Mph1 is a member of the conserved FANCM family of DNA motor proteins that play key roles in genome maintenance processes underlying Fanconi anemia, a cancer predisposition syndrome in humans. Here, we identify Mte1 as a novel interactor of the Mph1 helicase in Saccharomyces cerevisiae. In vitro, Mte1 (Mph1-associated telomere maintenance protein 1) binds directly to DNA with a preference for branched molecules such as D loops and fork structures. In addition, Mte1 stimulates the helicase and fork regression activities of Mph1 while inhibiting the ability of Mph1 to dissociate recombination intermediates. Deletion of MTE1 reduces crossover recombination and suppresses the sensitivity of mph1Δ mutant cells to replication stress. Mph1 and Mte1 interdependently colocalize at DNA damage-induced foci and dysfunctional telomeres, and MTE1 deletion results in elongated telomeres. Taken together, our data indicate that Mte1 plays a role in regulation of crossover recombination, response to replication stress, and telomere maintenance.

Department of Biology Masaryk University CZ 62500 Brno Czech Republic;

Department of Biology Masaryk University CZ 62500 Brno Czech Republic; National Centre for Biomolecular Research Masaryk University CZ 62500 Brno Czech Republic; International Clinical Research Center St Anne's University Hospital Brno CZ 656 91 Brno Czech Republic; Center for Biomolecular and Cellular Engineering St Anne's University Hospital Brno CZ 656 91 Brno Czech Republic;

Department of Biology University of Copenhagen DK 2200 Copenhagen N Denmark;

Department of Biology University of Copenhagen DK 2200 Copenhagen N Denmark; Center for Chromosome Stability Department of Cellular and Molecular Medicine University of Copenhagen DK 2200 Copenhagen N Denmark

Institute of Molecular Biology gGmbH 55128 Mainz Germany;

The Novo Nordisk Foundation Center for Protein Research Faculty of Health Sciences University of Copenhagen DK 2200 Copenhagen N Denmark;

Zobrazit více v PubMed

Abdallah P, Luciano P, Runge KW, Lisby M, Geli V, Gilson E, Teixeira MT. 2009. A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol 11: 988–993. PubMed PMC

Adams AK, Holm C. 1996. Specific DNA replication mutations affect telomere length in Saccharomyces cerevisiae. Mol Cell Biol 16: 4614–4620. PubMed PMC

Adams Martin A, Dionne I, Wellinger RJ, Holm C. 2000. The function of DNA polymerase α at telomeric G tails is important for telomere homeostasis. Mol Cell Biol 20: 786–796. PubMed

Adamson B, Smogorzewska A, Sigoillot FD, King RW, Elledge SJ. 2012. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat Cell Biol 14: 318–328. PubMed PMC

Askree SH, Yehuda T, Smolikov S, Gurevich R, Hawk J, Coker C, Krauskopf A, Kupiec M, McEachern MJ. 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci 101: 8658–8663. PubMed PMC

Bartsch S, Kang LE, Symington LS. 2000. RAD51 is required for the repair of plasmid double-stranded DNA gaps from either plasmid or chromosomal templates. Mol Cell Biol 20: 1194–1205. PubMed PMC

Bonetti D, Clerici M, Anbalagan S, Martina M, Lucchini G, Longhese MP. 2010. Shelterin-like proteins and Yku inhibit nucleolytic processing of Saccharomyces cerevisiae telomeres. PLoS Genet 6: e1000966. PubMed PMC

Bupp JM, Martin AE, Stensrud ES, Jaspersen SL. 2007. Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J Cell Biol 179: 845–854. PubMed PMC

Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. 2002. A monomeric red fluorescent protein. Proc Natl Acad Sci 99: 7877–7882. PubMed PMC

Carson MJ, Hartwell L. 1985. CDC17: an essential gene that prevents telomere elongation in yeast. Cell 42: 249–257. PubMed

Chamankhah M, Xiao W. 1999. Formation of the yeast Mre11–Rad50–Xrs2 complex is correlated with DNA repair and telomere maintenance. Nucleic Acids Res 27: 2072–2079. PubMed PMC

Chamankhah M, Fontanie T, Xiao W. 2000. The Saccharomyces cerevisiae mre11(ts) allele confers a separation of DNA repair and telomere maintenance functions. Genetics 155: 569–576. PubMed PMC

Chavez A, Agrawal V, Johnson FB. 2011. Homologous recombination-dependent rescue of deficiency in the structural maintenance of chromosomes (Smc) 5/6 complex. J Biol Chem 286: 5119–5125. PubMed PMC

