PIF1 disruption or NBS1 hypomorphism does not affect chromosome healing or fusion resulting from double-strand breaks near telomeres in murine embryonic stem cells

DNA Repair

Volumn 10, Issue 11, 2011, Pages 1164-1173

  Reynolds, Gloria E ^a   Gao, Qing ^b   Miller, Douglas ^a   Snow, Bryan E ^c   Harrington, Lea A ^d   Murnane, John P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chromosome fusion; Chromosome healing; Chromosome instability; Double strand break; NBS1; PIF1; Telomere

Indexed keywords

GENOMIC DNA; MRE11 PROTEIN; NIBRIN; PROTEIN; PROTEIN PIF1; PROTEIN XRS2; RAD50 PROTEIN; TELOMERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMOSOMAL PARAMETERS; CHROMOSOME FUSION; CHROMOSOME HEALING; CHROMOSOME REARRANGEMENT; DNA DEGRADATION; DNA POLYMORPHISM; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; EMBRYONIC STEM CELL; GENE DELETION; GENE DISRUPTION; GENE MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TELOMERE;

ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CHROMOSOME ABERRATIONS; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; EMBRYONIC STEM CELLS; FEMALE; GENE KNOCKOUT TECHNIQUES; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; SEQUENCE ALIGNMENT; TELOMERASE; TELOMERE;

MAMMALIA; MURINAE; SACCHAROMYCES CEREVISIAE;

EID: 80054723759     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.09.002     Document Type: Article

References (60)

