktivierungslicht (366nm) exponiert. Danach wurde die DNA isoliert und die CPDs mit T4-endonucleaseV geschnitten. Mittels indirektem Endlabeling könnten die CPDs im Zentromer der Chromosomen 3, 6 und 14 analysiert werden. PR, NER sowie PR mit NER zeigten eine starke Inhibition der Reparatur im Zentromer. Die Hemmung der Reparatur im Zentromer war auch in G1- und in G2/M-arretierten Zellen ersichtlich. Effi ziente 9
6 Reparatur wurde nur in der ndc10-1 Mutante, die ein zerstörtes Kinetochor aufweisen, beobachtet, aber nicht in cse4-1 und cbf1 Mutanten. Folglich scheinen UV- Schäden im Zentromer die Wechselwirkung zwischen DNA und Proteinen nicht zu beeinträchtigen. Daher erscheint eine stabile Kinetochorestruktur für die Hefezellen wichtiger zu sein, als die Reparatur von UV-Schäden im Zentromer. Strukturmodelle des Hefekinetochors basieren auf Beobachtungen von Chromatinfootprints mit geringer Aufl ösung, welche von 150 bis 250 bp variieren. Um dieses Problem genauer anzuschauen, verwendeten wir UV-Photofootprints und DNA- Reparaturfootprints mit einer Aufl ösung im Nukleotid Bereich. Unsere Resultate zeigten, dass Zentromer-Proteine 120 bp der Zentromer Elemente CDEII, CDEIII und 20 bp der fl ankierenden Region des CDEIII bedecken. Diese Ergebnisse stimmen mit einer kleinen Kinetochorstruktur überein. Zusätzliche Experimente mit UV dosen von 5 bis 150 J/m 2 zeigten, dass mit niedriger UV-Dosis ein Teil der Zellen den Schäden-induzierten Zellzyklushalt überwinden und die Zellteilung fortsetzten. Die Verminderung von CPDs im Zentromer unter diesen Umständen suggeriert, dass UV-Schäden im Zentromer mittels postreplikativer Reparaturwege überwunden werden könnten. 10
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