Advertisement

Biochemistry (Moscow)

, Volume 75, Issue 13, pp 1563–1583 | Cite as

Telomerase: Structure, functions, and activity regulation

  • M. I. ZverevaEmail author
  • D. M. Shcherbakova
  • O. A. Dontsova
Review

Abstract

Telomerase is the enzyme responsible for maintenance of the length of telomeres by addition of guanine-rich repetitive sequences. Telomerase activity is exhibited in gametes and stem and tumor cells. In human somatic cells proliferation potential is strictly limited and senescence follows approximately 50–70 cell divisions. In most tumor cells, on the contrary, replication potential is unlimited. The key role in this process of the system of the telomere length maintenance with involvement of telomerase is still poorly studied. No doubt, DNA polymerase is not capable to completely copy DNA at the very ends of chromosomes; therefore, approximately 50 nucleotides are lost during each cell cycle, which results in gradual telomere length shortening. Critically short telomeres cause senescence, following crisis, and cell death. However, in tumor cells the system of telomere length maintenance is activated. Besides catalytic telomere elongation, independent telomerase functions can be also involved in cell cycle regulation. Inhibition of the telomerase catalytic function and resulting cessation of telomere length maintenance will help in restriction of tumor cell replication potential. On the other hand, formation of temporarily active enzyme via its intracellular activation or due to stimulation of expression of telomerase components will result in telomerase activation and telomere elongation that can be used for correction of degenerative changes. Data on telomerase structure and function are summarized in this review, and they are compared for evolutionarily remote organisms. Problems of telomerase activity measurement and modulation by enzyme inhibitors or activators are considered as well.

Key words

telomerase senescence TERT telomerase RNA telomerase reaction cycle telomerase activity telomerase regulators 

Abbreviations

CTE

C-terminal TERT domain (C-terminal extension)

IFD

TERT domain (insertion in fingers domain)

Pif1p

helicase of Saccharomyces cerevisiae

TER

telomerase

RNA

TERRA, RNA transcribed from telomeric DNA (telomeric repeat-containing RNA)

TERT

telomerase reverse transcriptase

TLC1 RNA

telomerase RNA of Saccharomyces cerevisiae

TWJ

Y-like structural element of RNA (three way junction)

