Human telomeres replicate using chromosomespecific, rather than universal, replication programs

Journal of Cell Biology

Volumn 197, Issue 2, 2012, Pages 253-266

  Drosopoulos, William C ^a   Kosiyatrakul, Settapong T ^a   Yan, Zi ^a   Calderano, Simone G ^a   Schildkraut, Carl L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL TYPE; CHROMOSOME REPLICATION; DNA REPLICATION; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REPLISOME; SOMATIC CELL; TELOMERE; HELA CELL; HETEROCHROMATIN; HUMAN CHROMOSOME; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

DNA;

CELL LINE, TUMOR; CHROMOSOMES, HUMAN; DNA; DNA REPLICATION; EMBRYONIC STEM CELLS; HELA CELLS; HETEROCHROMATIN; HUMANS; TELOMERE;

EID: 84861933930     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201112083     Document Type: Article

References (49)

1. Aladjem, M.I. 2007. Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat. Rev. Genet. 8:588-600. http://dx.doi.org/10.1038/nrg2143
2. Anand, R.P., K.A. Shah, H. Niu, P. Sung, S.M. Mirkin, and C.H. Freudenreich. 2012. Overcoming natural replication barriers: differential helicase requirements. Nucleic Acids Res. 40:1091-1105. http://dx.doi.org/10.1093/nar/gkr836
3. Arnoult, N., C. Schluth-Bolard, A. Letessier, I. Drascovic, R. Bouarich-Bourimi, J. Campisi, S.H. Kim, A. Boussouar, A. Ottaviani, F. Magdinier, et al. 2010. Replication timing of human telomeres is chromosome arm-specific, influenced by subtelomeric structures and connected to nuclear localization. PLoS Genet. 6:e1000920. http://dx.doi.org/10.1371/journal.pgen.1000920
4. Atanasiu, C., Z. Deng, A. Wiedmer, J. Norseen, and P.M. Lieberman. 2006. ORC binding to TRF2 stimulates OriP replication. EMBO Rep. 7:716- 721. http://dx.doi.org/10.1038/sj.embor.7400730
5. Azzalin, C.M., P. Reichenbach, L. Khoriauli, E. Giulotto, and J. Lingner. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science. 318:798-801. http://dx.doi.org/10.1126/science.1147182
6. Benetti, R., M. García-Cao, and M.A. Blasco. 2007. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39:243-250. http://dx.doi.org/10.1038/ng1952
7. Berbenetz, N.M., C. Nislow, and G.W. Brown. 2010. Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet. 6:e1001092. http://dx.doi.org/10.1371/journal.pgen.1001092
8. Branzei, D., and M. Foiani. 2010. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11:208-219. http://dx.doi.org/ 10.1038/nrm2852
9. Brock, G.J., J. Charlton, and A. Bird. 1999. Densely methylated sequences that are preferentially localized at telomere-proximal regions of human chromosomes. Gene. 240:269-277. http://dx.doi.org/10.1016/S0378-1119(99) 00442-4
10. Chawla, R., S. Redon, C. Raftopoulou, H. Wischnewski, S. Gagos, and C.M. Azzalin. 2011. Human UPF1 interacts with TPP1 and telomerase and sustains telomere leading-strand replication. EMBO J. 30:4047-4058. http://dx.doi.org/10.1038/emboj.2011.280
11. Crabbe, L., R.E. Verdun, C.I. Haggblom, and J. Karlseder. 2004. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science. 306:1951-1953. http://dx.doi.org/10.1126/science.1103619
12. Cross, S., J. Lindsey, J. Fantes, S. McKay, N. McGill, and H. Cooke. 1990. The structure of a subterminal repeated sequence present on many human chromosomes. Nucleic Acids Res. 18:6649-6657. http://dx.doi.org/10.1093/nar/18.22.6649
13. de Lange, T., L. Shiue, R.M. Myers, D.R. Cox, S.L. Naylor, A.M. Killery, and H.E. Varmus. 1990. Structure and variability of human chromosome ends. Mol. Cell. Biol. 10:518-527.
14. Deng, Z., J. Dheekollu, D. Broccoli, A. Dutta, and P.M. Lieberman. 2007. The origin recognition complex localizes to telomere repeats and prevents telomere-circle formation. Curr. Biol. 17:1989-1995. http://dx.doi.org/ 10.1016/j.cub.2007.10.054