1. Blackburn E.H., Greider C.W., Szostak J.W. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 2006, 12:1133-1138.
2. Artandi S.E., DePinho R.A. Telomeres and telomerase in cancer. Carcinogenesis 2010, 31:9-18.
3. Diede S.J., Gottschling D.E. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerase α and δ. Cell 1999, 99:723-733.
4. Zhou J.-Q., Monson E.K., Teng S.-C., Schultz V.P., Zakian V.A. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 2000, 289:771-774.
5. Schulz V.P, Zakian V.A. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 1994, 76:145-155.
6. Pennaneach V., Putnam C.D., Kolodner R.D. Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol. Microbiol. 2006, 59:1357-1368.
7. Eugster A., Lanzuolo C., Bonneton M., Luciano P., Pollice A., Pulitzer J.F., Stegberg E., Berthiau A.S., Forstemann K., Corda Y., Lingner J., Geli V., Gilson E. The finger subdomain of yeast telomerase cooperates with Pif1p to limit telomere elongation. Nat. Struct. Mol. Biol. 2006, 13:734-739.
8. Diede S.J., Gottschling D.E. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 2001, 11:1336-1340.
9. Goudsouzian L.K., Tuzon C.T., Zakian V.A. S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol. Cell 2006, 24:603-610.
10. Chung W.H., Zhu Z., Papusha A., Malkova A., Ira G. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet. 2010, 6:e1000948.
11. Lydeard J.R., Lipkin-Moore Z., Jain S., Eapen V.V., Haber J.E. Sgs1 and exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLoS Genet. 2010, 6:e1000973.
12. Varley H., Di S., Scherer S.W., Royle N.J. Characterization of terminal deletions at 7q32 and 22q13.3 healed by de novo telomere addition. Am. J. Hum. Genet. 2000, 67:610-622.
13. Wong A.C., Ning Y., Flint J., Clark K., Dumanski J.P., Ledbetter D.H., McDermid H.E. Molecular characterization of a 130-kb terminal microdeletion at 22q in a child with mild mental retardation. Am. J. Hum. Genet. 1997, 60:113-120.
14. Flint J., Thomas K., Micklem G., Raynham H., Clark K., Doggett N.A., King A., Higgs D.R. The relationship between chromosome structure and function at a human telomeric region. Nat. Genet. 1997, 15:252-257.
15. Morin G.B. Recognition of a chromosome truncation site associated with α-thalassaemia by human telomerase. Nature 1991, 353:454-456.
16. Harrington L.A., Greider C.W. Telomerase primer specificity and chromosome healing. Nature 1991, 353:451-454.
17. Honma M., Sakuraba M., Koizumi T., Takashima Y., Sakamoto H., Hayashi M. Non-homologous end-joining for repairing I-SceI-induced DNA double strand breaks in human cells. DNA Repair (Amst) 2007, 6:781-788.
18. Lin Y., Waldman A.S. Capture of DNA sequences at double-strand breaks in mammalian cells. Genetics 2001, 158:1665-1674.
19. Rebuzzini P., Khoriauli L., Azzalin C.M., Magnani E., Mondello C., Giulotto E. New mammalian cellular systems to study mutations introduced at the break site by non-homologous end-joining. DNA Repair (Amst) 2005, 4:546-555.
20. Latre L., Genesca A., Martin M., Ribas M., Egozcue J., Blasco M.A., Tusell L. Repair of DNA broken ends is similar in embryonic fibroblasts with and without telomerase. Radiat. Res. 2004, 162:136-142.
21. Gao Q., Reynolds G.E., Wilcox A., Miller D., Cheung P., Artandi S.E., Murnane J.P. Telomerase-dependent and -independent chromosome healing in mouse embryonic stem cells. DNA Repair 2008, 7:1233-1249.
22. Sprung C.N., Reynolds G.E., Jasin M., Murnane J.P. Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:6781-6786.
23. Lo A.W.I., Sprung C.N., Fouladi B., Pedram M., Sabatier L., Ricoul M., Reynolds G.E., Murnane J.P. Chromosome instability as a result of double-strand breaks near telomeres in mouse embryonic stem cells. Mol. Cell. Biol. 2002, 22:4836-4850.
24. Snow B.E., Mateyak M., Paderova J., Wakeham A., Iorio C., Zakian V., Squire J., Harrington L. Murine Pif1 interacts with telomerase and is dispensable for telomere function in vivo. Mol. Cell. Biol. 2007, 27:1017-1026.
25. Mateyak M.K., Zakian V.A. Human PIF helicase is cell cycle regulated and associates with telomerase. Cell Cycle 2006, 5:2796-2804.
26. Williams R.S., Dodson G.E., Limbo O., Yamada Y., Williams J.S., Guenther G., Classen S., Glover J.N., Iwasaki H., Russell P., Tainer J.A. Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 2009, 139:87-99.
27. Lloyd J., Chapman J.R., Clapperton J.A., Haire L.F., Hartsuiker E., Li J., Carr A.M., Jackson S.P., Smerdon S.J. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 2009, 139:100-111.
28. Williams B.R., Mirzoeva O.K., Morgan W.F., Lin J., Dunnick W., Petrini J.H.J. A murine model of Nijmegen Breakage Syndrome. Curr. Biol. 2002, 12:648-653.
29. Stracker T.H., Couto S.S., Cordon-Cardo C., Matos T., Petrini J.H. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol. Cell 2008, 31:21-32.
30. Shull E.R., Lee Y., Nakane H., Stracker T.H., Zhao J., Russell H.R., Petrini J.H., McKinnon P.J. Differential DNA damage signaling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 2009, 23:171-180.
