Chromatin modifiers and recombination factors promote a telomere fold-back structure, that is lost during replicative senescence
Autoři:
Tina Wagner aff001; Lara Pérez-Martínez aff002; René Schellhaas aff002; Marta Barrientos-Moreno aff003; Merve Öztürk aff002; Félix Prado aff003; Falk Butter aff002; Brian Luke aff001
Působiště autorů:
Institute of Developmental Biology and Neurobiology (IDN), Johannes Gutenberg-Universität, Mainz, Germany
aff001; Institute of Molecular Biology (IMB) gGmbH, Mainz, Germany
aff002; Department of Genome Biology, Andalusian Molecular Biology and Regenerative Medicine Center (CABIMER), CSIC-University of Seville-University Pablo de Olavide, Seville, Spain
aff003
Vyšlo v časopise:
Chromatin modifiers and recombination factors promote a telomere fold-back structure, that is lost during replicative senescence. PLoS Genet 16(12): e1008603. doi:10.1371/journal.pgen.1008603
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008603
Souhrn
Telomeres have the ability to adopt a lariat conformation and hence, engage in long and short distance intra-chromosome interactions. Budding yeast telomeres were proposed to fold back into subtelomeric regions, but a robust assay to quantitatively characterize this structure has been lacking. Therefore, it is not well understood how the interactions between telomeres and non-telomeric regions are established and regulated. We employ a telomere chromosome conformation capture (Telo-3C) approach to directly analyze telomere folding and its maintenance in S. cerevisiae. We identify the histone modifiers Sir2, Sin3 and Set2 as critical regulators for telomere folding, which suggests that a distinct telomeric chromatin environment is a major requirement for the folding of yeast telomeres. We demonstrate that telomeres are not folded when cells enter replicative senescence, which occurs independently of short telomere length. Indeed, Sir2, Sin3 and Set2 protein levels are decreased during senescence and their absence may thereby prevent telomere folding. Additionally, we show that the homologous recombination machinery, including the Rad51 and Rad52 proteins, as well as the checkpoint component Rad53 are essential for establishing the telomere fold-back structure. This study outlines a method to interrogate telomere-subtelomere interactions at a single unmodified yeast telomere. Using this method, we provide insights into how the spatial arrangement of the chromosome end structure is established and demonstrate that telomere folding is compromised throughout replicative senescence.
Klíčová slova:
DNA damage – Histones – Chromatin – Polymerase chain reaction – Protein folding – Saccharomyces cerevisiae – Telomeres – Yeast
Zdroje
1. Palm W, de Lange T. How Shelterin Protects Mammalian Telomeres. Annu Rev Genet. 2008;42(1):301–34. doi: 10.1146/annurev.genet.41.110306.130350 18680434
2. Grandin N. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 2001 Mar 1;20(5):1173–83. doi: 10.1093/emboj/20.5.1173 11230140
3. Bonetti D, Clerici M, Anbalagan S, Martina M, Lucchini G, Longhese MP. Shelterin-like proteins and Yku inhibit nucleolytic processing of Saccharomyces cerevisiae telomeres. Haber JE, editor. PLoS Genet [Internet]. 2010 May 27;6(5):e1000966. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20523746 doi: 10.1371/journal.pgen.1000966 20523746
