Markers of cellular senescence. Telomere shortening as a marker of cellular senescence

Aging

Volumn 8, Issue 1, 2016, Pages 3-11

  Bernadotte, Alexandra ^a,b   Mikhelson, Victor M ^c   Spivak, Irina M ^c,d,e  

^a KAROLINSKA INSTITUTE   (Sweden)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c INSTITUTE OF CYTOLOGY   (Russian Federation)

^d ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^e PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

Author keywords

Aging; Biomarkers; Cellular senescence; Replicative senescence; Telomere; Telomere theory

Indexed keywords

GENETIC MARKER; H2AFX PROTEIN, HUMAN; HETEROCHROMATIN; HISTONE;

AGE; AGING; ANIMAL; CELL AGING; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; HETEROCHROMATIN; HUMAN; METABOLISM; PATHOLOGY; PHENOTYPE; REPRODUCIBILITY; TELOMERE; TELOMERE SHORTENING;

AGE FACTORS; AGING; ANIMALS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; HETEROCHROMATIN; HISTONES; HUMANS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; TELOMERE; TELOMERE SHORTENING;

EID: 84986567947     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100871     Document Type: Article

References (102)

1. Stein GH, Drullinger LF, Robetorye RS, Pereira-Smith OM, Smith JR. Senescent cells fail to express cdc2, cycA, and cycB in response to mitogen stimulation. Proc Natl Acad Sci U S A 1991;88:11012-11016.
2. Meyne J, Ratliff RL, Moyzis RK. Conservation of the human telomere sequence ( TTAGGG ). among vertebrates. Proc Natl Acad Sci U S A 1989;86:7049-7053.
3. Shiue L, Myers RM, Cox DR, Naylor SL, Killery ANNM, Varmus HE. Structure and Variability of Human Chromosome Ends. Mol Cell Biol 1990;10:518-527.
4. Wright WE, Tesmer VM, Huffman KE, Levene SD, Shay JW. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev 1997;11:2801-2809.
5. Hockemeyer D, Sfeir AJ, Shay JW, Wright WE, de Lange T. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J 2005;24:2667-2678. doi:10.1038/sj.emboj.7600733.
6. Olovnikov A. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol 1973;41:181-190.
7. Greider CW, Blackburn EH. The telomere terminal transferase of tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 1987;51:887-898. doi:10.1016/0092-8674(87)90576-9.
8. Chan SRWL, Blackburn EH. Telomeres and telomerase. Philos Trans R Soc B Biol Sci 2004;359:109-122. doi:10.1098/rstb.2003.1370.
9. Olovnikov A. Telomeres, telomerase, and aging: origin of the theory. Exp Gerontol 1996;31:443-448.
10. Olovnikov A. Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 1971;201:1496-9.
11. Hayflick L, Moorhead P. The serial cultivation of human diploid cell strains. Exp Cell Res 1961;25.
12. Harley C, Futcher A, Greider C. Telomeres shorten during ageing of human fibroblasts. Nature 1990;345:458-460.
13. Allsopp RC, Vaziri H, Pattersont C, Goldsteint S, Younglai E V, Futcher AB, et al. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA 1992;89:10114-10118.
14. Hao L-Y, Armanios M, Strong MA, Karim B, Feldser DM, Huso D, et al. Short telomeres, even in the presence of telomerase, limit tissue renewal capacity. Cell 2005;123:1121-1131. doi:10.1016/j.cell.2005.11.020.
15. Reichert S, Criscuolo F, Verinaud E, Zahn S, Massemin S. Telomere length correlations among somatic tissues in adult zebra finches. PLoS One 2013;8:e81496. doi:10.1371/journal.pone.0081496.
16. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. Telomere length in early life predicts lifespan. Proc Natl Acad Sci U S A 2012;109:1743-1748. doi:10.1073/pnas.1113306109.
17. Kaul Z, Cesare AJ, Huschtscha LI, Neumann A a, Reddel RR. Five dysfunctional telomeres predict onset of senescence in human cells. EMBO Rep 2012;13:52-59. doi:10.1038/embor.2011.227.
18. Griffith J, Bryant J, Fordyce C, Gilliland F, Joste N, Moyzis R. Reduced telomere DNA content is correlated with genomic instability and metastasis in invasive human breast carcinoma. Breast Cancer Res Treat 1999;54:59-64.
19. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, et al. Mammalian Telomeres End in a Large Duplex Loop. Cell 1999;97:503-514.
20. Smith JS, Chen Q, Yatsunyk LA, Nicoludis JM, Garcia MS, Kranaster R, et al. Rudimentary G-quadruplex-based telomere capping in Saccharomyces cerevisiae. Nat Struct Mol Biol 2011;18:478-485. doi:10.1038/nsmb.2033.Rudimentary.
21. Tanaka H, Beam MJ, Caruana K. The Presence of Telomere Fusion in Sporadic Colon Cancer Independently of Disease Stage, TP53/KRAS Mutation Status, Mean Telomere Length, and Telomerase Activity. Neoplasia 2014;16:814-823. doi:10.1016/j.neo.2014.08.009.
22. Capper R, Britt-compton B, Tankimanova M, Rowson J, Letsolo B, Man S, et al. The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev 2007;21:2495-2508. doi:10.1101/gad.439107.somatic.
23. Zou Y, Sfeir A, Gryaznov SM, Shay JW, Wright WE. Does a Sentinel or a Subset of Short Telomeres Determine Replicative Senescence? Mol Biol Cell 2004;15:3709-3718. doi:10.1091/mbc.E04.
24. Lundblad V, Szostak J. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 1989;57:633-643.
25. Shay JW, Wright WE. Role of telomeres and telomerase in cancer. Semin Cancer Biol 2011;21:349-353. doi:10.1016/j.semcancer.2011.10.001.Role.
26. Neumann AA, Watson CM, Noble JR, Pickett HA, Tam PPL, Reddel RR. Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev 2013;27:18-23. doi:10.1101/gad.205062.112.Freely.
27. Bojovic B, Crowe D. Dysfunctional telomeres promote genomic instability and metastasis in the absence of telomerase activity in oncogene induced mammary cancer. Mol Carcinog 2013;52:103-117.
28. Hovest MG, Bru N, Hosseini KS, Krieg T, Herrmann G. Senescence of Human Fibroblasts after Psoralen Photoactivation Is Mediated by ATR Kinase and Persistent DNA Damage Foci at Telomeres. Mol Biol Cell 2006;17:1758-1767. doi:10.1091/mbc.E05.
29. Daniali L, Benetos A, Susser E, Kark JD, Labat C, Kimura M, et al. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun 2013;4:1597. doi:10.1038/ncomms2602.
30. Sidorov I, Kimura M, Yashin A, Aviv A. Leukocyte telomere dynamics and human hematopoietic stem cell kinetics during somatic growth. Exp Hematol 2009;37:514-524. doi:10.1016/j.exphem.2008.11.009.
31. Youngren K, Jeanclos E, Aviv H, Kimura M, Stock J, Hanna M, et al. Synchrony in telomere length of the human fetus. Hum Genet 2014;102:640-643. doi:10.1007/s004390050755.
32. Bischoff C, Petersen H, Graakjaer J, Andersen-Ranberg, K Vaupel J, Bohr V, Kølvraa S, et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology 2006;17:190-194.