31. Gao Q., Reynolds G.E., Innes L., Pedram M., Jones E., Junabi M., Gao D.-W., Ricoule M., Sabatier L., Van Brocklin H., Franc B.L., Murnane J.P. Telomeric transgenes are silenced in adult mouse tissues and embryo fibroblasts, but are expressed in embryonic stem cells. Stem Cells 2007, 25:3085-3092.
32. Pedram M., Sprung C.N., Gao Q., Lo A.W.I., Reynolds G., Murnane J.P. Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell. Biol. 2006, 26:1865-1878.
33. Nagy A., Gertsenstein M., Vinersten K., Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press. 3rd ed.
34. Collins C., Rommens J.M., Kowbel D., Godfrey T., Tanner M., Hwang S.-I., Polikoff D., Nonet G., Cochran J., Myambo K., Jay K.E., Froula J., Cloutier T., Kou W.-L., Yaswen P., Dairkee S., Giovanola J., Hutchinson G.B., Isola J., Kallioniemi O.-P., Palazzolo M., Martin C., Ericsson C., Pinkel D., Albertson D., Li W.-B., Gray J.W. Positional cloning of ZNF217 and NABC1: genes amplified at 20q13.2 and overexpressed in breast carcinoma. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:8703-8708.
35. Richardson C., Moynahan M.E., Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 1998, 12:3831-3842.
36. Brisebois J.J., DuBow M.S. Selection for spontaneous null mutations in a chromosomally-integrated HSV-1 thymidine kinase gene yields deletions and a mutation caused by intragenic illegitimate recombination. Mutat. Res. 1993, 287:191-205.
37. Murata S., Matsuzaki T., Takai S., Yaoita H., Noda M. A new retroviral vector for detecting mutations and chromosomal instability in mammalian cells. Mutat. Res. 1995, 334:375-383.
38. Lo A.W.I., Sabatier L., Fouladi B., Pottier G., Ricoul M., Murnane J.P. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 2002, 6:531-538.
39. Zha S., Boboila C., Alt F.W. Mre11: roles in DNA repair beyond homologous recombination. Nat. Struct. Mol. Biol. 2009, 16:798-800.
40. Lavin M.F. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 2007, 26:7749-7758.
41. 1-3 repeats. Genes Dev. 1993, 7:2345-2356.
42. Kulkarni A., Zschenker O., Reynolds G., Miller D., Murnane J.P. The effect of telomere proximity on telomere position effect, chromosome healing and sensitivity to DNA double-strand breaks in a human tumor cell line. Mol. Cell. Biol. 2010, 30:578-589.
43. Murnane J.P. Telomere loss as a mechanism for chromosomal instability in human cancer. Cancer Res. 2010, 70:4255-4259.
44. Zschenker O., Kulkarni A., Miller D., Reynolds G.E., Granger-Locatelli M., Pottier G., Sabatier L., Murnane J.P. Increased sensitivity of subtelomeric regions to DNA double-strand breaks in a human tumor cell line. DNA Repair 2009, 8:886-900.
45. Makovets S., Blackburn E.H. DNA damage signalling prevents deleterious telomere addition at DNA breaks. Nat. Cell Biol. 2009, 11:1383-1386.
46. Karlseder J., Hoke K., Mirzoeva O.K., Bakkenist C., Kastan M.B., Petrini J.H., de Lange T. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2004, 2:E240.
47. Dewar J.M., Lydall D. Pif1- and Exo1-dependent nucleases coordinate checkpoint activation following telomere uncapping. EMBO J. 2010, 29:4020-4034.
48. Sabatier L., Ricoul M., Pottier G., Murnane J.P. The loss of a single telomere can result in genomic instability involving multiple chromosomes in a human tumor cell line. Mol. Cancer Res. 2005, 3:139-150.
49. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., Jackson S.P. Human CtIP promotes DNA end resection. Nature 2007, 450:509-514.
50. You Z., Shi L.Z., Zhu Q., Wu P., Zhang Y.W., Basilio A., Tonnu N., Verma I.M., Berns M.W., Hunter T. CtIP links DNA double-strand break sensing to resection. Mol. Cell 2009, 36:954-969.
51. Attwooll C.L., Akpinar M., Petrini J.H. The mre11 complex and the response to dysfunctional telomeres. Mol. Cell Biol. 2009, 29:5540-5551.
52. Deng Y., Guo X., Ferguson D.O., Chang S. Multiple roles for MRE11 at uncapped telomeres. Nature 2009, 460:914-918.
53. Rai R., Zheng H., He H., Luo Y., Multani A., Carpenter P.B., Chang S. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J. 2010, 29:2598-2610.
54. Rass E., Grabarz A., Plo I., Gautier J., Bertrand P., Lopez B.S. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 2009, 16:819-824.
55. Xie A., Kwok A., Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 2009, 16:814-818.
56. Deriano L., Stracker T.H., Baker A., Petrini J.H., Roth D.B. Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol. Cell 2009, 34:13-25.
57. Gao Y., Ferguson D.O., Xie W., Manis J.P., Sekiguchi J., Frank K.M., Chaudhuri J., Horner J., DePinho R.A., Alt F.W. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic instability and development. Nature 2000, 404:897-900.
58. Guirouilh-Barbat J., Huck S., Bertrand P., Pirzio L., Desmaze C., Sabatier L., Lopez B.S. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell 2004, 14:611-623.
59. Weinstock D.M., Brunet E., Jasin M. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 2007, 9:978-981.
60. Erdfelder E., Faul F., Buchner A. GPOWER: a general power analysis program. Behav. Res. Methods Instrum. Comput. 1996, 28:1-11.