4. Hardy CFJ, Sussel L, Shore D. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 1992;6(5):801–14. doi: 10.1101/gad.6.5.801 1577274
5. Wotton D, Shore D. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 1997;11(6):748–60. doi: 10.1101/gad.11.6.748 9087429
6. de Lange T. How Telomeres Solve the End-Protection Problem. Science (80-). 2009 Nov 13;326(5955):948–52. doi: 10.1126/science.1170633 19965504
7. Tomaska L, Makhov AM, Griffith JD, Nosek J. T-Loops in Yeast Mitochondria. Mitochondrion. 2002;1(5):455–9. doi: 10.1016/s1567-7249(02)00009-0 16120298
8. Tomaska L, Willcox S, Slezakova J, Nosek J, Griffith JD. Taz1 binding to a fission yeast model telomere: Formation of telomeric loops and higher order structures. J Biol Chem. 2004;279(49):50764–72. doi: 10.1074/jbc.M409790200 15383525
9. Muñoz-Jordán JL, Cross GAM, De Lange T, Griffith JD. T-Loops At Trypanosome Telomeres. EMBO J. 2001;20(3):579–88. doi: 10.1093/emboj/20.3.579 11157764
10. Cesare AJ, Quinney N, Willcox S, Subramanian D, Griffith JD. Telomere looping in P. sativum (common garden pea). Plant J. 2003;36(2):271–9. doi: 10.1046/j.1365-313x.2003.01882.x 14535890
11. Cesare AJ, Groff-Vindman C, Compton SA, McEachern MJ, Griffith JD. Telomere Loops and Homologous Recombination-Dependent Telomeric Circles in a Kluyveromyces lactis Telomere Mutant Strain. Mol Cell Biol. 2008;28(1):20–9. doi: 10.1128/MCB.01122-07 17967889
12. de Bruin D, Kantrow SM, Liberatore RA, Zakian VA. Telomere Folding Is Required for the Stable Maintenance of Telomere Position Effects in Yeast. Mol Cell Biol. 2000 Nov 1;20(21):7991–8000. doi: 10.1128/mcb.20.21.7991-8000.2000 11027269
13. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999;97(4):503–14. doi: 10.1016/s0092-8674(00)80760-6 10338214
14. Doksani Y, Wu JY, De Lange T, Zhuang X. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell. 2013;155(2):345–56. doi: 10.1016/j.cell.2013.09.048 24120135
15. Poschke H, Dees M, Chang M, Amberkar S, Kaderali L, Rothstein R, et al. Rif2 promotes a telomere fold-back structure through Rpd3L recruitment in budding yeast. Griffith JD, editor. PLoS Genet [Internet]. 2012 Sep 20;8(9):e1002960. Available from: https://dx.plos.org/10.1371/journal.pgen.1002960 23028367
16. Strahl-Bolsinger S, Hecht A, Luo K, Grunstein M. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev. 1997;11(1):83–93. doi: 10.1101/gad.11.1.83 9000052
17. Sarek G, Vannier JB, Panier S, Petrini HJ, Boulton SJ. TRF2 recruits RTEL1 to telomeres in s phase to promote t-loop unwinding. Mol Cell. 2015;57(4):622–35. doi: 10.1016/j.molcel.2014.12.024 25620558
18. Sarek G, Kotsantis P, Ruis P, Van Ly D, Margalef P, Borel V, et al. CDK phosphorylation of TRF2 controls t-loop dynamics during the cell cycle. Nature. 2019 Nov 13;575(7783):523–7. doi: 10.1038/s41586-019-1744-8 31723267
19. de Bruin D, Zaman Z, Liberatore RA, Ptashne M. Telomere looping permits gene activation by a downstream UAS in yeast. Nature. 2001 Jan;409(6816):109–13. doi: 10.1038/35051119 11343124
20. Van Ly D, Low RRJ, Frölich S, Bartolec TK, Kafer GR, Pickett HA, et al. Telomere Loop Dynamics in Chromosome End Protection. Mol Cell. 2018;71(4):510–525.e6. doi: 10.1016/j.molcel.2018.06.025 30033372