15. Ding, Q., and D.M. MacAlpine. 2011. Defining the replication program through the chromatin landscape. Crit. Rev. Biochem. Mol. Biol. 46:165-179. http://dx.doi.org/10.3109/10409238.2011.560139
16. Flynn, R.L., R.C. Centore, R.J. O'Sullivan, R. Rai, A. Tse, Z. Songyang, S. Chang, J. Karlseder, and L. Zou. 2011. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature. 471:532-536. http://dx.doi.org/10.1038/nature09772
17. Gilson, E., and V. Géli. 2007. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 8:825-838. http://dx.doi.org/10.1038/nrm2259
18. Griffith, J.D., L. Comeau, S. Rosenfield, R.M. Stansel, A. Bianchi, H. Moss, and T. de Lange. 1999. Mammalian telomeres end in a large duplex loop. Cell. 97:503-514. http://dx.doi.org/10.1016/S0092-8674(00)80760-6
19. Guan, Z., C.M. Hughes, S. Kosiyatrakul, P. Norio, R. Sen, S. Fiering, C.D. Allis, E.E. Bouhassira, and C.L. Schildkraut. 2009. Decreased replication origin activity in temporal transition regions. J. Cell Biol. 187:623-635. http://dx.doi.org/10.1083/jcb.200905144
20. Ivessa, A.S., J.Q. Zhou, V.P. Schulz, E.K. Monson, and V.A. Zakian. 2002. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16:1383-1396. http://dx.doi.org/10.1101/gad.982902
21. Karnani, N., C.M. Taylor, A. Malhotra, and A. Dutta. 2010. Genomic study of replication initiation in human chromosomes reveals the influence of transcription regulation and chromatin structure on origin selection. Mol. Biol. Cell. 21:393-404. http://dx.doi.org/10.1091/mbc.E09-08-0707
22. Kurth, I., and J. Gautier. 2010. Origin-dependent initiation of DNA replication within telomeric sequences. Nucleic Acids Res. 38:467-476. http://dx.doi.org/10.1093/nar/gkp929
23. Lipps, H.J., and D. Rhodes. 2009. G-quadruplex structures: in vivo evidence and function. Trends Cell Biol. 19:414-422. http://dx.doi.org/10.1016/j.tcb.2009.05.002
24. Lubelsky, Y., T. Sasaki, M.A. Kuipers, I. Lucas, M.M. Le Beau, S. Carignon, M. Debatisse, J.A. Prinz, J.H. Dennis, and D.M. Gilbert. 2011. Prereplication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res. 39:3141-3155. http://dx.doi.org/10.1093/ nar/gkq1276
25. Makovets, S., I. Herskowitz, and E.H. Blackburn. 2004. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol. Cell. Biol. 24:4019-4031. http://dx.doi.org/10.1128/MCB.24.9.4019-4031.2004
26. Martin, M.M., M. Ryan, R. Kim, A.L. Zakas, H. Fu, C.M. Lin, W.C. Reinhold, S.R. Davis, S. Bilke, H. Liu, et al. 2011. Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res. 21:1822-1832. http://dx.doi.org/10.1101/gr.124644.111
27. Méchali, M. 2010. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11:728-738. http://dx.doi.org/10.1038/nrm2976
28. Mesner, L.D., V. Valsakumar, N. Karnani, A. Dutta, J.L. Hamlin, and S. Bekiranov. 2011. Bubble-chip analysis of human origin distributions demonstrates on a genomic scale significant clustering into zones and significant association with transcription. Genome Res. 21:377-389. http://dx.doi.org/10.1101/gr.111328.110
29. Miller, K.M., O. Rog, and J.P. Cooper. 2006. Semi-conservative DNA replication through telomeres requires Taz1. Nature. 440:824-828. http://dx.doi.org/10.1038/nature04638
30. Mirkin, E.V., and S.M. Mirkin. 2007. Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev. 71:13-35. http://dx.doi.org/10.1128/MMBR.00030-06
31. Nergadze, S.G., B.O. Farnung, H. Wischnewski, L. Khoriauli, V. Vitelli, R. Chawla, E. Giulotto, and C.M. Azzalin. 2009. CpG-island promoters drive transcription of human telomeres. RNA. 15:2186-2194. http:// dx.doi.org/10.1261/rna.1748309
32. Norio, P., and C.L. Schildkraut. 2001. Visualization of DNA replication on individual Epstein-Barr virus episomes. Science. 294:2361-2364. http:// dx.doi.org/10.1126/science.1064603
