A method for measuring the distribution of the shortest telomeres in cells and tissues

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Lai, Tsung Po ^a   Zhang, Ning ^a   Noh, Jungsik ^a   Mender, Ilgen ^a   Tedone, Enzo ^a   Huang, Ejun ^a   Wright, Woodring E ^a   Danuser, Gaudenz ^a   Shay, Jerry W ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMETELSTAT;

AGING; BLOOD; CANCER; CELLS AND CELL COMPONENTS; CHROMOSOME; SOFTWARE;

ADULT; AGED; ANIMAL EXPERIMENT; ARTICLE; CALU-6 CELL LINE; CANCER GROWTH; COLON CANCER; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DNA SEQUENCE; ENTEROBACTERIA PHAGE MS2; FEMALE; FIBROSING ALVEOLITIS; HELA CELL LINE; HT-1080 CELL LINE; HUMAN; HUMAN CELL; IMAGE PROCESSING; JURKAT CELL LINE; LIMIT OF QUANTITATION; MALE; MOUSE; NIH 3T3 CELL LINE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; TELOMERE; TELOMERE LENGTH; TELOMERE SHORTENING; YOUNG ADULT; AGING; ANIMAL; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; MIDDLE AGED; NEOPLASM; NUCLEIC ACID AMPLIFICATION; PROCEDURES; SOFTWARE; SOUTHERN BLOTTING;

MUS;

ADULT; AGED; AGING; ANIMALS; BLOTTING, SOUTHERN; FEMALE; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MICE; MIDDLE AGED; NEOPLASMS; NIH 3T3 CELLS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; SOFTWARE; TELOMERE;

EID: 85033383677     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-01291-z     Document Type: Article

References (69)