21. Lingner J, Cooper JP, Cech TR. Telomerase and DNA end replication: No longer a lagging strand problem? Science (80-). 1995;269(5230):1533–4. doi: 10.1126/science.7545310 7545310
22. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J Mol Biol. 1992; doi: 10.1016/0022-2836(92)90096-3 1613801
23. Soudet J, Jolivet P, Teixeira MT. Elucidation of the DNA end-replication problem in saccharomyces cerevisiae. Mol Cell. 2014;53(6):954–64. doi: 10.1016/j.molcel.2014.02.030 24656131
24. Diede SJ, Gottschling DE. Telomerase-Mediated Telomere Addition In Vivo Requires DNA Primase and DNA Polymerases. Cell. 1999;99:723–33. doi: 10.1016/s0092-8674(00)81670-0 10619426
25. Teixeira MT, Arneric M, Sperisen P, Lingner J. Telomere length homeostasis is achieved via a switch between telomerase-extendible and-nonextendible states. Cell. 2004;117(3):323–35. doi: 10.1016/s0092-8674(04)00334-4 15109493
26. Lundblad V, Szostak JW. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell. 1989;57(4):633–43. doi: 10.1016/0092-8674(89)90132-3 2655926
27. Barthel FP, Wei W, Tang M, Martinez-Ledesma E, Hu X, Amin SB, et al. Systematic analysis of telomere length and somatic alterations in 31 cancer types. Nat Genet. 2017;49(3):349–57. doi: 10.1038/ng.3781 28135248
28. Lundblad V, Blackburn EH. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993;73(2):347–60. doi: 10.1016/0092-8674(93)90234-h 8477448
29. D’Adda Di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 2003;426(6963):194–8. doi: 10.1038/nature02118 14608368
30. Enomoto S, Glowczewski L, Berman J. MEC3, MEC1, and DDC2 Are Essential Components of a Telomere Checkpoint Pathway Required for Cell Cycle Arrest during Senescence in Saccharomyces cerevisiae. Mol Biol Cell. 2002;13(6):2001–15. doi: 10.1091/mboc.13.6.mk0602002001 12058065
31. Grandin N, Bailly A, Charbonneau M. Activation of Mrc1, a mediator of the replication checkpoint, by telomere erosion. Biol Cell. 2005;97(10):799–814. doi: 10.1042/BC20040526 15760303
32. IJpma AS, Greider CW. Short Telomeres Induce a DNA Damage Response in Saccharomyces cerevisiae. Mol Biol Cell. 2003;13(6):2001–15. doi: 10.1091/mbc.02-04-0057 12631718
33. Fallet E, Jolivet P, Soudet J, Lisby M, Gilson E, Teixeira MT. Length-dependent processing of telomeres in the absence of telomerase. Nucleic Acids Res. 2014;42(6):3648–65. doi: 10.1093/nar/gkt1328 24393774
34. Khadaroo B, Teixeira MT, Luciano P, Eckert-Boulet N, Germann SM, Simon MN, et al. The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat Cell Biol. 2009;11(8):980–7. doi: 10.1038/ncb1910 19597487
35. Zhu XD, Küster B, Mann M, Petrini JHJ, De Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet. 2000;25(3):347–52. doi: 10.1038/77139 10888888
36. Ritchie KB, Mallory JC, Petes TD. Interactions of TLC1 (Which Encodes the RNA Subunit of Telomerase), TEL1, and MEC1 in Regulating Telomere Length in the Yeast Saccharomyces cerevisiae. Mol Cell Biol. 1999;19(9):6065–75. doi: 10.1128/mcb.19.9.6065 10454554
37. Chan SWL, Chang J, Prescott J, Blackburn EH. Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr Biol. 2001 Aug;11(16):1240–50. doi: 10.1016/s0960-9822(01)00391-8 11525738
