Controlled light exposure microscopy reveals dynamic telomere microterritories throughout the cell cycle

Cytometry Part A

Volumn 75, Issue 5, 2009, Pages 428-439

  De Vos, Winnok H ^a   Hoebe, R A ^b   Joss, G H ^c   Haffmans, W ^b   Baatout, S ^d   Van Oostveldt, P ^a   Manders, E M M ^b  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c MACQUARIE UNIVERSITY   (Australia)

^d BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

Author keywords

Chromatin dynamics; CLEM; Live cell imaging; Nuclear organization; Telomere; TRF1; TRF2

Indexed keywords

TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2;

ARTICLE; CELL CYCLE; CELL NUCLEUS; CHROMATIN; CONTROLLED LIGHT EXPOSURE MICROSCOPY; DISSOCIATION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MICROSCOPE; MICROSCOPY; MITOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TELOMERE;

CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; RECOMBINANT FUSION PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2; TRANSFECTION;

EID: 65749098883     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.20699     Document Type: Article

References (63)

1. Greider CW. Telomeres do D-loop-T-loop. Cell 1999;97:419-422. (Pubitemid 29231163)
2. de Lange T. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev 2005;19:2100-2110. (Pubitemid 41330312)
3. Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet 2008;42: 16.1-16.34.
4. Smogorzewska A, van Steensel B, Bianchi A, Oelmann S, Schaefer MR, Schnapp G, de Lange T. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol 2000;20:1659-1668. (Pubitemid 30100185)
5. van Steensel B, Smogorzewska A, de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 1998;92:401-413. (Pubitemid 28093017)
6. Misteli T. Concepts in nuclear architecture. Bioessays 2005;27:477-487. (Pubitemid 40780850)
7. Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2001;2:292-301. (Pubitemid 33674777)
8. Cremer T, Kupper K, Dietzel S, Fakan S. Higher order chromatin architecture in the cell nucleus: On the way from structure to function. Biol Cell 2004; 96: 555-567. (Pubitemid 39562231)
9. Bystricky K, Laroche T, van HG, Blaszczyk M, Gasser SM. Chromosome looping in yeast: Telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J Cell Biol 2005;168:375-387. (Pubitemid 40205061)
10. Taddei A, Gasser SM. Multiple pathways for telomere tethering: Functional implications of subnuclear position for heterochromatin formation. Biochimica et Biophysica Acta (BBA) - Gene Struct Expr 2004;1677:120-128. (Pubitemid 38327096)
11. de Lange T. Human telomeres are attached to the nuclear matrix. EMBO J 1992;11:717-724.
12. Luderus ME, van Steensel B, Chong L, Sibon OC, Cremers FF, de Lange T. Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J Cell Biol 1996;135:867-881. (Pubitemid 26403765)
13. Weipoltshammer K, Schofer C, Almeder M, Philimonenko VV, Frei K, Wachtler F, Hozak P. Intranuclear anchoring of repetitive DNA sequences: Centromeres. Telomeres, and ribosomal DNA. J Cell Biol 1999;147:1409-1418.
14. Nagele RG, Velasco AQ, Anderson WJ, McMahon DJ, Thomson Z, Fazekas J, Wind K, Lee H. Telomere associations in interphase nuclei: Possible role in maintenance of interphase chromosome topology. J Cell Sci 2001;114:377-388.
15. Daniel A, St Heaps L. Chromosome loops arising from intrachromosomal tethering of telomeres occur at high frequency in G1 (non-cycling) mitotic cells: Implications for telomere capture. Cell Chromosome 2004;3:3.
16. Weierich C, Brero A, Stein S, von Hase J, Cremer C, Cremer T, Solovei I. Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res 2003;11:485-502. (Pubitemid 37041208)
17. Tam R, Smith KP, Lawrence JB. The 4q subtelomere harboring the FSHD locus is specifically anchored with peripheral heterochromatin unlike most human telomeres. J Cell Biol 2004;167:269-279. (Pubitemid 39435070)
18. Quina AS, Parreira L. Telomere-surrounding regions are transcription-permissive 3D nuclear compartments in human cells. Experiment Cell Res 2005;307:52-64. (Pubitemid 40732733)
