Holliday junction processing enzymes as guardians of genome stability

Trends in Biochemical Sciences

Volumn 39, Issue 9, 2014, Pages 409-419

  Sarbajna, Shriparna ^a   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

BLM; Bloom's syndrome; DNA repair; GEN1; Homologous recombination; MUS81; SLX1 SLX4

Indexed keywords

BLM TOPOISOMERASE III ALPHA RMI1 RMI2 COMPLEX; BLOOM SYNDROME HELICASE; CELL PROTEIN; ENDONUCLEASE; FANCONI ANEMIA PROTEIN; NUCLEASE; PROTEIN GEN1; PROTEIN MUS81; PROTEIN SLX4; UNCLASSIFIED DRUG; DNA; DOUBLE STRANDED DNA; RESOLVASE; CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; CRUCIFORM DNA;

CELL VIABILITY; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; DISSOLUTION; DNA CROSS LINKING; GENOMIC INSTABILITY; HOLLIDAY JUNCTION; HUMAN; MAMMAL CELL; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN PROCESSING; RECOMBINATION REPAIR; REVIEW; SOMATIC CELL; STRUCTURE ANALYSIS; TELOMERE; CROSS LINKING; DNA DAMAGE; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; MITOSIS; MORTALITY; ANIMAL; GENETIC RECOMBINATION; METABOLISM;

MAMMALIA;

ANIMALS; DNA DAMAGE; DNA REPLICATION; DNA, CRUCIFORM; GENOMIC INSTABILITY; HOLLIDAY JUNCTION RESOLVASES; HUMANS; RECOMBINATION, GENETIC;

EID: 84906939632     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.07.003     Document Type: Review

References (82)

