Flap endonuclease 1 limits telomere fragility on the leading strand

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 15133-15145

  Teasley, Daniel C ^a   Parajuli, Shankar ^a   Nguyen, Mai ^a   Moore, Hayley R ^a   Alspach, Elise ^a   Lock, Ying Jie ^a,b   Honaker, Yuchi ^a,c   Saharia, Abhishek ^a,d   Piwnica Worms, Helen ^a,e   Stewart, Sheila A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c USA   (United States)

^d DiscoveRx Corporation   (United States)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; DISEASES; DNA; DNA SEQUENCES; GENES; RNA;

DNA REPLICATIONS; FLAP ENDONUCLEASE-1; GENOME STABILITY; GENOMIC INSTABILITY; HYBRID STRUCTURE; MOLECULAR MECHANISM; NUCLEASE ACTIVITY; RNA POLYMERASE II;

NUCLEIC ACIDS;

FLAP ENDONUCLEASE; FLAP ENDONUCLEASE 1; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME FRAGILITY; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA HYBRIDIZATION; ENZYME INHIBITION; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HYDROLYSIS; IONIZING RADIATION; METAPHASE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RNA HYBRIDIZATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TELOMERE; DNA DAMAGE; DNA REPLICATION; GENETICS; HEK293 CELL LINE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BLOTTING, WESTERN; DNA DAMAGE; DNA REPLICATION; FLAP ENDONUCLEASES; HEK293 CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TELOMERE; TRANSCRIPTION, GENETIC;

EID: 84931281855     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.647388     Document Type: Article

References (53)