19. Cerda MC, Berrios S, Fernandez-Donoso R, Garagna S, Redi C. Organisation of complex nuclear domains in somatic mouse cells. Biol Cell 1999;91:55-65.
20. Chuang T, Moshir S, Garini Y, Chuang A, Young I, Vermolen B, Doel Rvd, Mougey V, Perrin M, Braun M, Kerr P, Fest T, Boukamp P, Mai S. The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol 2004;2:12. (Pubitemid 38964080)
21. Ermler S, Krunic D, Knoch TA, Moshir S, Mai S, Greulich-Bode KM, Boukamp P. Cell cycle-dependent 3D distribution of telomeres and telomere repeat-binding factor 2 (TRF2) in HaCaT and HaCaT-myc cells. Eur J Cell Biol 2004;83:681-690. (Pubitemid 40123832)
22. Louis SF, Vermolen BJ, Garini Y, Young IT, Guffei A, Lichtensztejn Z, Kuttler F, Chuang TC, Moshir S, Mougey V, Chuang AY, Kerr PD, Fest T, Boukamp P, Mai S. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA 2005;102:9613-9618. (Pubitemid 40981729)
23. Molenaar C, Wiesmeijer K, Verwoerd NP, Khazen S, Eils R, Tanke HJ, Dirks RW. Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J 2003;22:6631-6641. (Pubitemid 38009609)
24. Wright A, Bubb WA, Hawkins CL, Davies MJ. Singlet oxygen-mediated protein oxidation: Evidence for the formation of reactive side chain peroxides on tyrosine residues. Photochem Photobiol 2002;76:35-46.
25. Song L, Varma CA, Verhoeven JW, Tanke HJ. Influence of the triplet excited state on the photobleaching kinetics of fluorescein in microscopy. Biophys J 1996;70:2959-2968. (Pubitemid 26000977)
26. Song L, Hennink EJ, Young IT, Tanke HJ. Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy. Biophys J 1995;68:2588-2600.
27. Dixit R, Cyr R. Cell damage and reactive oxygen species production induced by fluorescence microscopy: Effect on mitosis and guidelines for non-invasive fluorescence microscopy. Plant J 2003;36:280-290.
28. Zhao B, Bilski PJ, He YY, Feng L, Chignell CF. Photo-induced reactive oxygen species generation by different water-soluble fullerenes (C) and their cytotoxicity in human keratinocytes. Photochem Photobiol 2008;84:1215-1223.
29. Hoebe RA, Van Oven CH, Gadella TW, Jr., Dhonukshe PB, Van Noorden CJ, Manders EMM. Controlled light-exposure microscopy reduces photobleaching and phototoxicity in fluorescence live-cell imaging. Nat Biotechnol 2007;25:249-253. (Pubitemid 46227126)
30. Hoebe RA, van der Voort H, Stap J, Van Noorden CJ, Manders EMM. Quantitative determination of the reduction of phototoxicity and photobleaching by controlled light exposure microscopy. J Microsc 2008;231:9-20.
31. Kanda T, Sullivan KF, Wahl GM. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 1998;8:377-385. (Pubitemid 28173996)
32. Takahashi K, Sawasaki Y, Hata J, Mukai K, Goto T. Spontaneous transformation and immortalization of human endothelial cells. In Vitro Cell Dev Biol 1990;26:265-274. (Pubitemid 20125482)
33. Brown J, Reading SJ, Jones S, Fitchett CJ, Howl J, Martin A, Longland CL, Michelangeli F, Dubrova YE, Brown CA. Critical evaluation of ECV304 as a human endothelial cell model defined by genetic analysis and functional responses: A comparison with the human bladder cancer derived epithelial cell line T24/83. Lab Invest 2000;80:37-45.
34. Bekaert S, Koll S, Thas O, Van Oostveldt P. Comparing telomere length of sister chromatids in human lymphocytes using three-dimensional confocal microscopy. Cytometry 2002;48:34-44. (Pubitemid 34454144)
35. Manders EMM, Stap J, Brakenhoff GJ, van DR, Aten JA. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 1992;103 (Part 3):857-862. (Pubitemid 23023255)
36. Manders EMM, Hoebe R, Strackee J, Vossepoel AM, Aten JA. Largest contour segmentation: A tool for the localization of spots in confocal images. Cytometry Part A 1996;23A:15-21.
37. Bergsma CB, Streekstra GJ, Smeulders AW, Manders EM. Velocity estimation of spots in three-dimensional confocal image sequences of living cells. Cytometry 2001;43:261-272. (Pubitemid 32240474)
38. Bornfleth H, Edelmann P, Zink D, Cremer T, Cremer C. Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy. Biophys J 1999;77:2871-2886. (Pubitemid 29519530)