33. Li H, Hedmer M, Wojdacz T, Hossain MB, Lindh CH, Tinnerberg Hô, et al. Oxidative Stress, Telomere Shortening, and DNA Methylation in Relation to Low-to-Moderate Occupational Exposure to Welding Fumes. Environ Mol Mutagen 2015;00:1-10. doi:10.1002/em.
34. Takubo K, Izumiyama-Shimomura, N Honma N, Sawabe M, Arai T, Kato M, Oshimura M, et al. Telomere lengths are characteristic in each human individual. Exp Gerontol 2002;37:523-531.
35. Baird D, Roger L, Osterman P, Svenson U, Nordfja K. Blood Cell Telomere Length Is a Dynamic Feature. PLoS One 2011;6:e21485. doi:10.1371/Citation.
36. Aviv A. Telomeres, sex, reactive oxygen species, and human cardiovascular aging. J Mol Med (Berl) 2002;80:689-695.
37. Carlson LE, Beattie TL, Giese-Davis J, Faris P, Tamagawa R, Fick LJ, et al. Mindfulness-based cancer recovery and supportiveexpressive therapy maintain telomere length relative to controls in distressed breast cancer survivors. Cancer 2014. doi:10.1002/cncr.29063.
38. Hemann MT, Strong M a, Hao L-Y, Greider CW. The Shortest Telomere, Not Average Telomere Length, Is Critical for Cell Viability and Chromosome Stability. Cell 2001;107:67-77. doi:10.1016/S0092-8674(01)00504-9.
39. Njajou OT, Cawthon RM, Damcott CM, Wu S-H, Ott S, Garant MJ, et al. Telomere length is paternally inherited and is associated with parental lifespan. Proc Natl Acad Sci U S A 2007;104:12135-12139. doi:10.1073/pnas.0702703104.
40. Herbig U, Ferreira M, Condel L, Carey D, Sedivy J. Cellular senescence in aging primates. Science 2006;311:1257.
41. Mikhelson V. Replicative mosaicism might explain the seeming contradictions in the telomere theory of aging. Mech Ageing Dev 2001;122:1361-1365.
42. Kong CM, Lee XW, Wang X. Telomere shortening in human diseases. FEBS J 2013;280:3180-3193. doi:10.1111/febs.12326.
43. Kota LN, Bharath S, Purushottam M, Moily NS, Sivakumar PT, Varghese M, et al. Reduced telomere length in neurodegenerative disorders may suggest shared biology. J Neuropsychiatry Clin Neurosci 2015;27:e92-96. doi:10.1176/appi.neuropsych.13100240.
44. Demissie S, Levy D, Benjamin EJ, Cupples L a, Gardner JP, Herbert a, et al. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham Heart Study. Aging Cell 2006;5:325-330. doi:10.1111/j.1474-9726.2006.00224.x.
45. Edo MD, Andrés V. Aging, telomeres, and atherosclerosis. Cardiovasc Res 2005;66:213-221. doi:10.1016/j.cardiores.2004.09.007.
46. Epel ES, Lin J, Wilhelm FH, Wolkowitz OM, Cawthon R, Adler NE, et al. Cell aging in relation to stress arousal and cardiovascular disease risk factors. Psychoneuroendocrinology 2006;31:277-287. doi:10.1016/j.psyneuen.2005.08.011.
47. Fitzpatrick AL, Kronmal R a, Kimura M, Gardner JP, Psaty BM, Jenny NS, et al. Leukocyte telomere length and mortality in the Cardiovascular Health Study. J Gerontol A Biol Sci Med Sci 2011;66:421-429. doi:10.1093/gerona/glq224.
48. Ramírez R, Carracedo J, Soriano S, Jiménez R, Martín-Malo A, Rodríguez M, et al. Stress-induced premature senescence in mononuclear cells from patients on long-term hemodialysis. Am J Kidney Dis 2005;45:353-359. doi:10.1053/j.ajkd.2004.10.022.
49. Boxall MC, Goodship THJ, Brown AL, Ward MC, von Zglinicki T. Telomere shortening and haemodialysis. Blood Purif 2006;24:185-189. doi:10.1159/000090517.
50. Broberg K, Björk J, Paulsson K, Höglund M, Albin M. Constitutional short telomeres are strong genetic susceptibility markers for bladder cancer. Carcinogenesis 2005;26:1263-1271. doi:10.1093/carcin/bgi063.