1. Sidorova, J. M. (2008) Roles of the Werner syndrome RecQ helicase in DNA replication. DNA Repair 7, 1776-1786
2. Singh, D. K., Ahn, B., and Bohr, V. A. (2009) Roles of RECQ helicases in recombination based DNA repair, genomic stability and aging. Biogerontology 10, 235-252
3. Gilson, E., and Géli, V. (2007) How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 8, 825-838
4. Burrow, A. A., Marullo, A., Holder, L. R., and Wang, Y.-H. (2010) Secondary structure formation and DNA instability at fragile site FRA16B. Nucleic Acids Res. 38, 2865-2877
5. Helmrich, A., Ballarino, M., and Tora, L. (2011) Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 44, 966-977
6. Letessier, A., Millot, G. A., Koundrioukoff, S., Lachagès, A.-M., Vogt, N., Hansen, R. S., Malfoy, B., Brison, O., and Debatisse, M. (2011) Cell typespecific replication initiation programs set fragility of the FRA3B fragile site. Nature 470, 120-123
7. Sfeir, A., Kosiyatrakul, S. T., Hockemeyer, D., MacRae, S. L., Karlseder, J., Schildkraut, C. L., and De Lange, T. (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138, 90-103
8. Martínez, P., Thanasoula, M., Muñoz, P., Liao, C., Tejera, A., McNees, C., Flores, J. M., Fernández-Capetillo, O., Tarsounas, M., and Blasco, M. A. (2009) Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev. 23, 2060-2075
9. McNees, C. J., Tejera, A. M., Martínez, P., Murga, M., Mulero, F., Fernandez-Capetillo, O., and Blasco, M. A. (2010) ATR suppresses telomere fragility and recombination but is dispensable for elongation of short telomeres by telomerase. J. Cell Biol. 188, 639-652
10. Vannier, J.-B., Pavicic-Kaltenbrunner, V., Petalcorin, M. I., Ding, H., and Boulton, S. J. (2012) RTEL1 Dismantles T Loops and Counteracts Telomeric G4-DNA to Maintain Telomere Integrity. Cell 149, 795-806
11. Stewart, J. A., Wang, F., Chaiken, M. F., Kasbek, C., Chastain, P. D., 2nd, Wright, W. E., and Price, C. M. (2012) Human CST promotes telomere duplex replication and general replication restart after fork stalling. EMBO J. 31, 3537-3549
12. Saharia, A., Teasley, D. C., Duxin, J. P., Dao, B., Chiappinelli, K. B., and Stewart, S. A. (2010) FEN1 ensures telomere stability by facilitating replication fork re-initiation. J. Biol. Chem. 285, 27057-27066
13. Vallabhaneni, H., O'Callaghan, N., Sidorova, J., and Liu, Y. (2013) Defective repair of oxidative base lesions by the DNA glycosylase Nth1 associates with multiple telomere defects. PLoS Genet. 9, e1003639
14. Dalcontres, M. S., Palacios, J. A., Mejias, D., and Blasco, M. A. (2014) TopoIIα prevents telomere fragility and formation of ultra thin DNA bridges during mitosis through TRF1-dependent binding to telomeres. Cell Cycle 13, 1463-1481
15. Chawla, R., Redon, S., Raftopoulou, C., Wischnewski, H., Gagos, S., and Azzalin, C. M. (2011) Human UPF1 interacts with TPP1 and telomerase and sustains telomere leading-strand replication. EMBO J. 30, 4047-4058
16. Arora, R., Lee, Y., Wischnewski, H., Brun, C. M., Schwarz, T., and Azzalin, C. M. (2014) RNaseH1 regulates TERRA-telomeric DNA hybrids and telomere maintenance in ALT tumour cells. Nat. Commun. 5, 5220
17. Rudolph, C. J., Dhillon, P., Moore, T., and Lloyd, R. G. (2007) Avoiding and resolving conflicts between DNA replication and transcription. DNA Repair 6, 981-993
18. Liu, B., Wong, M. L., Tinker, R. L., Geiduschek, E. P., and Alberts, B. M. (1993) The DNA replication fork can pass RNA polymerase without displacing the nascent transcript. Nature 366, 33-39
19. Prado, F., and Aguilera, A. (2005) Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24, 1267-1276
20. Pomerantz, R. T., and O'Donnell, M. (2008) The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456, 762-766
21. Sordet, O., Nakamura, A. J., Redon, C. E., and Pommier, Y. (2010) DNA double-strand breaks and ATM activation by transcription-blocking DNA lesions. Cell Cycle 9, 274-278
22. Skourti-Stathaki, K., and Proudfoot, N. J. (2014) A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev. 28, 1384-1396
23. Stewart, S. A., Ben-Porath, I., Carey, V. J., O'Connor, B. F., Hahn, W. C, and Weinberg, R. A. (2003) Erosion of the telomeric single-strand overhang at replicative senescence. Nat. Genet. 33, 492-496
24. Saharia, A., Guittat, L., Crocker, S., Lim, A., Steffen, M., Kulkarni, S., and Stewart, S. A. (2008) Flap endonuclease 1 contributes to telomere stability. Curr. Biol. 18, 496-500
25. Stewart, S. A., Dykxhoorn, D. M., Palliser, D., Mizuno, H., Yu, E. Y., An, D. S., Sabatini, D. M., Chen, I. S., Hahn, W. C., Sharp, P. A., Weinberg, R. A., and Novina, C. D. (2003) Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9, 493-501
26. Honaker, Y., and Piwnica-Worms, H. (2010) Casein kinase 1 functions as both penultimate and ultimate kinase in regulating Cdc25A destruction. Oncogene 29, 3324-3334
27. Lansdorp, P. M., Verwoerd, N. P., Van De Rijke, F. M., Dragowska, V., Little, M.-T., Dirks, R. W., Raap, A. K., and Tanke, H. J. (1996) Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5, 685-691
