Processing of homologous recombination repair intermediates by the Sgs1-Top3-Rmi1 and Mus81-Mms4 complexes

Cell Cycle

Volumn 10, Issue 18, 2011, Pages 3078-3085

  Hickson, Ian D ^a   Mankouri, Hocine W ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Eme1; GEN1; RecQ; RusA; Topoisomerase

Indexed keywords

DNA TOPOISOMERASE; ENDONUCLEASE; MMS4 PROTEIN; MUS81 PROTEIN; RECQ HELICASE; RESOLVASE; RMI1 PROTEIN; SGS1 PROTEIN; TOP3 PROTEIN; UNCLASSIFIED DRUG;

CELL CYCLE S PHASE; COMPLEX FORMATION; DNA STRUCTURE; FUNGAL STRAIN; GENE LOCUS; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; YEAST;

SACCHAROMYCES CEREVISIAE;

EID: 80052870830     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.18.16919     Document Type: Review

References (90)

1. Li D, Frazier M, Evans DB, Hess KR, Crane CH, Jiao L, et al. Single nucleotide polymorphisms of RecQ1, RAD54L and ATM genes are associated with reduced survival of pancreatic cancer. J Clin Oncol 2006; 24:1720-8; PMID:16520463; DOI:10.1200/ JCO.2005.04.4206.
2. Hu Y, Raynard S, Sehorn MG, Lu X, Bussen W, et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev 2007; 21:3073-84; PMID:18003859; DOI:10.1101/gad.1609107.
3. Ashton TM, Hickson ID. Yeast as a model system to study RecQ helicase function. DNA Repair (Amst) 2010; 9:303-14; PMID:20071248; DOI:10.1016/j. dnarep.2009.12.007.
4. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 1994; 14:8391-8; PMID:7969174.
5. Bennett RJ, Noirot-Gros MF, Wang JC. Interaction between yeast sgs1 helicase and DNA topoisomerase III. J Biol Chem 2000; 275:26898-905; PMID:10862619.
6. Fricke WM, Kaliraman V, Brill SJ. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J Biol Chem 2001; 276:8848-55; PMID:11124263; DOI:10.1074/jbc.M009719200.
7. Ui A, Seki M, Ogiwara H, Onodera R, Fukushige S, Onoda F, et al. The ability of Sgs1 to interact with DNA topoisomerase III is essential for damage- induced recombination. DNA Repair (Amst) 2005; 4:191-201; PMID:15590327; DOI:10.1016/j. dnarep.2004.09.002.
8. Onodera R, Seki M, Ui A, Satoh Y, Miyajima A, Onoda F, et al. Functional and physical interaction between Sgs1 and Top3 and Sgs1-independent function of Top3 in DNA recombination repair. Genes Genet Syst 2002; 77:11-21; PMID:12036100; DOI:10.1266/ggs.77.11.
9. Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, et al. The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem 2000; 275:9636-44; PMID:10734115; DOI:10.1074/ jbc.275.13.9636.
10. Johnson FB, Lombard DB, Neff NF, Mastrangelo MA, Dewolf W, Ellis NA, et al. Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells. Cancer Res 2000; 60:1162-7; PMID:10728666.
11. Wu L, Hickson ID. The Bloom's syndrome helicase stimulates the activity of human topoisomerase IIIalpha. Nucleic Acids Res 2002; 30:4823-9; PMID:12433984; DOI:10.1093/nar/gkf611.
12. Wu L, Hickson ID. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003; 426:870-4; PMID:14685245; DOI:10.1038/nature02253.
13. Plank JL, Wu J, Hsieh TS. Topoisomerase IIIalpha and Bloom's helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc Natl Acad Sci USA 2006; 103:11118-23; PMID:16849422; DOI:10.1073/ pnas.0604873103.
14. Yang J, Bachrati CZ, Ou J, Hickson ID, Brown GW. Human topoisomerase IIIalpha is a singlestranded DNA decatenase that is stimulated by BLM and RMI1. J Biol Chem 2010; 285:21426-36; PMID:20445207; DOI:10.1074/jbc.M110.123216.
15. Yin J, Sobeck A, Xu C, Meetei AR, Hoatlin M, Li L, et al. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J 2005; 24:1465-76; PMID:15775963; DOI:10.1038/sj.emboj.7600622.
