Genetic and physical interactions between the yeast ELG1 gene and orthologs of the Fanconi anemia pathway

Cell Cycle

Volumn 12, Issue 10, 2013, Pages 1625-1636

  Singh, Shivani ^a   Shemesh, Keren ^a   Liefshitz, Batia ^a   Kupiec, Martin ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

DNA damage; Elg1; Fanconi anemia; Genome stability; PCNA

Indexed keywords

DNA; ELG1 PROTEIN; HISTONE; HYDROXYUREA; METHYLMETHANE SULFONATE; MHF1 HISTONE; MHF2 HISTONE; PROTEIN; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHL1 PROTEIN, S CEREVISIAE; CYCLINE; DEAD BOX PROTEIN; ELG1 PROTEIN, S CEREVISIAE; MESYLIC ACID METHYL ESTER; MHF2 PROTEIN, S CEREVISIAE; MPH1 PROTEIN, S CEREVISIAE; NONHISTONE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; DNA DAMAGE; DNA REPLICATION; FANCONI ANEMIA; GENE INTERACTION; GENE MUTATION; HUMAN; DRUG EFFECTS; GENETICS; METABOLISM; MUTATION; PATHOLOGY; SACCHAROMYCES CEREVISIAE; SUMOYLATION; TWO HYBRID SYSTEM;

CARRIER PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DEAD-BOX RNA HELICASES; DNA DAMAGE; FANCONI ANEMIA; HUMANS; HYDROXYUREA; METHYL METHANESULFONATE; MUTATION; PROLIFERATING CELL NUCLEAR ANTIGEN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUMOYLATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84877932685     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24756     Document Type: Article

References (53)