28. Bailey, S. M., Cornforth, M. N., Kurimasa, A., Chen, D. J., and Goodwin, E. H. (2001) Strand-specific postreplicative processing of mammalian telomeres. Science 293, 2462-2465
29. Duxin, J. P., Dao, B., Martinsson, P., Rajala, N., Guittat, L., Campbell, J. L., Spelbrink, J. N., and Stewart, S. A. (2009) Human Dna2 is a nuclear and mitochondrial DNA maintenance protein. Mol. Cell. Biol. 29, 4274-4282
30. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., Chapter 7, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
31. Schoeftner, S., and Blasco, M. A. (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol. 10, 228-236
32. Azzalin, C M., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801
33. Sabouri, N., McDonald, K. R., Webb, C. J., Cristea, I. M., and Zakian, V. A. (2012) DNA replication through hard-to-replicate sites, including both highly transcribed RNA Pol II and Pol III genes, requires the S. pombe Pfh1 helicase. Genes Dev. 26, 581-593
34. Azvolinsky, A., Giresi, P. G., Lieb, J. D., and Zakian, V. A. (2009) Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34, 722-734
35. Bah, A., Wischnewski, H., Shchepachev, V., and Azzalin, C. M. (2012) The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res. 40, 2995-3005
36. Stewart, J. A., Campbell, J. L., and Bambara, R. A. (2006) Flap endonuclease disengages Dna2 helicase/nuclease from Okazaki fragment flaps. J. Biol. Chem. 281, 38565-38572
37. Rudd, M. D., and Luse, D. S. (1996) Amanitin greatly reduces the rate of transcription by RNA polymerase II ternary complexes but fails to inhibit some transcript cleavage modes. J. Biol. Chem. 271, 21549-21558
38. Bushnell, D. A., Cramer, P., and Kornberg, R. D. (2002) Structural basis of transcription: α-amanitin-RNA polymerase II cocrystal at 2.8 A resolution. Proc. Natl. Acad. Sci. U. S. A. 99, 1218-1222
39. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H, and Lieberman, P. M. (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35, 403-413
40. Balk, B., Maicher, A., Dees, M., Klermund, J., Luke-Glaser, S., Bender, K., and Luke, B. (2013) Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct. Mol. Biol. 20, 1199-1205
41. Parrish, J. Z., Yang, C., Shen, B., and Xue, D. (2003) CRN-1, a Caenorhabditis elegans FEN-1 homologue, cooperates with CPS-6/EndoG to promote apoptotic DNA degradation. EMBOJ. 22, 3451-3460
42. Zheng, L., Zhou, M., Chai, Q., Parrish, J., Xue, D., Patrick, S. M., Turchi, J. J., Yannone, S. M., Chen, D., and Shen, B. (2005) Novel function of the flap endonuclease 1 complex in processing stalled DNA replication forks. EMBORep. 6, 83-89
43. Liu, Y., Kao, H.-I., and Bambara, R. A. (2004) Flap endonuclease 1: a central component of DNA metabolism. Annu. Rev. Biochem. 73, 589-615
44. Li, X., Li, J., Harrington, J., Lieber, M. R., and Burgers, P. M. (1995) Lagging strand DNA synthesis at the eukaryotic replication fork involves binding and stimulation of FEN-1 by proliferating cell nuclear antigen. J. Biol. Chem. 270, 22109-22112
45. Guo, Z., Chavez, V., Singh, P., Finger, L. D., Hang, H., Hegde, M. L., and Shen, B. (2008) Comprehensive mapping of the C-terminus of flap endonuclease-1 reveals distinct interaction sites for five proteins that represent different DNA replication and repair pathways. J. Mol. Biol. 377, 679-690
46. Shen, B., Nolan, J. P., Sklar, L. A., and Park, M. S. (1996) Essential amino acids for substrate binding and catalysis of human flap endonuclease 1. J. Biol. Chem. 271, 9173-9176
47. Tsutakawa, S. E., Classen, S., Chapados, B. R., Arvai, A. S., Finger, L. D., Guenther, G., Tomlinson, C. G., Thompson, P., Sarker, A. H., Shen, B., Cooper, P. K., Grasby, J. A., and Tainer, J. A. (2011) Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily. Cell 145, 198-211
48. Bornarth, C. J., Ranalli, T. A., Henricksen, L. A., Wahl, A. F., and Bambara, R. A. (1999) Effect of flap modifications on human FEN1 cleavage. Biochemistry 38, 13347-13354
49. Atkinson, J., Gupta, M. K., and McGlynn, P. (2011) Interaction of Rep and DnaB on DNA. Nucleic Acids Res. 39, 1351-1359
50. Fu, Y. V., Yardimci, H., Long, D. T., Ho, T. V., Guainazzi, A., Bermudez, V. P., Hurwitz, J., Van Oijen, A., Schärer, O. D., and Walter, J. C. (2011) Selective by pass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146, 931-941
51. Muftuoglu, M., Wong, H. K., Imam, S. Z., Wilson, D. M., 3rd, Bohr, V. A., and Opresko, P. L. (2006) Telomere repeat binding factor 2 interacts with base excision repair proteins and stimulates DNA synthesis by DNA polymerase β. Cancer Res. 66, 113-124
52. Badie, S., Escandell, J. M., Bouwman, P., Carlos, A. R., Thanasoula, M., Gallardo, M. M., Suram, A., Jaco, I., Benitez, J., Herbig, U., Blasco, M. A., Jonkers, J., and Tarsounas, M. (2010) BRCA2 acts as a RAD51 loader to facilitate telomere replication and capping. Nat Struct. Mol. Biol. 17, 1461-1469
53. Popuri, V., Hsu, J., Khadka, P., Horvath, K., Liu, Y., Croteau, D. L., and Bohr, V. A. (2014) Human RECQL1 participates in telomere maintenance. Nucleic Acids Res. 42, 5671-5688