RTEL1: Functions of a disease-associated helicase

Trends in Cell Biology

Volumn 24, Issue 7, 2014, Pages 416-425

  Vannier, Jean Baptiste ^a   Sarek, Grzegorz ^a   Boulton, Simon J ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

DNA repair; DNA replication; Double strand break repair; Homologous recombination; Hoyeraal Hreidarsson syndrome; Telomeres

Indexed keywords

DNA HELICASE; REGULATOR OF TELOMERE LENGTH 1; UNCLASSIFIED DRUG; TELOMERE BINDING PROTEIN;

ASTROCYTOMA; CANCER SUSCEPTIBILITY; DNA REPAIR; DNA REPLICATION; GENE CONTROL; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GLIOBLASTOMA; GLIOMA; HOYERAAL HREIDARSSON SYNDROME; HUMAN; MEIOTIC RECOMBINATION; MITOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; REVIEW; SYNDROME; TELOMERE HOMEOSTASIS; ANIMAL; DYSKERATOSIS CONGENITA; GENETICS; INTELLECTUAL IMPAIRMENT; INTRAUTERINE GROWTH RETARDATION; METABOLISM; MICROCEPHALY; MUTATION; TELOMERE;

ANIMALS; DNA HELICASES; DYSKERATOSIS CONGENITA; FETAL GROWTH RETARDATION; HUMANS; INTELLECTUAL DISABILITY; MICROCEPHALY; MUTATION; TELOMERE; TELOMERE-BINDING PROTEINS;

EID: 84903156621     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2014.01.004     Document Type: Review

References (94)