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Greider, C. W., and Blackburn, E. H. (1987) Cell, 51, 887–898.PubMedGoogle Scholar
  2. 2.
    Shcherbakova, D. M., Zvereva, M. E., Shpanchenko, O. V., and Dontsova, O. A. (2006) Mol. Biol. (Moscow), 40, 1–15.Google Scholar
  3. 3.
    Osterhage, J. L., Talley, J. M., and Friedman, K. L. (2006) Nat. Struct. Mol. Biol., 13, 720–728.PubMedGoogle Scholar
  4. 4.
    Hsu, M., Yu, E. Y., Singh, S. M., and Lue, N. F. (2007) Eukaryot. Cell, 6, 1330–1338.PubMedGoogle Scholar
  5. 5.
    Collins, K. (2006) Nat. Rev. Mol. Cell. Biol., 7, 484–494.PubMedGoogle Scholar
  6. 6.
    Mozdy, A. D., Podell, E. R., and Cech, T. R. (2008) Mol. Cell. Biol., 28, 4152–4161.PubMedGoogle Scholar
  7. 7.
    Cristofari, G., and Lingner, J. (2006) EMBO J., 25, 565–574.PubMedGoogle Scholar
  8. 8.
    Denchi, E. L. (2009) DNA Repair (Amst.), 8, 1118–1126.Google Scholar
  9. 9.
    Janknecht, R. (2004) FEBS Lett., 564, 9–13.PubMedGoogle Scholar
  10. 10.
    Bollmann, F. M. (2007) Cancer Treat. Rev., 33, 704–709.PubMedGoogle Scholar
  11. 11.
    Schmitt, C. A. (2007) Biochim. Biophys. Acta, 1775, 5–20.PubMedGoogle Scholar
  12. 12.
    Masutomi, K., et al. (2003) Cell, 114, 241–253.PubMedGoogle Scholar
  13. 13.
    Kaszubowska, L. (2008) J. Physiol. Pharmacol., 59,Suppl. 9, 169–186.PubMedGoogle Scholar
  14. 14.
    Flores, I., Benetti, R., and Blasco, M. A. (2006) Curr. Opin. Cell. Biol., 18, 254–260.PubMedGoogle Scholar
  15. 15.
    Mitchell, J. R., Wood, E., and Collins, K. (1999) Nature, 402, 551–555.PubMedGoogle Scholar
  16. 16.
    Mitchell, J. R., Cheng, J., and Collins, K. (1999) Mol. Cell. Biol., 19, 567–576.PubMedGoogle Scholar
  17. 17.
    Armanios, M., et al. (2005) Proc. Natl. Acad. Sci. USA, 102, 15960–15964.PubMedGoogle Scholar
  18. 18.
    Chen, G., Tai, A. K., Lin, M., Chang, F., Terhorst, C., and Huber, B. T. (2007) Eur. J. Immunol., 37, 663–674.PubMedGoogle Scholar
  19. 19.
    Minamino, T., and Komuro, I. (2007) Circ. Res., 100, 15–26.PubMedGoogle Scholar
  20. 20.
    Ogami, M., et al. (2004) Arterioscler. Thromb. Vasc. Biol., 24, 546–550.PubMedGoogle Scholar
  21. 21.
    De Felice, B., Wilson, R. R., and Nacca, M. (2009) BMC Med. Genet., 10, 110.PubMedGoogle Scholar
  22. 22.
    Tarkanyi, I., and Aradi, J. (2008) Biochimie, 90, 156–172.PubMedGoogle Scholar
  23. 23.
    Hayflick, L. (1997) Biochemistry (Moscow), 62, 1180–1190.Google Scholar
  24. 24.
    Olovnikov, A. M. (1973) J. Theor. Biol., 41, 181–190.PubMedGoogle Scholar
  25. 25.
    Kelleher, C., Teixeira, M. T., Forstemann, K., and Lingner, J. (2002) Trends Biochem. Sci., 27, 572–579.PubMedGoogle Scholar
  26. 26.
    Lue, N. F. (2004) Bioessays, 26, 955–962.PubMedGoogle Scholar
  27. 27.
    Collins, K. (1999) Annu. Rev. Biochem., 68, 187–218.PubMedGoogle Scholar
  28. 28.
    Bosoy, D., and Lue, N. F. (2004) Nucleic Acids Res., 32, 93–101.PubMedGoogle Scholar
  29. 29.
    Chen, J. L., and Greider, C. W. (2003) EMBO J., 22, 304–314.PubMedGoogle Scholar
  30. 30.
    Forstemann, K., and Lingner, J. (2001) Mol. Cell. Biol., 21, 7277–7286.PubMedGoogle Scholar
  31. 31.
    Morin, G. B. (1989) Cell, 59, 521–529.PubMedGoogle Scholar
  32. 32.
    Greider, C. W. (1991) Mol. Cell. Biol., 11, 4572–4580.PubMedGoogle Scholar
  33. 33.
    Prowse, K. R., Avilion, A. A., and Greider, C. W. (1993) Proc. Natl. Acad. Sci. USA, 90, 1493–1497.PubMedGoogle Scholar
  34. 34.
    Cohn, M., and Blackburn, E. H. (1995) Science, 269, 396–400.PubMedGoogle Scholar
  35. 35.
    Lue, N. F., and Peng, Y. (1997) Nucleic Acids Res., 25, 4331–4337.PubMedGoogle Scholar
  36. 36.
    Prescott, J., and Blackburn, E. H. (1997) Genes Dev., 11, 2790–2800.PubMedGoogle Scholar
