RTEL1 contributes to DNA replication and repair and telomere maintenance

Molecular Biology of the Cell

Volumn 23, Issue 14, 2012, Pages 2782-2792

  Uringa, Evert Jan ^a,b   Lisaingo, Kathleen ^a   Pickett, Hilda A ^c,d   Brind'Amour, Julie ^a   Rohde, Jan Hendrik ^b   Zelensky, Alex ^e   Essers, Jeroen ^e,f   Lansdorp, Peter M ^a,b,g  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e Department of Cell Biology and Genetics   (Netherlands)

^f ERASMUS MEDICAL CENTER   (Netherlands)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; REGULATOR OF TELOMERE LENGTH 1; TELOMERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE REPRESSION; GENOME; HOMOLOGOUS RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SISTER CHROMATID EXCHANGE; TELOMERE; TELOMERE HOMEOSTASIS;

ANIMALS; CELLS, CULTURED; DNA; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA REPLICATION; EMBRYONIC STEM CELLS; FEMALE; GENE KNOCK-IN TECHNIQUES; GENOMIC INSTABILITY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SISTER CHROMATID EXCHANGE; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS;

MUS;

EID: 84863895896     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-03-0179     Document Type: Article

References (54)

1. Abraham J et al. (2003). Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J 22, 6137-6147. (Pubitemid 37463256)
2. Adams DJ et al. (2005). A genome-wide, end-sequenced 129Sv BAC library resource for targeting vector construction. Genomics 82, 753-758. (Pubitemid 41752956)
3. Bailey SM, Goodwin EH, Meyne J, Cornforth MN (1996). CO-FISH reveals inversions associated with isochromosome formation. Mutagenesis 11, 139-144. (Pubitemid 26085696)
4. Banaszynski LA, Chen LC, Maynard-Smith LA, Ooi AG, Wandless TJ (2006). A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126, 995-1004. (Pubitemid 44310772)
5. Barber LJ et al. (2008). RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 135, 261-271.
6. Bennardo N, Cheng A, Huang N, Stark JM (2008). Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4, e1000110.
7. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34. (Pubitemid 27431310)
8. Brewer BJ, Fangman WL (1987). The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51, 463-471.
9. Bryja V, Bonilla S, Cajanek L, Parish CL, Schwartz CM, Luo Y, Rao MS, Arenas E (2006). An efficient method for the derivation of mouse embryonic stem cells. Stem Cells 24, 844-849. (Pubitemid 44464717)
10. Bucholc M, Park Y, Lustig AJ (2001). Intrachromatid excision of telomeric DNA as a mechanism for telomere size control in Saccharomyces cerevisiae. Mol Cell Biol 21, 6559-6573. (Pubitemid 32927423)
11. Budzowska M et al. (2004). Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage-dependent recombination. EMBO J 23, 3548-3558. (Pubitemid 39265544)
12. Cesare AJ, Reddel RR (2010). Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 11, 319-330.
13. Chaganti RS, Schonberg S, German J (1974). A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc Natl Acad Sci USA 71, 4508-4512.
14. Cohen S, Lavi S (1996). Induction of circles of heterogeneous sizes in carcinogen-treated cells: two-dimensional gel analysis of circular DNA molecules. Mol Cell Biol 16, 2002-2014. (Pubitemid 26123720)
15. Copeland NG, Jenkins NA, Court DL (2001). Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2, 769-779. (Pubitemid 33685574)
16. de Lange T (2004). T-loops and the origin of telomeres. Nat Rev Mol Cell Biol 19, 323-329.
17. de Lange T (2005). Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 5, 2100-2110.
18. Ding H et al. (2004). Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 117, 873-886. (Pubitemid 38798854)
19. Dronkert ML, Beverloo HB, Johnson RD, Hoeijmakers JH, Jasin M, Kanaar R (2000). Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol Cell Biol 20, 3147-3156. (Pubitemid 30215027)
20. Durkin SG, Glover TW (2007). Chromosome fragile sites. Annu Rev Genet 41, 169-192.
21. Essers J, Hendriks RW, Swagemakers SM, Troelstra C, de Wit J, Bootsma D, Hoeijmakers JH, Kanaar R (1997). Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89, 195-204. (Pubitemid 27199892)
22. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, D'Andrea AD (2001). Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7, 249-262. (Pubitemid 32206493)
23. Gertsenstein M, Lobe C, Nagy A (2002). ES cell-mediated conditional transgenesis. Methods Mol Biol 185, 285-307.
24. Glover TW, Berger C, Coyle J, Echo B (1984). DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 67, 136-142. (Pubitemid 14095149)