51. Bagheri S, Nosrati M, Li S, Fong S, Torabian S, Rangel J, et al. Genes and pathways downstream of telomerase in melanoma metastasis. Proc Natl Acad Sci U S A 2006;103:11306-11311. doi:10.1073/pnas.0510085103.
52. Cai Z, Yan L-J, Ratka A. Telomere shortening and Alzheimer's disease. Neuromolecular Med 2013;15:25-48. doi:10.1007/s12017-012-8207-9.
53. Maeda T, Guan JZ, Koyanagi M, Higuchi Y, Makino N. Agingassociated alteration of telomere length and subtelomeric status in female patients with Parkinson's disease. J Neurogenet 2012;26:245-251. doi:10.3109/01677063.2011.651665.
54. Wolkowitz OM, Mellon SH, Epel ES, Lin J, Dhabhar FS, Su Y, et al. Leukocyte Telomere Length in Major Depression: Correlations with Chronicity, Inflammation and Oxidative Stress-Preliminary Findings. PLoS One 2011;6:e17837. doi:10.1371/journal.pone.0017837.
55. Willeit P, Raschenberger J, Heydon EE, Tsimikas S, Haun M, Mayr A, et al. Leucocyte telomere length and risk of type 2 diabetes mellitus: new prospective cohort study and literaturebased meta-analysis. PLoS One 2014; 9:e112483.
56. Willeit P, Willeit J, Kloss-Brandstätter A, Kronenberg F, Kiechl S. Fifteen-Year Follow-up of Association Between Telomere Length and Incident Cancer and Cancer Mortality. JAMA 2011;36:10-12.
57. Loprinzi P, Loenneke J. Lower Extremity Muscular Strength and Leukocyte Telomere Length: Implications of Muscular Strength in Attenuating Age-Related Chronic Disease. J Phys Act Heal 2015.
58. Passos JF, Saretzki G, Ahmed S, Nelson G, Richter T, Peters H, et al. Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol 2007;5:e110. doi:10.1371/journal.pbio.0050110.
59. Armanios M, Blackburn EH. The telomere syndromes. Nat Rev Genet 2013;13:693-704. doi:10.1038/nrg3246.The.
60. Mitchell J, Wood E, Collins K. A telomerase component is defective in the human disease dyskeratosis congenita. Nature 1999;402:551-555.
61. Heiss N, Knight S, Vulliamy T, Klauck S, Wiemann S, Mason P, et al. X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet 1998;19:32-38.
62. Wyllie F, Jones C, Skinner J, Haughton M, Wallis C, Wynford-Thomas, D Faragher R, et al. Telomerase prevents the accelerated cell ageing of Werner syndrome fibroblasts. Nat Genet 2000;24:16-17.
63. Barbaro P, Ziegler DS, Reddel RR. The wide-ranging clinical implications of the Short Telomere Syndromes. Intern Med J 2015; doi:10.1111/imj.12868.
64. Dimri GP, Leet X, Basile G, Acosta M, Scorrt G, Roskelley C, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995;92:9363-9367.
65. Lawless C, Wang C, Jurk D, Merz A, Zglinicki T Von, Passos JF. Quantitative assessment of markers for cell senescence. Exp Gerontol 2010;45:772-778. doi:10.1016/j.exger.2010.01.018.
66. Gary RK, Kindell SM. Quantitative assay of senescenceassociated beta-galactosidase activity in mammalian cell extracts. Anal Biochem 2005;343:329-334. doi:10.1016/j.ab.2005.06.003.
67. Kurz DJ, Decary S, Hong Y, Erusalimsky JD. Senescenceassociated β-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J Cell Sci 2000;20:3613-3622.
68. Pati S, Jain S, Behera M, Acharya AP, Panda SK, Senapati S. Xgal staining of canine skin tissues: A technique with multiple possible applications. J Nat Sci Biol Med 2014;5:245-249. doi:10.4103/0976-9668.136147.