33. Norio, P., and C.L. Schildkraut. 2004. Plasticity of DNA replication initiation in Epstein-Barr virus episomes. PLoS Biol. 2:e152. http://dx.doi.org/10.1371/journal.pbio.0020152
34. Norio, P., S. Kosiyatrakul, Q. Yang, Z. Guan, N.M. Brown, S. Thomas, R. Riblet, and C.L. Schildkraut. 2005. Progressive activation of DNA replication initiation in large domains of the immunoglobulin heavy chain locus during B cell development. Mol. Cell. 20:575-587. http://dx.doi.org/10.1016/j.molcel.2005.10.029
35. Oganesian, L., and J. Karlseder. 2009. Telomeric armor: the layers of end protection. J. Cell Sci. 122:4013-4025. http://dx.doi.org/10.1242/jcs.050567
36. Paeschke, K., T. Simonsson, J. Postberg, D. Rhodes, and H.J. Lipps. 2005. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol. 12:847-854. http://dx.doi.org/10.1038/nsmb982
37. Paeschke, K., J.A. Capra, and V.A. Zakian. 2011. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell. 145:678-691. http://dx.doi.org/10.1016/j.cell.2011.04.015
38. Riethman, H. 2008. Human telomere structure and biology. Annu. Rev. Genomics Hum. Genet. 9:1-19. http://dx.doi.org/10.1146/annurev.genom.8.021506.172017
39. Schepers, A., and P. Papior. 2010. Why are we where we are? Understanding replication origins and initiation sites in eukaryotes using ChIPapproaches. Chromosome Res. 18:63-77. http://dx.doi.org/10.1007/ s10577-009-9087-1
40. Schultz, S.S., S.C. Desbordes, Z. Du, S. Kosiyatrakul, I. Lipchina, L. Studer, and C.L. Schildkraut. 2010. Single-molecule analysis reveals changes in the DNA replication program for the POU5F1 locus upon human embryonic stem cell differentiation. Mol. Cell. Biol. 30:4521-4534. http://dx.doi.org/10.1128/MCB.00380-10
41. Sfeir, A., S.T. Kosiyatrakul, D. Hockemeyer, S.L. MacRae, J. Karlseder, C.L. Schildkraut, and T. de Lange. 2009. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell. 138:90-103. http://dx.doi.org/10.1016/j.cell.2009.06.021
42. Smith, J.S., Q. Chen, L.A. Yatsunyk, J.M. Nicoludis, M.S. Garcia, R. Kranaster, S. Balasubramanian, D. Monchaud, M.P. Teulade-Fichou, L. Abramowitz, et al. 2011. Rudimentary G-quadruplex-based telomere capping in Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 18:478-485. http://dx.doi.org/10.1038/nsmb.2033
43. Takai, K.K., S. Hooper, S. Blackwood, R. Gandhi, and T. de Lange. 2010. In vivo stoichiometry of shelterin components. J. Biol. Chem. 285:1457-1467. http://dx.doi.org/10.1074/jbc.M109.038026
44. Tatsumi, Y., K. Ezura, K. Yoshida, T. Yugawa, M. Narisawa-Saito, T. Kiyono, S. Ohta, C. Obuse, and M. Fujita. 2008. Involvement of human ORC and TRF2 in pre-replication complex assembly at telomeres. Genes Cells. 13:1045-1059. http://dx.doi.org/10.1111/j.1365-2443.2008.01224.x
45. Torres, J.Z., S.L. Schnakenberg, and V.A. Zakian. 2004. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24:3198-3212. http://dx.doi.org/10.1128/MCB.24.8.3198-3212.2004
46. Tourrière, H., and P. Pasero. 2007. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst.). 6:900-913. http:// dx.doi.org/10.1016/j.dnarep.2007.02.004
47. Valenzuela, M.S., Y. Chen, S. Davis, F. Yang, R.L. Walker, S. Bilke, J. Lueders, M.M. Martin, M.I. Aladjem, P.P. Massion, and P.S. Meltzer. 2011. Preferential localization of human origins of DNA replication at the 5'-ends of expressed genes and at evolutionarily conserved DNA sequences. PLoS ONE. 6:e17308. http://dx.doi.org/10.1371/journal.pone.0017308
48. Verdun, R.E., and J. Karlseder. 2006. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell. 127:709-720. http://dx.doi.org/10.1016/j.cell.2006.09.034
49. Williams, E.S., M.N. Cornforth, E.H. Goodwin, and S.M. Bailey. 2011. CO-FISH, COD-FISH, ReD-FISH, SKY-FISH. Methods Mol. Biol. 735:113-124. http://dx.doi.org/10.1007/978-1-61779-092-8_11