38. Chan SW, Blackburn EH. Telomerase and ATM/Tel1p Protect Telomeres from Nonhomologous End Joining Short. Mol Cell. 2003;11:1379–87. doi: 10.1016/s1097-2765(03)00174-6 12769860
39. Craven RJ, Greenwell PW, Dominska M, Petes TD, Hill C, Carolina N. Regulation of Genome Stability by TEL1 and MEC1, Yeast Homologs of the Mammalian ATM and ATR Genes. Genetics. 2002;507(June):16. 12072449
40. Mieczkowski PA, Mieczkowska JO, Dominska M, Petes TD. Genetic regulation of telomere-telomere fusions in the yeast Saccharomyces cerevisae. Proc Natl Acad Sci [Internet]. 2003 Sep 16;100(19):10854–9. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1934561100 12963812
41. Barrientos-Moreno M, Murillo-Pineda M, Muñoz-Cabello AM, Prado F. Histone depletion prevents telomere fusions in pre-senescent cells. PLoS Genet. 2018;14(6):1–22. doi: 10.1371/journal.pgen.1007407 29879139
42. Verdun RE, Karlseder J. The DNA Damage Machinery and Homologous Recombination Pathway Act Consecutively to Protect Human Telomeres. Cell. 2006;127(4):709–20. doi: 10.1016/j.cell.2006.09.034 17110331
43. Verdun RE, Crabbe L, Haggblom C, Karlseder J. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol Cell. 2005;20(4):551–61. doi: 10.1016/j.molcel.2005.09.024 16307919
44. Cesare AJ, Hayashi MT, Crabbe L, Karlseder J. The Telomere deprotection response is functionally distinct from the Genomic DNA damage response. Mol Cell. 2013;51(2):141–55. doi: 10.1016/j.molcel.2013.06.006 23850488
45. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing Chromosome Conformation. Science (80-) [Internet]. 2002 Feb 15;295(5558):1306–11. Available from: https://www.sciencemag.org/lookup/doi/10.1126/science.1067799 11847345
46. Teixeira MT. Saccharomyces cerevisiae as a Model to Study Replicative Senescence Triggered by Telomere Shortening. Front Oncol [Internet]. 2013;3(April):1–16. Available from: http://journal.frontiersin.org/article/10.3389/fonc.2013.00101/abstract 23638436
47. Teng S-C, Zakian VA. Telomere-Telomere Recombination Is an Efficient Bypass Pathway for Telomere Maintenance in Saccharomyces cerevisiae. Mol Cell Biol. 1999;19(12):8083–93. doi: 10.1128/mcb.19.12.8083 10567534
48. Hiraga SI, Botsios S, Donaldson AD. Histone H3 lysine 56 acetylation by Rtt109 is crucial for chromosome positioning. J Cell Biol. 2008;183(4):641–51. doi: 10.1083/jcb.200806065 19001125
49. Bystricky K, Laroche T, Van Houwe G, Blaszczyk M, Gasser SM. Chromosome looping in yeast: Telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J Cell Biol. 2005;168(3):375–87. doi: 10.1083/jcb.200409091 15684028
50. van Ruiten MS, Rowland BD. SMC Complexes: Universal DNA Looping Machines with Distinct Regulators. Trends Genet. 2018;34(6):477–87. doi: 10.1016/j.tig.2018.03.003 29606284
51. Pebernard S, Schaffer L, Campbell D, Head SR, Boddy MN. Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J. 2008;27(22):3011–23. doi: 10.1038/emboj.2008.220 18923417
52. Potts PR, Yu H. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol. 2007;14(7):581–90. doi: 10.1038/nsmb1259 17589526
53. Zhao X, Blobel G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc Natl Acad Sci U S A. 2005;102(13):4777–82. doi: 10.1073/pnas.0500537102 15738391
