Recombinogenic Telomeres in Diploid Sorex granarius (Soricidae, Eulipotyphla) Fibroblast Cells

REFERENCES

• Pfeiffer V, Lingner J. 2013. Replication of telomeres and the regulation of telomerase. Cold Spring Harb. Perspect. Biol. 5:a010405. http://dx.doi.org/10.1101/cshperspect.a010405.
   PubMed Web of Science ®Google Scholar
• Tumpel S, Rudolph KL. 2012. The role of telomere shortening in somatic stem cells and tissue aging: lessons from telomerase model systems. Ann. N. Y. Acad. Sci. 1266:28–39. http://dx.doi.org/10.1111/j.1749-6632.2012.06547.x.
   PubMed Web of Science ®Google Scholar
• Hug N, Lingner J. 2006. Telomere length homeostasis. Chromosoma 115:413–425. http://dx.doi.org/10.1007/s00412-006-0067-3.
   PubMed Web of Science ®Google Scholar
• Pickett HA, Cesare AJ, Johnston RL, Neumann AA, Reddel RR. 2009. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 28:799–809. http://dx.doi.org/10.1038/emboj.2009.42.
   PubMed Web of Science ®Google Scholar
• Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T. 1999. Mammalian telomeres end in a large duplex loop. Cell 97:503–514. http://dx.doi.org/10.1016/S0092-8674(00)80760-6.
   PubMed Web of Science ®Google Scholar
• Wang RC, Smogorzewska A, de Lange T. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119:355–368. http://dx.doi.org/10.1016/j.cell.2004.10.011.
   PubMed Web of Science ®Google Scholar
• Cesare AJ, Reddel RR. 2010. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 11:319–330. http://dx.doi.org/10.1038/nrg2763.
   PubMed Web of Science ®Google Scholar
• Gomes NM, Ryder OA, Houck ML, Charter SJ, Walker W, Forsyth NR, Austad SN, Venditti C, Pagel M, Shay JW, Wright WE. 2011. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10:761–768. http://dx.doi.org/10.1111/j.1474-9726.2011.00718.x.
   PubMed Web of Science ®Google Scholar
• Wyttenbach A, Borodin P, Hausser J. 1998. Meiotic drive favors Robertsonian metacentric chromosomes in the common shrew (Sorex araneus, Insectivora, Mammalia). Cytogenet. Cell Genet. 83:199–206. http://dx.doi.org/10.1159/000015178.
   PubMedGoogle Scholar
• Zhdanova NS, Karamisheva TV, Minina J, Astakhova NM, Lansdorp P, Kammori M, Rubtsov NB, Searle JB. 2005. Unusual distribution pattern of telomeric repeats in the shrews Sorex araneus and Sorex granarius. Chromosome Res. 13:617–625. http://dx.doi.org/10.1007/s10577-005-0988-3.
   PubMedGoogle Scholar
• Zhdanova NS, Minina JM, Karamisheva TV, Draskovic I, Rubtsov NB, Londono-Vallejo JA. 2007. The very long telomeres in Sorex granarius (Soricidae, Eulipothyphla) contain ribosomal DNA. Chromosome Res. 15:881–890. http://dx.doi.org/10.1007/s10577-007-1170-x.
   PubMedGoogle Scholar
• Zhdanova NS, Rogozina Iu I, Minina Iu M, Borodin PM, Rubtsov NB. 2009. Telomeric DNA allocation in chromosomes of common shrew Sorex araneus, Eulipotyphla. Tsitologiia 51:577–584.
   PubMedGoogle Scholar
• Draskovic I, Arnoult N, Steiner V, Bacchetti S, Lomonte P, Londono-Vallejo A. 2009. Probing PML body function in ALT cells reveals spatiotemporal requirements for telomere recombination. Proc. Natl. Acad. Sci. U. S. A. 106:15726–15731. http://dx.doi.org/10.1073/pnas.0907689106.
   PubMed Web of Science ®Google Scholar
• Everett RD, Earnshaw WC, Findlay J, Lomonte P. 1999. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18:1526–1538. http://dx.doi.org/10.1093/emboj/18.6.1526.
   PubMed Web of Science ®Google Scholar
• Londoño-Vallejo JA, Der-Sarkissian H, Cazes L, Bacchetti S, Reddel R. 2004. Alternative lengthening of telomeres is characterized by high rates of inter-telomeric exchange. Cancer Res. 64:2324–2327. http://dx.doi.org/10.1158/0008-5472.CAN-03-4035.
   PubMed Web of Science ®Google Scholar
• Londono-Vallejo JA, DerSarkissian H, Cazes L, Thomas G. 2001. Differences in telomere length between homologous chromosomes in humans. Nucleic Acids Res. 29:3164–3171. http://dx.doi.org/10.1093/nar/29.15.3164.
   PubMedGoogle Scholar
• Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. 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.