1. Paques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999, 63:349-404.
2. Bzymek M., et al. Double Holliday junctions are intermediates of DNA break repair. Nature 2010, 464:937-941.
3. Holliday R. A mechanism for gene conversion in fungi. Genet. Res. 1964, 5:282-304.
4. West S.C. Processing of recombination intermediates by the RuvABC proteins. Ann. Rev. Genet. 1997, 31:213-244.
5. Lilley D.M.J., White M.F. The junction-resolving enzymes. Nat. Rev. Mol. Cell Biol. 2001, 2:433-443.
6. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 2003, 4:435-445.
7. Chen X.B., et al. Human MUS81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 2001, 8:1117-1127.
8. Ip S.C.Y., et al. Identification of Holliday junction resolvases from humans and yeast. Nature 2008, 456:357-361.
9. Wechsler T., et al. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 2011, 471:642-646.
10. Wyatt H.D.M., et al. Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell 2013, 52:234-247.
11. Wu L., Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003, 426:870-874.
12. Svendsen J.M., et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009, 138:63-77.
13. Munoz I.M., et al. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 2009, 35:116-127.
14. Fekairi S., et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 2009, 138:78-89.
15. Elborough K.M., West S.C. Resolution of synthetic Holliday junctions in DNA by an endonuclease activity from calf thymus. EMBO J. 1990, 9:2931-2936.
16. West S.C. The search for a human Holliday junction resolvase. Biochem. Soc. Trans. 2009, 37:519-526.
17. Manthei K.A., Keck J.L. The BLM dissolvasome in DNA replication and repair. Cell. Mol. Life Sci. 2014, 70:4067-4084.
18. Yang J., et al. Human topoisomerase IIIα is a single-stranded DNA decatenase that is stimulated by BLM and RMI1. J. Biol. Chem. 2010, 285:21426-21436.
19. Xu D.Y., et al. RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev. 2008, 22:2843-2855.
20. Singh T.R., 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, 22:2856-2868.
21. Hoadley K.A., et al. Structure and cellular roles of the RMI core complex from the Bloom syndrome dissolvasome. Structure 2010, 18:1149-1158.
22. Bloom D. Congenital telangiectatic erythema resembling lupus erythematosus in dwarfs: probably a syndrome entity. AMA Am. J. Dis. Child. 1954, 88:754-758.
23. German J. Bloom syndrome: a Mendelian prototype of somatic mutational disease. Medicine (Baltimore) 1993, 72:393-406.
24. Chaganti R.S., et al. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:4508-4512.
25. Ciccia A., et al. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu. Rev. Biochem. 2008, 77:259-287.
26. Gwon G.H., et al. Crystal structures of the structure-selective nuclease MUS81-EME1 bound to flap DNA structures. EMBO J. 2014, 33:1061-1072.
27. Ciccia A., et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell 2007, 25:331-343.
28. Pepe A., West S.C. Substrate specificity of the MUS81-EME2 structure selective endonuclease. Nucleic Acids Res. 2014, 42:3833-3845.
29. Amangyeld T., et al. Human MUS81-EME2 can cleave a variety of DNA secondary structures including intact Holliday junction and nicked duplex. Nucleic Acids Res. 2014, 42:5846-5862.
30. Pepe A., West S.C. MUS81-EME2 promotes replication fork restart. Cell Rep. 2014, 7:1048-1055.
31. Mullen J.R., et al. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 2001, 157:103-118.
32. Castor D., et al. Cooperative control of Holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol. Cell 2013, 52:221-233.
33. Salewsky B., et al. The nuclease hSNM1B/Apollo is linked to the Fanconi anemia pathway via its interaction with FANCP/SLX4. Hum. Mol. Genet. 2012, 21:4948-4956.
34. Rass U., et al. Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev. 2010, 24:1559-1569.
35. Dutertre S., et al. Dephosphorylation and subcellular compartment change of the mitotic Bloom's syndrome DNA helicase in response to ionizing radiation. J. Biol. Chem. 2002, 277:6280-6286.
36. Matos J., et al. Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 2011, 147:158-172.
37. Matos J., West S.C. Holliday junction resolution: regulation in space and time. DNA Repair 2014, 19:176-181.
38. Sarbajna S., et al. Roles of SLX1-SLX4, MUS81-EME1 and GEN1 in avoiding genome instability and mitotic catastrophe. Genes Dev. 2014, 28:1124-1136.
39. Garner E., et al. Human GEN1 and the SLX4-associated nucleases MUS81 and SLX1 are essential for the resolution of replication-induced Holliday junctions. Cell Rep. 2013, 5:207-215.
40. Rass U. Resolving branched DNA intermediates with structure-specific nucleases during replication in eukaryotes. Chromosoma 2014, 122:499-515.
41. Mankouri H.W., Hickson I.D. The RecQ helicase-topoisomerase III-RMI1 complex: a structure-specific 'dissolvasome'. Trends Biochem. Sci. 2007, 32:538-546.
42. Davies S.L., et al. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol 2004, 24:1279-1291.
43. Ababou M., et al. ATM-dependent phosphorylation and accumulation of endogenous BLM protein in response to ionizing radiation. Oncogene 2000, 19:5955-5963.
44. Rao V.A., et al. Endogenous γH2AX-ATM-Chk2 checkpoint activation in Bloom's syndrome helicase deficient cells is related to DNA replication arrested forks. Mol. Cancer Res. 2007, 5:713-724.
45. Ralf C., et al. The Bloom's syndrome helicase can promote the regression of a model replication fork. J. Biol. Chem. 2006, 281:22839-22846.
46. Kim Y., et al. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 2013, 121:54-63.
47. Naim V., et al. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 2013, 15:1008-1015.
48. Hanada K., et al. The structure-specific endonuclease MUS81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 2007, 14:1096-1104.
49. Shimura T., et al. Bloom's syndrome helicase and MUS81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J. Mol. Biol. 2008, 375:1152-1164.
50. Regairaz M., et al. MUS81-mediated DNA cleavage resolves replication forks stalled by topoisomerase I-DNA complexes. J. Cell Biol. 2011, 195:739-749.
51. Ying S.M., et al. MUS81 promotes common fragile site expression. Nat. Cell Biol. 2013, 15:1001-1007.
52. Debatisse M., et al. Common fragile sites: mechanisms of instability revisited. Trends Genet. 2012, 28:22-32.
53. Chan K.L., et al. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 2009, 11:753-760.
54. Naim V., Rosselli F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 2009, 11:761-768.
55. Murfuni I., et al. The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation. Oncogene 2013, 32:610-620.
56. Neelsen K.J., et al. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 2013, 200:699-708.
57. Beck H., et al. Cyclin-dependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol. Cell. Biol. 2012, 32:4226-4236.
58. Shimura T., et al. Cyclin D1 overexpression perturbs DNA replication and induces replication-associated DNA double-strand breaks in acquired radioresistant cells. Cell Cycle 2013, 12:773-782.
59. Deans A.J., West S.C. DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 2011, 11:467-480.
60. Sengerová B., et al. Orchestrating the nucleases involved in DNA interstrand cross-link (ICL) repair. Cell Cycle 2011, 10:3999-4008.
61. Knipscheer P., et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009, 326:1698-1701.
62. Kim Y., et al. Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 2011, 43:142-146.
63. Stoepker C., et al. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet. 2011, 43:138-141.
64. Bogliolo M., et al. Mutations in the DNA repair endonuclease ERCC4/XPF cause Fanconi anemia. Am. J. Hum. Genet. 2013, 92:800-806.
65. Schuster B., et al. Whole exome sequencing reveals uncommon mutations in the recently identified Fanconi anemia gene SLX4/FANCP. Hum. Mutat. 2013, 34:93-96.
66. Farmer H., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
67. Bryant H.E., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
68. Hodskinson M.R.G., et al. Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol. Cell 2014, 54:472-484.
69. Douwel D.K., et al. XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol. Cell 2014, 54:460-471.
70. Hanada K., et al. The structure-specific endonuclease MUS81-EME1 promotes conversion of interstrand crosslinks into double-strand breaks. EMBO J. 2006, 25:4921-4932.
71. de Lange T. How telomeres solve the end-protection problem. Science 2009, 326:948-952.
72. Palm W., de Lange T. How Shelterin protects mammalian telomeres. Annu. Rev. Genet. 2008, 42:301-334.
73. Mocellin S., et al. Telomerase and the search for the end of cancer. Trends Mol. Med. 2013, 19:125-133.
74. Neumann A.A., et al. Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev. 2013, 27:18-23.
75. Wilson J.S., et al. Localization-dependent and independent roles of SLX4 in regulating telomeres. Cell Rep. 2013, 4:853-860.
76. Wan B., et al. SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 2013, 4:861-869.
77. Chan K.L., et al. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 2007, 26:3397-3409.
78. Baumann C., et al. PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 2007, 128:101-114.
79. Szakal B., Branzei D. Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover. EMBO J. 2013, 32:1155-1167.
80. Matos J., et al. Cell cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep. 2013, 4:76-86.
81. Gao M., et al. A novel role of human Holliday junction resolvase GEN1 in the maintenance of centrosome integrity. PLoS ONE 2012, 7:e49687.
82. Minocherhomji S., Hickson I.D. Structure-specific endonucleases: guardians of fragile site instability. Trends Cell Biol. 2014, 24:321-327.