69. Kawano H, Katsurabayashi S, Kakazu Y, Yamashita Y, Kubo N, Kubo M, et al. Long-term culture of astrocytes attenuates the readily releasable pool of synaptic vesicles. PLoS One 2012;7:e48034. doi:10.1371/journal.pone.0048034.
70. Choi J, Shendrik I, Peacocke M, Peehl D, Buttyan R, Ikeguchi EF, et al. Expression of senescence-associated beta-galactosidase in enlarged prostates from men with benign prostatic hyperplasia. Urology 2000;56:160-166.
71. Lee BY, Han JA, Im JS, Morrone A, Johung K, Goodwin EC, et al. Senescence-associated beta-galactosidase is lysosomal betagalactosidase. Aging Cell 2006;5:187-195.
72. Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ. Is betagalactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 2000;257:162-171.
73. Matsunaga H, Handa JT, Aotaki-keen AA, Sherwood SW, West MD, Hjelmeland LM. Beta-Galactosidase Histochemistry and Telomere Loss in Senescent Retinal Pigment Epithelial Cells. Invest Ophthalmol Vis Sci 1999;40:197-202.
74. Narita M, Nunez S, Heard E, Lin A, Hearn S, Spector D, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003;113:703-716.
75. Narita M, Narita M, Krizhanovsky V, Nuñez S, Chicas A, Hearn SA, et al. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006;126:503-514. doi:10.1016/j.cell.2006.05.052.
76. Zhang R, Poustovoitov M, Ye X, Santos H, Chen W, Daganzo S, et al. Formation of MacroH2A-containing senescenceassociated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell 2005;8:19-30.
77. Kreiling J, Tamamori-Adachi M, Sexton A, Jeyapalan J, Munoz-Najar U, Peterson A, et al. Age-associated increase in heterochromatic marks in murine and primate tissues. Aging Cell 2011;10:292-304. doi:10.1111/j.1474-9726.2010.00666.x.Ageassociated.
78. Kennedy AL, McBryan T, Enders GH, Johnson FB, Zhang R, Adams PD. Senescent mouse cells fail to overtly regulate the HIRA histone chaperone and do not form robust Senescence Associated Heterochromatin Foci. Cell Div 2010;5:16. doi:10.1186/1747-1028-5-16.
79. Kosar M, Bartkova J, Hubackova S, Hodny Z, Lukas J, Bartek J. Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type-and insult-dependent manner and follow expression of p16(ink4a). Cell Cycle 2011;10:457-468.
80. Zhang R, Chen W, Adams PD. Molecular Dissection of Formation of Senescence-Associated Heterochromatin Foci. Mol Cell Biol 2007;27:2343-2358. doi:10.1128/MCB.02019-06.
81. Di Micco R, Sulli G, Dobreva M, Liontos M, Botrugno O, Gargiulo G, et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 2011;13:292-302. doi:10.1038/ncb2170.Interplay.
82. Sedelnikova O, Horikawa I, Zimonjic D, Popescu N, Bonner W, Barrett J. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 2004;6:168-170.
83. Redon C, Nakamura A, Sordet O, Dickey J, Gouliaeva K, Tabb B, et al. γ-H2AX detection in peripheral blood lymphocytes, splenocytes, bone marrow, xenografts, and skin. Methods Mol Biol 2011;682:249-270.
84. Sharma A, Singh K, Almasan A. Histone H2AX phosphorylation: a marker for DNA damage. Methods Mol Biol 2012;920:613-626.
85. Balajee A, Geard C. Replication protein A and gamma-H2AX foci assembly is triggered by cellular response to DNA doublestrand breaks. Exp Cell Res 2004;300:320-634.
86. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000;10:886-895. doi:10.1016/S0960-9822(00)00610-2.
87. Kotenko K V, Bushmanov AY, Ozerov I V, Guryev D V, Anchishkina N a, Smetanina NM, et al. Changes in the number of double-strand DNA breaks in Chinese hamster V79 cells exposed to γ-radiation with different dose rates. Int J Mol Sci 2013;14:13719-13726. doi:10.3390/ijms140713719.
88. Sedelnikova O, Horikawa I, Redon C, Nakamura A, Zimonjic D, Popescu N, et al. Delayed kinetics of DNA double-strand break processing in normal and pathological aging. Aging Cell 2008;7:89-100.
89. Löbrich M, Shibata A, Beucher A, Fisher A, Ensminger M, Goodarzi A, et al. GammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010;9:662-669.
90. Rogakou EP, Pilch DR, Orr a. H, Ivanova VS, Bonner WM. DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139. J Biol Chem 1998;273:5858-5868. doi:10.1074/jbc.273.10.5858.
91. Furuta T, Takemura H, Liao Z-Y, Aune GJ, Redon C, Sedelnikova O a, et al. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replicationdependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 2003;278:20303-312. doi:10.1074/jbc.M300198200.
92. Burzynski S. Gene silencing-a new theory of aging. Med Hypotheses 2003;60:578-583.
93. Udugama M, Chang FTM, Chan FL, Tang MC, Pickett H a, McGhie JDR, et al. Histone variant H3.3 provides the heterochromatic H3 lysine 9 tri-methylation mark at telomeres. Nucleic Acids Res 2015; 43:10227-37:1-11. doi:10.1093/nar/gkv847.
94. Zhang X, Li B, Jonge N De, Xu D. The DNA methylation inhibitor induces telomere dysfunction and apoptosis of leukemia cells that is attenuated by telomerase. Oncotarget 2015;6:4888-900.
95. Guilleret I, Benhattar J. Demethylation of the human telomerase catalytic subunit (hTERT) gene promoter reduced hTERT expression and telomerase activity and shortened telomeres. Exp Cell Res 2003;289:326-334. doi:10.1016/S0014-4827(03)00281-7.
96. Dessain SK, Yu H, Reddel RR, Beijersbergen RL, Weinberg RA. Advances in Brief Methylation of the Human Telomerase Gene CpG Island 1. Cancer Res 2000;60:537-541.
97. Runov A, Vonsky M, Mikhelson V. DNA methylation level and telomere length as a basis for the biological aging clock model construction. Tsitologiia 2015;57:192-196.
98. Wilson KA., Stern DF. NFBD1/MDC1, 53BP1 and BRCA1 have both redundant and unique roles in the ATM pathway. Cell Cycle 2014;7:3584-3594. doi:10.4161/cc.7.22.7102.
99. Iwabuchi K, Matsui T, Hashimoto M, Matsumoto Y, Kurihara T, Date T. Characterization of a cancer cell line that expresses a splicing variant form of 53BP1: separation of checkpoint and repair functions in 53BP1. Biochem Biophys Res Commun 2008;376:509-513. doi:10.1016/j.bbrc.2008.09.022.
100. Wenger B, Schwegler M, Brunner M, Daniel C, Schmidt M, Fietkau R, et al. PML-nuclear bodies decrease with age and their stress response is impaired in aged individuals. BMC Geriatr 2014;14:42. doi:10.1186/1471-2318-14-42.
101. Ferbeyre G, Stanchina E De, Querido E, Baptiste N, Prives C, Lowe SW. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 2000;14:2015-2027.
102. Osterwald S, Deeg KI, Chung I, Parisotto D, Wörz S, Rohr K, et al. PML induces compaction, TRF2 depletion and DNA damage signaling at telomeres and promotes their alternative lengthening. J Cell Sci 2015;128:1887-1900. doi:10.1242/jcs.148296.