Peroxiredoxin 1 Protects Telomeres from Oxidative Damage and Preserves Telomeric DNA for Extension by Telomerase

Cell Reports

Volumn 17, Issue 12, 2016, Pages 3107-3114

  Aeby, Eric ^a   Ahmed, Wareed ^a   Redon, Sophie ^a   Simanis, Viesturs ^a   Lingner, Joachim ^a  

^a EPFL   (Switzerland)

Author keywords

oxidative stress; peroxiredoxin 1; telomerase; telomeres

Indexed keywords

PEROXIREDOXIN 1; TELOMERASE; 8-OXO-7-HYDRODEOXYGUANOSINE; DEOXYGUANOSINE; DNA; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; OXIDATIVE STRESS; PRDX1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; TELOMERE; TRANSCRIPTION ELONGATION; ANALOGS AND DERIVATIVES; CELL CYCLE; DNA DAMAGE; GENETICS; HETEROCHROMATIN; HUMAN; METABOLISM;

CELL CYCLE; CHROMATIN; DEOXYGUANOSINE; DNA; DNA DAMAGE; HETEROCHROMATIN; HUMANS; OXIDATIVE STRESS; PEROXIREDOXINS; REACTIVE OXYGEN SPECIES; TELOMERASE; TELOMERE;

EID: 85006759590     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.11.071     Document Type: Article

References (28)

1. Ahmed, S., Passos, J.F., Birket, M.J., Beckmann, T., Brings, S., Peters, H., Birch-Machin, M.A., von Zglinicki, T., Saretzki, G., Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J. Cell Sci. 121 (2008), 1046–1053.
2. Banfalvi, G., Cell cycle synchronization of animal cells and nuclei by centrifugal elutriation. Nat. Protoc. 3 (2008), 663–673.
3. Chae, H.Z., Robison, K., Poole, L.B., Church, G., Storz, G., Rhee, S.G., Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. USA 91 (1994), 7017–7021.
4. Cristofari, G., Reichenbach, P., Regamey, P.O., Banfi, D., Chambon, M., Turcatti, G., Lingner, J., Low- to high-throughput analysis of telomerase modulators with Telospot. Nat. Methods 4 (2007), 851–853.
5. Doksani, Y., Wu, J.Y., de Lange, T., Zhuang, X., Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 155 (2013), 345–356.
6. Forsyth, N.R., Evans, A.P., Shay, J.W., Wright, W.E., Developmental differences in the immortalization of lung fibroblasts by telomerase. Aging Cell 2 (2003), 235–243.
7. Fumagalli, M., Rossiello, F., Clerici, M., Barozzi, S., Cittaro, D., Kaplunov, J.M., Bucci, G., Dobreva, M., Matti, V., Beausejour, C.M., et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 14 (2012), 355–365.
8. 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 (Amst.) 7 (2008), 1233–1249.
9. Grolimund, L., Aeby, E., Hamelin, R., Armand, F., Chiappe, D., Moniatte, M., Lingner, J., A quantitative telomeric chromatin isolation protocol identifies different telomeric states. Nat. Commun., 4, 2013, 2848.
10. Haendeler, J., Hoffmann, J., Brandes, R.P., Zeiher, A.M., Dimmeler, S., Hydrogen peroxide triggers nuclear export of telomerase reverse transcriptase via Src kinase family-dependent phosphorylation of tyrosine 707. Mol. Cell. Biol. 23 (2003), 4598–4610.
11. Loor, G., Kondapalli, J., Schriewer, J.M., Chandel, N.S., Vanden Hoek, T.L., Schumacker, P.T., Menadione triggers cell death through ROS-dependent mechanisms involving PARP activation without requiring apoptosis. Free Radic. Biol. Med. 49 (2010), 1925–1936.
12. Majerska, J., Redon, S., Lingner, J., Quantitative telomeric chromatin isolation protocol for human cells. Methods, 2016, 10.1016/j.ymeth.2016.08.003 Published online August 9, 2016.
13. Miller, K.M., Rog, O., Cooper, J.P., Semi-conservative DNA replication through telomeres requires Taz1. Nature 440 (2006), 824–828.
14. Mourkioti, F., Kustan, J., Kraft, P., Day, J.W., Zhao, M.M., Kost-Alimova, M., Protopopov, A., DePinho, R.A., Bernstein, D., Meeker, A.K., Blau, H.M., Role of telomere dysfunction in cardiac failure in Duchenne muscular dystrophy. Nat. Cell Biol. 15 (2013), 895–904.
15. Neumann, C.A., Krause, D.S., Carman, C.V., Das, S., Dubey, D.P., Abraham, J.L., Bronson, R.T., Fujiwara, Y., Orkin, S.H., Van Etten, R.A., Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424 (2003), 561–565.
16. Oikawa, S., Kawanishi, S., Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett. 453 (1999), 365–368.
17. Ong, S.E., Mann, M., Stable isotope labeling by amino acids in cell culture for quantitative proteomics. Methods Mol. Biol. 359 (2007), 37–52.
18. Perkins, A., Nelson, K.J., Parsonage, D., Poole, L.B., Karplus, P.A., Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40 (2015), 435–445.
19. Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., Zhang, F., Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8 (2013), 2281–2308.
20. Sahin, E., Colla, S., Liesa, M., Moslehi, J., Müller, F.L., Guo, M., Cooper, M., Kotton, D., Fabian, A.J., Walkey, C., et al. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470 (2011), 359–365.
21. Sauerwald, A., Sandin, S., Cristofari, G., Scheres, S.H., Lingner, J., Rhodes, D., Structure of active dimeric human telomerase. Nat. Struct. Mol. Biol. 20 (2013), 454–460.
22. Sfeir, A., de Lange, T., Removal of shelterin reveals the telomere end-protection problem. Science 336 (2012), 593–597.
23. Sfeir, A., Kosiyatrakul, S.T., Hockemeyer, D., MacRae, S.L., Karlseder, J., Schildkraut, C.L., de Lange, T., Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138 (2009), 90–103.
24. Sun, L., Tan, R., Xu, J., LaFace, J., Gao, Y., Xiao, Y., Attar, M., Neumann, C., Li, G.M., Su, B., et al. Targeted DNA damage at individual telomeres disrupts their integrity and triggers cell death. Nucleic Acids Res. 43 (2015), 6334–6347.
25. Vannier, J.B., Pavicic-Kaltenbrunner, V., Petalcorin, M.I., Ding, H., Boulton, S.J., RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149 (2012), 795–806.
26. Vizcaíno, J.A., Deutsch, E.W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J.A., Sun, Z., Farrah, T., Bandeira, N., et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32 (2014), 223–226.
27. von Zglinicki, T., Oxidative stress shortens telomeres. Trends Biochem. Sci. 27 (2002), 339–344.
28. Wang, Z., Rhee, D.B., Lu, J., Bohr, C.T., Zhou, F., Vallabhaneni, H., de Souza-Pinto, N.C., Liu, Y., Characterization of oxidative guanine damage and repair in mammalian telomeres. PLoS Genet., 6, 2010, e1000951.