   PubMed Web of Science ®Google Scholar
• Ijdo JW, Wells RA, Baldini A, Reeders ST. 1991. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 19:4780. http://dx.doi.org/10.1093/nar/19.17.4780.
   PubMed Web of Science ®Google Scholar
• Arnoult N, Shin-Ya K, Londono-Vallejo JA. 2008. Studying telomere replication by Q-CO-FISH: the effect of telomestatin, a potent G-quadruplex ligand. Cytogenet. Genome Res. 122:229–236. http://dx.doi.org/10.1159/000167808.
   PubMedGoogle Scholar
• Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–2015. http://dx.doi.org/10.1126/science.7605428.
   PubMed Web of Science ®Google Scholar
• Wege H, Chui MS, Le HT, Tran JM, Zern MA. 2003. SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activity. Nucleic Acids Res. 31:E3-3. http://dx.doi.org/10.1093/nar/gng033.
   PubMed Web of Science ®Google Scholar
• Grummt I. 2003. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 17:1691–1702. http://dx.doi.org/10.1101/gad.1098503R.
   PubMed Web of Science ®Google Scholar
• Klein J, Grummt I. 1999. Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. Proc. Natl. Acad. Sci. U. S. A. 96:6096–6101. http://dx.doi.org/10.1073/pnas.96.11.6096.
   PubMed Web of Science ®Google Scholar
• Draskovic I, Londono-Vallejo A. 2013. Telomere recombination and alternative telomere lengthening mechanisms. Front. Biosci. 18:1–20. http://dx.doi.org/10.2741/4084.
   Google Scholar
• Murnane JP, Sabatier L, Marder BA, Morgan WF. 1994. Telomere dynamics in an immortal human cell line. EMBO J. 13:4953–4962.
   PubMed Web of Science ®Google Scholar
• Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59:4175–4179.
   PubMed Web of Science ®Google Scholar
• Rubtsov IB, Karamysheva TV, Minina Iu M, Zhdanova NS. 2008. 3D organization of interphase fibroblast nuclei in two closely related shrew species, Sorex granarius and S. araneus, differed by the structure of chromosome termini. Tsitologiia 50:430–438.
   PubMedGoogle Scholar
• Lomonte P, Morency E. 2007. Centromeric protein CENP-B proteasomal degradation induced by the viral protein ICP0. FEBS Lett. 581:658–662. http://dx.doi.org/10.1016/j.febslet.2007.01.027.
   PubMedGoogle Scholar
• Torok D, Ching RW, Bazett-Jones DP. 2009. PML nuclear bodies as sites of epigenetic regulation. Front. Biosci. (Landmark Ed.) 14:1325–1336.
   PubMedGoogle Scholar
• Cesare AJ, Griffith JD. 2004. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous T-loops. Mol. Cell. Biol. 24:9948–9957. http://dx.doi.org/10.1128/MCB.24.22.9948-9957.2004.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1038/nbt.1587.
   PubMed Web of Science ®Google Scholar
• Cesare AJ, Kaul Z, Cohen SB, Napier CE, Pickett HA, Neumann AA, Reddel RR. 2009. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 16:1244–1251. http://dx.doi.org/10.1038/nsmb.1725.
   PubMed Web of Science ®Google Scholar
• Kaul Z, Cesare AJ, Huschtscha LI, Neumann AA, Reddel RR. 2011. Five dysfunctional telomeres predict onset of senescence in human cells. EMBO Rep 13:52–59. http://dx.doi.org/10.1038/embor.2011.227.
   PubMed Web of Science ®Google Scholar
• Morrish TA, Greider CW. 2009. Short telomeres initiate telomere recombination in primary and tumor cells. PLoS Genet. 5:e1000357. http://dx.doi.org/10.1371/journal.pgen.1000357.
   PubMedGoogle Scholar
• Pascolo E, Wenz C, Lingner J, Hauel N, Priepke H, Kauffmann I, Garin-Chesa P, Rettig WJ, Damm K, Schnapp A. 2002. Mechanism of human telomerase inhibition by BIBR1532, a synthetic, non-nucleosidic drug candidate. J. Biol. Chem. 277:15566–15572. http://dx.doi.org/10.1074/jbc.M201266200.
   PubMed Web of Science ®Google Scholar
• Bah A, Wischnewski H, Shchepachev V, Azzalin CM. 2012. The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res. 40:2995–3005. http://dx.doi.org/10.1093/nar/gkr1153.
   PubMed Web of Science ®Google Scholar
• O'Sullivan RJ, Arnoult N, Lackner DH, Oganesian L, Haggblom C, Corpet A, Almouzni G, Karlseder J. 2014. Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat. Struct. Mol. Biol. 21:167–174. http://dx.doi.org/10.1038/nsmb.2754.
   PubMed Web of Science ®Google Scholar
• Plantinga MJ, Pascarelli KM, Merkel AS, Lazar AJ, von Mehren M, Lev D, Broccoli D. 2013. Telomerase suppresses formation of ALT-associated single-stranded telomeric C-circles. Mol. Cancer Res. 11:557–567. http://dx.doi.org/10.1158/1541-7786.MCR-13-0013.
