Repair of UV induced DNA-lesions by photolyase in yeast S. cerevisiae at the chromatin level
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1 Research Collection Doctoral Thesis Repair of UV induced DNA-lesions by photolyase in yeast S. cerevisiae at the chromatin level Author(s): Suter, Bernhard Publication Date: 1999 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 Repair of UV Induced DNA-Lesionsby Photolyase in Yeast S. cerevisiaeat the Chromatin Level A dissertationsubmittedto the Swiss Federal Institute of Technology(ETH) Zürich For the degree of Doctor of Natural Sciences Presented by Bernhard Suter Dipl. phil. nat. Universität Bern Born February 25u\ 1970 Citizen of Schwyz, SZ Acceptedon the recommendationof Prof. Dr. Fritz Thoma, examiner Prof. Dr. FriedrichWürgler, co-examiner Prof. Dr. Ulrich Suter, co-examiner Zürich, 1999
3 ^ 1. Summary 1. Summary DNA leslons which are induced by the ultravioiet (UV) component of solar radiation interfere with biological processes like transcription and repiication and, if not repaired, can lead to cell death, mutations and cancer. Cyclobutane pyrimidine dimers (CPDs) and, to a lesser extent, 6-4 pyrimidinepyrimidone photoproducts [(6-4)PPs], are the main classes of stable UV lesions. In many organisms, UV lesions are either removed by nucleotide excision repair (NER) or by photoreactivation. NER involves many different enzymes, exerting DNA damage recognition, excision of an oligonucleotide containing the lesion, DNA synthesisand ligation. NER is faster in the transcribed Strand of active genes than in the non-transcribedstrand and in inactive genes (transcription coupled repair). Photoreactivation is a process where a Single enzyme, DNA photolyase, recognises a UV lesion and exerts repair using energy of blue light. Photolyases specific for CPDs are found in numerous microorganisms including yeast S. cerevisiae, in plants and also in animals including vertebrates. More recently, photolyases specific for (6-4)PPs were identified in several species. In eukaryotic cells, DNA is folded into nucieosomes and higher order chromatin structures. Regulatory regions are associated with regulatory proteins and active genes are occupied by transcribing polymerases. Modulation by chromatin structures was shown for the NER mechanism. The aim was to study how CPD-photolyase can recognise DNA lesions in chromatin and genes. In the first part of the thesis (published by Suter, B,, Livingstone, Z.M. and Thoma, F. (1997). EMBO J ), we analysed photoreactivation in the yeast minichromosomes YRpTRURAP and YRpCSI by the indirect endlabeling technique, which allowed direct comparison with the chromatin structure. We found a distinct modulation of DNA-repair by photolyase in chromatin. Fast repair was found in nucleosome free regions and in linker DNA, whereas nucleosomal DNA was repaired more slowly. Fast repair of CPDs by photolyase in open Promoters Supports an important biological role in the restoration of these regulatory elements. In the transcribed URA3 and HIS3 genes, photoreactivationwas fast in the nontranscribed Strand and slow in the transcribed Strand, demonstrating preferential repair of the non-transcribed Strand. Analysis of photoreactivation in the induced and repressed chromosomal GAL10 gene demonstrated that this strand-specificity is dependent on transcription (Livingstone-Zatchej, M., Meier, A., Suter, B. and Thoma, F. (1997). Nucleic Aeids Res ). Inhibition of photoreactivation in the transcribed Strand can be explained by RNA-polymeraseswhich are stalled at CPD lesions, thereby preventing access for photolyase. Fast repair in the non-transcribedstrand by photolyase complements fast repair of the transcribed Strand by NER, suggesting that the two repair pathways exert complementary roles in repair of active genes. -1-