  37. 37.
    Teixeira, M. T., Arneric, M., Sperisen, P., and Lingner, J. (2004) Cell, 117, 323–335.PubMedGoogle Scholar
  38. 38.
    Prescott, J., and Blackburn, E. H. (1997) Genes Dev., 11, 528–540.PubMedGoogle Scholar
  39. 39.
    Lue, N. F., and Li, Z. (2007) Nucleic Acids Res., 35, 5213–5222.PubMedGoogle Scholar
  40. 40.
    Chang, M., Arneric, M., and Lingner, J. (2007) Genes Dev., 21, 2485–2494.PubMedGoogle Scholar
  41. 41.
    Niu, H., Xia, J., and Lue, N. F. (2000) Mol. Cell Biol., 20, 6806–6815.PubMedGoogle Scholar
  42. 42.
    Petrov, A. V., Dokudovskaya, S. S., Sokolov, K. A., Lavrik, O. I., Favre, A., Dontsova, O. A., and Bogdanov, A. A. (1998) FEBS Lett., 436, 35–40.PubMedGoogle Scholar
  43. 43.
    Huard, S., and Autexier, C. (2004) Nucleic Acids Res., 32, 2171–2180.PubMedGoogle Scholar
  44. 44.
    Oulton, R., and Harrington, L. (2004) Mol. Biol. Cell, 15, 3244–3256.PubMedGoogle Scholar
  45. 45.
    Theimer, C. A., and Feigon, J. (2006) Curr. Opin. Struct. Biol., 16, 307–318.PubMedGoogle Scholar
  46. 46.
    Autexier, C., and Lue, N. F. (2006) Annu. Rev. Biochem., 75, 493–517.PubMedGoogle Scholar
  47. 47.
    Lue, N. F., Lin, Y. C., and Mian, I. S. (2003) Mol. Cell. Biol., 23, 8440–8449.PubMedGoogle Scholar
  48. 48.
    Friedman, K. L., Heit, J. J., Long, D. M., and Cech, T. R. (2003) Mol. Biol. Cell, 14, 1–13.PubMedGoogle Scholar
  49. 49.
    Xia, J., Peng, Y., Mian, I. S., and Lue, N. F. (2000) Mol. Cell. Biol., 20, 5196–5207.PubMedGoogle Scholar
  50. 50.
    Bosoy, D., Peng, Y., Mian, I. S., and Lue, N. F. (2003) J. Biol. Chem., 278, 3882–3890.PubMedGoogle Scholar
  51. 51.
    Friedman, K. L., and Cech, T. R. (1999) Genes Dev., 13, 2863–2874.PubMedGoogle Scholar
  52. 52.
    Jacobs, S. A., Podell, E. R., and Cech, T. R. (2006) Nat. Struct. Mol. Biol., 13, 218–225.PubMedGoogle Scholar
  53. 53.
    Rouda, S., and Skordalakes, E. (2007) Structure, 15, 1403–1412.PubMedGoogle Scholar
  54. 54.
    Gillis, A. J., Schuller, A. P., and Skordalakes, E. (2008) Nature, 455, 633–637.PubMedGoogle Scholar
  55. 55.
    Romi, E., Baran, N., Gantman, M., Shmoish, M., Min, B., Collins, K., and Manor, H. (2007) Proc. Natl. Acad. Sci. USA, 104, 8791–8796.PubMedGoogle Scholar
  56. 56.
    Richards, S., et al. (2008) Nature, 452, 949–955.PubMedGoogle Scholar
  57. 57.
    Nugent, C. I., and Lundblad, V. (1998) Genes Dev., 12, 1073–1085.PubMedGoogle Scholar
  58. 58.
    Weinrich, S. L., et al. (1997) Nat. Genet., 17, 498–502.PubMedGoogle Scholar
  59. 59.
    Peng, Y., Mian, I. S., and Lue, N. F. (2001) Mol. Cell., 7, 1201–1211.PubMedGoogle Scholar
  60. 60.
    Eugster, A., et al. (2006) Nat. Struct. Mol. Biol., 13, 734–739.PubMedGoogle Scholar
  61. 61.
    Boule, J. B., Vega, L. R., and Zakian, V. A. (2005) Nature, 438, 57–61.PubMedGoogle Scholar
  62. 62.
    Zhang, D. H., Zhou, B., Huang, Y., Xu, L. X., and Zhou, J. Q. (2006) Nucleic Acids Res., 34, 1393–1404.PubMedGoogle Scholar
  63. 63.
    Zhou, J., Monson, E. K., Teng, S. C., Schulz, V. P., and Zakian, V. A. (2000) Science, 289, 771–774.PubMedGoogle Scholar
  64. 64.
    Mangahas, J. L., Alexander, M. K., Sandell, L. L., and Zakian, V. A. (2001) Mol. Biol. Cell, 12, 4078–4089.PubMedGoogle Scholar
  65. 65.
    Jacobs, S. A., Podell, E. R., Wuttke, D. S., and Cech, T. R. (2005) Protein Sci., 14, 2051–2058.PubMedGoogle Scholar
  66. 66.
    Moriarty, T. J., Ward, R. J., Taboski, M. A., and Autexier, C. (2005) Mol. Biol. Cell, 16, 3152–3161.PubMedGoogle Scholar
  67. 67.
    Lue, N. F., and Peng, Y. (1998) Nucleic Acids Res., 26, 1487–1494.PubMedGoogle Scholar
  68. 68.
    Lue, N. F. (2005) J. Biol. Chem., 280, 26586–26591.PubMedGoogle Scholar
  69. 69.