1. Palm, W. & de Lange, T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334 (2008).
2. Olovnikov, A. M. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41, 181-190 (1973).
3. Watson, J. D. Origin of concatemeric T7 DNA. Nat. New Biol. 239, 197-201 (1972).
4. Fitzpatrick, A. L. et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am. J. Epidemiol. 165, 14-21 (2007).
5. Sampson, M. J., Winterbone, M. S., Hughes, J. C., Dozio, N. & Hughes, D. A. Monocyte telomere shortening and oxidative DNA damage in type 2 diabetes. Diabetes Care 29, 283-289 (2006).
6. Wiemann, S. U. et al. Hepatocyte telomere shortening and senescence are general markers of human liver cirrhosis. FASEB J. 16, 935-942 (2002).
7. Shay, J. W. Role of telomeres and telomerase in aging and cancer. Cancer Discov. 6, 584-593 (2016).
8. Holohan, B., Wright, W. E. & Shay, J. W. Cell biology of disease: telomeropathies: an emerging spectrum disorder. J. Cell Biol. 205, 289-299 (2014).
9. Armanios, M. & Blackburn, E. H. The telomere syndromes. Nat. Rev. Genet. 13, 693-704 (2012).
10. Opresko, P. L. & Shay, J. W. Telomere-associated aging disorders. Ageing Res. Rev. 33, 52-66 (2017).
11. Herbig, U., Jobling, W. A., Chen, B. P., Chen, D. J. & Sedivy, J. M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14, 501-513 (2004).
12. Fumagalli, M. et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 14, 355-365 (2012).
13. Hemann, M. T., Strong, M. A., Hao, L. Y. & Greider, C. W. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107, 67-77 (2001).
14. Zou, Y., Sfeir, A., Gryaznov, S. M., Shay, J. W. & Wright, W. E. Does a sentinel or a subset of short telomeres determine replicative senescence? Mol. Biol. Cell 15, 3709-3718 (2004).
15. Campisi, J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 75, 685-705 (2013).
16. Vera, E., Bernardes de Jesus, B., Foronda, M., Flores, J. M. & Blasco, M. A. The rate of increase of short telomeres predicts longevity in mammals. Cell Rep. 2, 732-737 (2012).
17. Montpetit, A. J. et al. Telomere length: a review of methods for measurement. Nurs. Res. 63, 289-299 (2014).
18. Nussey, D. H. et al. Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol. Evol. 5, 299-310 (2014).
19. Vera, E. & Blasco, M. A. Beyond average: potential for measurement of short telomeres. Aging. 4, 379-392 (2012).
20. Kimura, M. et al. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat. Protoc. 5, 1596-1607 (2010).
21. Cawthon, R. M. Telomere measurement by quantitative PCR. Nucleic. Acids Res. 30, e47 (2002).
22. Holland, A. J. & Cleveland, D. W. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 10, 478-487 (2009).
23. Lansdorp, P. M. et al. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5, 685-691 (1996).
24. Aubert, G., Hills, M. & Lansdorp, P. M. Telomere length measurement-caveats and a critical assessment of the available technologies and tools. Mutat. Res. 730, 59-67 (2012).
25. Wieser, M. et al. Nuclear flow FISH: isolation of cell nuclei improves the determination of telomere lengths. Exp. Gerontol. 41, 230-235 (2006).
26. Gasser, S. M., Hediger, F., Taddei, A., Neumann, F. R. & Gartenberg, M. R. The function of telomere clustering in yeast: the circe effect. Cold Spring. Harb. Symp. Quant. Biol. 69, 327-337 (2004).
27. Ramirez, M. J. & Surralles, J. Laser confocal microscopy analysis of human interphase nuclei by three-dimensional FISH reveals dynamic perinucleolar clustering of telomeres. Cytogenet. Genome. Res. 122, 237-242 (2008).
28. Baird, D. M., Rowson, J., Wynford-Thomas, D. & Kipling, D. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat. Genet. 33, 203-207 (2003).
29. Bendix, L., Horn, P. B., Jensen, U. B., Rubelj, I. & Kolvraa, S. The load of short telomeres, estimated by a new method, Universal STELA, correlates with number of senescent cells. Aging. Cell 9, 383-397 (2010).
30. Ding, Z. et al. Estimating telomere length from whole genome sequence data. Nucleic. Acids Res. 42, e75 (2014).
31. Nersisyan, L. & Arakelyan, A. Computel: computation of mean telomere length from whole-genome next-generation sequencing data. PLoS ONE 10, e0125201 (2015).
32. Castle, J. C. et al. DNA copy number, including telomeres and mitochondria, assayed using next-generation sequencing. BMC. Genomics. 11, 244 (2010).
33. Lee, M. et al. Comparative analysis of whole genome sequencing-based telomere length measurement techniques. Methods 114, 4-15 (2017).
34. Steinert, S., Shay, J. W. & Wright, W. E. Modification of subtelomeric DNA. Mol. Cell. Biol. 24, 4571-4580 (2004).
35. Sfeir, A. J., Chai, W., Shay, J. W. & Wright, W. E. Telomere-end processing the terminal nucleotides of human chromosomes. Mol. Cell 18, 131-138 (2005).
36. Hockemeyer, D., Sfeir, A. J., Shay, J. W., Wright, W. E. & de Lange, T. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24, 2667-2678 (2005).
37. Lai, T. P., Wright, W. E. & Shay, J. W. Generation of digoxigenin-incorporated probes to enhance DNA detection sensitivity. Biotechniques 60, 306-309 (2016).
38. Ruiz-Herrera, A., Nergadze, S. G., Santagostino, M. & Giulotto, E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet. Genome Res. 122, 219-228 (2008).
39. Wood, A. M. et al. TRF2 and lamin A/C interact to facilitate the functional organization of chromosome ends. Nat. Commun. 5, 5467 (2014).
40. Lavrentieva, I. et al. High polymorphism level of genomic sequences flanking insertion sites of human endogenous retroviral long terminal repeats. FEBS. Lett. 443, 341-347 (1999).
41. Herbert, B. S. et al. Lipid modification of GRN163, an N3′- >P5′ thiophosphoramidate oligonucleotide, enhances the potency of telomerase inhibition. Oncogene. 24, 5262-5268 (2005).
42. Frink, R. E. et al. Telomerase inhibitor imetelstat has preclinical activity across the spectrum of non-small cell lung cancer oncogenotypes in a telomere length dependent manner. Oncotarget 7, 31639-31651 (2016).
43. Min, J., Wright, W. E. & Shay, J.W. Alternative lengthening of telomeres can be maintained by preferential elongation of lagging strands. Nucleic Acids Res. 45, 2615-2628 (2017).
44. Harley, C. B., Futcher, A. B. & Greider, C. W. Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460 (1990).
45. DePinho, R. A. & Polyak, K. Cancer chromosomes in crisis. Nat. Genet. 36, 932-934 (2004).
46. Druliner, B. R. et al. Time lapse to colorectal cancer: telomere dynamics define the malignant potential of polyps. Clin. Transl. Gastroenterol. 7, e188 (2016).
47. Armanios, M. Y. et al. Telomerase mutations in families with idiopathic pulmonary fibrosis. N. Engl. J. Med. 356, 1317-1326 (2007).
48. Tsakiri, K. D. et al. Adult-onset pulmonary fibrosis caused by mutations in telomerase. Proc. Natl. Acad. Sci. USA 104, 7552-7557 (2007).
49. Diaz de Leon, A. et al. Telomere lengths, pulmonary fibrosis and telomerase (TERT) mutations. PLoS ONE 5, e10680 (2010).
50. Cronkhite, J. T. et al. Telomere shortening in familial and sporadic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 178, 729-737 (2008).
51. Stuart, B. D. et al. Exome sequencing links mutations in PARN and RTEL1 with familial pulmonary fibrosis and telomere shortening. Nat. Genet. 47, 512-517 (2015).
52. Vallejo, A. N., Weyand, C. M. & Goronzy, J. J. T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends Mol. Med. 10, 119-124 (2004).
53. Pawelec, G. et al. Human immunosenescence: is it infectious? Immunol. Rev. 205, 257-268 (2005).
54. Epel, E. S. et al. Accelerated telomere shortening in response to life stress. Proc. Natl Acad. Sci. USA 101, 17312-17315 (2004).
55. Salvador, L. et al. A natural product telomerase activator lengthens telomeres in humans: a randomized, double blind, and placebo controlled study. Rejuvenation Res. 19, 478-484 (2016).
56. Meznikova, M., Erdmann, N., Allsopp, R. & Harrington, L. A. Telomerase reverse transcriptase-dependent telomere equilibration mitigates tissue dysfunction in mTert heterozygotes. Dis. Model. Mech. 2, 620-626 (2009).
57. Erdmann, N., Liu, Y. & Harrington, L. Distinct dosage requirements for the maintenance of long and short telomeres in mTert heterozygous mice. Proc. Natl. Acad. Sci. USA 101, 6080-6085 (2004).
58. Lejnine, S., Makarov, V. L. & Langmore, J. P. Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc. Natl. Acad. Sci. USA 92, 2393-2397 (1995).
59. Keane, M. et al. Insights into the evolution of longevity from the bowhead whale genome. Cell Rep. 10, 112-122 (2015).
60. Gomes, N. M. et al. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10, 761-768 (2011).
61. Henson, J. D., Neumann, A. A., Yeager, T. R. & Reddel, R. R. Alternative lengthening of telomeres in mammalian cells. Oncogene. 21, 598-610 (2002).
62. Lin, J. et al. Systematic and cell type-specific telomere length changes in subsets of lymphocytes. J. Immunol. Res. 2016, 5371050 (2016).
63. Lin, Y. et al. Age-associated telomere attrition of lymphocytes in vivo is coordinated with changes in telomerase activity, composition of lymphocyte subsets and health conditions. Clin. Sci. 128, 367-377 (2015).
64. Weng, N. P., Akbar, A. N. & Goronzy, J. CD28(-) T cells: their role in the ageassociated decline of immune function. Trends Immunol. 30, 306-312 (2009).
65. Theodoris, C. V. et al. Long telomeres protect against age-dependent cardiac disease caused by NOTCH1 haploinsufficiency. J. Clin. Invest. 127, 1683-1688 (2017).
66. Mender, I., & Shay, J. W. Telomere Restriction Fragment (TRF)Analysis. Bio Protoc. 5, e1658 (2015).
67. Min, J., Wright, W. E., & Shay, J. W. Alternative lengthening of telomeres mediated by mitotic DNA synthesis engages break-induced replication processes. Mol. Cell. Biol. (2017).
68. Mender, I., & Shay, J. W. Telomere dysfunction induced foci (TIF)analysis. Bio. Protoc. 5, e1656 (2015).
69. Poon, S. S., & Lansdorp, P. M. Quantitative fluorescence in situ hybridization (Q-FISH). Curr. Protoc. Cell Biol. Chapter 18, Unit18 14 (2001).