   PubMedGoogle Scholar
• Cerone MA, Londoño-Vallejo JA, Bacchetti S. 2001. Telomere maintenance by telomerase and by recombination can coexist in human cells. Hum. Mol. Genet. 10:1945–1952. http://dx.doi.org/10.1093/hmg/10.18.1945.
   PubMed Web of Science ®Google Scholar
• Grobelny JV, Kulp-McEliece M, Broccoli D. 2001. Effects of reconstitution of telomerase activity on telomere maintenance by the alternative lengthening of telomeres (ALT) pathway. Hum. Mol. Genet. 10:1953–1961. http://dx.doi.org/10.1093/hmg/10.18.1953.
   PubMedGoogle Scholar
• Perrem K, Colgin LM, Neumann AA, Yeager TR, Reddel RR. 2001. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol. Cell. Biol. 21:3862–3875. http://dx.doi.org/10.1128/MCB.21.12.3862-3875.2001.
   PubMed Web of Science ®Google Scholar
• Neumann AA, Watson CM, Noble JR, Pickett HA, Tam PP, Reddel RR. 2013. Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev. 27:18–23. http://dx.doi.org/10.1101/gad.205062.112.
   PubMed Web of Science ®Google Scholar
• Ouellette MM, Liao M, Herbert BS, Johnson M, Holt SE, Liss HS, Shay JW, Wright WE. 2000. Subsenescent telomere lengths in fibroblasts immortalized by limiting amounts of telomerase. J. Biol. Chem. 275:10072–10076. http://dx.doi.org/10.1074/jbc.275.14.10072.
   PubMedGoogle Scholar
• Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, Haber JE, Iliakis G, Kallioniemi OP, Halazonetis TD. 2014. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 343:88–91. http://dx.doi.org/10.1126/science.1243211.
   PubMed Web of Science ®Google Scholar
• Lydeard JR, Jain S, Yamaguchi M, Haber JE. 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448:820–823. http://dx.doi.org/10.1038/nature06047.
   PubMed Web of Science ®Google Scholar
• McEachern MJ, Haber JE. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75:111–135. http://dx.doi.org/10.1146/annurev.biochem.74.082803.133234.
   PubMed Web of Science ®Google Scholar
• Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, Deem A, Ira G, Haber JE, Lobachev KS, Malkova A. 2013. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502:389–392. http://dx.doi.org/10.1038/nature12584.
   PubMed Web of Science ®Google Scholar
• Der-Sarkissian H, Vergnaud G, Borde YM, Thomas G, Londono-Vallejo JA. 2002. Segmental polymorphisms in the proterminal regions of a subset of human chromosomes. Genome Res. 12:1673–1678. http://dx.doi.org/10.1101/gr.322802.
   PubMedGoogle Scholar
• Mefford HC, Trask BJ. 2002. The complex structure and dynamic evolution of human subtelomeres. Nat. Rev. Genet. 3:91–102. http://dx.doi.org/10.1038/nrg727.
   PubMed Web of Science ®Google Scholar
• Ventura M, Catacchio CR, Alkan C, Marques-Bonet T, Sajjadian S, Graves TA, Hormozdiari F, Navarro A, Malig M, Baker C, Lee C, Turner EH, Chen L, Kidd JM, Archidiacono N, Shendure J, Wilson RK, Eichler EE. 2011. Gorilla genome structural variation reveals evolutionary parallelisms with chimpanzee. Genome Res. 21:1640–1649. http://dx.doi.org/10.1101/gr.124461.111.
   PubMedGoogle Scholar
• Ventura M, Catacchio CR, Sajjadian S, Vives L, Sudmant PH, Marques-Bonet T, Graves TA, Wilson RK, Eichler EE. 2012. The evolution of African great ape subtelomeric heterochromatin and the fusion of human chromosome 2. Genome Res. 22:1036–1049. http://dx.doi.org/10.1101/gr.136556.111.
   PubMedGoogle Scholar
• Novo CL, Arnoult N, Liu W-Y, Castro Vega LJ, Gibaud A, Dutrillaux B, Bacchetti S, Londono-Vallejo A. 2013. The heterochromatic chromosome caps in great apes impact telomere metabolism. Nucleic Acids Res. 41:4792–4801. http://dx.doi.org/10.1093/nar/gkt169.
   PubMedGoogle Scholar
• Helleday T. 2003. Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res. 532:103–115. http://dx.doi.org/10.1016/j.mrfmmm.2003.08.013.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/j.cell.2009.06.021.
   PubMed Web of Science ®Google Scholar
• Stimpson KM, Sullivan LL, Kuo ME, Sullivan BA. 2014. Nucleolar organization, ribosomal DNA array stability, and acrocentric chromosome integrity are linked to telomere function. PLoS One 9:e92432. http://dx.doi.org/10.1371/journal.pone.0092432.
   PubMedGoogle Scholar