    Hardy, C. D., Schultz, C. S., and Collins, K. (2001) J. Biol. Chem., 276, 4863–4871.PubMedGoogle Scholar
  70. 70.
    Harrington, L. A., and Greider, C. W. (1991) Nature, 353, 451–454.PubMedGoogle Scholar
  71. 71.
    Baran, N., Haviv, Y., Paul, B., and Manor, H. (2002) Nucleic Acids Res., 30, 5570–5578.PubMedGoogle Scholar
  72. 72.
    Hammond, P. W., Lively, T. N., and Cech, T. R. (1997) Mol. Cell. Biol., 17, 296–308.PubMedGoogle Scholar
  73. 73.
    Wallweber, G., Gryaznov, S., Pongracz, K., and Pruzan, R. (2003) Biochemistry, 42, 589–600.PubMedGoogle Scholar
  74. 74.
    Melek, M., Greene, E. C., and Shippen, D. E. (1996) Mol. Cell. Biol., 16, 3437–3445.PubMedGoogle Scholar
  75. 75.
    Alves, D., Li, H., Codrington, R., Orte, A., Ren, X., Klenerman, D., and Balasubramanian, S. (2008) Nat. Chem. Biol., 4, 287–289.PubMedGoogle Scholar
  76. 76.
    Lai, C. K., Mitchell, J. R., and Collins, K. (2001) Mol. Cell. Biol., 21, 990–1000.PubMedGoogle Scholar
  77. 77.
    O’Connor, C. M., Lai, C. K., and Collins, K. (2005) J. Biol. Chem., 280, 17533–17539.PubMedGoogle Scholar
  78. 78.
    Moriarty, T. J., Marie-Egyptienne, D. T., and Autexier, C. (2004) Mol. Cell. Biol., 24, 3720–3733.PubMedGoogle Scholar
  79. 79.
    Zaug, A. J., Podell, E. R., and Cech, T. R. (2008) Nat. Struct. Mol. Biol., 15, 870–872.PubMedGoogle Scholar
  80. 80.
    Ji, H., Platts, M. H., Dharamsi, L. M., and Friedman, K. L. (2005) Mol. Cell. Biol., 25, 9103–9114.PubMedGoogle Scholar
  81. 81.
    Ji, H., Adkins, C. J., Cartwright, B. R., and Friedman, K. L. (2008) Mol. Cell. Biol., 28, 2380–2390.PubMedGoogle Scholar
  82. 82.
    Chen, J. L., Opperman, K. K., and Greider, C. W. (2002) Nucleic Acids Res., 30, 592–597.PubMedGoogle Scholar
  83. 83.
    Miller, M. C., Liu, J. K., and Collins, K. (2000) EMBO J., 19, 4412–4422.PubMedGoogle Scholar
  84. 84.
    Lai, C. K., Miller, M. C., and Collins, K. (2002) Genes Dev., 16, 415–420.PubMedGoogle Scholar
  85. 85.
    Lin, J., and Blackburn, E. H. (2004) Genes Dev., 18, 387–396.PubMedGoogle Scholar
  86. 86.
    Zhou, X. Z., and Lu, K. P. (2001) Cell, 107, 347–359.PubMedGoogle Scholar
  87. 87.
    Banik, S. S., and Counter, C. M. (2004) J. Biol. Chem., 279, 51745–51748.PubMedGoogle Scholar
  88. 88.
    Forstemann, K., and Lingner, J. (2005) EMBO Rep., 6, 361–366.PubMedGoogle Scholar
  89. 89.
    Hossain, S., Singh, S., and Lue, N. F. (2002) J. Biol. Chem., 277, 36174–36180.PubMedGoogle Scholar
  90. 90.
    Huard, S., Moriarty, T. J., and Autexier, C. (2003) Nucleic Acids Res., 31, 4059–4070.PubMedGoogle Scholar
  91. 91.
    Banik, S. S., Guo, C., Smith, A. C., Margolis, S. S., Richardson, D. A., Tirado, C. A., and Counter, C. M. (2002) Mol. Cell. Biol., 22, 6234–6246.PubMedGoogle Scholar
  92. 92.
    Armbruster, B. N., Banik, S. S., Guo, C., Smith, A. C., and Counter, C. M. (2001) Mol. Cell. Biol., 21, 7775–7786.PubMedGoogle Scholar
  93. 93.
    Gandhi, L., and Collins, K. (1998) Genes Dev., 12, 721–733.PubMedGoogle Scholar
  94. 94.
    Roy, J., Fulton, T. B., and Blackburn, E. H. (1998) Genes Dev., 12, 3286–3300.PubMedGoogle Scholar
  95. 95.
    Zhu, J., Wang, H., Bishop, J. M., and Blackburn, E. H. (1999) Proc. Natl. Acad. Sci. USA, 96, 3723–3728.PubMedGoogle Scholar
  96. 96.
    Blackburn, E. H. (2005) FEBS Lett., 579, 859–862.PubMedGoogle Scholar
  97. 97.
    Maringele, L., and Lydall, D. (2002) Genes Dev., 16, 1919–1933.PubMedGoogle Scholar
  98. 98.
    Zubko, M. K., Guillard, S., and Lydall, D. (2004) Genetics, 168, 103–115.PubMedGoogle Scholar
  99. 99.
    Gravel, S., Larrivee, M., Labrecque, P., and Wellinger, R. J. (1998) Science, 280, 741–744.PubMedGoogle Scholar
  100. 100.