1. Bochman M.L., et al. DNA secondary structures: stability and function of G-quadruplex structures. Nat. Rev. Genet. 2012, 13:770-780.
2. Kruisselbrink E., et al. Mutagenic capacity of endogenous G4 DNA underlies genome instability in FANCJ-defective C. elegans. Curr. Biol. 2008, 18:900-905.
3. Paeschke K., et al. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 2011, 145:678-691.
4. Griffith J.D., et al. Mammalian telomeres end in a large duplex loop. Cell 1999, 97:503-514.
5. Wang R.C., et al. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 2004, 119:355-368.
6. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005, 19:2100-2110.
7. Sugiyama T., et al. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 1997, 272:7940-7945.
8. Ogawa T., et al. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 1993, 259:1896-1899.
9. Sung P., Robberson D.L. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 1995, 82:453-461.
10. Svendsen J.M., et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009, 138:63-77.
11. Lo Y.C., et al. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 2006, 26:4086-4094.
12. Wu L., et al. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4068-4073.
13. Vannier J.B., et al. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 2012, 149:795-806.
14. Ballew B.J., et al. A recessive founder mutation in regulator of telomere elongation helicase 1, RTEL1, underlies severe immunodeficiency and features of Hoyeraal-Hreidarsson syndrome. PLoS Genet. 2013, 9:e1003695.
15. Ballew B.J., et al. Germline mutations of regulator of telomere elongation helicase 1, RTEL1, in dyskeratosis congenita. Hum. Genet. 2013, 132:473-480.
16. Deng Z., et al. Inherited mutations in the helicase RTEL1 cause telomere dysfunction and Hoyeraal-Hreidarsson syndrome. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E3408-E3416.
17. Le Guen T., et al. Human RTEL1 deficiency causes Hoyeraal-Hreidarsson syndrome with short telomeres and genome instability. Hum. Mol. Genet. 2013, 22:3239-3249.
18. Walne A.J., et al. Constitutional mutations in RTEL1 cause severe dyskeratosis congenita. Am. J. Hum. Genet. 2013, 92:448-453.
19. Fairman-Williams M.E., et al. SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 2010, 20:313-324.
20. Marchler-Bauer A., et al. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 2009, 37:D205-D210.
21. White M.F. Structure, function and evolution of the XPD family of iron-sulfur-containing 5'->3' DNA helicases. Biochem. Soc. Trans. 2009, 37:547-551.
22. Gari K., et al. MMS19 links cytoplasmic iron-sulfur cluster assembly to DNA metabolism. Science 2012, 337:243-245.
23. Stehling O., et al. MMS19 assembles iron-sulfur proteins required for DNA metabolism and genomic integrity. Science 2012, 337:195-199.
24. Zhu L., et al. Telomere length regulation in mice is linked to a novel chromosome locus. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:8648-8653.
25. Ding H., et al. Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 2004, 117:873-886.
26. Uringa E.J., et al. RTEL1 contributes to DNA replication and repair and telomere maintenance. Mol. Biol. Cell 2012, 23:2782-2792.
27. Vannier J.B., et al. RTEL1 is a replisome-associated helicase that promotes telomere and genome-wide replication. Science 2013, 342:239-242.
28. Barber L.J., et al. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 2008, 135:261-271.
29. Sung P., Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 2006, 7:739-750.
30. Mets D.G., Meyer B.J. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 2009, 139:73-86.
31. Youds J.L., et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 2010, 327:1254-1258.
32. Rosu S., et al. Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 2011, 334:1286-1289.
33. Doksani Y., et al. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 2013, 155:345-356.
34. Amiard S., et al. A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 2007, 14:147-154.
35. Gilson E., Geli V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 2007, 8:825-838.
36. Wan B., et al. SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 2013, 4:861-869.
37. Wilson J.S., et al. Localization-dependent and -independent roles of SLX4 in regulating telomeres. Cell Rep. 2013, 4:853-860.
38. Sfeir A., et al. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 2009, 138:90-103.
39. Durkin S.G., Glover T.W. Chromosome fragile sites. Annu. Rev. Genet. 2007, 41:169-192.
40. Andressoo J.O., et al. Nucleotide excision repair and its connection with cancer and ageing. Adv. Exp. Med. Biol. 2005, 570:45-83.
41. Bridge W.L., et al. The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair. Nat. Genet. 2005, 37:953-957.
42. Levitus M., et al. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group. J. Nat. Genet. 2005, 37:934-935.
43. Levran O., et al. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 2005, 37:931-933.
44. Litman R., et al. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 2005, 8:255-265.
45. Capo-Chichi J.M., et al. Identification and biochemical characterization of a novel mutation in DDX11 causing Warsaw breakage syndrome. Hum. Mutat. 2013, 34:103-107.
46. van der Lelij P., et al. Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1. Am. J. Hum. Genet. 2010, 86:262-266.
47. Wrensch M., et al. Variants in the CDKN2B and RTEL1 regions are associated with high-grade glioma susceptibility. Nat. Genet. 2009, 41:905-908.
48. Shete S., et al. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009, 41:899-904.
49. Liu Y., et al. Polymorphisms of LIG4, BTBD2, HMGA2, and RTEL1 genes involved in the double-strand break repair pathway predict glioblastoma survival. J. Clin. Oncol. 2010, 28:2467-2474.
50. Rajaraman P., et al. Genome-wide association study of glioma and meta-analysis. Hum. Genet. 2012, 131:1877-1888.
51. Melin B., et al. Known glioma risk loci are associated with glioma with a family history of brain tumours - a case-control gene association study. Int. J. Cancer 2013, 132:2464-2468.
52. Egan K.M., et al. Cancer susceptibility variants and the risk of adult glioma in a US case-control study. J. Neurooncol. 2011, 104:535-542.