39. Lippincott-Schwartz J, Snapp E, Kenworthy A. Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2001;2:444-456. (Pubitemid 33680583)
40. Mattern KA, Swiggers SJ, Nigg AL, Lowenberg B, Houtsmuller AB, Zijlmans JM. Dynamics of protein binding to telomeres in living cells: Implications for telomere structure and function. Mol Cell Biol 2004;24:5587-5594.
41. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: Analysis by quantitative immunocolocalization. J Neurosci 2004;24:4070-4081.
42. Dynek JN, Smith S. Resolution of sister telomere association is required for progression through mitosis. Science 2004;304:97-100. (Pubitemid 38451464)
43. Gerlich D, Koch B, Dupeux F, Peters JM, Ellenberg J. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr Biol 2006;16:1571-1578. (Pubitemid 44142999)
44. Vourc'h C, Taruscio D, Boyle AL, Ward DC. Cell cycle-dependent distribution of telomeres. centromeres, and chromosome-specific subsatellite domains in the interphase nucleus of mouse lymphocytes. Exper Cell Res 1993;205:142-151.
45. Amrichova J, Lukasova E, Kozubek S, Kozubek M. Nuclear and territorial topography of chromosome telomeres in human lymphocytes. Exp Cell Res 2003;289:11-26. (Pubitemid 36993833)
46. Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet 2007;8:299-309. (Pubitemid 46439289)
47. Koering CE, Pollice A, Zibella MP, Bauwens S, Puisieux A, Brunori M, Brun C, Martins L, Sabatier L, Pulitzer JF, Gilson E. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Reports 2002;3:1055-1061. (Pubitemid 35469897)
48. Baur JA, Zou Y, Shay JW, Wright WE. Telomere position effect in human cells. Science 2001;292:2075-2077. (Pubitemid 32691573)
49. Benetti R, Garcia-Cao M, Blasco MA. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet 2007;39:243-250. (Pubitemid 46184357)
50. Zou Y, Gryaznov SM, Shay JW, Wright WE, Cornforth MN. Asynchronous replication timing of telomeres at opposite arms of mammalian chromosomes. Proc Natl Acad Sci USA 2004;101:12928-12933. (Pubitemid 39167560)
51. Hultdin M, Gronlund E, Norrback KF, Just T, Taneja K, Roos G. Replication timing of human telomeric DNA and other repetitive sequences analyzed by fluorescence in situ hybridization and flow cytometry. Exp Cell Res 2001;271:223-229. (Pubitemid 33141203)
52. Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 2008;10:228-236.
53. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007;318:798-801.
54. Maxwell SA, Capp D, Acosta SA. Telomerase activity in immortalized endothelial cells undergoing p53-mediated apoptosis. Biochem Biophys Res Commun 1997;241:642-645. (Pubitemid 28036710)
55. Cerone MA, Londono-Vallejo JA, Bacchetti S. Telomere maintenance by telomerase and by recombination can coexist in human cells. Hum Mol Genet 2001;10:1945-1952. (Pubitemid 32910539)
56. Cornforth MN, Eberle RL. Termini of human chromosomes display elevated rates of mitotic recombination. Mutagenesis 2001;16:85-89. (Pubitemid 32049217)
57. Stout K, van der Maarel S, Frants RR, Padberg GW, Ropers HH, Haaf T. Somatic pairing between subtelomeric chromosome regions: Implications for human genetic disease? Chromosome Res 1999;7:323-329.
58. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS. Long-range directional movement of an interphase chromosome site. Curr Biol 2006;16:825-831.
59. 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;20:551-561. (Pubitemid 41668640)
60. Zhu XD, Kuster B, Mann M, Petrini JH, de Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet 2000;25:347-352. (Pubitemid 30437327)
61. Tanaka H, Mendonca MS, Bradshaw PS, Hoelz DJ, Malkas LH, Meyn MS, Gilley D. DNA damage-induced phosphorylation of the human telomere-associated protein TRF2. Proc Natl Acad Sci USA 2005;102:15539-15544. (Pubitemid 41528829)
62. Bradshaw PS, Stavropoulos DJ, Meyn MS. Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage. Nat Genet 2005;37:193-197.
63. Heintzmann R, Ficz G. Breaking the resolution limit in light microscopy. Methods Cell Biol 2007;81:561-580.