    Garvik, B., Carson, M., and Hartwell, L. (1995) Mol. Cell. Biol., 15, 6128–6138.PubMedGoogle Scholar
  101. 101.
    Steinberg-Neifach, O., and Lue, N. F. (2006) Nucleic Acids Res., 34, 2710–2722.PubMedGoogle Scholar
  102. 102.
    Hsu, M., McEachern, M. J., Dandjinou, A. T., Tzfati, Y., Orr, E., Blackburn, E. H., and Lue, N. F. (2007) Proc. Natl. Acad. Sci. USA, 104, 11682–11687.PubMedGoogle Scholar
  103. 103.
    Sarin, K. Y., Cheung, P., Gilison, D., Lee, E., Tennen, R. I., Wang, E., Artandi, M. K., Oro, A. E., and Artandi, S. E. (2005) Nature, 436, 1048–1052.PubMedGoogle Scholar
  104. 104.
    Park, J. I., et al. (2009) Nature, 460, 66–72.PubMedGoogle Scholar
  105. 105.
    Zappulla, D. C., and Cech, T. R. (2004) Proc. Natl. Acad. Sci. USA, 101, 10024–10029.PubMedGoogle Scholar
  106. 106.
    Dandjinou, A. T., Levesque, N., Larose, S., Lucier, J. F., Abou Elela, S., and Wellinger, R. J. (2004) Curr. Biol., 14, 1148–1158.PubMedGoogle Scholar
  107. 107.
    Romero, D. P., and Blackburn, E. H. (1991) Cell, 67, 343–353.PubMedGoogle Scholar
  108. 108.
    Chen, J. L., Blasco, M. A., and Greider, C. W. (2000) Cell, 100, 503–514.PubMedGoogle Scholar
  109. 109.
    Lin, J., Ly, H., Hussain, A., Abraham, M., Pearl, S., Tzfati, Y., Parslow, T. G., and Blackburn, E. H. (2004) Proc. Natl. Acad. Sci. USA, 101, 14713–14718.PubMedGoogle Scholar
  110. 110.
    Qiao, F., and Cech, T. R. (2008) Nat. Struct. Mol. Biol., 15, 634–640.PubMedGoogle Scholar
  111. 111.
    Livengood, A. J., Zaug, A. J., and Cech, T. R. (2002) Mol. Cell. Biol., 22, 2366–2374.PubMedGoogle Scholar
  112. 112.
    Lai, C. K., Miller, M. C., and Collins, K. (2003) Mol. Cell, 11, 1673–1683.PubMedGoogle Scholar
  113. 113.
    Miller, M. C., and Collins, K. (2002) Proc. Natl. Acad. Sci. USA, 99, 6585–6590.PubMedGoogle Scholar
  114. 114.
    Ware, T. L., Wang, H., and Blackburn, E. H. (2000) EMBO J., 19, 3119–3131.PubMedGoogle Scholar
  115. 115.
    Legassie, J. D., and Jarstfer, M. B. (2005) Biochemistry, 44, 14191–14201.PubMedGoogle Scholar
  116. 116.
    Seto, A. G., Umansky, K., Tzfati, Y., Zaug, A. J., Blackburn, E. H., and Cech, T. R. (2003) RNA, 9, 1323–1332.PubMedGoogle Scholar
  117. 117.
    Chen, J. L., and Greider, C. W. (2003) Genes Dev., 17, 2747–2752.PubMedGoogle Scholar
  118. 118.
    Leonardi, J., Box, J. A., Bunch, J. T., and Baumann, P. (2008) Nat. Struct. Mol. Biol., 15, 26–33.PubMedGoogle Scholar
  119. 119.
    Webb, C. J., and Zakian, V. A. (2008) Nat. Struct. Mol. Biol., 15, 34–42.PubMedGoogle Scholar
  120. 120.
    Chen, J. L., and Greider, C. W. (2005) Proc. Natl. Acad. Sci. USA, 102, 8080–8085; discussion 8077–8089.PubMedGoogle Scholar
  121. 121.
    Theimer, C. A., Blois, C. A., and Feigon, J. (2005) Mol. Cell, 17, 671–682.PubMedGoogle Scholar
  122. 122.
    Antal, M., Boros, E., Solymosy, F., and Kiss, T. (2002) Nucleic Acids Res., 30, 912–920.PubMedGoogle Scholar
  123. 123.
    Leeper, T. C., and Varani, G. (2005) RNA, 11, 394–403.PubMedGoogle Scholar
  124. 124.
    Ly, H., Blackburn, E. H., and Parslow, T. G. (2003) Mol. Cell. Biol., 23, 6849–6856.PubMedGoogle Scholar
  125. 125.
    Chen, Y., Fender, J., Legassie, J. D., Jarstfer, M. B., Bryan, T. M., and Varani, G. (2006) EMBO J., 25, 3156–3166.PubMedGoogle Scholar
  126. 126.
    Richards, R. J., Wu, H., Trantirek, L., O’Connor, C. M., Collins, K., and Feigon, J. (2006) RNA, 12, 1475–1485.PubMedGoogle Scholar
  127. 127.
    Mason, D. X., Goneska, E., and Greider, C. W. (2003) Mol. Cell. Biol., 23, 5606–5613.PubMedGoogle Scholar
  128. 128.
    Prathapam, R., Witkin, K. L., O’Connor, C. M., and Collins, K. (2005) Nat. Struct. Mol. Biol., 12, 252–257.PubMedGoogle Scholar
  129. 129.