16. Chang M, Bellaoui M, Zhang C, Desai R, Morozov P, Delgado-Cruzata L, et al. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J 2005; 24:2024-33; PMID:15889139; DOI:10.1038/ sj.emboj.7600684.
17. Mullen JR, Nallaseth FS, Lan YQ, Slagle CE, Brill SJ. Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol Cell Biol 2005; 25:4476-87; PMID:15899853; DOI:10.1128/ MCB.25.11.4476-87.2005.
18. Wu L, Bachrati CZ, Ou J, Xu C, Yin J, Chang M, et al. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc Natl Acad Sci USA 2006; 103:4068-73; PMID:16537486; DOI:10.1073/pnas.0508295103.
19. Raynard S, Bussen W, Sung P. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha and BLAP75. J Biol Chem 2006; 281:13861-4; PMID:16595695; DOI:10.1074/jbc. C600051200.
20. Chen CF, Brill SJ. Binding and activation of DNA topoisomerase III by the Rmi1 subunit. J Biol Chem 2007; 282:28971-9; PMID:17693398; DOI:10.1074/ jbc.M705427200.
21. Raynard S, Zhao W, Bussen W, Lu L, Ding YY, Busygina V, et al. Functional role of BLAP75 in BLM-topoisomerase IIIalpha-dependent holliday junction processing. J Biol Chem 2008; 283:15701-8; PMID:18390547; DOI:10.1074/jbc. M802127200.
22. Xu D, Guo R, Sobeck A, Bachrati CZ, Yang J, Enomoto T, et al. RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev 2008; 22:2843-55; PMID:18923082; DOI:10.1101/gad.1708608.
23. Singh TR, Ali AM, Busygina V, Raynard S, Fan Q, Du CH, et al. BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev 2008; 22:2856-68; PMID:18923083; DOI:10.1101/gad.1725108.
24. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol 2010; 17:1377-82; PMID:20935631; DOI:10.1038/nsmb.1919.
25. Mankouri HW, Hickson ID. The RecQ helicasetopoisomerase III-Rmi1 complex: a DNA structure- specific 'dissolvasome'? Trends Biochem Sci 2007; 32:538-46; PMID:17980605; DOI:10.1016/j. tibs.2007.09.009.
26. Chu WK, Hickson ID. RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer 2009; 9:644-54; PMID:19657341; DOI:10.1038/nrc2682.
27. German J. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine 1993; 72:393-406; PMID:8231788.
28. Brewer BJ, Fangman WL. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 1987; 51:463-71; PMID:2822257; DOI:10.1016/0092-8674(87)90642-8.
29. Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, Cotta-Ramusino C, et al. Rad51- dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev 2005; 19:339-50; PMID:15687257; DOI:10.1101/ gad.322605.
30. Mankouri HW, Hickson ID. Top3 processes recombination intermediates and modulates checkpoint activity after DNA damage. Mol Biol Cell 2006; 17:4473-83; PMID:16899506; DOI:10.1091/mbc. E06-06-0516.
31. Mankouri HW, Ngo HP, Hickson ID. Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol Biol Cell 2007; 18:4062-73; PMID:17671161; DOI:10.1091/mbc.E07-05-0490.
32. Liberi G, Foiani M. The double life of Holliday junctions. Cell Res 2010; 20:611-3; PMID:20502439; DOI:10.1038/cr.2010.73.
33. Ashton TM, Mankouri HW, Heidenblut A, McHugh PJ, Hickson ID. Pathways for Holliday Junction Processing during Homologous Recombination in Saccharomyces cerevisiae. Mol Cell Biol 2011; 31:1921-33; PMID:21343337; DOI:10.1128/MCB. 01130-10.
34. Mankouri HW, Ashton TM, Hickson ID. Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc Natl Acad Sci USA 2011; 108:4944-9; PMID:21383164; DOI:10.1073/pnas.1014240108.