25. Greider CW, Blackburn EH (1985). Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43, 405-413. (Pubitemid 16213265)
26. Henson JD, Cao Y, Huschtscha LI, Chang AC, Au AY, Pickett HA, Reddel RR (2009). DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat Biotechnol 27, 1181-1185.
27. Hirano S et al. (2005). Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J 24, 418-427. (Pubitemid 40216145)
28. Hussain S et al. (2004). Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum Mol Genet 13, 1241-1248. (Pubitemid 38877877)
29. Kipling D, Cooke HJ (1990). Hypervariable ultra-long telomeres in mice. Nature 347, 400-402.
30. Lansdorp PM, Verwoerd NP, van de Rijke FM, Dragowska V, Little MT, Dirks RW, Raap AK, Tanke HJ (1996). Heterogeneity in telomere length of human chromosomes. Hum Mol Genet 5, 685-691. (Pubitemid 26141285)
31. Liu P, Jenkins NA, Copeland NG (2003). A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13, 476-484. (Pubitemid 36395405)
32. Moynahan ME, Pierce AJ, Jasin M (2001). BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 7, 263-272. (Pubitemid 32206494)
33. Niedernhofer LJ, Essers J, Weeda G, Beverloo B, de Wit J, Muijtjens M, Odijk H, Hoeijmakers JH, Kanaar R (2001). The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J 20, 6540-6549. (Pubitemid 33078726)
34. Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P, Patel KJ (2004). The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15, 607-620. (Pubitemid 39141787)
35. Niida H, Matsumoto T, Satoh H, Shiwa M, Tokutake Y, Furuichi Y, Shinkai Y (1998). Severe growth defect in mouse cells lacking the telomerase RNA component. Nat Genet 19, 203-206. (Pubitemid 28248807)
36. Perry P, Wolff S (1974). New Giemsa method for the differential staining of sister chromatids. Nature 251, 156-158.
37. Petermann E, Helleday T (2010). Pathways of mammalian replication fork restart. Nat Rev Mol Cell Biol 11, 683-687.
38. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T (2010). Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 37, 492-502.
39. Pickett HA, Henson JD, Au AY, Neumann AA, Reddel RR (2011). Normal mammalian cells negatively regulate telomere length by telomere trimming. Hum Mol Genet 20, 4684-4692.
40. Pryde F, Khalili S, Robertson K, Selfridge J, Ritchie AM, Melton DW, Jullien D, Adachi Y (2005). 53BP1 exchanges slowly at the sites of DNA damage and appears to require RNA for its association with chromatin. J Cell Sci 118, 2043-2055. (Pubitemid 40723847)
41. Sen D, Gilbert W (1992). Guanine quartet structures. Methods Enzymol 211, 191-199.
42. Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T (2009). Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138, 90-103.
43. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, Cortez D (2011). Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25, 1320-1327.
44. Sonoda E, Sasaki MS, Morrison C, Yamaguchi-Iwai Y, Takata M, Takeda S (1999). Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol Cell Biol 19, 5166-5169. (Pubitemid 29289554)
45. Takai H, Smogorzewska A, de Lange T (2003). DNA damage foci at dysfunctional telomeres. Curr Biol 13, 1549-1556. (Pubitemid 37078413)
46. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, D'Andrea AD (2002). S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100, 2414-2420.
47. Thompson LH, Hinz JM (2009). Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: mechanistic insights. Mutat Res 668, 54-72.
48. Uringa EJ, Youds JL, Lisaingo K, Lansdorp PM, Boulton SJ (2011). RTEL1: an essential helicase for telomere maintenance and the regulation of homologous recombination. Nucleic Acids Res 39, 1647-1655.
49. Wang RC, Smogorzewska A, de Lange T (2004). Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368. (Pubitemid 39423838)
50. Wang W, Seki M, Narita Y, Sonoda E, Takeda S, Yamada K, Masuko T, Katada T, Enomoto T (2000). Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J 19, 3428-3435. (Pubitemid 30428220)
51. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG (2005). Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33, e36.
52. Yamamoto K et al. (2005). Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol Cell Biol 25, 34-43. (Pubitemid 40039797)
53. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, NJ ON, Rose AM, West SC, Meyer BJ, Boulton SJ (2010). RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327, 1254-1258.
54. Zijlmans JM, Martens UM, Poon SS, Raap AK, Tanke HJ, Ward RK, Lansdorp PM (1997). Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc Natl Acad Sci USA 94, 7423-7428. (Pubitemid 27345331)