    Brown, Y., Abraham, M., Pearl, S., Kabaha, M. M., Elboher, E., and Tzfati, Y. (2007) Nucleic Acids Res., 35, 6280–6289.PubMedGoogle Scholar
  130. 130.
    Zappulla, D. C., Goodrich, K., and Cech, T. R. (2005) Nat. Struct. Mol. Biol., 12, 1072–1077.PubMedGoogle Scholar
  131. 131.
    Venteicher, A. S., Meng, Z., Mason, P. J., Veenstra, T. D., and Artandi, S. E. (2008) Cell, 132, 945–957.PubMedGoogle Scholar
  132. 132.
    Witkin, K. L., and Collins, K. (2004) Genes Dev., 18, 1107–1118.PubMedGoogle Scholar
  133. 133.
    O’Connor, C. M., and Collins, K. (2006) Mol. Cell. Biol., 26, 2029–2036.PubMedGoogle Scholar
  134. 134.
    Feng, J., et al. (1995) Science, 269, 1236–1241.PubMedGoogle Scholar
  135. 135.
    Fu, D., and Collins, K. (2006) Genes Dev., 20, 531–536.PubMedGoogle Scholar
  136. 136.
    Mitchell, J. R., and Collins, K. (2000) Mol. Cell, 6, 361–371.PubMedGoogle Scholar
  137. 137.
    Pogacic, V., Dragon, F., and Filipowicz, W. (2000) Mol. Cell. Biol., 20, 9028–9040.PubMedGoogle Scholar
  138. 138.
    Dragon, F., Pogacic, V., and Filipowicz, W. (2000) Mol. Cell. Biol., 20, 3037–3048.PubMedGoogle Scholar
  139. 139.
    Seto, A. G., Zaug, A. J., Sobel, S. G., Wolin, S. L., and Cech, T. R. (1999) Nature, 401, 177–180.PubMedGoogle Scholar
  140. 140.
    Chapon, C., Cech, T. R., and Zaug, A. J. (1997) RNA, 3, 1337–1351.PubMedGoogle Scholar
  141. 141.
    Mozdy, A. D., and Cech, T. R. (2006) RNA, 12, 1721–1737.PubMedGoogle Scholar
  142. 142.
    Teixeira, M. T., Forstemann, K., Gasser, S. M., and Lingner, J. (2002) EMBO Rep., 3, 652–659.PubMedGoogle Scholar
  143. 143.
    Gallardo, F., Olivier, C., Dandjinou, A. T., Wellinger, R. J., and Chartrand, P. (2008) EMBO J., 27, 748–757.PubMedGoogle Scholar
  144. 144.
    Box, J. A., Bunch, J. T., Tang, W., and Baumann, P. (2008) Nature, 456, 910–914.PubMedGoogle Scholar
  145. 145.
    Hughes, T. R., Evans, S. K., Weilbaecher, R. G., and Lundblad, V. (2000) Curr. Biol., 10, 809–812.PubMedGoogle Scholar
  146. 146.
    Lingner, J., Cech, T. R., Hughes, T. R., and Lundblad, V. (1997) Proc. Natl. Acad. Sci. USA, 94, 11190–11195.PubMedGoogle Scholar
  147. 147.
    Zhou, J., Hidaka, K., and Futcher, B. (2000) Mol. Cell. Biol., 20, 1947–1955.PubMedGoogle Scholar
  148. 148.
    Virta-Pearlman, V., Morris, D. K., and Lundblad, V. (1996) Genes Dev., 10, 3094–3104.PubMedGoogle Scholar
  149. 149.
    Evans, S. K., and Lundblad, V. (1999) Science, 286, 117–120.PubMedGoogle Scholar
  150. 150.
    Snow, B. E., Erdmann, N., Cruickshank, J., Goldman, H., Gill, R. M., Robinson, M. O., and Harrington, L. (2003) Curr. Biol., 13, 698–704.PubMedGoogle Scholar
  151. 151.
    Neidle, S. (2009) Curr. Opin. Struct. Biol., 19, 239–250.PubMedGoogle Scholar
  152. 152.
    Wong, H. M., Payet, L., and Huppert, J. L. (2009) Curr. Opin. Mol. Ther., 11, 146–155.PubMedGoogle Scholar
  153. 153.
    Meyne, J., Ratliff, R. L., and Moyzis, R. K. (1989) Proc. Natl. Acad. Sci. USA, 86, 7049–7053.PubMedGoogle Scholar
  154. 154.
    Wright, J. H., and Zakian, V. A. (1995) Nucleic Acids Res., 23, 1454–1460.PubMedGoogle Scholar
  155. 155.
    Bourns, B. D., Alexander, M. K., Smith, A. M., and Zakian, V. A. (1998) Mol. Cell. Biol., 18, 5600–5608.PubMedGoogle Scholar
  156. 156.
    Smith, C. D., Smith, D. L., DeRisi, J. L., and Blackburn, E. H. (2003) Mol. Biol. Cell, 14, 556–570.PubMedGoogle Scholar
  157. 157.
    Gao, H., Cervantes, R. B., Mandell, E. K., Otero, J. H., and Lundblad, V. (2007) Nat. Struct. Mol. Biol., 14, 208–214.PubMedGoogle Scholar
  158. 158.
    Pennock, E., Buckley, K., and Lundblad, V. (2001) Cell, 104, 387–396.PubMedGoogle Scholar
  159. 159.
    Fisher, T. S., Taggart, A. K., and Zakian, V. A. (2004) Nat. Struct. Mol. Biol., 11, 1198–1205.PubMedGoogle Scholar