35. Doe CL, Ahn JS, Dixon J, Whitby MC. Mus81- Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J Biol Chem 2002; 277:32753-9; PMID:12084712; DOI:10.1074/jbc. M202120200.
36. Sharples GJ, Chan SN, Mahdi AA, Whitby MC, Lloyd RG. Processing of intermediates in recombination and DNA repair: identification of a new endonuclease that specifically cleaves Holliday junctions. EMBO J 1994; 13:6133-42; PMID:7813450.
37. Ip SC, Rass U, Blanco MG, Flynn HR, Skehel JM, West SC. Identification of Holliday junction resolvases from humans and yeast. Nature 2008; 456:357-61; PMID:19020614; DOI:10.1038/nature07470.
38. Rass U, Compton SA, Matos J, Singleton MR, Ip SC, Blanco MG, et al. Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev 2010; 24:1559-69; PMID:20634321; DOI:10.1101/ gad.585310.
39. Chan SN, Harris L, Bolt EL, Whitby MC, Lloyd RG. Sequence specificity and biochemical characterization of the RusA Holliday junction resolvase of Escherichia coli. J Biol Chem 1997; 272:14873-82; PMID:9169457; DOI:10.1074/jbc.272.23.14873.
40. Chan SN, Vincent SD, Lloyd RG. Recognition and manipulation of branched DNA by the RusA Holliday junction resolvase of Escherichia coli. Nucleic Acids Res 1998; 26:1560-6; PMID:9512524; DOI:10.1093/nar/26.7.1560.
41. Mankouri HW, Ngo HP, Hickson ID. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol Biol Cell 2009; 20:1683-94; PMID:19158388; DOI:10.1091/mbc.E08-08-0877.
42. Schwartz EK, Heyer WD. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 2011; 120:109-27; PMID:21369956; DOI:10.1007/s00412-010-0304-7.
43. Doe CL, Dixon J, Osman F, Whitby MC. Partial suppression of the fission yeast rqh1(-) phenotype by expression of a bacterial Holliday junction resolvase. EMBO J 2000; 19:2751-62; PMID:10835372; DOI:10.1093/emboj/19.11.2751.
44. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR, Russell P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 2001; 107:537-48; PMID:11719193; DOI:10.1016/S0092- 8674(01)00536-0.
45. Lorenz A, West SC, Whitby MC. The human Holliday junction resolvase GEN1 rescues the meiotic phenotype of a Schizosaccharomyces pombe mus81 mutant. Nucleic Acids Res 2010; 38:1866-73; PMID:20040574; DOI:10.1093/nar/gkp1179.
46. Odagiri N, Seki M, Onoda F, Yoshimura A, Watanabe S, Enomoto T. Budding yeast mms4 is epistatic with rad52 and the function of Mms4 can be replaced by a bacterial Holliday junction resolvase. DNA Repair (Amst) 2003; 2:347-58; PMID:12547397; DOI:10.1016/S1568-7864(02)00234-3.
47. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol 2003; 23:3487-96; PMID:12724407; DOI:10.1128/ MCB.23.10.3487-96.2003.
48. Coté AG, Lewis SM. Mus81-dependent doublestrand DNA breaks at in vivo-generated cruciform structures in S. cerevisiae. Mol Cell 2008; 31:800-12; PMID:18922464; DOI:10.1016/j.molcel. 2008.08.025.
49. Blanco MG, Matos J, Rass U, Ip SC, West SC. Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S. cerevisiae. DNA Repair (Amst) 2010; 9:394-402; PMID:20106725; DOI:10.1016/j. dnarep.2009.12.017.
50. Rodriguez-Lopez AM, Whitby MC, Borer CM, Bachler MA, Cox LS. Correction of proliferation and drug sensitivity defects in the progeroid Werner's Syndrome by Holliday junction resolution. Rejuvenation Res 2007; 10:27-40; PMID:17378750; DOI:10.1089/rej.2006.0503.
51. Blais V, Gao H, Elwell CA, Boddy MN, Gaillard PH, Russell P, et al. RNA interference inhibition of Mus81 reduces mitotic recombination in human cells. Mol Biol Cell 2004; 15:552-62; PMID:14617801; DOI:10.1091/mbc.E03-08-0580.