54. Noël J-F, Wellinger RJ. Abrupt telomere losses and reduced end-resection can explain accelerated senescence of Smc5/6 mutants lacking telomerase. DNA Repair (Amst) [Internet]. 2011 Mar 7;10(3):271–82. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1568786410003873 doi: 10.1016/j.dnarep.2010.11.010 21190904
55. Chavez A, George V, Agrawal V, Johnson FB. Sumoylation and the Structural Maintenance of Chromosomes (Smc) 5/6 Complex Slow Senescence through Recombination Intermediate Resolution. J Biol Chem [Internet]. 2010 Apr 16;285(16):11922–30. Available from: http://www.jbc.org/lookup/doi/10.1074/jbc.M109.041277 20159973
56. Morawska M, Ulrich HD. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast. 2013 Sep;30(9):341–51. doi: 10.1002/yea.2967 23836714
57. Hirano T, Mitchison TJ. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell. 1994 Nov;79(3):449–58. doi: 10.1016/0092-8674(94)90254-2 7954811
58. Strunnikov A V., Hogan E, Koshland D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev. 1995;9(5):587–99. doi: 10.1101/gad.9.5.587 7698648
59. Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N, Nuebler J, et al. A pathway for mitotic chromosome formation. Science (80-) [Internet]. 2018 Feb 9;359(6376):eaao6135. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29348367 doi: 10.1126/science.aao6135 29348367
60. Rao SSP, Huang S-C, Glenn St Hilaire B, Engreitz JM, Perez EM, Kieffer-Kwon K-R, et al. Cohesin Loss Eliminates All Loop Domains. Cell. 2017 Oct;171(2):305–320.e24. doi: 10.1016/j.cell.2017.09.026 28985562
61. Wutz G, Várnai C, Nagasaka K, Cisneros DA, Stocsits RR, Tang W, et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J. 2017 Dec 15;36(24):3573–99. doi: 10.15252/embj.201798004 29217591
62. Singh BN, Hampsey M. A Transcription-Independent Role for TFIIB in Gene Looping. Mol Cell. 2007;27(5):806–16. doi: 10.1016/j.molcel.2007.07.013 17803944
63. Zaman Z, Heid C, Ptashne M. Telomere looping permits repression “at a distance” in yeast. Curr Biol. 2002;12(11):930–3. doi: 10.1016/s0960-9822(02)00865-5 12062058
64. Cockell M, Palladino F, Laroche T, Kyrion G, Liu C, Lustig AJ, et al. The carboxy termini of Sir4 and RAP1 affect Sir3 localization: Evidence for a multicomponent complex required for yeast telomeric silencing. J Cell Biol. 1995;129(4):909–24. doi: 10.1083/jcb.129.4.909 7744964
65. Gottschling DE, Aparicio OM, Billington BL, Zakian VA. Position effect at S. cerevisiae telomeres: Reversible repression of Pol II transcription. Cell. 1990;63(4):751–62. doi: 10.1016/0092-8674(90)90141-z 2225075
66. Imai SI, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000;403(6771):795–800. doi: 10.1038/35001622 10693811
67. Rundlett SE, Carmen AA, Kobayashi R, Bavykin S, Turner BM, Grunstein M. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci U S A. 1996;93(25):14503–8. doi: 10.1073/pnas.93.25.14503 8962081
68. Sun ZW, Hampsey M. A general requirement for the Sin3-Rpd3 histone deacetylase complex in regulating silencing in Saccharomyces cerevisiae. Genetics. 1999;152(3):921–32. 10388812
69. Vannier D, Balderes D, Shore D. Evidence That the Transcriptional Regulators SIN3 and RPD3, and a Novel Gene (SDS3) with Similar Functions, Are Involved in Transcriptional Silencing in S. cerevisiae. Genetics. 1996;(144):1343–53.