  160. 160.
    Smogorzewska, A., and de Lange, T. (2004) Annu. Rev. Biochem., 73, 177–208.PubMedGoogle Scholar
  161. 161.
    De Lange, T. (2005) Genes Dev., 19, 2100–2110.PubMedGoogle Scholar
  162. 162.
    Gilson, E., and Geli, V. (2007) Nat. Rev. Mol. Cell. Biol., 8, 825–838.PubMedGoogle Scholar
  163. 163.
    Guedin, A., de Cian, A., Gros, J., Lacroix, L., and Mergny, J. L. (2008) Biochimie, 90, 686–696.PubMedGoogle Scholar
  164. 164.
    Johnson, J. E., Smith, J. S., Kozak, M. L., and Johnson, F. B. (2008) Biochimie, 90, 1250–1263.PubMedGoogle Scholar
  165. 165.
    Griffith, J. D., Comeau, L., Rosenfield, S., Stansel, R. M., Bianchi, A., Moss, H., and de Lange, T. (1999) Cell, 97, 503–514.PubMedGoogle Scholar
  166. 166.
    Wei, C., and Price, M. (2003) Cell. Mol. Life Sci., 60, 2283–2294.PubMedGoogle Scholar
  167. 167.
    Lei, M., Zaug, A. J., Podell, E. R., and Cech, T. R. (2005) J. Biol. Chem., 280, 20449–20456.PubMedGoogle Scholar
  168. 168.
    Lee, J., Mandell, E. K., Tucey, T. M., Morris, D. K., and Lundblad, V. (2008) Nat. Struct. Mol. Biol., 15, 990–997.PubMedGoogle Scholar
  169. 169.
    Luke, B., Panza, A., Redon, S., Iglesias, N., Li, Z., and Lingner, J. (2008) Mol. Cell, 32, 465–477.PubMedGoogle Scholar
  170. 170.
    Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J. (2007) Science, 318, 798–801.PubMedGoogle Scholar
  171. 171.
    Schoeftner, S., and Blasco, M. A. (2008) Nat. Cell. Biol., 10, 228–236.PubMedGoogle Scholar
  172. 172.
    Luke, B., and Lingner, J. (2009) EMBO J., 28, 2503–2510.PubMedGoogle Scholar
  173. 173.
    Sharon, E., Freeman, R., Riskin, M., Gil, N., Tzfati, Y., and Willner, I. (2010) Anal. Chem., 82, 8390–8397.Google Scholar
  174. 174.
    Greider, C. W., and Blackburn, E. H. (1985) Cell, 43, 405–413.PubMedGoogle Scholar
  175. 175.
    Cohen, S. B., Graham, M. E., Lovrecz, G. O., Bache, N., Robinson, P. J., and Reddel, R. R. (2007) Science, 315, 1850–1853.PubMedGoogle Scholar
  176. 176.
    Skvortsov, D. A., Rubtsova, M. P., Zvereva, M. I., Kisseljov, F. L., and Dontsova, O. A. (2009) Acta Naturae, 49–65.Google Scholar
  177. 177.
    Cohen, S. B., and Reddel, R. R. (2008) Nat. Meth., 5, 355–360.Google Scholar
  178. 178.
    Kim, N. W., and Wu, F. (1997) Nucleic Acids Res., 25, 2595–2597.PubMedGoogle Scholar
  179. 179.
    Fajkus, J. (2006) Clin. Chim. Acta, 371, 25–31.PubMedGoogle Scholar
  180. 180.
    Sahin, E., and DePinho1, R. A. (2010) Nature, 464, 520–528.PubMedGoogle Scholar
  181. 181.
    Lin, J., Epel, E., Cheon, J., Kroenke, C., Sinclair, E., Bigos, M., Wolkowitz, O., Mellon, S., and Blackburn, E. (2010) J. Immunol. Meth., 352, 71–80.Google Scholar
  182. 182.
    Harley, C. B., Liu, W., Blasco, M., Vera, E., Andrews, W. H., Briggs, L. A., and Raffaele, J. M. (2010) Rejuvenation Res., ahead of print.Google Scholar
  183. 183.
    Passos, J. F., et al. (2007) PLoS Biol., 5, e110.PubMedGoogle Scholar
  184. 184.
    Haendeler, J., Hoffmann, J., Diehl, J. F., Vasa, M., Spyridopoulos, I., Zeiher, A. M., and Dimmeler, S. (2004) Circ. Res., 94, 768–775.PubMedGoogle Scholar
  185. 185.
    Tanaka, Y., Moritoh, Y., and Miwa, N. (2007) J. Cell. Biochem., 102, 689–703.PubMedGoogle Scholar
  186. 186.
    Dong, X. X., Hui, Z. J., Xiang, W. X., Rong, Z. F., Jian, S., and Zhu, C. J. (2007) J. Cardiovasc. Pharmacol., 49, 111–115.PubMedGoogle Scholar
  187. 187.
    Flores, I., and Blasco, M. A. (2010) FEBS Lett., 584, 3826–3830.PubMedGoogle Scholar
  188. 188.
    Datta, A., Bellon, M., Sinha-Datta, U., Bazarbachi, A., Lepelletier, Y., Canioni, D., Waldmann, T. A., Hermine, O., and Nicot, C. (2006) Blood, 108, 1021–1029.PubMedGoogle Scholar
  189. 189.