4 1. Summary The minichromosomes YRpTRURAPand YRpCSI contain the ARS1 origin of replication,which is nucleosome free but associated with protein complexes that regulate the initiation of DNA replication in a cell cycle dependent manner. In the second part of my thesis, I analysed the role of photolyase in repair of this regulatory region and its possible interference with DNA binding complexes. DNA damage formation and repair in ARS1 were analysed at nucleotide resolution using the primer extension technique and compared with the data for NER (R. Wellinger, ETHthesis no ). CPD repair by photolyase in the ARS1 region was much faster than repair by NER, suggesting a predominant role of photoreactivationfor the removal of CPDs in ARS1. Furthermore, photoreactivation was heterogeneous within the nucleosome free region indicating that photoreactivationis affected by bound proteins. NER shows rather homogeneous repair at different Sites. The different modulation of both mechanfsms in ARS1 suggests that the sequences associated with factors are differently accessible to the Single enzyme photolyase and to the complex NER mechanism. In YRpCSI where the ARS1 region is weakly transcribed from the adjacent PET56 promoter, modulation of photoreactivationis altered compared with YRpTRURAP, where ARS1 is not transcribed. We suggest that ARS1 binding proteins may be transiently displaced by transcribing polymerases or by an altered chromatin structure. In the third part of the thesis, I analysed photoreactivation in a yeast promoter (URA3) at nucleotide resolution. CPD-repairby photolyase shows fast repair rates at all Sites in URA3 promoter region including sites for transcription factor binding and T-tracts [poly(da-dt) sequences]. However, photoreactivation in the nucleosome positions flanking the URA3 promoter showed a distinct modulation. Repair of lesions in the internal nucleosomal region was slower compared with lesions dose to the edge of the nucleosome. In contrast to NER (Wellinger, R.E. and Thoma, F. (1997). EMBO J ), photoreactivation is heterogeneous in the transcribedstrand of the URA3 gene. We suppose that photoreactivation in the transcribed Strand is affected by both transcription and chromatin structure. Besides photoreactivation, I investigated the induction of UV damage in poly(da-dt) sequences. Poly(dA-dT) sequences are upstreamelements in constitutive yeast Promoters and may exert a role in transcription by their structural properties. In vitro, T-tracts adopt an unusual structure different from normal B-DNA, which is reflected in the pattern of UV damage formation in DNA. To test whether T-tract structure exists in cellular chromatin, we compared UV damage formation in vitro and in vivo in poly(da-dt) sequences of constitutive Promoters (URA3 and DED1). Using the primer extension technique. UV damage formation at each dipyrimidinesite within poly(da-dt) sequences could be determined. UV damage patterns generated in the poly(da-dt) tracts of the URA3 and DED1 Promoters in vivo and in naked DNA were almost identical. However, when the DNA was irradiated in the presenceof 50% DMSO, which disrupts T-tract structure, the pattern of damage formation was altered. We conclude that poly(da-dt) sequences adopt T-tract structures in Iiving cells. Assuming that the T-tract structure has
5 1. Summary specific functions, it is conceivable that these functions will be affected if the structure is altered by the induction of DNA damage. Efficient photoreactivation will restore the structure of T-tracts and also their specific function. However, we found that not all T-tracts adopt the typical T-tract stucture. The UV damage pattern in one T-tract of the DED1 poly(da-dt) sequence cannot be referred to a typical T-tract structure. -3-
