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Here, we present a strategy for identification of factors affecting the maintenance of common fragile sites (CFSs), which are genomic loci that are particularly sensitive to RS and suffer from increased breakage and rearrangements in tumors. A DNA probe designed to match the high flexibility island sequence typical for the commonly expressed CFS (FRA16D) was used as specific DNA affinity bait. Proteins significantly enriched at the FRA16D fragment under normal and replication stress conditions were identified using stable isotope labeling of amino acids in cell culture-based quantitative mass spectrometry. The identified proteins interacting with the FRA16D fragment included some known CFS stabilizers, thereby validating this screening approach. Among the hits from our screen so far not implicated in CFS maintenance, we chose Xeroderma pigmentosum protein group C (XPC) for further characterization. XPC is a key factor in the DNA repair pathway known as global genomic nucleotide excision repair (GG-NER), a mechanism whose several components were enriched at the FRA16D fragment in our screen. Functional experiments revealed defective checkpoint signaling and escape of DNA replication intermediates into mitosis and the next generation of XPC-depleted cells exposed to RS. Overall, our results provide insights into an unexpected biological role of XPC in response to replication stress and document the power of proteomics-based screening strategies to elucidate mechanisms of pathophysiological significance.<\/jats:p>","DOI":"10.1021\/acs.jproteome.6b00622","type":"journal-article","created":{"date-parts":[[2016,10,30]],"date-time":"2016-10-30T11:21:04Z","timestamp":1477826464000},"page":"4505-4517","source":"Crossref","is-referenced-by-count":5,"title":["Role of DNA Repair\nFactor Xeroderma Pigmentosum Protein\nGroup C in Response to Replication Stress As Revealed by DNA Fragile\nSite Affinity Chromatography and Quantitative Proteomics"],"prefix":"10.1021","volume":"15","author":[{"given":"Lucie","family":"Beresova","sequence":"first","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]},{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Vesela","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivo","family":"Chamrad","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiri","family":"Voller","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masayuki","family":"Yamada","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomas","family":"Furst","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rene","family":"Lenobel","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarina","family":"Chroma","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan","family":"Gursky","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katerina","family":"Krizova","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Mistrik","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiri","family":"Bartek","sequence":"additional","affiliation":[{"name":"Palacky University , , ,","place":["Olomouc, Czech Republic"]},{"name":"Danish Cancer Society Research Center , ,","place":["Copenhagen, Denmark"]},{"name":"Karolinska Institute , , ,","place":["Stockholm, Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2016,10,30]]},"reference":[{"key":"2026081810434438300_cit1","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1007\/BF00272988","article-title":"DNA polymerase alpha\ninhibition by aphidicolin induces gaps and breaks at common fragile\nsites in human chromosomes","volume":"67","author":"Glover","year":"1984","journal-title":"Hum. Genet."},{"key":"2026081810434438300_cit2","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1023\/A:1014261909613","article-title":"Fragile sites\nin human and Macaca fascicularis chromosomes are breakpoints in chromosome\nevolution","volume":"10","author":"Ruiz-Herrera","year":"2002","journal-title":"Chromosome Res."},{"key":"2026081810434438300_cit3","doi-asserted-by":"publisher","first-page":"1126","DOI":"10.1016\/j.dnarep.2006.05.010","article-title":"Common fragile sites\nas targets for chromosome rearrangements","volume":"5","author":"Arlt","year":"2006","journal-title":"DNA\nRepair"},{"key":"2026081810434438300_cit4","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1073\/pnas.0708097105","article-title":"Replication stress induces tumor-like microdeletions\nin FHIT\/FRA3B","volume":"105","author":"Durkin","year":"2008","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"key":"2026081810434438300_cit5","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.canlet.2005.07.039","article-title":"The molecular basis of rare and common\nfragile sites","volume":"232","author":"Schwartz","year":"2006","journal-title":"Cancer Lett."