1. Kee Y, D'Andrea AD. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 2010; 24:1680-94; PMID:20713514; http://dx.doi.org/10.1101/gad.1955310
2. Bagby GC, Alter BP. Fanconi anemia. Semin Hematol 2006; 43:147-56; PMID:16822457; http://dx.doi.org/10.1053/j.seminhematol.2006.04.005
3. Niedernhofer LJ, Lalai AS, Hoeijmakers JH. Fanconi anemia (cross)linked to DNA repair. Cell 2005; 123:1191-8; PMID:16377561; http://dx.doi.org/10.1016/ j.cell.2005.12.009
4. Moldovan GL, D'Andrea AD. How the fanconi anemia pathway guards the genome. Annu Rev Genet 2009; 43:223-49; PMID:19686080; http://dx.doi.org/10. 1146/annurev-genet-102108-134222
5. Kennedy RD, Chen CC, Stuckert P, Archila EM, De la Vega MA, Moreau LA, et al. Fanconi anemia pathway-deficient tumor cells are hypersensitive to inhibition of ataxia telangiectasia mutated. J Clin Invest 2007; 117:1440-9; PMID:17431503; http://dx.doi.org/10.1172/JCI31245
6. Knipscheer P, Räschle M, Smogorzewska A, Enoiu M, Ho TV, Schärer OD, et al. The Fanconi anemia pathway promotes replication- dependent DNA interstrand cross-link repair. Science 2009; 326:1698-701; PMID:19965384; http://dx.doi.org/10.1126/science.1182372
7. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 2007; 25:331-43; PMID:17289582; http://dx.doi.org/10.1016/ j.molcel.2007.01.003
8. Singh TR, Saro D, Ali AM, Zheng XF, Du CH, Killen MW, et al. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 2010; 37:879-86; PMID:20347429; http://dx.doi.org/ 10.1016/j.molcel.2010.01.036
9. Yan Z, Delannoy M, Ling C, Daee D, Osman F, Muniandy PA, et al. A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 2010; 37:865-78; PMID:20347428; http://dx.doi.org/10.1016/j.molcel.2010.01.039
10. Zhou W, Otto EA, Cluckey A, Airik R, Hurd TW, Chaki M, et al. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat Genet 2012; 44:910-5; PMID:22772369; http://dx.doi.org/10.1038/ng.2347
11. Villamil MA, Chen J, Liang Q, Zhuang Z. A noncanonical cysteine protease USP1 is activated through active site modulation by USP1-associated factor 1. Biochemistry 2012; 51:2829-39; PMID:22439892; http://dx.doi.org/10.1021/ bi3000512
12. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER 3rd, Hurov KE, Luo J, et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007; 129:289-301; PMID:17412408; http://dx.doi.org/10.1016/j.cell.2007.03.009
13. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D'Andrea AD, et al. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 2005; 17:331-9; PMID:15694335; http://dx.doi.org/10.1016/j.molcel.2005. 01.008
14. Lee KY, Yang K, Cohn MA, Sikdar N, D'Andrea AD, Myung K. Human ELG1 regulates the level of ubiquitinated proliferating cell nuclear antigen (PCNA) through Its interactions with PCNA and USP1. J Biol Chem 2010; 285:10362-9; PMID:20147293; http://dx.doi.org/10.1074/jbc.M109.092544
15. Yang K, Moldovan GL, Vinciguerra P, Murai J, Takeda S, D'Andrea AD. Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev 2011; 25:1847-58; PMID:21896657; http://dx.doi.org/10.1101/gad.17020911
16. Sato K, Ishiai M, Toda K, Furukoshi S, Osakabe A, Tachiwana H, et al. Histone chaperone activity of Fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J 2012; 31:3524-36; PMID:22828868; http://dx.doi.org/10.1038/emboj.2012.197
17. Kolodner RD, Putnam CD, Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 2002; 297:552-7; PMID:12142524; http://dx.doi.org/10.1126/science.1075277
18. Aroya SB, Kupiec M. The Elg1 replication factor C-like complex: a novel guardian of genome stability. DNA Repair (Amst) 2005; 4:409-17; PMID:15725622; http://dx.doi.org/10.1016/j.dnarep.2004.08.003
19. Ulrich HD. Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair (Amst) 2009; 8:461-9; PMID:19217833; http://dx.doi.org/10.1016/j.dnarep.2009.01.006
20. Prakash S, Johnson RE, Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 2005; 74:317-53; PMID:15952890; http://dx.doi.org/10.1146/annurev.biochem.74.082803. 133250
21. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002; 419:135-41; PMID:12226657; http://dx.doi.org/10.1038/nature00991
22. Papouli E, Chen S, Davies AA, Huttner D, Krejci L, Sung P, et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol Cell 2005; 19:123-33; PMID:15989970; http://dx.doi.org/10. 1016/j.molcel.2005.06.001
23. Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 2005; 436:428-33; PMID:15931174
24. Bellaoui M, Chang M, Ou J, Xu H, Boone C, Brown GW. Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J 2003; 22:4304-13; PMID:12912927; http://dx.doi.org/10.1093/emboj/cdg406
25. Ben-Aroya S, Koren A, Liefshitz B, Steinlauf R, Kupiec M. ELG1, a yeast gene required for genome stability, forms a complex related to replication factor C. Proc Natl Acad Sci USA 2003; 100:9906-11; PMID:12909721; http://dx.doi.org/10.1073/pnas.1633757100
26. Kanellis P, Agyei R, Durocher D. Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr Biol 2003; 13:1583-95; PMID:13678589; http://dx.doi.org/10.1016/S0960-9822(03)00578-5
27. Ogiwara H, Ui A, Enomoto T, Seki M. Role of Elg1 protein in double strand break repair. Nucleic Acids Res 2007; 35:353-62; PMID:17170004; http://dx.doi.org/10.1093/nar/gkl1027
28. Smith S, Hwang JY, Banerjee S, Majeed A, Gupta A, Myung K. Mutator genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2004; 101:9039-44; PMID:15184655; http://dx.doi.org/10.1073/pnas.0403093101
29. Smolikov S, Mazor Y, Krauskopf A. ELG1, a regulator of genome stability, has a role in telomere length regulation and in silencing. Proc Natl Acad Sci USA 2004; 101:1656-61; PMID:14745004; http://dx.doi.org/10.1073/pnas.0307796100