6 1. Zusammenfassung 1. Zusammenfassung Schäden in der DNA, die durch ultraviolettes (UV) Licht verursacht werden, stören grundlegende Lebensvorgänge wie Transkription und Replikation. Diese Schäden können, sofern sie nicht repariert werden, zu Zelltod, Mutationen und Krebs führen. Cyclobutan Pyrimidin Dimere (CPDs), und zu einem geringeren Anteil, 6-4 Pyrimidin Pyrimidon Photoprodukte f(6-4)pps] bilden die Hauptklassen der stabilen UV-Schäden. In vielen Organismen werden UV-Schäden entweder durch die Nukleotid Excisions Reparatur (NER) oder durch Photoreaktivierung entfernt. NER benotigt viele Enzyme, die an den folgenden Schritten beteiligt sind: Schadenserkennung und Ausschneiden des beschädigten Oligonukleotids, DNA Synthese und Ligation. Die Reparatur durch NER ist schneller im transkribierten Strang von aktiven Genen, als in deren nichttranskribiertem Strang oder in inaktiven Genen (Transkriptions-gekoppelteReparatur). Beim Prozess der Photoreaktivierung erkennt ein einzelnes Enzym, DNA Photolyase, einen UV-Schaden und führt anschliessend die Reparatur mit Hilfe von blauem Licht aus. Wegen ihrer hohen Effizienz ist Photoreaktivierung ein wichtiger Reparaturmechanismus von Organismen, welche dem UV-Licht ausgesetzt sind. Photolyasen, die spezifisch für CPDs sind, wurden in verschiedenen Mikroorganismen, einschliesslich S. cerevisiae, in Pflanzen, sowie auch in Tieren, einschliesslich Wirbeltieren, gefunden. Neuerdings wurden in verschiedenen Arten auch Photolyasen gefunden, die spezifisch für (6-4)PPs sind. In eukaryontischen Zellen ist die DNA in Nukleosomen und in Chromatinstrukturen höherer Ordung verpackt. Regulatorische Regionen sind assoziiert mit Proteinen und aktive Gene werden von transkribierenden Polymerasen besetzt. Es ist bereits bekannt, dass der NER-Mechanismuseiner Modulation durch Chromatinstrukturen unterliegt. Unsere Ziel war es herauszufinden, wie das Reparaturenzym Photolyase einen Schaden im Chromatin und in den Genen lebender Zellen erkennenkann. Im ersten Teil meiner Doktorarbeit (publiziert in Suter. B., Livingstone, Z.M. and Thoma, F. (1997). EMBO J ) untersuchten wir Photoreaktivierung in den Hefemini chromosomen YRpTRURAP und YRpCSI. Dabei gestattete uns die Technik der indirekten Endmarkierung einen direkten Vergleich mit der Chromatinstruktur.Wir wiesen nach, dass die Reparatur der DNA durch Photolyase im Chromatin deutlich moduliertwird. Schnelle Reparatur wurde in nukleosomenfreienregionen und in Linker-DNA gefunden, während nukleosomale DNA langsamer repariert wurde. Die schnelle Reparatur von CPDs in offenen Promotoren zeigt eine wichtige Rolle in der Wiederherstellung dieser regulatorischen Elemente. In den transkribierten URA3- und H/S3-Genen stand der schnellen Photoreaktivierung im nichttranskribierten Strang eine langsame im transkribierten Strang gegenüber. Die Untersuchung der Photoreaktivierung im induzierten und reprimierten chromosomalen GAL10-4-
7 1. Zusammenfassung Gen zeigte, dass diese Strangspezifität transkriptionsabhängig ist (Livingstone-Zatchej,M., Meier, A., Suter, B. and Thoma, F. (1997). Nucleic Aeids Res ). Die Hemmung der Photoreaktivierung im transkribierten Strang kann durch RNA-Polymerasen erklärt werden, die an einem CPD blockiert sind und so den Zugang für die Photolyase verhindern. Schnelle Reparatur durch die Photolyase im nichttransknbierten Strang ist komplementär zur schnellen Reparatur durch NER im transkribierten Strang. Dies zeigt, dass die beiden Reparaturwege ergänzende Funktionen in der Reparatur aktiver Gene ausüben. Die beiden Minichromosomen YRpTRURAPund YRpCSI enthalten als Replikationsursprung die ARS1 Sequenz. Diese ist, zwar frei von Nukleosomen, aber mit Proteinkomplexen assoziiert, welche, abhängig vom Zellzyklus, die DNA Replikation in die Wege leiten. Im zweiten Teil meiner Arbeit untersuchte ich die Rolle der Photolyase in der Reparatur dieser regulatorischen Region und ihre mögliche Behinderung durch an DNA