},{"key":"2026081810434438300_cit6","doi-asserted-by":"publisher","first-page":"7143","DOI":"10.1128\/MCB.23.20.7143-7151.2003","article-title":"Molecular\nbasis of expression of\ncommon and rare fragile sites","volume":"23","author":"Zlotorynski","year":"2003","journal-title":"Mol. Cell. Biol."},{"key":"2026081810434438300_cit7","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.molcel.2007.06.012","article-title":"An AT-Rich\nsequence in human common fragile site FRA16D\ncauses fork stalling and chromosome breakage in S. cerevisiae","volume":"27","author":"Zhang","year":"2007","journal-title":"Mol. 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Cell Biol."},{"key":"2026081810434438300_cit19","first-page":"4054","article-title":"The Fragile histidine triad\/commn chromosome fragile\nsite 3B locus and repair-deficient cancers","volume":"61","author":"Turner","year":"2002","journal-title":"Cancer Res."},{"key":"2026081810434438300_cit20","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1038\/nature05327","article-title":"Oncogene-induced senescence is a\nDNA damage response\ntriggered by DNA hyper-replication","volume":"444","author":"Di\nMicco","year":"2006","journal-title":"Nature"},{"key":"2026081810434438300_cit21","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1016\/j.cell.2011.03.044","article-title":"Nucleotide deficiency\npromotes genomic instability in early stage\nof cancer development","volume":"145","author":"Bester","year":"2011","journal-title":"Cell"},{"key":"2026081810434438300_cit22","doi-asserted-by":"publisher","first-page":"864","DOI":"10.1038\/nature03482","article-title":"DNA damage\nresponse as a candidate anti-cancer barrier in early human tumorigenesis","volume":"434","author":"Bartkova","year":"2005","journal-title":"Nature"},{"key":"2026081810434438300_cit23","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1038\/nature05268","article-title":"Oncogene-induced\nsenescence is part of the tumorigenesis barrier imposed by DNA damage\ncheckpoints","volume":"444","author":"Bartkova","year":"2006","journal-title":"Nature"},{"key":"2026081810434438300_cit24","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1038\/nature03485","article-title":"Activation\nof the DNA damage checkpoint and genomic instability in human precancerous\nlesions","volume":"434","author":"Gorgoulis","year":"2005","journal-title":"Nature"},{"key":"2026081810434438300_cit25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1476-4598-12-29","article-title":"Replication\nstress induces specific enrichment of RECQ1 at common fragile site\nFRA3B and FRA16D","volume":"12","author":"Lu","year":"2013","journal-title":"Mol. 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A."},{"key":"2026081810434438300_cit28","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1101\/gr.081711.108","article-title":"A SILAC-based\nDNA protein interaction\nscreen that identifies candidate binding proteins to functional DNA\nelements","volume":"19","author":"Mittler","year":"2009","journal-title":"Genome Res."},{"key":"2026081810434438300_cit29","doi-asserted-by":"publisher","first-page":"2149","DOI":"10.1101\/gr.151878.112","article-title":"Quantitative\ninteraction screen of\ntelomeric repeat-containing RNA reveals novel TERRA regulators","volume":"23","author":"Scheibe","year":"2015","journal-title":"Genome Res."},{"key":"2026081810434438300_cit30","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1083\/jcb.200805092","article-title":"Identifying specific protein interaction\npartners using quantitative mass spectrometry and bead proteomes","volume":"183","author":"Trinkle-Mulcahy","year":"2008","journal-title":"J. Cell Biol."},{"key":"2026081810434438300_cit31","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1083\/jcb.200911091","article-title":"Quantitative\nproteomics combined with BAC TransgeneOmics reveals in vivo protein\ninteractions","volume":"189","author":"Hubner","year":"2010","journal-title":"J. Cell Biol."},{"key":"2026081810434438300_cit32","doi-asserted-by":"publisher","first-page":"4140","DOI":"10.1074\/jbc.M808174200","article-title":"HCLK2 is required\nfor activity of\nthe DNA damage response kinase ATR","volume":"284","author":"Danielsen","year":"2009","journal-title":"J. Biol.\nChem."},{"key":"2026081810434438300_cit33","doi-asserted-by":"publisher","first-page":"3406","DOI":"10.1093\/nar\/gkg595","article-title":"Mfold web\nserver for nucleic acid folding and hybridization prediction","volume":"31","author":"Zuker","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"2026081810434438300_cit34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/0471250953.bi0206s21","article-title":"Using TESS\nto predict transcription factor binding sites in DNA sequence","author":"Schug","year":"2008","journal-title":"Curr. Protoc Bioinformatics"},{"key":"2026081810434438300_cit35","doi-asserted-by":"publisher","first-page":"2856","DOI":"10.1038\/nprot.2006.468","article-title":"In-gel digestion\nfor mass spectrometric characterization of proteins and proteomes","volume":"1","author":"Shevchenko","year":"2006","journal-title":"Nat. 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Proteomics"},{"key":"2026081810434438300_cit39","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1093\/bioinformatics\/btp101","article-title":"ClueGO: a Cytoscape plug-in to decipher\nfunctionally grouped gene ontology and pathway annotation networks","volume":"25","author":"Bindea","year":"2009","journal-title":"Bioinformatics"},{"key":"2026081810434438300_cit40","doi-asserted-by":"publisher","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: a software environment for integrated models\nof biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome\nRes."},{"key":"2026081810434438300_cit41","doi-asserted-by":"publisher","first-page":"2459","DOI":"10.1101\/gad.224568.113","article-title":"ATR-Chk1-APC\/Ccdh1-dependent stabilization\nof Cdc7-ASK (Dbf4) kinase is required for DNA lesion bypass under\nreplication stress","volume":"27","author":"Yamada","year":"2013","journal-title":"Genes Dev."},{"key":"2026081810434438300_cit42","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1074\/mcp.M200025-MCP200","article-title":"Stable isotope\nlabeling\nof amino acids in cell culture, SILAC, as a simple and accurate approach\nto expression proteomics","volume":"1","author":"Ong","year":"2002","journal-title":"Mol. Cell. Proteomics"},{"key":"2026081810434438300_cit43","doi-asserted-by":"publisher","first-page":"2650","DOI":"10.1038\/nprot.2006.427","article-title":"A practical recipe\nfor stable isotope labeling by amino acids in\ncell culture (SILAC)","volume":"1","author":"Ong","year":"2007","journal-title":"Nat. Protoc."},{"key":"2026081810434438300_cit44","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1093\/nar\/gkg034","article-title":"STRING: a database of predicted functional\nassociations between proteins","volume":"31","author":"von\nMering","year":"2003","journal-title":"Nucleic acids\nRes."},{"key":"2026081810434438300_cit45","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1021\/cr040483f","article-title":"Molecular\nmechanisms of mammalian global genome nucleotide\nexcision repair","volume":"106","author":"Gillet","year":"2006","journal-title":"Chem. Rev."},{"key":"2026081810434438300_cit46","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/S1097-2765(00)80132-X","article-title":"J Xeroderma pigmentosum group C protein complex is\nthe initiator of Global Genome Nucleotide Excision repair","volume":"2","author":"Sugasawa","year":"1998","journal-title":"Mol. Cell"},{"key":"2026081810434438300_cit47","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1016\/j.cell.2005.02.035","article-title":"UV-induced\nubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase\ncomplex","volume":"121","author":"Sugasawa","year":"2005","journal-title":"Cell"},{"key":"2026081810434438300_cit48","doi-asserted-by":"publisher","first-page":"5664","DOI":"10.1128\/MCB.25.13.5664-5674.2005","article-title":"Centrin-2 stimulates\nnucleotide excision repair by interacting with xeroderma pigmentousum\ngroup C protein","volume":"25","author":"Nishi","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"2026081810434438300_cit49","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.molcel.2007.06.014","article-title":"Sealing of chromosomal\nDNA nicks\nduring nucleotide excision repair requires XRCC1 and DNA ligase III\nalpha in a cell-cycle-specific manner","volume":"27","author":"Moser","year":"2007","journal-title":"Mol.\nCell"},{"key":"2026081810434438300_cit50","doi-asserted-by":"publisher","first-page":"46906","DOI":"10.1074\/jbc.M307254200","article-title":"In vivo recruitment\nof XPC to UV induced cyclobutane pyrimidine dimers by the DDB2 gene\nproduct","volume":"278","author":"Fitch","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2026081810434438300_cit51","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/S1568-7864(01)00008-8","article-title":"A molecular mechanism\nfor DNA damage recognition by the xeroderma pigmentosum group C protein\ncomplex","volume":"1","author":"Sugasawa","year":"2002","journal-title":"DNA Repair"},{"key":"2026081810434438300_cit52","doi-asserted-by":"publisher","first-page":"653","DOI":"10.1002\/jmr.2308","article-title":"Human and yeast\nDNA damage recognition complexes bind with high affinity DNA structures\nmimicking in size transcription bubble","volume":"26","author":"Krasikova","year":"2013","journal-title":"J. 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