Chen YH, Choi K, Szakal B, Arenz J, Duan X, Ye H, Branzei D, Zhao X. 2009. Interplay between the Smc5/6 complex and the Mph1 helicase in recombinational repair. Proc Natl Acad Sci 106: 21252–21257. PubMed PMC

Chen YH, Szakal B, Castellucci F, Branzei D, Zhao X. 2013. DNA damage checkpoint and recombinational repair differentially affect the replication stress tolerance of Smc6 mutants. Mol Biol Cell 24: 2431–2441. PubMed PMC

Choi K, Szakal B, Chen YH, Branzei D, Zhao X. 2010. The Smc5/6 complex and Esc2 influence multiple replication-associated recombination processes in Saccharomyces cerevisiae. Mol Biol Cell 21: 2306–2314. PubMed PMC

Choi DH, Kwon SH, Kim JH, Bae SH. 2012. Saccharomyces cerevisiae Cmr1 protein preferentially binds to UV-damaged DNA in vitro. J Microbiol 50: 112–118. PubMed

Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367–1372. PubMed

Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, Mann M. 2009. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4: 698–705. PubMed

d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature (London) 426: 194–198. PubMed

de Bruin D, Kantrow SM, Liberatore RA, Zakian VA. 2000. Telomere folding is required for the stable maintenance of telomere position effects in yeast. Mol Cell Biol 20: 7991–8000. PubMed PMC

de Bruin D, Zaman Z, Liberatore RA, Ptashne M. 2001. Telomere looping permits gene activation by a downstream UAS in yeast. Nature (London) 409: 109–113. PubMed

de Godoy LM, Olsen JV, de Souza GA, Li G, Mortensen P, Mann M. 2006. Status of complete proteome analysis by mass spectrometry: SILAC labeled yeast as a model system. Genome Biol 7: R50. PubMed PMC

Dewar JM, Lydall D. 2010. Pif1- and Exo1-dependent nucleases coordinate checkpoint activation following telomere uncapping. EMBO J 29: 4020–4034. PubMed PMC

Dewar JM, Lydall D. 2012. Similarities and differences between ‘uncapped’ telomeres and DNA double-strand breaks. Chromosoma 121: 117–130. PubMed

Duxin JP, Walter JC. 2015. What is the DNA repair defect underlying Fanconi anemia? Curr Opin Cell Biol 37: 49–60. PubMed PMC

Finkelstein J, Antony E, Hingorani MM, O'Donnell M. 2003. Overproduction and analysis of eukaryotic multiprotein complexes in Escherichia coli using a dual-vector strategy. Anal Biochem 319: 78–87. PubMed

Gallina I, Colding C, Henriksen P, Beli P, Nakamura K, Offman J, Mathiasen DP, Silva S, Hoffmann E, Groth A, et al. 2015. Cmr1/WDR76 defines a nuclear genotoxic stress body linking genome integrity and protein quality control. Nat Commun 6: 6533. PubMed PMC

Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature (London) 415: 141–147. PubMed

Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. 2003. Global analysis of protein expression in yeast. Nature (London) 425: 737–741. PubMed

Gilmore JM, Sardiu ME, Venkatesh S, Stutzman B, Peak A, Seidel CW, Workman JL, Florens L, Washburn MP. 2012. Characterization of a highly conserved histone related protein, Ydl156w, and its functional associations using quantitative proteomic analyses. Mol Cell Proteomics 11: M111.011544. PubMed PMC

Goldstein AL, McCusker JH. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553. PubMed

Goudsouzian LK, Tuzon CT, Zakian VA. 2006. S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol Cell 24: 603–610. PubMed

Gravel S, Larrivee M, Labrecque P, Wellinger RJ. 1998. Yeast Ku as a regulator of chromosomal DNA end structure. Science 280: 741–744. PubMed

Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T. 1999. Mammalian telomeres end in a large duplex loop. Cell 97: 503–514. PubMed

Hardy CF, Sussel L, Shore D. 1992. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev 6: 801–814. PubMed

Heim R, Tsien RY. 1996. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6: 178–182. PubMed

Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature (London) 415: 180–183. PubMed

Ho CK, Mazon G, Lam AF, Symington LS. 2010. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol Cell 40: 988–1000. PubMed PMC

Horigome C, Oma Y, Konishi T, Schmid R, Marcomini I, Hauer MH, Dion V, Harata M, Gasser SM. 2014. SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol Cell 55: 626–639. PubMed