70. Rubertis F De, Kadosh D, Henchoz S, Pauli D, Reuter G, Struhl K, et al. The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast. Nature. 1996;(384):589–591. doi: 10.1038/384589a0 8955276
71. Keogh M, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, et al. Cotranscriptional Set2 Methylation of Histone H3 Lysine 36 Recruits a Repressive Rpd3 Complex. Cell [Internet]. 2005 Nov;123(4):593–605. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0092867405011591 doi: 10.1016/j.cell.2005.10.025 16286008
72. Iglesias N, Redon S, Pfeiffer V, Dees M, Lingner J, Luke B. Subtelomeric repetitive elements determine TERRA regulation by Rap1/Rif and Rap1/Sir complexes in yeast. EMBO Rep. 2011;12(6):587–93. doi: 10.1038/embor.2011.73 21525956
73. Graf M, Bonetti D, Lockhart A, Serhal K, Kellner V, Maicher A, et al. Telomere Length Determines TERRA and R-Loop Regulation through the Cell Cycle. Cell. 2017;170(1):72–85.e14. doi: 10.1016/j.cell.2017.06.006 28666126
74. Pasquier E, Wellinger RJ. In vivo chromatin organization on native yeast telomeric regions is independent of a cis-telomere loopback conformation. Epigenetics Chromatin [Internet]. 2020 Dec 22;13(1):23. Available from: https://doi.org/10.1186/s13072-020-00344-w 32443982
75. Hocher A, Ruault M, Kaferle P, Descrimes M, Garnier M, Morillon A, et al. Expanding heterochromatin reveals discrete subtelomeric domains delimited by chromatin landscape transitions. Genome Res. 2018 Dec;28(12):1867–81. doi: 10.1101/gr.236554.118 30355601
76. Ochs F, Karemore G, Miron E, Brown J, Sedlackova H, Rask M-B, et al. Stabilization of chromatin topology safeguards genome integrity. Nature [Internet]. 2019 Oct 23;574(7779):571–4. Available from: http://www.nature.com/articles/s41586-019-1659-4 doi: 10.1038/s41586-019-1659-4 31645724
77. Nautiyal S, DeRisi JL, Blackburn EH. The genome-wide expression response to telomerase deletion in Saccharomyces cerevisiae. Proc Natl Acad Sci [Internet]. 2002 Jul 9;99(14):9316–21. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.142162499 12084816
78. Aparicio OM. Location, location, location: it’s all in the timing for replication origins. Genes Dev. 2013 Jan 15;27(2):117–28. doi: 10.1101/gad.209999.112 23348837
79. Hannan A, Abraham NM, Goyal S, Jamir I, Priyakumar UD, Mishra K. Sumoylation of Sir2 differentially regulates transcriptional silencing in yeast. Nucleic Acids Res. 2015;43(21):10213–26. doi: 10.1093/nar/gkv842 26319015
80. Martin SG, Laroche T, Suka N, Grunstein M, Gasser SM. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 1999;97(5):621–33. doi: 10.1016/s0092-8674(00)80773-4 10367891
81. Platt JM, Ryvkin P, Wanat JJ, Donahue G, Ricketts MD, Barrett SP, et al. Rap1 relocalization contributes to the chromatin-mediated gene expression profile and pace of cell senescence. Genes Dev. 2013;27(12):1406–20. doi: 10.1101/gad.218776.113 23756653
82. O’Sullivan RJ, Kubicek S, Schreiber SL, Karlseder J. Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat Struct Mol Biol. 2010;17(10):1218–25. doi: 10.1038/nsmb.1897 20890289
83. Cesare AJ, Karlseder J. A three-state model of telomere control over human proliferative boundaries. Curr Opin Cell Biol. 2012;24(6):731–8. doi: 10.1016/j.ceb.2012.08.007 22947495
84. Cesare AJ, Kaul Z, Cohen SB, Napier CE, Pickett HA, Neumann AA, et al. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat Struct Mol Biol. 2009;16(12):1244–51. doi: 10.1038/nsmb.1725 19935685
85. Balk B, Maicher A, Dees M, Klermund J, Luke-Glaser S, Bender K, et al. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol. 2013;20(10):1199–206. doi: 10.1038/nsmb.2662 24013207
86. Shevchenko A, Tomas H, Havli J, Olsen J V, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc [Internet]. 2006 Dec 25;1(6):2856–60. Available from: http://www.nature.com/articles/nprot.2006.468 doi: 10.1038/nprot.2006.468 17406544
87. Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc [Internet]. 2007 Aug;2(8):1896–906. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17703201 doi: 10.1038/nprot.2007.261 17703201
88. Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res [Internet]. 2019 Jan 8;47(D1):D419–26. Available from: https://academic.oup.com/nar/article/47/D1/D419/5165346 doi: 10.1093/nar/gky1038 30407594
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