30. Scholes DT, Banerjee M, Bowen B, Curcio MJ. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 2001; 159:1449-65; PMID:11779788
31. Sikdar N, Banerjee S, Lee KY, Wincovitch S, Pak E, Nakanishi K, et al. DNA damage responses by human ELG1 in S phase are important to maintain genomic integrity. Cell Cycle 2009; 8:3199-207; PMID:19755857; http://dx.doi.org/10. 4161/cc.8.19.9752
32. Bell DW, Sikdar N, Lee KY, Price JC, Chatterjee R, Park HD, et al.; NISC Comparative Sequencing Program. Predisposition to cancer caused by genetic and functional defects of mammalian Atad5. PLoS Genet 2011; 7:e1002245; PMID:21901109; http://dx.doi.org/10.1371/journal.pgen.1002245
33. Parnas O, Zipin-Roitman A, Pfander B, Liefshitz B, Mazor Y, Ben-Aroya S, et al. Elg1, an alternative subunit of the RFC clamp loader, preferentially interacts with SUMOylated PCNA. EMBO J 2010; 29:2611-22; PMID:20571511; http://dx.doi.org/10.1038/emboj.2010.128
34. Scheller J, Schürer A, Rudolph C, Hettwer S, Kramer W. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 2000; 155:1069-81; PMID:10880470
35. Schürer KA, Rudolph C, Ulrich HD, Kramer W. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from Homologous recombination, but not from postreplicative repair. Genetics 2004; 166:1673-86; PMID:15126389; http://dx.doi.org/10.1534/genetics.166.4.1673
36. Laha S, Das SP, Hajra S, Sau S, Sinha P. The budding yeast protein Chl1p is required to preserve genome integrity upon DNA damage in S-phase. Nucleic Acids Res 2006; 34:5880-91; PMID:17062629; http://dx.doi.org/10.1093/nar/gkl749
37. Ehret GB, Munroe PB, Rice KM, Bochud M, Johnson AD, Chasman DI, et al.; International Consortium for Blood Pressure Genome-Wide Association Studies; CARDIoGRAM consortium; CKDGen Consortium; KidneyGen Consortium; EchoGen consortium; CHARGE-HF consortium. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature 2011; 478:103-9; PMID:21909115; http://dx.doi.org/10.1038/nature10405
38. Parnas O, Amishay R, Liefshitz B, Zipin-Roitman A, Kupiec M. Elg1, the major subunit of an alternative RFC complex, interacts with SUMO-processing proteins. Cell Cycle 2011; 10:2894-903; PMID:21869594; http://dx.doi.org/10. 4161/cc.10.17.16778
39. Chavez A, Agrawal V, Johnson FB. Homologous recombination-dependent rescue of deficiency in the structural maintenance of chromosomes (Smc) 5/6 complex. J Biol Chem 2011; 286:5119-25; PMID:21138837; http://dx.doi.org/10. 1074/jbc.M110.201608
40. Huang RY, Eddy M, Vujcic M, Kowalski D. Genomewide screen identifies genes whose inactivation confer resistance to cisplatin in Saccharomyces cerevisiae. Cancer Res 2005; 65:5890-7; PMID:15994967; http://dx.doi.org/10. 1158/0008-5472.CAN-04-4093
41. 2 heterotetramer and functions as a heterotetramer. Structure 2012; 20:364-70; PMID:22325783; http://dx.doi.org/10.1016/j.str.2011.12.012
42. Davidson MB, Brown GW. The N- and C-termini of Elg1 contribute to the maintenance of genome stability. DNA Repair (Amst) 2008; 7:1221-32; PMID:18482875; http://dx.doi.org/10.1016/j.dnarep.2008.04.001
43. Amin NS, Holm C. In vivo analysis reveals that the interdomain region of the yeast proliferating cell nuclear antigen is important for DNA replication and DNA repair. Genetics 1996; 144:479-93; PMID:8889514
44. Merrill BJ, Holm C. The RAD52 recombinational repair pathway is essential in pol30 (PCNA) mutants that accumulate small single-stranded DNA fragments during DNA synthesis. Genetics 1998; 148:611-24; PMID:9504910
45. Daee DL, Ferrari E, Longerich S, Zheng XF, Xue X, Branzei D, et al. Rad5-dependent DNA repair functions of the Saccharomyces cerevisiae FANCM protein homolog Mph1. J Biol Chem 2012; 287:26563-75; PMID:22696213; http://dx.doi.org/10.1074/jbc.M112.369918
46. Ward TA, Dudášová Z, Sarkar S, Bhide MR, Vlasáková D, Chovanec M, et al. Components of a Fanconi-like pathway control Pso2-independent DNA interstrand crosslink repair in yeast. PLoS Genet 2012; 8:e1002884; PMID:22912599; http://dx.doi.org/10.1371/journal.pgen. 1002884
47. Skibbens RV. Chl1p, a DNA helicase-like protein in budding yeast, functions in sister-chromatid cohesion. Genetics 2004; 166:33-42; PMID:15020404; http://dx.doi.org/10.1534/genetics.166.1.33
48. Parnas O, Zipin-Roitman A, Mazor Y, Liefshitz B, Ben-Aroya S, Kupiec M. The ELG1 clamp loader plays a role in sister chromatid cohesion. PLoS ONE 2009; 4:e5497; PMID:19430531; http://dx.doi.org/10.1371/journal.pone.0005497
49. Davidson MB, Katou Y, Keszthelyi A, Sing TL, Xia T, Ou J, et al. Endogenous DNA replication stress results in expansion of dNTP pools and a mutator phenotype. EMBO J 2012; 31:895-907; PMID:22234187; http://dx.doi.org/10. 1038/emboj.2011.485
50. Karras GI, Fumasoni M, Sienski G, Vanoli F, Branzei D, Jentsch S. Noncanonical Role of the 9-1-1 Clamp in the Error-Free DNA Damage Tolerance Pathway. Mol Cell 2013; 49:536-46; PMID:23260657
51. Ruhland A, Haase E, Siede W, Brendel M. Isolation of yeast mutants sensitive to the bifunctional alkylating agent nitrogen mustard. Mol Gen Genet 1981; 181:346-51; PMID:7017347; http://dx.doi.org/10.1007/BF00425609
52. Chen YH, Choi K, Szakal B, Arenz J, Duan X, Ye H, et al. Interplay between the Smc5/6 complex and the Mph1 helicase in recombinational repair. Proc Natl Acad Sci USA 2009; 106:21252-7; PMID:19995966; http://dx.doi.org/10.1073/ pnas.0908258106
53. James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 1996; 144:1425-36; PMID:8978031