53. Gallus G.N., et al. Alu-element insertion in an OPA1 intron sequence associated with autosomal dominant optic atrophy. Mol. Vis. 2010, 16:178-183.
54. Alonso C.R., Akam M. A Hox gene mutation that triggers nonsense-mediated RNA decay and affects alternative splicing during Drosophila development. Nucleic Acids Res. 2003, 31:3873-3880.
55. Dehainault C., et al. A deep intronic mutation in the RB1 gene leads to intronic sequence exonisation. Eur. J. Hum. Genet. 2007, 15:473-477.
56. Bovolenta M., et al. Identification of a deep intronic mutation in the COL6A2 gene by a novel custom oligonucleotide CGH array designed to explore allelic and genetic heterogeneity in collagen VI-related myopathies. BMC Med. Genet. 2010, 11:44.
57. Gilbertson R.J., Ellison D.W. The origins of medulloblastoma subtypes. Annu. Rev. Pathol. 2008, 3:341-365.
58. Wu X., et al. Generation of a mouse model for studying the role of upregulated RTEL1 activity in tumorigenesis. Transgenic Res. 2012, 21:1109-1115.
59. Bai C., et al. Overexpression of M68/DcR3 in human gastrointestinal tract tumors independent of gene amplification and its location in a four-gene cluster. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:1230-1235.
60. Pitti R.M., et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature 1998, 396:699-703.
61. Muleris M., et al. Identification of amplified DNA sequences in breast cancer and their organization within homogeneously staining regions. Genes Chromosomes Cancer 1995, 14:155-163.
62. Clevers H., Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012, 149:1192-1205.
63. Armanios M. Syndromes of telomere shortening. Annu. Rev. Genomics Hum. Genet. 2009, 10:45-61.
64. Armanios M., et al. Short telomeres are sufficient to cause the degenerative defects associated with aging. Am. J. Hum. Genet. 2009, 85:823-832.
65. Armanios M., Blackburn E.H. The telomere syndromes. Nat. Rev. Genet. 2012, 13:693-704.
66. Lopez-Otin C., et al. The hallmarks of aging. Cell 2013, 153:1194-1217.
67. Campisi J., d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 2007, 8:729-740.
68. Kuilman T., et al. The essence of senescence. Genes Dev. 2010, 24:2463-2479.
69. Ortega J.A., et al. Congenital dyskeratosis. Zinsser-Engman-Cole syndrome with thymic dysplasia and aplastic anemia. Am. J. Dis. Child. 1972, 124:701-704.
70. Coulthard S., et al. Chromosomal breakage analysis in dyskeratosis congenita peripheral blood lymphocytes. Br. J. Haematol. 1998, 102:1162-1164.
71. Dokal I. Dyskeratosis congenita in all its forms. Br. J. Haematol. 2000, 110:768-779.
72. Dokal I. Dyskeratosis congenita. Hematology Am. Soc. Hematol. Educ. Program 2011, 2011:480-486.
73. Vulliamy T., et al. The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature 2001, 413:432-435.
74. Savage S.A., et al. TINF2, a component of the shelterin telomere protection complex, is mutated in dyskeratosis congenita. Am. J. Hum. Genet. 2008, 82:501-509.
75. Walne A.J., et al. TINF2 mutations result in very short telomeres: analysis of a large cohort of patients with dyskeratosis congenita and related bone marrow failure syndromes. Blood 2008, 112:3594-3600.
76. Walne A.J., et al. Genetic heterogeneity in autosomal recessive dyskeratosis congenita with one subtype due to mutations in the telomerase-associated protein NOP10. Hum. Mol. Genet. 2007, 16:1619-1629.
77. Zhong F., et al. Disruption of telomerase trafficking by TCAB1 mutation causes dyskeratosis congenita. Genes Dev. 2011, 25:11-16.
78. Mitchell J.R., et al. A telomerase component is defective in the human disease dyskeratosis congenita. Nature 1999, 402:551-555.
79. Heiss N.S., et al. X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat. Genet. 1998, 19:32-38.
80. Vulliamy T.J., et al. Mutations in dyskeratosis congenita: their impact on telomere length and the diversity of clinical presentation. Blood 2006, 107:2680-2685.
81. Knight S.W., et al. Unexplained aplastic anaemia, immunodeficiency, and cerebellar hypoplasia (Hoyeraal-Hreidarsson syndrome) due to mutations in the dyskeratosis congenita gene, DKC1. Br. J. Haematol. 1999, 107:335-339.
82. Marrone A., et al. Telomerase reverse-transcriptase homozygous mutations in autosomal recessive dyskeratosis congenita and Hoyeraal-Hreidarsson syndrome. Blood 2007, 110:4198-4205.
83. Knight S., et al. Dyskeratosis Congenita (DC) Registry: identification of new features of DC. Br. J. Haematol. 1998, 103:990-996.
84. Walne A.J., Dokal I. Advances in the understanding of dyskeratosis congenita. Br. J. Haematol. 2009, 145:164-172.
85. Walne A.J., et al. Mutations in C16orf57 and normal-length telomeres unify a subset of patients with dyskeratosis congenita, poikiloderma with neutropenia and Rothmund-Thomson syndrome. Hum. Mol. Genet. 2010, 19:4453-4461.
86. Faure G., et al. The C-terminal extension of human RTEL1, mutated in Hoyeraal-Hreidarsson syndrome, contains Harmonin-N-like domains. Proteins 2013, 10.1002/prot.24438.
87. Fan L., et al. XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell 2008, 133:789-800.
88. Wolski S.C., et al. Crystal structure of the FeS cluster-containing nucleotide excision repair helicase XPD. PLoS Biol. 2008, 6:e149.
89. Singleton M.R., et al. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76:23-50.
90. Kellenberger E., et al. Solution structure of the C-terminal domain of TFIIH P44 subunit reveals a novel type of C4C4 ring domain involved in protein-protein interactions. J. Biol. Chem. 2005, 280:20785-20792.
91. Cesare A.J., Reddel R.R. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 2010, 11:319-330.
92. Kim J.H., et al. SCFhFBH1 can act as helicase and E3 ubiquitin ligase. Nucleic Acids Res. 2004, 32:2287-2297.
93. Pugh R.A., et al. The iron-containing domain is essential in Rad3 helicases for coupling of ATP hydrolysis to DNA translocation and for targeting the helicase to the single-stranded DNA-double-stranded DNA junction. J. Biol. Chem. 2008, 283:1732-1743.
94. Rudolf J., et al. The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol. Cell 2006, 23:801-808.