Hughes TR, Weilbaecher RG, Walterscheid M, Lundblad V. 2000. Identification of the single-strand telomeric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein. Proc Natl Acad Sci 97: 6457–6462. PubMed PMC

Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. 2003. Global analysis of protein localization in budding yeast. Nature (London) 425: 686–691. PubMed

Kalocsay M, Hiller NJ, Jentsch S. 2009. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33: 335–343. PubMed

Keppler-Ross S, Noffz C, Dean N. 2008. A new purple fluorescent color marker for genetic studies in Saccharomyces cerevisiae and Candida albicans. Genetics 179: 705–710. PubMed PMC

Khadaroo B, Teixeira MT, Luciano P, Eckert-Boulet N, Germann SM, Simon MN, Gallina I, Abdallah P, Gilson E, Geli V, et al. 2009. The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat Cell Biol 11: 980–987. PubMed

Khmelinskii A, Keller PJ, Bartosik A, Meurer M, Barry JD, Mardin BR, Kaufmann A, Trautmann S, Wachsmuth M, Pereira G, et al. 2012. Tandem fluorescent protein timers for in vivo analysis of protein dynamics. Nat Biotechnol 30: 708–714. PubMed

Kucejova B, Foury F. 2003. Search for protein partners of mitochondrial single-stranded DNA-binding protein Rim1p using a yeast two-hybrid system. Folia Microbiol (Praha) 48: 183–188. PubMed

Le S, Moore JK, Haber JE, Greider CW. 1999. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152: 143–152. PubMed PMC

Lin JJ, Zakian VA. 1996. The Saccharomyces CDC13 protein is a single-strand TG1–3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proc Natl Acad Sci 93: 13760–13765. PubMed PMC

Lin YH, Chang CC, Wong CW, Teng SC. 2009. Recruitment of Rad51 and Rad52 to short telomeres triggers a Mec1-mediated hypersensitivity to double-stranded DNA breaks in senescent budding yeast. PLoS One 4: e8224. PubMed PMC

Lisby M, Geli V. 2009. DNA damage response to eroded telomeres. Cell Cycle 8: 3617–3618. PubMed

Lisby M, Rothstein R. 2015. Cell biology of mitotic recombination. Cold Spring Harb Perspect Biol 7: a016535. PubMed PMC

Lisby M, Mortensen UH, Rothstein R. 2003. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572–577. PubMed

Liu NN, Han TX, Du LL, Zhou JQ. 2010. A genome-wide screen for Schizosaccharomyces pombe deletion mutants that affect telomere length. Cell Res 20: 963–965. PubMed

Longhese MP, Bonetti D, Manfrini N, Clerici M. 2010. Mechanisms and regulation of DNA end resection. EMBO J 29: 2864–2874. PubMed PMC

Luke-Glaser S, Luke B. 2012. The Mph1 helicase can promote telomere uncapping and premature senescence in budding yeast. PLoS One 7: e42028. PubMed PMC

Luke-Glaser S, Poschke H, Luke B. 2012. Getting in (and out of) the loop: regulating higher order telomere structures. Front Oncol 2: 180. PubMed PMC

Lundblad V, Szostak JW. 1989. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57: 633–643. PubMed

Lydall D, Weinert T. 1997. Use of cdc13–1-induced DNA damage to study effects of checkpoint genes on DNA damage processing. Methods Enzymol 283: 410–424. PubMed

Mankouri HW, Ngo HP, Hickson ID. 2009. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol Biol Cell 20: 1683–1694. PubMed PMC

Marcand S, Gilson E, Shore D. 1997. A protein-counting mechanism for telomere length regulation in yeast. Science 275: 986–990. PubMed

Maringele L, Lydall D. 2002. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Δ mutants. Genes Dev 16: 1919–1933. PubMed PMC

Matulova P, Marini V, Burgess RC, Sisakova A, Kwon Y, Rothstein R, Sung P, Krejci L. 2009. Cooperativity of Mus81.Mms4 with Rad54 in the resolution of recombination and replication intermediates. J Biol Chem 284: 7733–7745. PubMed PMC

Mazon G, Symington LS. 2013. Mph1 and Mus81–Mms4 prevent aberrant processing of mitotic recombination intermediates. Mol Cell 52: 63–74. PubMed PMC

Milne GT, Jin S, Shannon KB, Weaver DT. 1996. Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol Cell Biol 16: 4189–4198. PubMed PMC

Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature (London) 455: 770–774. PubMed PMC

Mitchel K, Lehner K, Jinks-Robertson S. 2013. Heteroduplex DNA position defines the roles of the Sgs1, Srs2, and Mph1 helicases in promoting distinct recombination outcomes. PLoS Genet 9: e1003340. PubMed PMC

Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, Varela E, Hediger F, Gasser SM, Krogan NJ. 2008. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322: 597–602. PubMed PMC

Nugent CI, Hughes TR, Lue NF, Lundblad V. 1996. Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274: 249–252. PubMed

Nugent CI, Bosco G, Ross LO, Evans SK, Salinger AP, Moore JK, Haber JE, Lundblad V. 1998. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr Biol 8: 657–660. PubMed

Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273: 1392–1395. PubMed

Oza P, Jaspersen SL, Miele A, Dekker J, Peterson CL. 2009. Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23: 912–927. PubMed PMC

Panico ER, Ede C, Schildmann M, Schurer KA, Kramer W. 2010. Genetic evidence for a role of Saccharomyces cerevisiae Mph1 in recombinational DNA repair under replicative stress. Yeast 27: 11–27. PubMed

Prakash R, Krejci L, Van Komen S, Anke Schurer K, Kramer W, Sung P. 2005. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3′ to 5′ DNA helicase. J Biol Chem 280: 7854–7860. PubMed

Prakash R, Satory D, Dray E, Papusha A, Scheller J, Kramer W, Krejci L, Klein H, Haber JE, Sung P, et al. 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23: 67–79. PubMed PMC

Pryde FE, Louis EJ. 1999. Limitations of silencing at native yeast telomeres. EMBO J 18: 2538–2550. PubMed PMC

Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al. 2012. The Pfam protein families database. Nucleic Acids Res 40: D290–D301. PubMed PMC

Qiu Y, Antony E, Doganay S, Koh HR, Lohman TM, Myong S. 2013. Srs2 prevents Rad51 filament formation by repetitive motion on DNA. Nat Commun 4: 2281. PubMed PMC

Rappsilber J, Mann M, Ishihama Y. 2007. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896–1906. PubMed

Raschle M, Van Komen S, Chi P, Ellenberger T, Sung P. 2004. Multiple interactions with the Rad51 recombinase govern the homologous recombination function of Rad54. J Biol Chem 279: 51973–51980. PubMed

Reid R, Lisby M, Rothstein R. 2002. Cloning-free genome alterations in Saccharomyce cerevisiae using adaptamer-mediated PCR. Methods Enzymol 350: 258–277. PubMed

Robin JD, Ludlow AT, Batten K, Magdinier F, Stadler G, Wagner KR, Shay JW, Wright WE. 2014. Telomere position effect: regulation of gene expression with progressive telomere shortening over long distances. Genes Dev 28: 2464–2476. PubMed PMC

Sabatier P. 2014. Intrabody engineering for monitoring of DNA damaged induced post-translational modifications. Master thesis, University of Copenhagen, Denmark.

Sabourin M, Tuzon CT, Zakian VA. 2007. Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol Cell 27: 550–561. PubMed PMC

Sarek G, Vannier JB, Panier S, Petrini JH, Boulton SJ. 2015. TRF2 recruits RTEL1 to telomeres in S phase to promote t-loop unwinding. Mol Cell 57: 622–635. PubMed PMC

Scheller J, Schurer A, Rudolph C, Hettwer S, Kramer W. 2000. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155: 1069–1081. PubMed PMC

Schober H, Ferreira H, Kalck V, Gehlen LR, Gasser SM. 2009. Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23: 928–938. PubMed PMC

Schurer KA, Rudolph C, Ulrich HD, Kramer W. 2004. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from Homologous recombination, but not from postreplicative repair. Genetics 166: 1673–1686. PubMed PMC

Sebesta M, Burkovics P, Haracska L, Krejci L. 2011. Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities. DNA Repair (Amst) 10: 567–576. PubMed PMC

Sherman F, Fink GR, Hicks JB. 1986. Methods in Yeast Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27. PubMed PMC

Silva S, Gallina I, Eckert-Boulet N, Lisby M. 2012. Live cell microscopy of DNA damage response in Saccharomyces cerevisiae. Methods Mol Biol 920: 433–443. PubMed

Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, Clark AB, Kunkel TA, Harper JW, Colaiacovo MP, et al. 2010. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39: 36–47. PubMed PMC