    Hajek, M., Matulova, N., Votruba, I., Holy, A., and Tloust’ova, E. (2005) Biochem. Pharmacol., 70, 894–900.PubMedGoogle Scholar
  190. 190.
    Sluis-Cremer, N., Temiz, N. A., and Bahar, I. (2004) Curr. HIV Res., 2, 323–332.PubMedGoogle Scholar
  191. 191.
    Herschhorn, A., and Hizi, A. (2010) Cell Mol. Life Sci., 67, 2717–2747.PubMedGoogle Scholar
  192. 192.
    Ueno, T., Takahashi, H., Oda, M., Mizunuma, M., Yokoyama, A., Goto, Y., Mizushina, Y., Sakaguchi, K., and Hayashi, H. (2000) Biochemistry, 39, 5995–6002.PubMedGoogle Scholar
  193. 193.
    Mouscadet, J. F., and Desmaele, D. (2010) Molecules, 15, 3048–3078.PubMedGoogle Scholar
  194. 194.
    Yamakuchi, M., Nakata, M., Kawahara, K., Kitajima, I., and Maruyama, I. (1997) Cancer Lett., 119, 213–219.PubMedGoogle Scholar
  195. 195.
    Paritala, H., and Firestine, S. M. (2009) Bioorg. Med. Chem. Lett., 19, 1584–1587.PubMedGoogle Scholar
  196. 196.
    Yamakuchi, M., Nakata, M., Kawahara, K., Kitajima, I., and Maruyama, I. (1997) Cancer Lett., 119, 213–219.PubMedGoogle Scholar
  197. 197.
    Naasani, I., Seimiya, H., Yamori, T., and Tsuruo, T. (1999) Cancer Res., 59, 4004–4011.PubMedGoogle Scholar
  198. 198.
    Lipps, H. J., and Rhodes, D. (2009) Trends Cell. Biol., 19, 414–422.PubMedGoogle Scholar
  199. 199.
    Balasubramanian, S., and Neidle, S. (2009) Curr. Opin. Chem. Biol., 13, 345–353.PubMedGoogle Scholar
  200. 200.
    Neidle, S. (2010) FEBS J., 277, 1118–1125.PubMedGoogle Scholar
  201. 201.
    Damm, K., et al. (2001) EMBO J., 20, 6958–6968.PubMedGoogle Scholar
  202. 202.
    Huang, H. S., Chou, C. L., Guo, C. L., Yuan, C. L., Lu, Y. C., Shieh, F. Y., and Lin, J. J. (2005) Bioorg. Med. Chem., 13, 1435–1444.PubMedGoogle Scholar
  203. 203.
    Eitsuka, T., Nakagawa, K., Suzuki, T., and Miyazawa, T. (2005) Biochim. Biophys. Acta, 1737, 1–10.PubMedGoogle Scholar
  204. 204.
    Rangarajan, S., and Friedman, S. H. (2007) Bioorg. Med. Chem. Lett., 17, 2267–2273.PubMedGoogle Scholar
  205. 205.
    Wang, X., Hao, M. W., Dong, K., Lin, F., Ren, J. H., and Zhang, H. Z. (2009) Arch. Pharm. Res., 32, 1263–1269.PubMedGoogle Scholar
  206. 206.
    Hayakawa, N., Nozawa, K., Ogawa, A., Kato, N., Yoshida, K., Akamatsu, K., Tsuchiya, M., Nagasaka, A., and Yoshida, S. (1999) Biochemistry, 38, 11501–11507.PubMedGoogle Scholar
  207. 207.
    Chen, J. L., and Greider, C. W. (2004) Proc. Natl. Acad. Sci. USA, 101, 14683–14684.PubMedGoogle Scholar
  208. 208.
    Dikmen, Z. G., Ozgurtas, T., Gryaznov, S. M., and Herbert, B. S. (2009) Biochim. Biophys. Acta, 1792, 240–247.PubMedGoogle Scholar
  209. 209.
    Gryaznov, S. M. (2010) Chem. Biodivers, 7, 477–493.PubMedGoogle Scholar
  210. 210.
    Maida, Y., Yasukawa, M., Furuuchi, M., Lassmann, T., Possemato, R., Okamoto, N., Kasim, V., Hayashizaki, Y., Hahn, W. C., and Masutomi, K. (2009) Nature, 461, 230–235.PubMedGoogle Scholar
  211. 211.
    Parkinson, E. K., Fitchett, C., and Cereser, B. (2008) Cytogenet. Genome Res., 122, 273–280.PubMedGoogle Scholar
  212. 212.
    Gandellini, P., Folini, M., Bandiera, R., de Cesare, M., Binda, M., Veronese, S., Daidone, M. G., Zunino, F., and Zaffaroni, N. (2007) Biochem. Pharmacol., 73, 1703–1714.PubMedGoogle Scholar
  213. 213.
    Beliveau, A., Bassett, E., Lo, A. T., Garbe, J., Rubio, M. A., Bissell, M. J., Campisi, J., and Yaswen, P. (2007) Proc. Natl. Acad. Sci. USA, 104, 4431–4436.PubMedGoogle Scholar
  214. 214.
    Gu, B., Bessler, M., and Mason, P. J. (2009) Cell Cycle, 8, 6–10.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • M. I. Zvereva
    • 1
    Email author
  • D. M. Shcherbakova
    • 1
  • O. A. Dontsova
    • 1
  1. 1.Faculty of ChemistryLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations