Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening

Cell

Volumn 88, Issue 5, 1997, Pages 657-666

  Makarov, Vladimir L ^a   Hirose, Yoko ^a   Langmore, John P ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL IMMORTALIZATION; CHROMOSOME STRUCTURE; DNA NICK TRANSLATION; FIBROBLAST; HUMAN; HUMAN CELL; LEUKOCYTE; PRIORITY JOURNAL; TELOMERE; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

EUKARYOTA;

EID: 0031000884     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81908-X     Document Type: Article

References (54)

1. Allshire, R.C., Dempster, M., and Hastie, N.D. (1989). Human telomeres contain at least three types of G-rich repeats distributed nonrandomly. Nucl. Acids Res. 17, 4611-4627.
2. Biessmann, H., and Mason, J.M. (1988). Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J. 7, 1081-1086.
3. Birren, B., and Lai, E. (1993). Pulsed field gel electrophoresis: a practical guide. (San Diego: Academic Press).
4. Blackburn, E.H. (1991). Structure and function of telomeres. Nature 350, 569-573.
5. Blackburn, E.H. (1992). Telomerases. Annu. Rev. Biochem. 61, 113-129.
6. Blackburn, E.H., and Gall, J.G. (1978). A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol. 720, 33-53.
7. Broccoli, D., Young, J.W., and de Lange, T. (1995). Telomerase activity in normal and malignant hematopoietic cells. Proc. Natl. Acad. Sci. USA 92, 9082-9086.
8. Bryan, T.M., Englezou, A., Gupta, J., Bacchetti, S., and Reddel, R.R. (1995). Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14, 4240-4248.
9. Cardenas, M.E., Bianchi, A., and de Lange, T. (1993). A Xenopus egg factor with DNA-binding properties characteristic of terminusspecific telomeric proteins. Genes Dev. 7, 870-882.
10. Collins, K., and Greider, C.W. (1993). Tetrahymena telomerase catalyses nucleolytic cleavage and nonprocessive elongation. Genes Dev. 7, 1364-1376.
11. de Lange, T. (1994). Activation of telomerase in a human tumor. Proc. Natl. Acad. Sci. USA 91, 2882-2885.
12. Dixit, V.M., Marks, R.M., Sarma, V., and Prochownik, E.V. (1989). The antimitogenic action of tumor necrosis factor is associated with increased AP-1/c-jun proto-oncogene transcription. J. Biol. Chem. 264, 16905-16909.
13. Garvik, B., Carson, M., and Hartwell, L. (1995). Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15, 6128-6138.
14. Gottschling, D.E., and Zakian, V.A. (1986). Telomere proteins: specific recognition and protection of the natural termini of Oxitricha macronuclear DNA. Cell 47, 195-205.
15. Goulian, M., Richards, S.H., Heard, C.J., and Bigsby, B.M. (1990). Discontinuous DNA synthesis by purified mammalian proteins. J. Biol. Chem. 265, 18461-18471.
16. Greider, C.W. (1995). Telomerase biochemistry and regulation. In Telomeres, Volume 29, E.H. Blackburn and C.W. Greider, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 35-68.
17. Harley, C.B. (1991). Telomere loss: mitotic clock or genetic time bomb? Mutat. Res. 256, 271-282.
18. Harley, C.B. (1995). Telomeres and aging. In Telomeres, Volume 29, E.H. Blackburn and C.W. Greider, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 247-263.
19. Harley, C.B., and Villeponteau, B. (1995). Telomeres and telomerase in aging and cancer. Curr. Opin. Genet. Dev. 5, 249-255.
20. Harley, C.B., Futcher, A.B., and Greider, C.W. (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460.
21. Henderson, E. (1995). Telomere DNA structure. In Telomeres, Volume 29, E.H. Blackburn, and C.W. Greider, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 11-34.
22. Henderson, E.R., and Blackburn, E.H. (1989). An overhanging 3′ terminus is a conserved feature of telomeres. Mol. Cell. Biol. 9, 345-348.
23. Henderson, E.R., Larson, D., Melton, W., Shampay, J., Spangler, E., Greider, C., Ryan, T., and Blackburn, E. (1988). Structure, synthesis, and regulation of telomeres. Cancer Cells 6, 453-461.
24. Holland, P.M., Abramson, R.D., Watson, R., and Gelfand, D.H. (1991). Detection of specific polymerase chain reaction product by utilizing the 5′ → 3′ exonuclease activity of Thermus aquaticus DNA polymerase. Proc. Natl. Acad. Sci. USA 88, 7276-7280.
25. Ishimi, Y., Claude, A., Bullock, P., and Hurwitz, J. (1988). Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J. Biol. Chem. 263, 19723-19733.
26. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, W.E., Weinrich, S.L, and Shay, J.W. (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015.
27. Klobutcher, L.A., Swanton, M.T., Donini, P., and Prescott, D.M. (1981). All gene-sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3′ terminus. Proc. Natl. Acad. Sci. USA 78, 3015-3019.
28. Lejnine, S., Makarov, V.L., and Langmore, J.P. (1995). Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc. Natl. Acad. Sci. USA 92, 2393-2397.
29. Levis, R.W. (1989). Viable deletions of a telomere from a Drosophila chromosome. Cell 58, 791-801.
30. Li, B., and Lustig, A.J. (1996). A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev. 10, 1310-1326.
31. Lingner, J., and Cech, T.R. (1996). Purification of telomerase from Euplotes aediculatuss: requirement of a primer 3′ overhang. Proc. Natl. Acad. Sci. USA 93, 10712-10717.
32. Lingner, J., Cooper, J.P., and Cech, T.R. (1995). Telomerase and DNA end replication: no longer a lagging strand problem? Science 269, 1533-1534.
33. Longley, M.J., Bennett, S.E., and Mosbaugh, D.W. (1990). Characterization of the 5′ to 3′ exonuclease associated with Thermus aquaticus DNA polymerase. Nucleic Acids Res. 18, 7317-7322.
34. Lundblad, V., and Szostak, J.W. (1989). A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57, 633-643.
35. Makarov, V.L., Lejnine, S., Bedoyan, J., and Langmore, J.P. (1993). Nucleosomal organization of telomere-specific chromatin in rat. Cell 73, 775-787.
36. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1982). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
37. McClintock, B. (1939). The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc. Natl. Acad. Sci. USA 25, 405-416.
38. Murnane, J.P., Sabatier, L., Marder, B.A., and Morgan, W.F. (1994). Telomere dynamics in an immortal human cell line. EMBO J. 13, 4953-4962.
39. Nugent, C.I., Hughes, T.R., Lue, N.F., and Lundblad, V. (1996). Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274, 249-252.
40. Olovnikov, A.M. (1973). A theory of marginotomy. J. Theor. Biol. 41, 181-190.
41. Pluta, A.F., Kaine, B.P., and Spear, B.B. (1982). The terminal organization of macronuclear DNA in Oxitricha fallax. Nucleic Acids Res. 70, 8145-8154.
42. Price, C.M. (1990). Telomere structure in Euplotes crassus: characterization of DNA-protein interactions and isolation of a telomerebinding protein. Mol. Cell. Biol. 10, 3421-3431.
43. Sandell, L.S., and Zakian, V.A. (1993). Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75, 729-739.
44. Shay, J.W., Brasiskyté, D., Ouellette, M., Piatyszek, M.A., Werbin, H., Ying, Y., and Wright, W.E. (1994). Analysis of telomerase and telomeres. Meth. Mol. Genet. 5, 263-280.
45. Siegal, G., Turchi, J.J., Myers, T.W., and Bambara, R.A. (1992). A 5′ to 3′ exonuclease functionally interacts with calf DNA polymerase e. Proc. Natl. Acad. Sci. USA 89, 9377-9381.
46. Strahl, C., and Blackburn, E.H. (1996). Effects of reverse transcriptase inhibitors on telomere length and telomerase activity in two immortalized human cell lines. Mol. Cell. Biol. 16, 53-65.
47. Tseng, B.Y., Erickson, J.M., and Goulian, M. (1979). Initiator RNA of nascent DNA from animal cells. J. Mol. Biol. 129, 531-545.
48. Wang, S.-S., and Zakian, V.A. (1990). Telomere-telomere recombination provides an express pathway for telomere acquisition. Nature 345, 456-458.
49. Watson, J.D. (1972). Origin of concatemeric DNA. Nature New Biol. 239, 197-201.
50. Wellinger, R.J., Wolf, A.J., and Zakian, V.A. (1993a). Sacharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72, 51-60.
51. Wellinger, R.J., Wolf, A.J., and Zakian, V.A. (1993b). Origin activation and formation of single strand TG1-3 tails occur sequentially in late S phase on a yeast linear plasmid. Mol. Cell. Biol. 13, 4057-4065.
52. Wellinger R.J., Ethier, K., Labrecque, P., and Zakian, V.A. (1996). Evidence for a new step in telomere maintenance. Cell 85, 423-433.
53. Zakian, V.A. (1989). Structure and function of telomeres. Annu. Rev. Genet. 23, 579-604.
54. Zakian, V.A. (1995). Telomeres: beginning to understand the end. Science 270, 1601-1607.