Srikumar T, Lewicki MC, Costanzo M, Tkach JM, van Bakel H, Tsui K, Johnson ES, Brown GW, Andrews BJ, Boone C, et al. 2013. Global analysis of SUMO chain function reveals multiple roles in chromatin regulation. J Cell Biol 201: 145–163. PubMed PMC

Strahl-Bolsinger S, Hecht A, Luo K, Grunstein M. 1997. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 11: 83–93. PubMed

Sugiyama T, New JH, Kowalczykowski SC. 1998. DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc Natl Acad Sci 95: 6049–6054. PubMed PMC

Sung P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241–1243. PubMed

Sung MK, Huh WK. 2007. Bimolecular fluorescence complementation analysis system for in vivo detection of protein–protein interaction in Saccharomyces cerevisiae. Yeast 24: 767–775. PubMed

Symington LS, Rothstein R, Lisby M. 2014. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198: 795–835. PubMed PMC

Takai H, Smogorzewska A, de Lange T. 2003. DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549–1556. PubMed

Teixeira MT, Arneric M, Sperisen P, Lingner J. 2004. Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell 117: 323–335. PubMed

Thomas BJ, Rothstein R. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56: 619–630. PubMed

Tkach JM, Yimit A, Lee AY, Riffle M, Costanzo M, Jaschob D, Hendry JA, Ou J, Moffat J, Boone C, et al. 2012. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol 14: 966–976. PubMed PMC

Van Komen S, Macris M, Sehorn MG, Sung P. 2006. Purification and assays of Saccharomyces cerevisiae homologous recombination proteins. Methods Enzymol 408: 445–463. PubMed

Vannier JB, Sarek G, Boulton SJ. 2014. RTEL1: functions of a disease-associated helicase. Trends Cell Biol 24: 416–425. PubMed

Vega LR, Phillips JA, Thornton BR, Benanti JA, Onigbanjo MT, Toczyski DP, Zakian VA. 2007. Sensitivity of yeast strains with long G-tails to levels of telomere-bound telomerase. PLoS Genet 3: e105. PubMed PMC

Ward TA, Dudasova Z, Sarkar S, Bhide MR, Vlasakova D, Chovanec M, McHugh PJ. 2012. Components of a Fanconi-like pathway control Pso2-independent DNA interstrand crosslink repair in yeast. PLoS Genet 8: e1002884. PubMed PMC

Wellinger RJ, Zakian VA. 2012. Everything you ever wanted to know about Saccharomyces cerevisiae telomeres: beginning to end. Genetics 191: 1073–1105. PubMed PMC

Whitby MC. 2010. The FANCM family of DNA helicases/translocases. DNA Repair (Amst) 9: 224–236. PubMed

Xue X, Choi K, Bonner J, Chiba T, Kwon Y, Xu Y, Sanchez H, Wyman C, Niu H, Zhao X, et al. 2014. Restriction of replication fork regression activities by a conserved SMC complex. Mol Cell 56: 436–445. PubMed PMC

Xue X, Choi K, Bonner JN, Szakal B, Chen YH, Papusha A, Saro D, Niu H, Ira G, Branzei D, et al. 2015a. Selective modulation of the functions of a conserved DNA motor by a histone fold complex. Genes Dev 29: 1000–1005. PubMed PMC

Xue X, Sung P, Zhao X. 2015b. Functions and regulation of the multitasking FANCM family of DNA motor proteins. Genes Dev 29: 1777–1788. PubMed PMC

Xue X, Papusha A, Choi K, Bonner JN, Kumar S, Niu H, Kaur H, Zheng X-F, Donnianni RA, Lu L, et al. 2016. Differential regulation of the anti-crossover and replication fork regression activities of Mph1 by Mte1. Genes Dev (this issue). doi: 10.1101/gad.276139.115. PubMed DOI PMC

Yimit A, Riffle M, Brown GW. 2015. Genetic regulation of Dna2 localization during the DNA damage response. G3 (Bethesda) 5: 1937–1944. PubMed PMC

Yu Y, Ren JY, Zhang JM, Suo F, Fang XF, Wu F, Du LL. 2013. A proteome-wide visual screen identifies fission yeast proteins localizing to DNA double-strand breaks. DNA Repair (Amst) 12: 433–443. PubMed

Zheng XF, Prakash R, Saro D, Longerich S, Niu H, Sung P. 2011. Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. DNA Repair (Amst) 10: 1034–1043. PubMed PMC