bindende Komplexe. Dazu wurde die Bildung und die Reparatur der Schaden in ARS1 auf Nukleotidauflösung unter Verwendungder 'Primer Extension' Technik untersucht und mit den entsprechenden Daten für den NER verglichen (R. Wellinger, ETH-Diss Nr ). CPDs in der ARS1 Region wurden viel schneller durch die Photolyase als durch NER repariert, was darauf hindeutet, dass Photoreaktivierung in der Reparatur von CPDs in der ARS1 Region eine vorherrschende Stellung einnimmt. Ferner war die Photoreaktivierunginnerhalbder nukleosomenfreien Region heterogen, was auf eine Auswirkung von gebundenen Proteinen hindeutet. NER wies dagegen eine eher homogene Reparatur an verschiedenen Stellen auf. Die unterschiedlichemodulation beider Mechanismenin ARS1 legt nahe, dass die mit Faktoren assoziierte Sequenzen sich in ihrer Zugänglichkeit für die Photolyase und den komplexen NER-Mechanismusunterscheiden. In YRpCSI, wo die ARS1 Region vom anliegenden PET56 Promotoraus schwach transkribiert wird, war die Photoreaktivierung anders moduliert, als in YRpTRURAP, wo ARS1 nicht transkribiert wird. Wir vermuten, dass Proteine, welche an ARS1 binden, durch transkribierende Polymerasen vorübergehendentfernt werden könnten. Im dritten Teil untersuchte ich die Photoreaktivierung in einem Hefepromotor (URA3). Die Entfernung von CPDs durch Photolyase zeigte schnelle Reparaturraten an allen Stellen im URA3 Promotor, einschliessich der Bindungsstellen der Transkriptionsfaktorenund der 'T- Tracts' in der poly(da-dt)-sequenz.demgegenüber war die Photoreaktivierung deutlich moduliert an den Positionen der Nukleosomen, welche den URA3 Promotor flankieren. Die Reparatur war langsamer im inneren Bereich der Nukleosomen, verglichen mit den nahe am Nukleosomenende gelegenen Stellen. Die Photoreaktivierung ist, im Gegensatz zu NER (Wellinger and Thoma 1997), heterogen im transkribierten Strang des URA3 Gens. Die Daten lassen vermuten, dass die Photoreaktivierungin einem transkribierten Strang sowohl durch die Transkription, als auch durch die Chromatinstrukturbeeinflusst werden kann.
8 1. Zusammenfassung Neben der Photoreaktivierung konzentrierte ich meine Untersuchungen auf die UV- Schadensbildung in Poly(dA-dT) Sequenzen. Poly(dA-dT) Sequenzen sind regulatorische Elemente konstitutiver Hefepromotoren und beeinflussen die Transkription möglicherweise durch ihre strukturellen Eigenschaften. T-tracts' nehmen eine unübliche Struktur an, die sich von normaler B-DNA unterscheidetund sich im Muster der Schadensbildungniederschlägt. Um zu untersuchen, ob die T-tract' Struktur in der Zelle tatsächlich existiert, verglichen wir die Bildung von UV-Schäden in Poly(dA-dT) Sequenzen von konstitutiven Promotoren (URA3 und DED1)in vitro und In vivo. Mit Hilfe der 'Primer Extension' Technik konnten wir die UV- Schadensbildung an jeder Dipyrimidin-Stelle ermitteln. Die Muster der UV-Schadensbildung in den T-Tracts' der Promotoren von URA3 und DED1 sind in vivo und in nackter DNA fast identisch. Das Muster der UV-Schadensbildung war dagegen anders, wenn die DNA in 50% DMSO, was die Struktur des T-Tracts' auflöst, bestrahlt wurde. Die Daten zeigen, dass Poly(dA-dT) Sequenzen in der lebenden Zelle eine T-Tract' Struktur annehmen. Mögliche Funktionen der T-tracts', die durch ihre strukurellen Eigenschaften bedingt werden, könnten aufgehoben werden, wenn sich durch Schadensbildungdie DNA Struktur ändert. Entfernung der Schäden durch Photoreaktivierungkönnte zur Wiederherstellung der DNA Struktur und ihrer möglichen Funktionen führen. Nicht alle T-tracts' scheinen in der für T-tracts' typischen Konformation vorzuliegen.das Muster der Schadensbildungin einem bestimmten T-Tract' in der Poly(dA-dT) Sequenz des DED1 Promotors kann weder durch eine typische T-Tract' Struktur, noch durch eine Standard B-DNA erklärt werden.
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