52. Jessop L, Lichten M. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol Cell 2008; 31:313-23; PMID:18691964; DOI:10.1016/j.molcel.2008.05. 021.
53. Jessop L, Rockmill B, Roeder GS, Lichten M. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet 2006; 2:155; PMID:17002499; DOI:10.1371/ journal.pgen.0020155.
54. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, Hunter N. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 2007; 130:259-72; PMID:17662941; DOI:10.1016/j.cell.2007. 05.035.
55. Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N. RecQ helicase, Sgs1 and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell 2008; 31:324-36; PMID:18691965; DOI:10.1016/j.molcel. 2008.07.006.
56. Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 1997; 88:375-84; PMID:9039264; DOI:10.1016/ S0092-8674(00)81876-0.
57. Karow JK, Constantinou A, Li JL, West SC, Hickson ID. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc Natl Acad Sci USA 2000; 97:6504-8; PMID:10823897; DOI:10.1073/pnas.100448097.
58. Bennett RJ, Keck JL, Wang JC. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J Mol Biol 1999; 289:235-48; PMID:10366502; DOI:10.1006/jmbi.1999.2739.
59. Cejka P, Kowalczykowski SC. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J Biol Chem 2010; 285:8290-301; PMID:20086270; DOI:10.1074/jbc.M109. 083196.
60. Gaskell LJ, Osman F, Gilbert RJ, Whitby MC. Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates? EMBO J 2007; 26:1891-901; PMID:17363897; DOI:10.1038/sj.emboj.7601645.
61. Taylor ER, McGowan CH. Cleavage mechanism of human Mus81-Eme1 acting on Hollidayjunction structures. Proc Natl Acad Sci USA 2008; 105:3757-62; PMID:18310322; DOI:10.1073/ pnas.0710291105.
62. Gaillard PH, Noguchi E, Shanahan P, Russell P. The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol Cell 2003; 12:747-59; PMID:14527419; DOI:10.1016/S1097-2765(03)00342-3.
63. Cromie GA, Hyppa RW, Taylor AF, Zakharyevich K, Hunter N, Smith GR. Single Holliday junctions are intermediates of meiotic recombination. Cell 2006; 127:1167-78; PMID:17174892; DOI:10.1016/j. cell.2006.09.050.
64. Ho CK, Mazon G, Lam AF, Symington LS. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol Cell 2010; 40:988- 1000; PMID:21172663; DOI:10.1016/j.molcel. 2010.11.016.
65. Tay YD, Wu L. Overlapping roles for Yen1 and Mus81 in cellular Holliday junction processing. J Biol Chem 2010; 285:11427-32; PMID:20178992; DOI:10.1074/jbc.M110.108399.
66. Ehmsen KT, Heyer WD. Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease. Nucleic Acids Res 2008; 36:2182-95; PMID:18281703; DOI:10.1093/nar/gkm1152.
67. Fricke WM, Bastin-Shanower SA, Brill SJ. Substrate specificity of the Saccharomyces cerevisiae Mus81- Mms4 endonuclease. DNA Repair (Amst) 2005; 4:243-51; PMID:15590332; DOI:10.1016/j. dnarep.2004.10.001.
68. Chang JH, Kim JJ, Choi JM, Lee JH, Cho Y. Crystal structure of the Mus81-Eme1 complex. Genes Dev 2008; 22:1093-106; PMID:18413719; DOI:10.1101/ gad.1618708.
69. Ehmsen KT, Heyer WD. A junction branch point adjacent to a DNA backbone nick directs substrate cleavage by Saccharomyces cerevisiae Mus81- Mms4. Nucleic Acids Res 2009; 37:2026-36; PMID:19211663; DOI:10.1093/nar/gkp038.
70. Hollingsworth NM, Brill SJ. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 2004; 18:117-25; PMID:14752007; DOI:10.1101/gad.1165904.
71. Osman F, Dixon J, Doe CL, Whitby MC. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol Cell 2003; 12:761-74; PMID:14527420; DOI:10.1016/S1097- 2765(03)00343-5.
72. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, et al. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 2006; 25:4921-32; PMID:17036055; DOI:10.1038/sj.emboj.7601344.
73. Interthal H, Heyer WD. MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol Gen Genet 2000; 263:812-27; PMID:10905349; DOI:10.1007/ s004380000241.
74. Mazina OM, Mazin AV. Human Rad54 protein stimulates human Mus81-Eme1 endonuclease. Proc Natl Acad Sci USA 2008; 105:18249-54; PMID:19017809; DOI:10.1073/pnas.0807016105.
75. Matulova P, Marini V, Burgess RC, Sisakova A, Kwon Y, Rothstein R, et al. Cooperativity of Mus81. Mms4 with Rad54 in the resolution of recombination and replication intermediates. J Biol Chem 2009; 284:7733-45; PMID:19129197; DOI:10.1074/jbc. M806192200.
76. Bugreev DV, Hanaoka F, Mazin AV. Rad54 dissociates homologous recombination intermediates by branch migration. Nat Struct Mol Biol 2007; 14:746- 53; PMID:17660833; DOI:10.1038/nsmb1268.
77. Bugreev DV, Mazina OM, Mazin AV. Rad54 protein promotes branch migration of Holliday junctions. Nature 2006; 442:590-3; PMID:16862129; DOI:10.1038/nature04889.
78. Zhang R, Sengupta S, Yang Q, Linke SP, Yanaihara N, Bradsher J. BLM helicase facilitates Mus81 endonuclease activity in human cells. Cancer Res 2005; 65:2526-31; PMID:15805243; DOI:10.1158/0008- 5472.CAN-04-2421.
79. Schwacha A, Kleckner N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 1995; 83:783-91; PMID:8521495; DOI:10.1016/0092-8674(95)90191-4.
80. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N. Double Holliday junctions are intermediates of DNA break repair. Nature 2010; 464:937-41; PMID:20348905; DOI:10.1038/nature08868.
81. Wechsler T, Newman S, West SC. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 2011; 471:642- 6; PMID:21399624; DOI:10.1038/nature09790.
82. Ii M, Brill SJ. Roles of SGS1, MUS81 and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr Genet 2005; 48:213- 25; PMID:16193328; DOI:10.1007/s00294-005- 0014-5.
83. Petermann E, Helleday T. Pathways of mammalian replication fork restart. Nat Rev Mol Cell Biol 2010; 11:683-7; PMID:20842177; DOI:10.1038/ nrm2974.
84. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 2001; 157:103-18; PMID:11139495.
85. Kaliraman V, Brill SJ. Role of SGS1 and SLX4 in maintaining rDNA structure in Saccharomyces cerevisiae. Curr Genet 2002; 41:389-400; PMID:12228808; DOI:10.1007/s00294-002-0319-6.
86. Stoepker C, Hain K, Schuster B, Hilhorst-Hofstee Y, Rooimans MA, Steltenpool J, et al. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 2011; 43:138-41; PMID:21240277; DOI:10.1038/ng.751.
87. Kim Y, Lach FP, Desetty R, Hanenberg H, Auerbach AD, Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 2011; 43:142-6; PMID:21240275; DOI:10.1038/ng.750.
88. Wu F, Liu SY, Tao YM, Ou DP, Fang F, Yang LY. Decreased expression of methyl methansulfonate and ultraviolet-sensitive gene clone 81 (Mus81) is correlated with a poor prognosis in patients with hepatocellular carcinoma. Cancer 2008; 112:2002-10; PMID:18327812; DOI:10.1002/cncr.23396.
89. Wu F, Shirahata A, Sakuraba K, Kitamura Y, Goto T, Saito M. Downregulation of Mus81 as a potential marker for the malignancy of gastric cancer. Anticancer Res 2010; 30:5011-4; PMID:21187482.
90. Wu F, Shirahata A, Sakuraba K, Kitamura Y, Goto T, Saito M, et al. Downregulation of Mus81 as a novel prognostic biomarker for patients with colorectal carcinoma. Cancer Sci 2011; 102:472- 7; PMID:21175991; DOI:10.1111/j.1349- 7006.2010.01790.x.